Responses of Cool Season Grain Legumes to Soil Abiotic Stresses

COOLSEASON GRAINLEGUMESTO SOIL

RESPONSES OF

ABIOTIC STRESSES H. P. S. Jayasundara, B. D. Thomson, and C. Tang Cooperative Research Centre for Legumes in Mediterranean Agriculture University of Western Australia Nedlands, Western Australia 6907 Australia

I. Introduction 11. Soil ,4cidity A. Responses of Cool Season Grain Legumes to Soil Acidity B. Factors Relating to Poor Growth in Acidic Soils C. Effects of Soil Acidity on Nodulation and N2 Fixation D. Genetic Variation in Response to Soil Acidity 111. Soil Salinity and Sodicity A. Responses of Cool Season Grain Legumes to Soil Salinity B. Responses of Cool Season Grain Legumes to Sodicity C. Factors Relating to Poor Growth in Saline and Sodic Soils D. Factors Influencing Salinity Response E. Effects of Salinity and Sodicity on Nodulation and N z Fixation F. Genetic Variation in Response to Salinity and Sodicity W. Soil Alkalinity A. Responses of Cool Season Grain Legumes to Soil Alkalinity B. Factors Relating to Poor Growth in Alkaline Soils C. Effects of Soil Alkalinity on Nodulation and N 2 Fixation D. Genetic Variation in Response to Soil Alkalinity V. Soil Compaction A. Responses of Cool Season Grain Legumes to Soil Compaction B. Factors Relating to Poor Growth in Compacted Soils C. Effects of Soil Compaction on Nodulation and N2 Fixation D. Genetic Variation in Response to Soil Compaction VI. Waterlogging A. Responses of Cool Season Grain Legumes to Waterlogging B. Physiology of Waterlogging Stress C. Effects of Waterlogging on Nodulation and N, Fixation D. Genetic Variation in Tolerance to Waterlogging VII. Conclusions References

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I. INTRODUCTION Grain legumes are an important source of dietary protein for many people throughout the world, particularly for those in developing countries. They also constitute a major component of animal feed in developed countries. Grain legumes play a major role in low-input agricultural systems because of their ability to fix atmospheric nitrogen. Their contribution of biologically fixed nitrogen is a key factor in sustaining long-term soil fertility in cereal production both in the developed and developing worlds. Grain legumes can be categorized into two major groups, based on their geographical and climatic distribution in the world: (1) warm season grain legumes and (2) cool season grain legumes. Warm season grain legumes, which include soybean (Glycine m a ) , common bean (Phaseolus vulgaris), cowpea (Vigna unguiculata),mungbean (Vigna radiata),blackgram (Vigna mungo), pigeon pea (Cujanus cajan),and several other species with regional importance, e.g., adzuki bean (Vigna angularis)and lima bean (Phaseoluslunatus), are cultivated in tropical and subtropical climatic regions of the world. Major cool season grain legumes include chickpea (Cicer arietinum L.), faba bean (Vicia faba L.), lentil (Lens culinaris Medik.), and field pea (Pisum sativum L.), which are the main food legumes, and lupins (predominantly Lupinus angustifolius, L. abtus, and L. luteus) and vetches (Viciasp.), which are mainly used as animal feed. There is a considerable production of Luthyrus safivus (chickling pea or chickling vetch), particularly in India, Bangladesh, Nepal, and Ethiopia, but the future potential of this species as a food or feed legume largely depends c n introduction of cultivars with low concentrations of antinutritional factors (Oram and Agcaoili, 1994). Cool season grain legumes are primarily cultivated in temperate, mediterranean, and subtropical regions in the world but are also grown at high altitudes in the tropics (e.g., Ethiopia). Cool season grain legumes occupied nearly 40% of the total world grain legume producing area (67.2 X lo6 ha) but contributed more than 50% of the total world grain legume production (58.0 X lo6 tonnes) during the period from 1992 to 1994 (FAO, 1994). Of the total cool season grain legume production (29.5 X lo6 tonnes), field pea comprised the biggest share with 49% of the total, followed by chickpea (24%), faba bean (13%), lentil (9%), and lupins (4%) (FAO, 1994; Cox, 1997). Over 80% of the total world production of faba bean and lentil and almost all of the world production of chickpea occurred in developing countries, whereas about 85% of total field pea production occurred in developed countries (FAO, 1994). Australia produces the greatest share (80%) of world lupin (Cox, 1997). Current production and future expansion of cool season grain legumes are constrained by biotic and abiotic factors. Biotic constraints for cool season grain legumes include diseases, insect pests, and, for some species, competition from weeds, e.g., Orobanche spp. (Saxena, 1993), and these aspects have been dis-

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cussed in several recent reviews (Bond et al., 1991; Singh el at., 1991; Ali et al., 1991; Erskine et ai.,1991). The most common abiotic factors that constrain the yield of cool season grain legumes are moisture stress and extremes of temperatures (both heat and cold), and these constraints have received the most attention (Buddenhagen and Richards, 1988; Saxena, 1993). Other abiotic constraints for cool season grain legumes are mainly soil related and include acidity, alkalinity, salinity, sodicity, waterlogging, and deficiency or toxicity of mineral nutrients (Saxena, 1993). Soil abiotic stresses may act directly on plant growth but may also interact with root growth to affect the water and nutrient relations of the plant. The extent of limitation imposed by soil-related abiotic stresses on cool season grain legume production has not been estimated on a worldwide scale, but it is of considerable importance at the regional level. Currently, there are about 950 X lo6 ha (about 6% of the world’s land area) of “salt-affected land” worldwide and include both saline and sodic soils (Flowers and Ye0 1995). A large proportion of this land is distributed in the major cool season grain legume producing regions, e.g., in the Indian subcontinent, where more than 70% of the world’s chickpea production and nearly 30% of the world’s lentil production originates (FAO, 1994). Between 14.1 X lo6 and 34.3 X 106 ha is salt affected (Singh, 1992; Abrol er al., 1988). Moreover, the problem of secondary salinization is ever increasing due to either rising water tables resulting from clearing of native vegetation for cultivation (e.g., Australia, McWilliam, 1986) or inadequate drainage in irrigated land (e.g., India and Pakistan, Singh. 1992). According to Szabolcs (1 987) about half of the existing irrigation systems in the world are more or less under the influence of secondary salinization, alkalization, and waterlogging due to mismanagement. In India alone an average of 11% of the potential irrigated area is subjected to salinity, and an average of 18% is waterlogged (Singh, 1992). Transient waterlogging can also affect the growth of cool season grain legumes in rain-fed mediterranean environments due to the high concentration of rainfall during winter, particularly where soil drainage is poor. We were unable to find reliable estimates of world production losses of cool season grain legumes due to waterlogging or to the total area of land affected by waterlogging. As with other soil abiotic stresses, the extent of constraint imposed by soil acidity on cool season grain legume production has not been accurately estimated. According to Uexkull and Mutert (1994), of about 3190 X lo6 ha total potentially arable land in the world, nearly 80% (about 2500 X lo6 ha) is acidic. Although a large proportion (about 68%) of these acidic soils occur in the humid tropics, a considerable proportion is also distributed in Australia, North America, and Europe (Uexkull and Mutert, 1994) where the potential for cool season grain legume production is high. As a regional example, acidic soils (pH H,O < 6.0) occupy around 15 million ha of arable land in southern Australia (Porter and McLaughlin, 1992), and this is already a considerable barrier for expansion of cool season grain legumes (particularly chickpea and faba bean) production in this region.

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The primary propose of this review is to pool current knowledge and understanding of the responses of different cool season grain legumes to soil abiotic stresses and to identify the major limitations to plant growth, as well as to explore the extent of inter- and intraspecific genetic variation in response to soil abiotic stresses for most commonly cultivated cool season grain legumes. We have mainly focused on experimental evidence directly relevant to cool season grain legumes, but in discussing principals examples from tropical grain legumes are considered, particularly when information is not available for cool season grain legumes. We have divided the major soil abiotic stresses into five sections (acidity, salinity and sodicity, alkalinity, soil structural problems, and waterlogging), but it should be remembered that in most situations these stresses are closely related, e.g., sodicity and soil structural problems, salinity and waterlogging. In each section, the responses of cool season grain legumes to a particular stress are discussed first and followed by the major factors contributing to reduced growth and yield. The effects of these factors on symbiotic nitrogen fixation are considered separately. We end each section by considering the extent of intraspecific variation in response of particular stress factor for the major cool season grain legumes.

11. SOIL ACIDITY Acidification is a natural soil-forming process favoured by high rainfall, low evaporation, leaching of basic cations, and high oxidative biological activity that produces acids (Rowell, 1978).Human activities, such as intensive agriculture and industrialization, can accelerate the rate of acidification (Helyar and Porter, 1989). The major constraints to plant growth in acidic soils are toxicities of H+, aluminium, and manganese and deficiencies of calcium, magnesium, phosphorus, and molybdenum (Foy, 1984). The relative importance of these constraints may vary with soil type, parent material, soil pH, soil structure and texture, and plant species. Acidity in the surface soil can be ameliorated with liming, but subsoil acidity is a serious constraint to plant growth because it can not be easily ameliorated with surface application of lime (Helyar and Porter, 1989).The chemistry of acidic soils has been comprehensively reviewed by Thomas and Hargrove ( 1984) and Ritchie (1989).

A. RESPONSESOF COOLSEASONGRAINLEGUMES TO SOILACIDITY Soil acidity considerably limits the productivity of cool season grain legumes. This is clearly demonstrated by large improvements in growth and yield observed

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for many species in response to liming (Jessop and Mahoney, 1982; Mahler and McDole, 1985; Brooke eta[., 1989).Under field conditions in northeastern Victoria, liming acidic soils with pH (CaCI,) 4.4 improved grain yield of field pea by about 50% and chickpea by more than 140% (Brook er al., 1989). Vegetative growth of faba bean, field pea, and chickpea on acid soils with pH 5.4 (H,O) was increased by more than 200% in response to liming (Jessop and Mahoney, 1982). Mahler and McDole (1987) found that a decrease in soil pH by one unit from a critical level of about 5.5 (H,O) caused around 80% decrease in the grain yield of field pea and lentil. The responses of cool season grain legumes to soil acidity may vary between species (Fig. 1). Among commonly cultivated species, lentil appears to be the most sensitive species, growth being reduced at pH < 7 in nutrient solution even when mineral nitrogen was supplied (Tang and Thomson, 1996). In contrast, the growth of lupins (L. nlbus and L. u ~ g u ~were ~ not ~ affected ~ ~ ~until i pH ~ ~< 5) (Fig. 1). Chickpea was also affected by pH below 7.0 when dependent on biological N, fixation but was relatively less affected when mineral nitrogen was supplied (Tang and Thomson, 1996). Field pea and faba bean were moderately sensitive to low pH, growth being reduced at pH < 6 (Fig. 1 ) . These comparisons between species, however, were based on growth responses to one factor in acidity stress, i.e., high H + activity or low pH. Our present knowledge on the differential responses of cool

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Figure 1 Effects of pH and bicarbonate ions on relative shoot fresh weight (N2-fixing plants) of six cool season grain legume species grown i n nutrient solutions for 23 days (redrawn from Tang and Thornson, 1996).

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season grain legumes to other factors associated with soil acidity, i.e., A1 and Mn toxicity, are limited to only a few species. Results from several studies, for example, have shown that lupins are relatively more tolerant of high concentrations of A1 than are faba bean (Guerrier and Morard, 1978; Horst and Goppel, 1986a; Grauer and Horst, 1990). Among lupin species L. luteus is relatively more tolerant of high A1 than is L. angusfifolius (Can and Sweetingham, 1994). In an acidic soil containing 30 ppm exchangeable A13+ and 50 ppm exchangeable Mn2+ at pH (CaCl,) 4.4, chickpea yield responded more to liming than that of field pea, which in turn responded more than that of lupin (Brooke et al., 1989). Cool season grain legumes generally appear to be more sensitive to acidity than do cereals (Mahler and McDole, 1987; Brook et al., 1989; Yan et a/., 1992); for example, the minimum acceptable pH (H,O) for maximum grain yield of lentil and field pea were 5.65 and 5.52, respectively, compared with 5.23 for barley and 5.19 for wheat (Mahler and McDole, 1987).

B. FACTORS RELATINGTO POORGROWTHIN ACIDICSOILS 1. Hydrogen Ion Toxicity High H+ activity at low pH can directly affect grain legume growth; however, this is compounded and often overshadowed by Al toxicity, Mn toxicity, and deficiencies of Ca, Mg, and P (Foy, 1984). Thus, most evidence for inhibitory effects of H+ on growth of cool season grain legumes has come from solution culture experiments (Evans et al., 1980; van Beusichem, 1982; Schubert et al., 1990a; Yan et al., 1992;Tang and Thomson, 1996). Schubert et al. (1990a), for example, found that shoot dry matter of faba bean dependent on mineral nitrogen decreased by more than 25% when solution pH was reduced from 7.0 to 5.5. Similarly, Tang and Thomson (1996) found that shoot growth of a number of cool season grain legumes (lentil, chickpea, faba bean, and field pea) supplied with mineral N declined at pH below 5.0 in the nutrient solution. These results suggest a direct effect of high H+ on grain legume growth. The reductions in shoot growth of grain legume species at low pH is normally associated with more severe depressions in root growth; for example, solution pH at 5.5 reduced root dry matter of field pea by about 40% even without a decrease in shoot dry matter (van Beusichem, 1982). In faba bean, the rate of root elongation was about 80% lower at pH 4.0 than at pH 6.5 in the solution culture (Yan et a/., 1992). The effects of low pH in the bulk soil in reducing root growth can be accentuated by decreased rhizosphere pH in plants dependent on N, fixation compared with plants fed with nitrate (van Beusichem and Langelaan, 1984). The depressions in root elongation and shoot growth associated with high concentrations of Ht are related to decreased proton extrusion from roots (van Beu-

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sichem, 1982; Schubert etal., 1990a; Yan elal., 1992). In faba bean growth in nutrient solutions, increasing H+ activity decreased net H+ extrusion from roots with a concurrent reduction in the rate of root elongation (Yan et a[., 1992). At pH Values below 4.0 both root elongation and net extrusion of H + in faba bean had ceased (Yan er al., 1992). The impairment of net H + extrusion at low pH may be attributed to an inhibition of H+-ATPase activity (Marschner, 1995) or reentry of H+ into root cells (Yan et ai., 1992). Low pH can impair membrane integrity, particularly at low external Ca2+ concentrations (Foy, 1984). Increasing Ca2+ concentration from 0.1 mM to 5 mM in the rooting medium significantly increased both net H+ release from the roots and the rate of root elongation in faba bean at pH 4.1 (Yan et ul., 1992). Hydrogen ion extrusion from the root is an important process required for the uptake of nutrients (Marschner, 1995) and the regulation of cytoplasmic pH (Felle, 1988). Consequently, the inhibition of H + extrusion at low pH may lead to both limited nutrient uptake and disturbed cytoplasmic pH regulation.

2. Aluminium Toxicity Aluminium toxicity is probably the most dominant growth-limiting factor in acidic soils. With decreasing pH, the solubility of A1 in soils increases sharply, particularly at pH below 5.0 (Foy, 1984). However, Al-mediated inhibition of growth is not directly correlated with total soluble A1 in the soil because of the high variation in relative toxicity of different A1 ion species (Taylor, 1988). The chemical reactions that form different A1 species are highly pH dependent; thus the phytotoxicity of A1 also varies with soil pH (Ritchie, 1989). In addition, many other soil factors-ie., type of clay minerals, organic matter levels, and ionic strength-as well as plant factors may influence the extent of phytotoxicity of different A1 species (Foy, 1984). In general, toxicity is decreased when A1 is complexed with organic ligands, F- and SO:-, whereas the activity of A13+ and Al-hydroxy species are considered to be most phytotoxic (Ritchie, 1989). Aluminium primarily affects root growth, particularly root elongation and lateral branching. In faba bean, root elongation is decreased by about 50% in the presence of 9.3 mM m-3 AICI, in the rooting medium (Grauer and Horst, 1990), whereas in field pea, root elongation was completely inhibited by 100 mM m p 3 AlCl, in the solution (Matsumoto, 1991). Numerous reports of tropical grain legumes also demonstrate the inhibitory effects of A1 on root growth (e.g., cowpea, Horst et al., 1983; common bean, Buerkert et al., 1990; soybean, Foy er al., 1993). Aluminium-affected roots are stubby as a result of the inhibition of elongation and lateral branching (Foy, 1984; Matsumoto, 1991 ). In the field, poor root penetration into acidic subsoils results in plants that are shallow rooted ( e g , faba bean, Hartmann and Aldag, 1989; chickpea and field pea, Seifu, 1993) and therefore inefficient in exploring nutrients and water from deeper soil layers (Foy, 1992).

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Most shoot symptoms resulting from A1 toxicity are secondary and often similar to deficiencies of P, Ca, and Mg (Foy, 1984). Aluminium taken up by plants is normally sequestered in roots and not easily translocated to shoots until at least the retaining capacity of roots is exceeded (e.g., faba bean and field pea, Wagatsuma, 1984). Thus, growth depressions resulting from A1 toxicity may not be well correlated with leaf A1 concentrations (Taylor, 1988). Some evidence indicates that A1 might inhibit the biosynthesis of cytokinins in the root apex, which regulates shoot growth under normal conditions (Pan et al., 1989). It is generally believed, however, that reduced shoot growth due to A1 toxicity is primarily due to limited supply of nutrients, particularly Ca, Mg, and P, as well as water stress (Marschner, 1995). The mechanisms of A1 toxicity are complex and still not fully understood. Aluminium has been found to interfere with a large number of physiological processes in root cells (Matsumoto, 1991). These may be grouped into four categories (Taylor, 1988): (1) inhibition of DNA synthesis and mitosis, (2) disruption of membrane structure and function, (3) inhibition of cell elongation, and (4) disruption of uptake and translocation of mineral nutrients and metabolism. Inhibition of cell division by high concentrations of AI3+ is the primary cause for restricted root elongation in some grain legumes (e.g., cowpea, Host et al., 1983; field pea, Matsumoto, 1991). Aluminium interferes with nucleic acid metabolism in root meristematic cells of field pea (Matsumoto, 1991). Restricted cell elongation, however, also contributes greatly to reduced root elongation, especially at moderate concentrations of external A13+ (Marschner, 1991). AIuminium has a high affinity for phospholipids in plasma membranes (Haug and Shi, 199 1); thus A1 can bind to the plasma membrane of the root rhizodermal and cortical cells and thereby impair its normal functioning (e.g., field pea, Wagatsuma ef al., 1995). All cool season grain legume species are not equally affected by high concentrations of A1 in the rooting medium. Roots of some species can withstand relatively high concentrations of A1 without significant inhibition of elongation. In lupin (L. luteus), for example, between 3 and 4 mg A1 g-I dry weight might accumulate in root apical zone before root elongation is inhibited, whereas less than 1 mg A1 g-’ dry weight is sufficient to inhibit root elongation in faba bean (Horst and Goppel, 1986b). Low concentrations of A]“+ (0.5-2 mg 1-’) at low pH may even stimulate plant growth, particularly in Al-tolerant species or cultivars (e.g., field pea cv. Uspekh, Klimashevskii et al., 1970; lupin, Horst and Goppel, 1986b), which may be related to a possible amelioration of H + ion toxicity by small concentrations of Aln+ (Marschner, 1995). Although some plant species can tolerate high concentrations of aluminium by internal activation in older leaves (e.g., tea, Matsumoto ef al., 1976), the majority of crop species or cultivars tolerant to A1 achieve this ability mainly by “exclusion” of A1 from sensitive sites, i.e., cytoplasm, plasma membrane-apoplasm interface, and the apoplasm in root cells (Marschner, 1995). The mechanisms that may be involved in A1 exclusion are

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(Taylor, 1995) (1) immobilization of A1 at the cell wall or low cell wall CEC, (2) selective permeability of the plasma membrane, (3) formation of a plant-induced pH barrier in the rhizosphere or root appoplasm, (4) exudation of chelator ligands, (5) exudation of phosphate, and (6) A1 efflux. Of these, the exudation of chelator legands is a frequently observed adaptive mechanism in a number of grain legumes species (e.g., L. luteus, Guerrier et a/., 1977; cowpea, Host et al., 1983; soybean, Horst et a/., 1990; chickpea, Rai, 1991). In some instances A1 tolerance has been associated with greater efficiency of uptake and translocation of P (e.g., field pea cv. Uspekh, Klimashevskii et al., 1970) and Ca (e.g., cowpea, Horst, 1987). 3. Manganese Toxicity The availability of Mn2+ and, hence, the potential for manganese toxicity increases with decreasing pH in the soil provided sufficient quantities of total manganese are present (Foy, 1984). In general, manganese toxicity can occur at relatively higher pH levels than those required for A1 toxicity (Fox et al., 1991). Unlike aluminium, manganese absorbed by plant roots is easily transported to shoots. Thus, in most plants, including grain legumes, manganese toxicity first affects shoot growth (Foy, 1984). Roots, however, may also be affected if the toxicity becomes severe (e.g., soybean, Suresh et al., 1989). In general, the reduction in shoot growth due to Mn toxicity is correlated well with leaf Mn concentration (e.g., soybean, Bethlenfalvay and Franson, 1989; cowpea, Vega et a/., 1992). The common symptoms of Mn toxicity in grain legumes are interveinal chlorosis and “crinkle leaf’ in young leaves (e.g., soybean, Heenan and Carter, 1977) and formation of brown speckles in mature leaves (e.g., common bean, Horst and Marschner, 1978; cowpea, Wissemeier and Horst, 1992). Some of these symptoms (such as crinkle leaf and chlorosis) are probably related to induced deficiencies of Ca and Mg (Maschner, 1995). Apart from the interferences with Ca and Mg nutrition, excess Mn disrupts phytohormone balance (e.g., activities of IAA), certain enzyme activities (e.g., RuBPcarboxilase) and, membrane functions in leaf tissues (Horst, 1988). For cool season grain legumes, only limited information is available on critical toxic levels of Mn at which growth is adversely affected. Of different species, lupins (L. angustifolius and L. albus) appear to be relatively tolerant to high concentrations of Mn since they can accumulate relatively higher concentrations of Mn than most other species without apparent toxicity symptoms (Gladstones, 1962). In L. angustifolius toxicity was reported at shoot Mn 2 2000 ppm, whereas in chickpea toxicity occurs at 2 520 ppm manganese in shoots (Reuter and Robinson, 1986). Among other cool season grain legumes, toxicity symptoms were apparent when plants had > 1000 ppm Mn in faba bean and > 1700 ppm Mn in field pea (Snowball and Robson, 1991; Weir and Cresswell, 1993). For comparison, in some common tropical grain legumes (e.g., soybean, common bean,

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cowpea, pigeon pea) growth was reduced by Mn at concentrations between 140 and 1600 ppm in the shoots (Edvards and Asher, 1982). The mechanisms of Mn tolerance are located predominantly in shoots (Horst, 1988). In Mn-tolerant cowpea cultivars manganese was uniformly distributed in mature leaves, whereas in sensitive cultivars with the same manganese content, manganese was accumulated in localized spots that correlated with chlorotic and necrotic patches (Horst, 1983). Other proposed mechanisms for tolerance to high concentrations of manganese are ( 1) restricted translocation of manganese to young leaves, ( 2 ) undisturbed translocation of Ca from mature leaves to young leaves, and (3) formation of stable manganese complexes, for example, with oxalic acid and polyphenols (Horst, 1988).

4. Nutrient Deficiencies Apart from low pH and toxicities of Al"+ and Mn3+, decrease of Ca, Mg and P uptake, and Mo deficiency can also limit growth of cool season grain legumes in acidic soils. Decreasing medium pH, for example, from 6.0 to 4.0 depressed the uptake of Ca and Mg by field pea and L. albus (Findenegg, 1987) and decreasing pH from 7.0 to 4.0 depressed the uptake of Ca, Mg, and P by faba bean (Schubert et al., 1990a). Deficiencies of these nutrients at low pH occur either due to reduced availability in soil or to interactions with high concentrations of H', A]"+, and Mn2+.Increasing external Al"+ concentrations decreased the uptake of Ca and Mg in faba bean and L. luteus (Horst and Goppel, 1986b). Marschner (1995) implicated high concentrations of Hi, Al"+, and Mn2+ as the primary reason for inhibited uptake or deficiencies of Ca and Mg in acidic soils. High external concentrations of H + at low pH can inhibit net Ht extrusion from roots (e.g., field pea, van Beusichem, 1982; faba bean, Yan ef al., 1992), which is essential for the uptake of nutrients (Marschner, 1991). In addition, high concentrations of Al"+ and Mn2+ can compete with Ca2+ and Mg2+ for binding at cation exchange sites in the apoplasm, further reducing the uptake of Ca2+ and Mg2+ (Marschner, 1991). In many instances, the risk of Al"+ and/or Mn2+-induced deficiencies of Ca and Mg and, thus, the severity of acidity-induced growth inhibition can be ameliorated by increasing external concentrations of Ca2+ and/or Mg2+ (Foy, 1992). In many instances plants effected by Al toxicity may exhibit symptoms similar to those of P deficiency (Foy, 1992). In a majority of acidic soils, P deficiency may occur due to high P-fixing capacity and/or precipitation of P to form less soluble aluminium phosphates in the soil (Rowell, 1987). Moreover, A1 can immobilize P on root surfaces, cell walls, and in the free spaces of plant roots presumably as aluminium phosphate, preventing P from being available for translocation to shoots and metabolism (e.g., cowpea, de Manzi and Cartwright, 1984). In addition, restricted root growth by A1 may further limit the uptake of relatively immobile P in the soil (Foy, 1992).

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In contrast with other micronutrients the availability of Mo is reduced with decreasing pH; thus deficiency of Mo is highly likely in acidic soils (Gupta and Lipsett, 1981). Molybdenum deficiency may particularly affect growth of legumes because of high requirements for Mo of plants dependent on biological N, fixation (see discussion later) (Coventry and Evans, 1989). Liming generally corrects Mo deficiency unless the soil is absolutely deficient of Mo (Foy, 1992).Large yield improvements in response to application of Mo have been observed in acidic soils deficient in Mo (e.g., soybean, Burmester et al., 1988; groundnut (Amchis hypogaea), Hafner et a/., 1992).

C. EFFECTSOF SOILACIDITYON NODULATION AND N, FIXATION Nodulation and N,fixation are particularly sensitive to soil acidity. This is clearly indicated by higher sensitivity of these species to acidity when dependent on biological N, fixation than on mineral nitrogen (Evans er d., 1980; van Beusichem and Langelaan, 1984; Schubert et at.. 1990b; Tang and Thomson, 1996). In general, nodulation declines at pH below 5.0 in most species including lupin, which is regarded as relatively acidity tolerant (Fig. 2). The impairment of the symbiosis arises from poor survival of the microsymbiont (field pea, Evans e f al., 1993; faba

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Figure 2 Effects of pH and bicarbonate ions on nodulation of six cool season grain legume species grown in nutrient solutions for 13 days (redrawn from Tang and Thomson, 1996).

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bean, Carter etal., 1995), inhibition of the nodulation process (field pea, Lie, 1969; Evans et af., 1980), and inhibition of nodule functioning (lentil, Rai and Prasad, 1983; field pea, Paulino et al., 1987; faba bean, Schubert et af.,1990b; chickpea, Rai, 1991). In most cool season grain legumes (except lupins), the nodule bacteria are fastgrowing rhizobia, and these are relatively more sensitive to acidity than slowgrowing bradyrhizobia, which nodulate most tropical grain legumes and lupins (Graham and Paker, 1964). Thus, rhizobial survival is an important limiting factor for nodulation in most cool season grain legumes growing in acidic soils. In some acidic soils, populations of Rhizobium spp. are extremely low. As an example, Amarger (1988) found that in acidic soils in France with pH < 5.5, Rhizobium leguminosarum bv. viciae was undetectable, whereas sufficient numbers of effective rhizobia of this species were often present in soils with alkaline reaction. Similar observations have been made in some acidic soils in Western Australia and southwest Victoria (Evans et al., 1993; Carter et al., 1995). That inadequate rhizobial populations limit nodulation in acidic soils was demonstrated by increased nodulation achieved through inoculation with appropriate rhizobia (e.g., faba bean, Carter et al., 1995; field pea, Evens et al., 1993; Seifu, 1993) and by increased rhizobial numbers and nodulation achieved through correcting soil acidity by liming (e.g., lentil, field pea, Mahler and McDole, 1985; Mohebbi and Mahler, 1989). Of various acidity factors, high concentrations of Hi andAl"+ and P deficiency appeared to be the major inhibitory factors for rhizobial growth (Coventry and Evans, 1989). In addition, Ca deficiency is an important limiting factor for some Rhizobium spp. (Howieson et al., 1995). Considerable genetic variation in response to acidity exists in rhizobia nodulating different cool season grain legumes (e.g., lentil, Rai and Prasad, 1983; chickpea, Rai, 1991; faba bean, Carter et al., 1995). Thus, it may be possible to extend the growth of cool season grain legumes to acidic soils by selection of acidic soil tolerant rhizobia (Howieson, 1995). Nodule initiation is also highly sensitive to acidity (Lie, 1969; Evans et al., 1980). In field pea, nodule initiation was 10 times more sensitive to acidity than was rhizobial growth, nodulation being completely inhibited at a medium pH 4.8 even when adequate populations of rhizobia were present (Evens et al., 1980). The inhibition of nodulation in field pea by acidity occurred in early stages of the infection process (Lie, 1969), suggesting that the most sensitive steps are probably rhizobial attachment, invasion, and development of the infection thread. Attachment of rhizobia to the host root is quite rapid, occurring within 2 hours of inoculation in field pea (Broughton et al., 1980). Evidence with other legumes also indicates that rhizobial attachment to root hairs (e.g., common bean, Vargas and Graham, 1988) as well as nod gene induction (e.g., subterranean clover, Richardson et al., 1988) are inhibited by acidity. The most adverse acidity factors inhibit-

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ing these processes are excess H+ and Al"+ and deficiency of Ca and P (Coventry and Evens, 1989). Howieson (1995) suggested that symbiotic tolerance achieved through the host plant in some species (e.g., Medicugo spp.) is largely due to the plant's ability to produce rhizobial nod gene inducers and stable exudates required for rhizobial attachment under acid soil stress. The development of nodules that have already been initiated appear to be little affected by soil acidity, and their specific nitrogenase activity may also not be significantly reduced (Lie, 1969). Nitrogen fixation per plant, however, may be significantly reduced in line with decreased nodule weight per plant (due to fewer nodule numbers). In field pea grown in nutrient solutions, for example, decreasing pH from 7.0 to 5 . 2 resulted in more than 60% reduction in total nitrogenase activity per plant (Paulino et af., 1987). Adding 3 p,M A1 (as Al,(SO,),) to the nutrient solution at pH 5.2 reduced nitrogenase activity by a further 20%, whereas number of nodules per plant and plant dry matter were not affected, suggesting a possible direct effect of Al"+ on nitrogenase activity (Paulino et al., 1987). Both nodule development and N, fixation may be restricted by Mo deficiency in acidic soils (Coventry and Evans, 1989). Molybdenum is a component of several enzymes, including nitrogenase, which is essential for N, fixation (Marschner, 1995). The requirement for Mo is several times higher in nodules than in any other plant part (Brodrick and Giller, 1991), and thus its deficiency can considerably reduce N, fixation. In groundnut growing in Mo-deficient acid soils, addition of Mo and P increased nodule dry weight (125%), specific nitrogenase activity (20%), and N uptake (55%)compared to P application alone (Hafner et al., 1992). Application of Mo to soybean grown in a Mo-deficient soil increased both N yield (33%) and seed yield (22%) in plants dependent on N, fixation but not in plants dependent on mineral N, indicating the greater importance of Mo for N, fixation compared to host plant growth (Parker and Harris, 1977).

D. GENETICVARIATION INRESPONSETO Son. ACIDITY The use of acid-tolerant species is an important agronomic practice complementary to liming. It is perhaps more important in situations where subsoil acidity inhibits root growth. Since soil acidity is a complex stress factor, plant adaptation to acidic soils often involves a combination of adaptive mechanisms, such as the link between Al-tolerance and efficient uptake and translocation of P (e.g., field pea cv. Uspekh, Klimashevskii etal., 1970; pigeon pea, Fujita et al., 1995) and the link between Al-tolerance and low internal requirements of Ca (e.g., cowpea, Horst, 1987). Similarly, Mn tolerance may be linked with efficient uptake and translocation of Ca (Horst, 1988). Since Al toxicity and Mn toxicity are the most

90

H. P. S. JAYASUNDARA ETAL.

dominant constraints in many acidic soils, tolerance to these two stresses has been used as a criteria for acid soil tolerance. These two characters, however, are not interconnected (Marschner, 1995). Although interspecific variation in tolerance to soil acidity has been demonstrated in cool season grain legumes (Horst and Goppel, 1986a,b; Grauer and Horst, 1990; Carr and Sweetingham, 1994; Tang and Thomson, 1996), the extent of intraspecific variation is almost unknown. In two separate studies where few genotypes from field pea and chickpea have been tested for Al-tolerance, results indicate that a considerable intraspecific variation is present. Klimanshevskii et al. (1970), for example, found that in two field pea cultivars grown in nutrient solutions containing aluminium (supplied as Al2(SO&), a relatively Al-tolerant cultivar showed only 32% reduction in growth (total dry matter) at 11 mg A13+ I - ' , whereas this level of A13' was completely detrimental to an Al-sensitive cultivar. Similarly, Rai (1991) found that at a solution concentration of 5 ppmA13+, shoot dry weight of a sensitive chickpea cultivar reduced by 70%, whereas that of a relatively tolerant cultivar reduced only by 27%. A wide intraspecific variation has been found in tropical grain legumes for both A1 tolerance (cowpea, Horst et al., 1983; Horst, 1987; common bean, Vargas and Graham, 1988; soybean, Campbell and Carter, 1990; Foy et al., 1993) and Mn tolerance (cowpea, Horst, 1982; soybean, Mascarenhas et al., 1995). Results from these studies indicate that, in general, intraspecific variation for Al-tolerance is more prominent in root growth than in shoot growth. Thus, the rate of root elongation in the presence of A1 appeared to be a useful selection criteria for the identification of intraspecific variation for A1 tolerance (Campbell and Carter, 1990; Foy et al., 1993). In 12 diverse soybean genotypes, the relative rate of root elongation in solutions containing A1 was well correlated with the relative rate of shoot growth in acidic soils (Campbell and Carter, 1990). In contrast to A1 tolerance, Mn tolerance is primarily related to the plants' ability to tolerate high concentrations of Mn in leaves (soybean, Heenan and Carter, 1977; Horst, 1983). Cultivars susceptible to Mn toxicity often develop distinct toxicity symptoms, making it relatively easy to recognize. Application of Mn to petiole and rating the induced Mn toxicity symptoms, for example, appeared to be a suitable screening technique for selection of tolerant cowpea genotypes at the vegetative stage (Horst, 1982). In cowpea, however, Mn tolerance at the vegetative stage is not necessarily correlated with Mn tolerance at the reproductive stage (Kang and Fox, 1980; Horst, 1982) because grain yield can be reduced severely by high internal concentrations of Mn without a significant decrease in vegetative growth (Kang and Fox, 1980). A separate screening is therefore suggested for identifying Mn tolerance at the reproductive stage (Horst, 1982). The reduction in grain formation following application of Mn to the peduncle was found to be a promising method for identifying genotypes tolerant to excess Mn at the reproductive stage (Horst, 1982).

GRAIN LEGUME RESPONSES TO SOIL ABIOTIC STRESSES

91

111. SOIL SALJNTY AND SODICITY Salt-affected soils are abundant in arid and semiarid regions of the world. Common ions contributing to this problem are Ca2+, Mg2+, Nat, CI-, SO:-, HCO;, and in some instances K C and No; (Bernstein, 1975). In a saline soil, electrical conductivity of the saturated extract (EC,) is > 4 dS m- (equivalent to 40 mM NaCl) and exchangeable sodium percentage (ESP) is < 15 (Gupta and Abrol, 1990). In these soils chlorides and sulphate salts of Ca and Mg are predominant, and soil pH is usually < 8.2. In some saline soils, however, ESPexceeds 15 and these are defined as saline-sodic soils (Gupta and Abrol, 1990). The effects of salinity and sodicity on plant growth in saline-sodic soils are nonadditive and noninteractive, with growth being primarily limited by salinity (Bemstein, 1975; Gupta and Abrol, 1990). In nonsaline sodic soils (ESP > 15, ECe < 4 dS m- I ) the total salt concentration is low with decreases in exchangeable Ca2+ and Mg'+ being balanced by increases in exchangeable Naf (Bemstein, 1975). Bicarbonate and carbonates are prevalent anions in these soils, and pH is often greater than 8.2 (Gupta and Abrol, 1990). The physical conditions of sodic soils are poor (Naidu and Rengasamy, 1993),and in addition to Na toxicity, conditions such as hard setting, surface crusting, compaction, and transient waterlogging may limit plant growth in these soils (discussed in detail in Sec. V and VI).

'

-

A. RESPONSESOF COOLSEASONGRAINLEGUMES TO SOILS A L ~ N I - ~ Y The majority of published reports on the responses of cool season grain legumes to salinity are based on experiments conducted under greenhouse conditions and to a limited extent experiments using confined field microplots with artificially created saline soils. Moreover, these experiments are highly variable both in the duration of the treatments and the stage of growth at which treatments were imposed. Notwithstanding these problems, the results from these experiments demonstrate that all aspects of growth are severely inhibited by soil salinity. The experimental results also show that the sensitivity to salinity can vary between stages of crop growth.

1. Germination and Seedling Growth Germination and seedling emergence are two indispensable parameters for the establishment of a better crop because failure at this phase will reflect badly in the final yield. Therefore, a substantial amount of research has been conducted to document the effect of soil salinity on germination and seedling growth. In most cool season grain legumes, seed germination is progressively delayed by salinity, but final germination percentage is not reduced until salinity is increased to relatively

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H. P. S. JAYASUNDARA ETAL.

high levels, i.e., 6.2-9.0 dS m-' (e.g., faba bean, Hamid and Thalibudeen, 1976; lentil, Ayoub 1977; faba bean and field pea, Dua er al., 1989; chickpea, Yadav et al., 1989; faba bean and L. albus, Shaddad et al., 1990). The results from these experiments also show that most species are more tolerant to salinity at germination than at subsequent growth. There are considerable differences between species in terms of the level of salinity when germination and seedling emergence are significantly reduced. Germination and seedling emergence of faba bean, for example, were not reduced even at 9 dS m-' EC,, whereas both parameters of field pea were significantly reduced at salinity levels greater than 6 dS m-I (Dua et al., 1989). Faba bean also appears to be more tolerant to NaCl salinity than does L. albus at germination (Shaddad et al., 1990). In lentil, germination and seedling emergence (up 7 days after the radicle emergence) were not reduced by NaCl up to 7.9 dS m- (Ayoub, 1977), whereas those of chickpea were reduced by 4.2 dS m-' (Yadav et al., 1989). It is difficult to make generalizations about the response to salinity at germination and seedling emergence of different cool season grain legumes because comparisons have not been made under uniform conditions. The delay in germination under saline conditions may be mainly attributed to reduced rate of water uptake, particularly at initial stages of the germination process. In common bean, for example, initial stages of germination (up to radicle emergence) were more affected by osmotic stress created by polyethylene glycol (carbowax 1540)than by iso-osmotic concentrations of NaCl (Prisco and O'Leary, 1970). In contrast, seedling growth was inhibited more by NaCl stress than by polyethylene glycol. After radicle emergence, early seedling growth is largely dependent on the mobilization of reserves from the cotyledons to embryonic axis. Inhibition of seedling growth by external NaCl may largely be due to restricted translocation of reserves from the cotyledons and various assimilatory processes resulting from specific ion effects (Corchete and Guerra, 1986).

'

2. Plant Growth and Seed Yield Salinity reduces vegetative growth depending on the sensitivity of the species and the intensity of salinity. Generally, root growth is less affected than shoot growth (e.g., common bean, Wignarajah, 1990; field pea, soybean and common bean, Cordovilla etal., 1995a; faba bean, Cordovilla er al., 1996), thus the shoot-root ratio is decreased. Lupins (L. albus and L. luteus), however, are exceptions, root growth being more reduced by salinity than shoot growth (van Stevenink et d., 1982; Jeschke et al., 1986). Although root growth is less affected than shoot growth, some morphological and structural changes may occur in roots under salinity stress. In field pea such changes include thickening and curving of the roots and a reduction in the diameter of the roots and vascular cylinder because of the suppression of meristematic activity (Setia and Narang, 1985; Soloman et al., 1986).

93

GRAIN LEGUME RESPONSES TO SOIL AEUOTIC STRESSES

The sensitivity or tolerance of different crop species to salinity is commonly expressed as relative reduction in dry matter or seed yield as a function of increasing salinity (Mass and Hoffman, 1977). After a threshold salinity level the relative growth or yield is reduced linearly with increasing salinity (EC,). This is expressed as Y, = 100 - b (EC, - U ) where Y, = relative growth or yield; n = threshold salinity level in EC, units (dS m- '), which is maximum allowable salinity without significant reduction in yield; b = slope or the percentage yield reduction per unit of EC, after the threshold level. Different species can be classified into four groups: ( 1 ) sensitive, (2) moderately sensitive, ( 3 )moderately tolerant, and (4) tolerant, using the threshold salinity level and slope of the response curve (Mass and Hoffman, 1977). According to this classification, vegetative growth of the majority of cool season

3

~~~

80-

m

U

c

U

8

b

8

70

--

0 Faba bean (1)

rn Faba bean (2) A Faba bean (3)

60--

x Pea (4)

50-~

0 Chickpea(6)

4i--

0 Lentil (5)

0 Chickpea (7) ~

Figure 3 Effects of salinity on relative dry matter yield of' different cool season grain legumes compared to nonsalinized control plants; data are from iI ) Hamid and Talibudeen, 1976; (2)Abd-Alla, 1992; (3)Ayers and Eberhard, 1950; ( 4 )Cerda ei a/..1982; ( 5 )Ayoub, 1977;(6) Manchanda and Sharma, 1989; (7) Johansen et d.,(1990).Planrs in all experiments have been grown in artificially salinized (mainly with NaCl and Na,SO,) soil or sand in the greenhouse for 2-3 months. Classification of salinity tolerance (groups separated by solid lines) is baaed on Maas and Hoffman, 1977.

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H. P. S. JAYASUNDAEU ETAL.

Often the response of seed yield to salinity is not similar to the response of vegetative growth to salinity. In field micro-plots containing artificially salinized soils (with NaCl), for example, increasing salinity from 1.3 to 5.3 dS m- almost completely inhibited the seed yield of lentil (by 92%), whereas total plant dry matter was reduced only by 48% (a decrease in the harvest index from 0.3 to 0.03) (Ayoub, 1977). Similar decreases in harvest index have been observed for field pea growing in soil with mixed salinity (Cl- and SO:) (Lal, 1985). For chickpea, increasing salinity (Cl- dominate) from 1.9 to 5.1 dS m- completely inhibited pod formation, whereas plant dry matter was reduced only by 50% under greenhouse conditions (Manchanda and Sharma, 1989). Thus species comparisons based only on vegetative growth may not be adequate for selection of crops to saline soils. Some examples for threshold and critical salinity levels and slope of salinity response curve based on seed yield of commonly cultivated cool season grain legumes (except lupins for which published data are not available) are summarized in Table I. From these data as well as those in Fig. 3, it is apparent that faba bean

'

'

Table I Threshold Salinity Level (CJ, Critical Salinity Level (C5& and Slope of the Response Curve (Percentage Decline in Yield per Unit Increase in Salinity) for Seed Yield of Some Widely Cultivated Cool Season Grain Legumes" ~~~

Species Chickpea (C. urietinum)

CI dominant (C I-SO, ratio SO, dominant (CI-SO, ratio NaCI-CaS0,MgSO, ratio

Lentil (L. culirzaris) Faba bean (V faho)

Pea ( P . sativum)

c,

Type of salinity

=

7:3)

=

3:7)

=

(dSm-')

(dSm-')

Slope (9)

2.1

4

55

Manchanda and Sharma, 1989

5.1

8

46

Manchanda and Sharma, 1989

1.7

4

24

Dua. 1992

1.8

5

26

Ayoub, 1917

ND" 5.5

9 8.5

ND

El Karouri, 1979

12

1986 Rabie er d..

2.6

9

9

2.8

8

11.5

Cerda ei a/., 1982 Lal, 1985

C.4,)

Reference

7:2:1

NaCl CI dominant SO, dominant

NaCI-CaCI, ratio

=

I :1

NaCl and CaClz NaCI-CaCI, ratio

=

I :I

"Values were recalculated from the references indicated. "C,,, salinity at 50% yield reduction. 'ND = no data.

GRAIN LEGUME RESPONSES TO SOIL ABIOTIC STRESSES

95

is relatively more tolerant to salinity than other grain legumes, whereas chickpea and lentil are highly sensitive. These observations need to be confirmed in experiments, both in the greenhouse and in the field, that compare the response of a range of grain legumes to salinity under uniform conditions.

B. RESPONSES OF COOLSEASON GRAINLEGUMES TO SODICITY Compared with the substantial amount of research on the response of cool season grain legumes to soil salinity, only few research publications have considered their response to soil sodicity. As with salinity, soil sodicity adversely affects cool season grain legumes from the beginning of crop establishment. In the few experiments where effects of increasing ESP (at EC, < 4 dS m-I) on growth of cool season grain legumes have been studied, results indicate that both germination and seedling emergence are significantly reduced with increasing ESP. For example, in nine chickpea cultivars tested in isolated field plots with ESP from 15 to 28 at EC, < 2.4 dS m- I, seedling emergence was markedly reduced at ESP > 20 (Kumar, 1985).For lentil, although germination was not reduced by sodicity up to ESP 30, seedlings survived only when ESP was less than 25 (Tewari and Singh, I99 I). The adverse effects of sodicity on chickpea progressively increased through the establishment phase, and seedling mortality increased from 10% in the control (15 ESP) to 83% at 28 ESP (Kumar, 1985). Toxicity due to excess Na+ was concluded to be the main reason for the seedling mortality in chickpea. Vegetative and reproductive growth of cool season grain legumes is also reduced by soil sodicity (Abrol and Bhumbla, 1979; Kumar, 1985; Singh and Abrol, 1987; Singh et al., 1993). In chickpea grown on field microplots, an increase of sodicity from 15 to 20 ESP reduced leaf area by 50% and leaf dry weight by 48% (Kumar, 1985). Similarly, in lentil an increase of sodicity from 10 to 15 ESP reduced total plant biomass by 60% (Singh et al., 1993). As with salinity, seed yield appears more sensitive to sodicity than does vegetative growth; for example, the level at which a 50% reduction of seed yield occur was around 10 ESP for chickpea (Abrol and Bhumbla, 1979) and less than 15 ESP for lentil (Abrol and Bhumbla, 1979; Singh et al., 1993). In both species, number of pods per plant and 1000 seed weight were severely decreased, whereas number of seeds per pod was little affected. In contrast, both vegetative and reproductive growth of pea appear relatively less affected by sodicity, with 50% reduction in seed yield occurring at 35 ESP(Dua and Sharma, 1993). We are not aware of any studies related to yield response of faba bean and lupins to sodicity. In some common tropical grain legumes, however, a 50% reduction of seed yield occurred at ESPof around 15-20 (groundnut, Singh and Abrol, 1985; soybean, Singh and Abrol, 1986). In comparison, rapeseed (Brassicu napus), a moderately sodicity-tolerant species, can withstand 35 ESP without significant reduction of growth or yield (Porcelli e f al., 1995).

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H. P. S. JAYASUNDARA ETAL.

C. FACTORSRELATINGTO POORGROWTHIN SALINE A N D SODK SOILS

Salt stress has three major components: ( 1 ) water stress caused by salt acting as an osmoticum, ( 2 ) ion toxicity, and ( 3 ) nutrient imbalances. In saline soils and saline-sodic soils, all three factors may contribute to reduced growth, whereas in sodic soils ion toxicity (particularly Na+) and nutrient imbalances may contribute to reduced growth. In addition, other soil physical problems in sodic soils, i.e., surface crusting, hard setting (compaction), and transient waterlogging, may also contribute to reduced growth (Naidu and Rengasamy, 1993). In sodic soils it is difficult to isolate any single growth-limiting factor as the most important one, but intolerant crops may be affected by Na toxicity at relatively low levels of ESP when physical effects of sodicity are absent (Bernstein, 1975). The effects of sodic soils on cool season grain legume growth resulting from Na toxicity are considered in this section. The problems associated with structural degradation are discussed under topics on effects of poor structural conditions and waterlogging on cool season grain legumes (Sec. V and VI, respectively), and the constraints associated with high pH are considered under effects of soil alkalinity (Sec. IV).

1. Water Stress Leaf expansion is the earliest affected visible plant parameter by salinity (Munns and Termaat, 1986). The rate of transpiration is also reduced (Abbas et al., 1991). These rapid responses to root-zone salinity are largely related to changes in leafwater status in response to low external water potential (Munns andTermaat, 1986). In L. albus the hydraulic resistance of the plant is increased by approximately four times soon after exposure to 100 mM NaCl (Munns and Passiora, 1984), and this may greatly exacerbate the effect of low external water potential in decreasing the leaf-water potential. The reduced leaf-water potential is not directly responsible for the retardation of growth, as indicated by results that if the leaf-water potential is artificially increased (applying an external pressure similar to osmotic potential), leaf expansion rate remains reduced (e.g., L. albus, Munns and Termaat, 1986). Plant hormone-mediated signals originating from roots in response to low external water potential have been implicated in immediate inhibition of shoot growth in salt stressed plants (Munns and Termaat, 1986). It is believed that, in most plants, stress induces an accumulation of abscisic acid. Abscisic acid has been found to be involved in the regulation of growth and development of plants and in transmitting signals from roots to shoots (e.g., L. albus, Wolf et al., 1990).

2. Ion Toxicity In plants exposed to salt stress for a long duration, growth inhibition may be largely related to a gradual buildup of toxic Na+ and C1- ions in the plant (Munns

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97

and Termaat, 1986). For a plant to grow well under saline conditions the supply of ions to the leaves must be regulated. Ideally, most of the salts should be excluded from the roots, and the small fraction arriving in the shoot should be partitioned so that it does not accumulate to toxic concentrations. Most grain legume species, however, are generally poor salt regulators and poor in cornpartmentalising Na+ and CI- in the leaves (Lauchli, 1984). In L. albus exposed to NaCl ranging from 0 to 100 mM, the concentrations of Na+ and C1- in the xylem sap increased linearly with increasing salinity and averaged 10% of the external NaCl concentration. By contrast in barley, a moderately salt-tolerant species, Na' and C1- concentrations in the xylem reached only 4% of the external concentration in plants exposed to 100 mM NaCl (Munns, 1988). For some species, a minor buildup of Naf and C1V ions in the shoot may not be adverse, especially if the ion concentration does not increase with time due to an equivalent shoot growth (L. luteus, Van Stevenink eral., 1982; common bean, Wignarajah, 1990). Under these conditions growth may be maintained or even stimulated (e.g., L. luteus, Van Stevenink et al., 1982; faba bean and L. albus at < 80 mM NaC1, shaddad et a f . , 1990). An increase in the leaf fresh-weight-dry-weight ratio (succulence) has also been observed along with growth stimulation (van Steveninck et al., 1982; Wignarajah, 1990). These salinity responses are halophytic in nature and are considered mechanisms for tolerance (Greenway and Munns, 1980). These responses, however, are not common for most grain legumes and can only be seen under low levels of salinity. In most cool season grain legumes internal Na+ and CI- concentrations generally increase gradually with time and with increasing external salt concentration (Ayoub, 1977; Yousef and Sprent, 1983; Lauter and Munns, 1987). In chickpea exposed to combined NaCl and Na,SO, (30 mM Na+, 15 mM CI-, and 7.5 mM SO:-), Na+ and C1- concentrations increased rapidly during the first 4 days and then gradually to reach a steady state after 10 days. By this time relative growth rate was reduced, and stress symptoms had appeared (Lauter and Munns, 1987). The relative importance of Na+ and C1- as the major ion causing toxicity may vary among species. In field pea, for example, internal Na concentration remained unchanged, whereas C1 concentration increased significantly with increasing NaCl salinity from 1.8 to 10 dS/m EC,. Within this range plant dry matter decreased by more than 60% (Cerda et al., 1982). In contrast, dry matter yield reduction in chickpea was more strongly correlated with shoot Na concentration than with shoot CI concentration (Lauter and Munns, 1987). The rate of photosynthesis is also reduced by high leaf Na+ and C1- concentrations, especially when ionic relations in the chloroplast are affected (Seeman and Critchley, 1985). In common bean, photosynthetic rate per unit leaf area declined by 75% over a range of 0-300 mM CI- in leaves (Seeman and Critchley, 1985). This decrease may result either from a feedback inhibition, as carbohydrates often accumulate in leaves after exposure to salinity due to reduced sink activity (Munns and Termaat, 1986), or from reduced chlorophyll concentration

98

H. P. S. JAYASUNDARA ETAL.

(Seeman and Critchley, 1985). In plants subjected to prolonged salt stress, reduced growth is more associated with a reduction in photosynthetic leaf area than a reduction in photosynthetic rate per unit leaf area (Munns and Termaat, 1986). Accumulated Naf and C1- in a salt-stressed plant are not uniformly distributed in different plant parts (Greenway and Munns, 1980). Generally, ion concentrations are higher in mature leaves than in younger leaves, and this corresponds with earlier death in older leaves (lupin, Munns, 1988; chickpea, Dua, 1992). In L. albus Nat concentration in the leaflet midrib sap of the oldest leaves increased to about 40 mM 7 days after exposure to 160 mM external NaCl, and the salt injury was first developed in these leaves (Munns, 1988). The concentration at which toxic symptoms appear in old leaves depends on the ability of the plant to compartmentalize salt in the vacuole (Munns and Termaat, 1986). An accumulation of salt in the cytoplasm interferes with metabolism and membrane permeability, and excessive concentrations in the cell wall cause a loss of turgor and loss of water (Munns and Termaat, 1986).

3. Nutrient Imbalances The uptake of excessive amounts of Na+ and C1- by salt-affected plants generally interferes with the uptake of essential macronutrients, and this may also disturb normal growth. There is a general trend for decreased uptake of K', Ca2+, Mg2+, and NO-; with increasing internal Na+ and C1- in grain legumes (Munns, 1988; Jeschke et af.,1992; Cachorro et al., 1994; Gouia et al., 1994). The presence of 50 mM NaCl in the culture solution decreased K + uptake by 41% in common bean, compared to only 12% in cotton, a salt-tolerant plant (Gouia et al., 1994). The uptake and xylem transport of Ca2+ and Mg2+ were also decreased (Gouia et al., 1994). A significant negative correlation between the uptake of Na+ and the uptake of K + is generally found in many cool season grain legume species (e.g., field pea, Cerda et al., 1982; faba beans, Yousef and Sprent, 1983; lentils, Ashraf and Waheed, 1993a). Thus internal K-Na ratio is decreased under saline conditions. When the K-Na ratio is decreased below a critical level, normal functioning of metabolic processes are disturbed in nonhalophytes (Wyn Jones et al., 1979). Under saline conditions high external Na+ greatly reduces the activity of Ca2+ in the solution (Grattan and Grieve, 1994) and may displace Ca2+ from the plasmalemma of the root cells, leading to disruption of ion uptake and transport regulation and membrane integrity (Cramer et al., 1985). Often the increasing external Ca2' concentration has been found to improve the relative salinity tolerance in many plants, including grain legumes (Guerrier and Pinel, 1989; Cachorro et al., 1994). This beneficial effect of Ca2+ appears to be associated with counteracting effects on toxic Na+ accumulation. In common bean grown in solutions containing 80 mM NaC1, for example, increasing external Ca2+ supply from 0.2 to 5 mM

G

W LEGUME RESPONSES T O SOIL ABIOTIC STRESSES

99

reduced shoot Na concentration by about 40% with a concurrent increase in shoot growth by about 64% (Cachorro et al., 1994). High phosphorus supply under saline conditions may increase P uptake considerably, leading to growth depressions resulting from P toxicity (Grattan and Grieve, 1994). L. luteus, for example, a species tolerant to 50 mM external NaCl (van Steveninck etal., 1982). is highly sensitive to salinity (50 d e x t e r n a l NaCl) in the presence of 2 mM inorganic P (Treeby and van Steveninck, 1988). Similarly, several soybean cultivars were severely injured when solution P concentration exceeds 0.12 mM (Gratton and Mass, 1988). These cultivars accumulated large quantities of P in the leaf when they were grown above this critical P concentration (0.12 mM) in the solution regardless of the Ca*+-Na+ ratio or type of salt used. In soybean salinity injury was related both to high P and to CI- concentrations in the leaf (Gratton and Mass, 1988).

D. FACTORS INFLUENCINGSALINITYRESPONSE Salinity response of plants is dependent on several other factors, including stage of growth, type of anions (C1- or SO:-), nutritional factors, and environment. Generally, most cool season grain legumes can withstand a comparatively higher level of salinity at germination than at later growth (compare the values given in Sec. 1II.A.I with threshold salinity levels for growth and yield in Fig. 3 and Table I). This may be beneficial for establishment in the field where salt concentration is relatively high at the soil surface compared to the sub soil. Sensitivity to salinity, however, may increase over time as growth progresses (Ayoub, 1977; El Karouri, 1979; Siddiqui and Kumar, 1985; Mor and Manchanda, 1992), mainly due to salt accumulation over a longer period. In some species late vegetative growth and reproductive growth appears relatively more tolerant to moderate salinity compared with earlier growth (e.g., faba bean, Hamid and Thalibudeen, 1976; Abd-Alla, 1992). In general, CI- appears more harmful than SO:- for many cool season grain legumes (Manchanda and Sharma, 1989; Dua, 1992). Leopold and Willing ( 1 984) suggested that CI- may be more deleterious to membrane functions than SO:-. When 133 m M Na,SO, was replaced by iso-osmotic 200 mM NaCI, membrane leakage increased by about 28% in soybean leaf tissues (teopold and Willing, 1984). Lauter and Munns (1986) reported that harmful effects of salinity on chickpea at low levels of salinity are related to the accumulation of Na in shoots regardless of the dominant anion, whether it is CI- or SO:-. Application of fertilizer, i.e., NO,, may sometimes modify the severity of salinity damage (Lauter et al., 1981; Rabie et al., 1986; Cordovilla et al., 1996). The nature of the response to applied nutrients, however, may depend on the intensity of salinity (Rabie et al., 1986; Grattan and Grieve, 1994). Under mild salinity, nu-

100

H. P. S. JAYASUNDARA E T A .

trient deficiency may limit growth more than salinity; thus, a positive interaction or an “improved salt tolerance” can occur in response to nutrients supply. At moderate to high salinity, addition of nutrients may either have no interaction or a negative interaction on plant growth (Grattan and Grieve, 1994). Comparisons of salinity response of different cool season grain legumes can be misleading because of the influence of environmental factors. Any climatic factor that reduces the amount of transpiration per unit of carbon fixed will also reduce the rate of accumulation of salt in leaves and therefore prolong their effective life (Munns and Termaat, 1986). This would occur if the plant had an inherently high water-use efficiency (Munns and Termaat, 1986) or was grown under conditions that increase the ratio of photosynthesis to transpiration, such as high humidity (e.g., chickpea; faba bean, El Karouri, 1979; Lauter and Munns, 1987), high CO, (e.g., common bean; Schwarz and Gale, 1984), and low light intensity (e.g., faba bean; Helal and Mengel, 1981). High air temperature, on the other hand, increases rate of transpiration and thus the flow of ion to the shoot and the severity of salinity injury (e.g., lentil, Ayoub, 1977).

E. EFFECTSOF SALNTY AND SODICI-I-Y ON NODULATION AND N, FIXATION Results from a few experiments have shown that plants relying on biological N, fixation are more sensitive to salinity than plants relying on fertilizer N (Lauter et al., 1981; Yousef and Sprent, 1983), suggesting relatively higher sensitivity of the symbiosis to salinity than host plant growth. The adverse effects of salinity on the legume-rhizobium symbiosis include decreased nodulation, nodule dry weight, and decreased N, fixation (Lauter et al., 1981; Yousef and Sprent, 1983; Sigleton and Bohlool, 1983; Subbarao ef al., 1990; Abd-Alla, 1992; Delgado et al., 1993). Rhizobia nodulating most cool season grain legumes appear to be relatively tolerant of soil salinity (Graham and Parker, 1964). The growth of 14 strains of chickpea rhizobia for example, was not affected in yeast extract mannitol medium salinized with 340 mM NaC1, a level at which most grain legumes could not survive (Elsheikh and Wood, 1990). Thus, the survival and growth of rhizobia in the rhizosphere may not be a major limiting factor for poor nodulation in cool season grain legumes under saline conditions. The early steps of nodulation appear to be the most sensitive to salinity. An external NaCl of 80 mM, for example, inhibited the nodule formation in soybean without reducing the number of rhizobia in the medium and root colonization (Singleton and Bohlool, 1984). Moreover, delaying the application of salt stress by 96 hours increased nodule number, nodule dry weight, and shoot N concentration (Singleton and Bohlool, 1984). The impairment of nodulation by salinity has been suggested to be due to a reduction in number of root hairs and the formation of in-

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101

fection threads in lucerne (Lakshmi-Kumari et al., 1974) and in lateral expansion of root hairs, reduced root curling, and a reduction in both the number of root hairs that contained the infection threads and the proportion of these that led to nodule initiation in faba bean (Zahran and Sprent, 1986). It appears that once the symbiosis is well established the salinity response is similar in both N,-fixing and N-fed plants. In pigeonpea, for example, when salt stress was applied to well-nodulated plants, shoot dry matter was not significantly different from that of N-fed plants, but when the salt stress was imposed at seed sowing, shoot dry matter of symbiotically dependent plants was depressed more (70%) than that in N-fed plants (40%) (Subbarao et al., 1990). There was no difference in Na+ and C1- uptake behavior or distribution in pigeon pea as influenced by the type of N nutrition under salt stress (Subbarao et al., 1990). The nodules already formed are unaffected by salinity since average weight per nodule was either increased or remained unchanged (e.g., chickpea, Lauter et al., 1981; faba bean, Yousef and Sprent, 1983; soybean, Singleton and Bohlool, 1984; pigeon pea, Subbarao er al., 1990). This response may be a compensation for reduced specific nitrogenase activity in salt-affected plants (Sprent et al., 1988). Total nitrogenase activity, however, is decreased under salt stress in proportion to reduced nodulation and nodule dry weight (Singleton and Bohlool, 1984).Nitrogen fixation may also be affected either by direct inhibitory effects of salt on the nitrogenase enzyme (e.g., field pea, Delgado et al., 1993; Faba bean, Cordovilla er af.. 1996)and 0, diffusion (Serraj et al., 1994) or indirectly by restricted host plant growth (e.g., soybean, Singleton and Bohlool, 1983). Host plant appears to have a major role in the tolerance of the symbiosis under salt stress (Rai et at., 1985; Velagaleti et al., 1990; Cordovilla et al., 1995b). In 15 genotypes of faba bean inoculated with a salt-tolerant strain of R. leguminosarum biovar. viciae, three genotypes with relatively more tolerance to 75 mM NaCl (based on relative shoot and root growth) also had a greater number of nodules and nodule dry weight per plant (Cordovilla et al., 1995b). Similarly, in 16 soybean cultivars screened for salinity tolerance (80 mM NaCl), shoot and root growth, nodulation, nodule dry weight, and nitrogenase activity were severely depressed in 11 salt-sensitive cultivars, whereas 5 salt-tolerant cultivars continued to grow and fix N,, although their shoot growth, nodulation, and nodule dry weights were marginally reduced (Velagaleti et al., 1990). For soybean, the important features of successful symbiosis under salt stress were the resistance of roots to salt stress, only moderate reduction in nodulation and nitrogenase activity, and continued growth and nitrogenase activity (though slightly depressed) until seed setting (Velagaleti et al., 1990). Only a few studies have been conducted on the effect of sodicity on nodulation and N, fixation in cool season grain legumes. Available evidence suggests that sodicity affects the legume-rhizobium symbiosis in a similar manner to salinity. In lentil, for example, both nodule number and nodule dry weight decreased by

H. P. S. JAYASUNDARA ETAL.

102

67-76% at 20 ESP relative to those at 10 ESP (Singh et al., 1993). Nitrogenase activity was completely inhibited in lentil nodules at 20 ESP (Singh ef al., 1993). Impaired N, fixation was further evident by progressive decline in N concentration in different plant parts of lentil with increasing sodicity.

F. GENETIC VARIATION INRESPONSE TO SALINITY AND SODICITY For cool season grain legumes several studies have been conducted on intraspecific variation in salinity tolerance within a particular species (Table 11). Few

Table I1 Some Examples of Intraspecific Variation of Salinity Response in Four Widely Cultivated Cool Season Grain Legumes

Species Chickpea (C.arietinum)

Number of

Parameter

genotypes

evaluated

4 160 81

% germination

2.8

Survival C,,,for dry matter"

NA"

< 1.5

Reference Kheradnam and Ghorashy, 1973 Lauter and Munns, 1986 Johansen eta/.. 1990 Dua, 1992

C,, C,,, and the slope' % germination

2.6 13

C,, for dry matter

10.5 NA

Ashraf and Waheed, 1990

11

YOgermination and relative seedling dry matter Relative seed yield

NA

Ashraf and Waheed, 1993

15

Relative dry matter

NA

C,, pod yield and the slope Rate of root elongation

4

Cordovilla eta!., I995 Cerda et al., 1982

20 10 Lentil

d Cso(1

S

Saxena and Rewari, 1992 Rai, 1983

(L. culinaris) 133

Faba bean (V faba) Field pea ( P sativum)

2 3

8.3

Poljakoff-Mayber etal., 1981

"The difference in C,, for most-sensitive genotype and most-tolerance genotypes (dS m-I). "C,, salinity at SO% yield reduction (dS m- I). 'C, = threshold salinity level (dS m-'). %A = not available.

GRAIN LEGUME RESPONSES TO SOIL ABIOTIC STRESSES

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studies have been conducted on intraspecific variation in response to sodicity. In most instances where intraspecific variation in salinity tolerance has been studied only a few genotypes or cultivars have been included; thus potential intraspecific variation has not been thoroughly investigated. Of most widely cultivated cool season grain legumes, chickpea has received the greatest evaluation. Lauter and Munns (1986), for example, tested 160 genotypes of chickpea for their tolerance to salinity (imposed at I week after emergence) in terms of survival after 9 weeks in solution cultures salinized with 50 mM NaCl or 25 mM Na,SO,. There was some variation in the development of salinity damage and survival of different genotypes, but this variation was very narrow. Quantifying salinity tolerance accurately by observations based only on survival is difficult however. In another series of experiments, 81 genotypes of chickpea were screened under glasshouse conditions in sand culture salinized with a mixture of NaCI, Na,SO,, and CaCl, in the ratio 7: 1:2 (Johansen et al., 1990). Plants were grown in sand with different salinity levels (1, 2, 3, and 5 dS m-I) for 3 months. Results from these experiments indicated that the extent of variation based on the critical salinity level was also very narrow (e.g., < 1.5 dS/m between most-tolerant genotype and most-sensitive genotype) and thus unlikely to be of any practical importance. Under field conditions in microplots filled with artificially salinized soils (C1- dominant, ECe 2 - 8 dS m-'), Dua (1992) tested 20 genotypes of chickpea for their threshold and critical salinity levels and slope of the response curve in terms of seed yield. The threshold salinity level varied from 4.0 dS m- in the most-tolerant genotype to 1.O dS m-I in the most-intolerant genotype. Values for the slope of the response curve (the percentage decrease in relative yield per unit increase in salinity beyond the threshold level) were higher for genotypes with high threshold values than those with low threshold values. Since a combination of a high threshold salinity value and a low slope value is considered for optimum salt tolerance (Mass and Hoffman, 1977), these genotypes were considered undesirable (Dua, 1992). Therefore, it appears that a substantial improvement of salinity tolerance in chickpea would be difficult by conventional breeding methods. The variation in the response of the chickpea-rhizobia symbiosis to salinity has not yet been explored. For lentil, a considerable genotypic variation in response to salinity has been observed at germination and early seedling growth (Ashraf and Waheed, 1990). Of 133 genotypes (from Pakistan) evaluated, 7 genotypes produced relative dry matter (relative to dry matter of plant grown without NaCl) greater than 120% in sand cultures salinized with SO mM NaC1, whereas another set of 20 genotypes produced relative dry matter in the range of 80- 120%. In all other genotypes relative dry matter yield was less than 65%. In a followup genotypic evaluation in lentil, the three most tolerant and two moderately tolerant genotypes showed a positive correlation between the degrees of salt tolerance at different growth stages up to physiological maturity, indicating that for these genotypes salinity tolerance exhibited at early growth stage was conferred at the adult stage (Ashraf and Waheed,

'

104

H. P. S. JAYASUNDARA ETAL.

1993a).Rai (1983) has also demonstrated a broad variation in salinity response for lentil with only five genotypes. The critical salinity level ranged from 0.5% NaCl (-7 dS m- EC,) for most sensitive genotype to 1.1% NaCl (- 15 dS m-' EC,) for most tolerant genotype for plants grown in sand culture salinized with NaCl. These results suggest that there may be a greater possibility for genetic improvement of salinity tolerance for lentil than for chickpea. Two additional studies also indicate a large intraspecific variation in response to salinity in field pea (Cerda et al., 1982) and faba bean (Cordovilla et al., 1995a). A substantial genetic variation in these two legumes may be found if a large number of genotypes were evaluated. Wild relatives of cultivated grain legumes may be a substantial source for genetic variation for salinity tolerance (e.g., pigeon pea, Johansen et al., 1990); however, only limited efforts have been made for evaluation of genetic variation in the wild types of cultivated cool season grain legumes. Where attempts have been made to evaluate wild relatives for salinity tolerance, the results so far have been discouraging; for example, the wild species of Cicer tested were more intolerant to salinity than were the cultivated species (Johansen etal., 1990). In contrast, two wild pea species (P elatius and P. falvum) had a greater salinity tolerance compared to three cultivated pea cultivars based on relative rates of root elongation under saline conditions (Poljakoff-Mayber efal., 1981). A more comprehensive evaluation of wild species related to cultivated cool season grain legumes may therefore be warranted if adequate genetic variation among existing genotypes cannot be found.

w.SOILALKALINITY Soil alkalinity (pH > 7 in H,O) is associated with carbonates in the soil. The most common carbonate present in soils is calcite or pure CaCO,. Soils with free CaCO, (defined as calcareous soils) may develop pH greater than 7 (usually 7-8.5) depending on the equilibria between CaCO,, H,O, and CO,. Calcerous subsoils may develop even higher alkalinity (pH > 8.5) due to poor aeration (Rowel, 1987). Some calcareous soils also have excess Na (exchangeable Nat > 15%), and these (sodic) soils may be extremely alkaline (pH > 8.5) due to the powerful alkaline hydrolysis of sodium carbonates and bicarbonate salts (Gupta and Abrol, 1990). Soil alkalinity adversely affects plant growth mainly by nutritional disorders, Fe deficiency in particular, and P, Zn, and Mn deficiencies (Naidu and Rengasamy, 1993). Growth of some species may also be affected directly by high pH, excessive concentrations of HCO;, and excessive Ca2+ in alkaline soils (Tang et al., 1992a; de Silva et al., 1994; Pissaloux et al., 1995).Apart from alkalinity, alkaline sodic soils may pose additional problems to plant growth, such as sodium toxicity and mechanical impedance (Sec. III.C.2 and V, respectively).

GFUIN LEGUME RESPONSES TO SOIL ABIOTIC STRESSES

105

A. RESPONSESOF COOLSEASON GRAINLEGUMES TO SOILALKALINITY The response of different cool season grain legumes to soil alkalinity varies depending on the species and growing conditions (Saxena and Sheldarke, 1980; Atwell, 1991; Tang et al., 1995a). A slight increase in soil alkalinity can result in a drastic reduction in growth of some species, whereas others are not affected; for example, a subsoil alkalinity of pH 7.2 with 2% CaCO, resulted in about 50% reduction in shoot dry matter of narrow-leafed lupin (L. angustifolius),whereas field pea was not affected (Tang et al., 1993a). The growth of other widely cultivated cool season grain legumes are generally less affected by alkalinity up to pH 8 but can be severely depressed at pH above 8 (Fig. 1). Stunted growth and the development of leaf chlorosis are common adverse effects induced by soil alkalinity in these species (Saxena and Sheldarke, 1980; Sakal et al., 1984; Singh et al., 1986; Hamze et a/., 1987; Chaney et al., 1992; Erskine et al., 1993). The components of growth most affected by soil alkalinity may vary among species. Generally, in lupins root growth is more affected than shoot growth (White and Robson, 1989a; Tang et al., 1993b). In contrast, in chickpea, lentil, field pea, and faba bean shoot growth was more affected than root growth in alkaline nutrient solutions (Tang and Thomson, 1996). These differences among species may reflect differences in the mode of action of soil alkalinity on plant growth. In narrow-leafed lupin, growth can be reduced by alkalinity without symptoms of iron deficiency (Tang et al., 1993a). It has been proposed that for this species poor root growth directly limits plant growth in alkaline soils (Tang et al., 1993b). For other cool season grain legumes iron deficiency is thought to be the important factor limiting growth and yield in alkaline soils (Saxena and Sheldrake, 1980; Kannan, 1983; Sakal et al., 1984; Erskine el al., 1993).

B. FACTORSRELATING TO POORGROWTHnv ALwm Sons 1. Iron Deficiency Iron deficiency is probably the predominant growth-limiting factor for many cool season grain legumes in alkaline soils (Saxena and Sheldarke, 1980; Sakal et al., 1984; 1984; Kaur et al., 1984; Singh et al., 1986; White, 1990; Erskine et al., 1993). In lentil, iron deficiency resulted in up to 47% reductions of seed yield, in sensitive genotypes (Erskine et a/., 1993). Similarly, iron deficiency depressed both vegetative growth (up to 52%) and seed yield (up to 77%) in chickpea growing in calcareous vertisols in India (Saxena and Sheldrake, 1980; Kaur et al., 1984). Narrow-leafed lupins growing in fine-textured alkaline soils in Western Australia often produce low dry matter and may sometimes display iron deficien-

106

H. P. S. JAYASUNDARA ET AL.

cy symptoms (White and Robson, 1989b). Incidence of iron deficiency appears relatively less in faba bean (Tang and Thomson, 1996) and pea (Atwell, 1991;Tang et al., 1992a) compared with other species. The symptoms of iron deficiency are usually manifested as interveinal chlorosis of the younger leaves (Korcak, 1987). This symptom, often termed “lime-induced chlorosis”, appears very early in susceptible cultivars (Saxena and Sheldrake, 1980; Plessner etal., 1992; Tang etal., 1995a).The expression of symptoms in young leaves is attributed to the inability to redistribute iron within the plant (Korcak, 1987). Under severe deficiency, leaflets may develop necrosis and die (e.g., chickpea, Saxena and Sheldrake, 1980; White and Robson, 1989; lupins, Plessner et al., 1992). In most instances the development and severity of the symptoms are exacerbated by environmental and soil conditions prevailing in the growing season (discussed later). Early symptoms of iron deficiency may disappear as plants mature, but adverse effects can persist even after the disappearance of symptoms and may be reflected in low seed yields (Saxena and Sheldrake, 1980). The causes of iron deficiency in plants growing in alkaline soils are complex. The deficiency may be due to the unavailability of iron to plants or failure in susceptible plants to translocate iron that is already absorbed (Korcak, 1987). Most plants are able to respond to “Fe-stress” in alkaline soils by modification of their rhizosphere in order to alter Fe solubility and thus avoid Fe deficiency (Romheld and Marschner, 1986). Rhizosphere acidification, release of Fe’+ reductants, release of Fe chelates, and reduction of Fe3+ to Fez+ at the plasma membrane of the root cells are some adaptive mechanisms by which plants increase Fe availability in the rhizosphere (Romheld and Marschner, 1986; Korcak, 1987). In addition, distinct root morphological and anatomical changes, i.e., thickening of the root apex, increased root hair formation, increased development of lateral roots, and formation of rhizodermal transfer cells, that may lead to greater localized changes in the rhizosphere may occur in response to Fe stress (Romheld and Marschner, 1986). These root responses are under genetic control of the plant, and species able to strongly acidify and reduce the rhizosphere grow better in calcareous soils than species poor in acidifying and reducing the rhizosphere (Romheld and Marschner, 1986). Chickpea cultivars resistant to Fe deficiency, for example, decreased the solution pH from 6.4 to 3.5 over a 17-day period, whereas susceptible cultivars did not cause significant changes to the solution pH (Kannan, 1981). Various soil chemical factors (CaCO,, Ca2+, HCO;, CO:-) have been implicated in the incidence and severity of iron deficiency. In most situations high concentration of HCO; in the soil soiution is the most important factor inducing iron deficiency (Fleming et al., 1984; Inskeep and Bloom, 1986; Loeppert et al., 1988). Increasing HCO, concentration is highly correlated with the development of iron chlorosis in sensitive plants in both solution culture (Hamze et al., 1987; Chaney er al., 1992) and in the field (Inskeep and Bloom, 1986). The mechanisms by which HCO; induces iron deficiency may be related to its buffering ability and

GRAIN LEGUME RESPONSES TO SOIL ABIOTIC STRESSES

107

resulting deleterious effects on the plant’s expression of Fe stress response and probably reduced translocation of iron from roots to shoots (Flemming et al., 1984). Often the visual symptoms of iron deficiency are not correlated with the total soil CaCO, content but are well correlated with active CaCO, (the fraction of CaCO, in clay and fine silt) in the soil (Inskeep and Bloom, 1986; Loeppert et al., 1988). Since the dissolution of CaCO, occurs as a surface reaction, the HCO; concentration in the soil solution is dependent on the reactive surface area of CaCO,. Environmental factors (particularly wet conditions and low temperatures) and soil physical properties that adversely affect soil water relations and soil aeration exacerbate iron chlorosis (White and Robson, 1989b; Hamze e? ul., 1987). Inskeep and Bloom (1986) found that iron chlorosis was often more severe in soybean in relatively wet areas in the field. Also, iron chlorosis is often severe in fine-textured soils in which aeration is slower compared to coarse-textured soils (White, 1990; Chaney et al., 1992). Furthermore, iron deficiency did not occur in narrow-leafed lupins grown in well-aerated soils with 2% CaCO, but occurred in the same soil when aeration was impaired (White and Robson, 1989b).The aeration effects in inducing iron deficiency symptoms are not due to an oxygen deficiency to the root system, because the changes in soil aeration required to induce iron deficiency are marginal (e.g., a decrease of air-filled porosity from 27 to 21% for lupin) and considerably higher than the critical soil aeration level (10% air-filled porosity) below which root functioning is impaired by oxygen deficiency (White and Robson, 1989b).The effects of high soil moisture and low aeration on exacerbating iron deficiency arise from increased soil HCO; concentrations resulting from a build-up of CO, in the soil environment (Inskeep and Bloom, 1986).Restricted aeration may be due either to soil compaction or poor water relations, which are common in calcareous and sodic soils (Gupta and Abrol, 1990, Naidu and Rengasamy, 1993). It is not clear whether HCO; has a direct physiological effect on plant growth. In most cool season grain legumes, shoot growth is severely depressed by HCO; without symptoms of iron deficiency or reduction in root growth (Tang and Thomson, 1996). High concentrations of HCO; is also associated with high pH. Thus, it is difficult to separate the effect of HCO, from that of high pH on plant growth. Millar and Thorn (1956) reported that the respiration of excised bean roots immersed in Hoagland’s solution was significantly inhibited by HCO,. The inhibitory effects increased with increasing HCO; concentration, independent of solution pH, and were more severe in chlorosis-susceptible plants, i.e., common bean, lupins and soybean, than in chlorosis resistant plants, i.e., wheat, barley and tomato (Millar and Thom, 1956). Soil Na+ concentration is positively correlated with the severity of iron chlorosis (Inskeep and Bloom, 1986; Loeppert et al., 1988). In alkaline sodic soils pH is dependent on the amount of NaHCO, in the soil solution (Rowel, 1987) and may generally be higher than that of a normal alkaline soil (Gupta and Abrol, 1990). Nutritional problems, as a consequence of higher pH and excess Na, intensify in

108

H. P. S. JAYASUNDARA ET AL.

these soils compared with those in calcareous soils (Rowel, 1987). Atwell (1991) found that growth of L. pilosus and field pea, two alkaline tolerant species, was severely depressed (by 42 and 55%, respectively) in a alkaline sodic soil (solonized brown soils with 83 mol m P 3 Na concentration and 8.13 pH). Growth reductions for these species were not due to iron deficiency, because no symptoms were apparent. In the same soil L. angustifolius developed severe chlorosis, and its growth was depressed by more than 70%. Thus, factors other than iron deficiency may be important in limiting the growth of L. pilosus and field pea under these conditions.

2. High pH The high pH in alkaline soils can directly inhibit root growth and thereby shoot growth (Atwell, 1991; Tang et ul., 1992a). In buffered nutrient solutions bubbled with C0,-free air to prevent the buildup of high concentrations of HCO;, root elongation in L. angustifolius was reduced by 40% when the pH increased from 5.5 to 6.0, whereas that of field pea was not affected (Fig. 4). The root elongation in other commonly cultivated cool season grain legumes (chickpea, lentil, faba

100

-

80 -

60

-

40 -

.

20

I

3

4

L. angustfoli.us L. albus P. sativum I

I

I

1

5

6

7

8

Solution pH

9

Figure 4 Relative root elongation rates of two lupin species and field pea grown in buffered nutrient solutions between pH 4 and 8 (redrawn from Tang et 01.. 1992a; and Tang and Thornson, 1996).

GRAIN LEGUME RESPONSES TO SOIL ABIOTIC STRESSES

109

bean) and in several potentially important species (i.e., Vicia satiua, V narbonensis, l? benghalensis, and Lathyrus sativus) appears less sensitive to alkalinity up to pH 8 (Tang and Thomson, 1996). The decreased root elongation in L. angustifofius above pH 6.0 is due to decreased cell elongation (50-65% lower cell length relative to that at pH 5.0),rather than to a reduced cell division (Tang et al., 1992a). The inhibition of cell elongation by high pH was rapid (occurring within 1 hour after the exposure of roots to high pH) and readily reversible, suggesting that high pH directly affects the cells in the elongating zone (Tang er al., 1992a). Furthermore, the roots exposed to pH 6 or above exhibited physical damage of the root surface and reduced root-hair formation (Tang et al., 1993~). The mechanisms by which the high pH impairs cell elongation in L. angustifolus is not properly understood but may be associated with the regulation of cellwall rheological properties (Tang et al., 1992a). It has been suggested that cell growth is dependent on cell-wall acidification and related cell-wall loosening characteristics (Taiz, 1984). Thus, pH above 6.0 possibly decreases the degree of cellwall acidification, thereby preventing the loosening of cellulose microfibrils in the wall. Alternatively, pH above 6.0 may impair plasma membrane integrity, leading to poor cell-wall formation (Tang et al., 1992a). Differences in root elongation between these species may be due to different efficiencies in proton efflux by their roots at pH above 6.0 or to different buffering capacity in their apoplast (Tang et al., 1992a). Roots grown at high pH may be thicker than roots grown at optimum pH; thus, root dry matter may not necessarily change under alkaline conditions (Tang and Thomson, 1996). Shoot growth, however, is inhibited by high pH (Tang and Thomson, 1996), possibly as a consequence of the impairment of uptake of water and nutrients resulting from reduced root length, physical damage to root surface, and reduced root-hair formation (Tang et al., I992a, 1 9 9 3 ~ Tang ) . and Thomson (1996) found that shoot fresh weights were well correlated with the total root length in a range of cool season grain legumes (chickpea, lentil, faba bean, pea, and lupins) growing in high pH nutrient solutions.

3. Excess Ca2+ High calcium concentration in the rhizosphere may have direct adverse effects on some species growing in alkaline soils (Jessop et al., 1990; de Silva et af., 1994; Pissaloux et al., 1995). In L. luteus, high concentrations of Ca2+ in the rhizosphere resulted in reduced leaf conductance (Ruiz et al., 1993). Moreover, de Silva et al. (1994) found considerable reductions in the rate of leaf expansion, rate of transpiration, and rate of net assimilation in L. luteus with increasing external Ca2+ concentration (supplied as Ca(NO,),) from 1 to 15 mol mP3 under glasshouse conditions. High rhizosphere Ca2+ also had direct effects on carbon assimilation of the plant, which was independent from the effects of reduced stomata1 conductance

110

H. P. S. JAYASUNDARA ETAL.

(De Silva e fal., 1994). Pissaloux et al. (1995) also found that increasing Ca2+ concentration in the nutrient solution (supplied as CaCl,) from 2.5 to 10 mol mP3 decreased growth of L. albus significantly. There was no visible sign of leaf chlorosis in either study (De Silva et al., 1994;Pissaloux etal., 1995).Tang e f al. (1995b), however, found that adding 0.33 g CaSO, per kg soil containing 0-10 g of CaCO, per kg soil (soil pH ranging from 4.8 to 7.3) increased Ca concentration in the soil solution by 1.7 to 6.6-fold and in leaves by 10-30% but did not depress shoot growth of L. angusfifolius. Reasons for these inconsistencies are not clear.

4. Other Nutritional Disorders Apart from iron, the availability of P, Zn, and Mn, and in some instances Cu and B, is low in alkaline soils. The availability of P decreases with increasing pH in the soil, particularly when the total P and soil organic matter levels are low (Marschner, 1995). Decreased availability coupled with restricted root growth often cause P deficiency in cool season grain legumes growing in alkaline soils (Mahler et al., 1988). The solubility of Zn decreases 30-45 times for each unit increase in soil pH in the range of pH 5.5-7.0 (Marschner, 1995). Zinc deficiency is a widespread problem in calcareous soils in India where chickpea and lentil are important components in the farming systems. (Takkar, 1993). Limitations to growth and yield due to Zn deficiency are demonstrated by considerable yield responses to Zn application for chickpea (Yadav and Shukla, 1983; Singh and Grupta, 1986; Ahlawat, 1990).The activity of Mn2+ decreases logarithmically for each unit increase in pH, with minimum activity at around pH 9.0 (Lindsay, 1979, cited in Naidu and Rengasamy, 1993). Manganese deficiency has been reported in chickpea (Rashid et at., 1990), and application of Mn to chickpea improved nodulation, dry matter production, and yield (Ahlawat, 1990). Atwell (1991) observed that shoot Cu concentration in narrow-leafed lupin growing in alkaline sodic soils was lower than the normal sufficiency range. The availability of B is largely influenced by soil pH, being most available in the acidic pH range and less available with increasing pH, primarily due to the adsorption by soil colloids (Mahler et d., 1988); for example, yield responses of chickpea to B application (2.5 Kg B ha- ') has been observed in calcareous soils in India (Ahlawat, 1990). B concentration in some other alkaline soils, however, may be inherently high, particularly where the parent material contained high concentrations of B (Nable and Paull, 1991). Continuous irrigation using water containing moderately high concentrations of B can also lead to accumulation of B in these soils (Nable and Paull, 1991). Boron toxicity is, therefore, much more likely to occur than B deficiency under these conditions. Additionally, toxic concentrations of B may develop with over-application of B fertilizer when correcting B deficiency (Nable and Paull, 1991). Boron toxicity in crops growing in alkaline soils has been reported in the United States, southern Australia, India, and Pak-

GRAIN LEGUME RESPONSES TO SOIL ABIOTIC STRESSES

111

istan (Nable and Paull, 1991). In southern Australia reductions of cereal yield up to 17% resulting from B toxicity have been reported (Nable and Paull, 1991). Cool season grain legumes are also likely to be affected by B toxicity in these soils. Under controlled environmental conditions the majority of commercial cultivars of chickpea, lentil, field pea, faba bean, and lupin are highly sensitive to B toxicity (J. Paull, unpublished data). Faba bean, however, appeared to be relatively more tolerant to B toxicity compared with field pea, lentil, and chickpea (J. Paull, unpublished data). Experimental evidence, particularly with field pea, has shown a large genetic variation in tolerance to high B concentrations in the soil and nutrient solutions (Nable and Paull, 1991; Baheri et al., 1992).

C. EFFECTS OF ALKALNI-~Y ON NODULATION AND N, FIXATION Soil alkalinity can impair symbiotic N, fixation in cool season grain legumes through adverse effects on the microsymbiont as well as on infection and nodule development. Nodule functioning may also be affected directly by nutritional disorders associated with alkalinity or indirectly by poor host plant growth. Survival of the rhizobia that nodulate cool season grain legumes in alkaline soils may vary depending on their genetic characteristics. Generally, fast-growing biovars of R. leguminosarum, which nodulate lentil, faba bean, and pea, and R. ciceri, which nodulate chickpea, are relatively tolerant to moderate soil alkalinity (pH 7.0-8.3) (Graham and Parker, 1964; Elsheikh and Wood, 1989). In contrast, Bradyrhizobia (slow growing), which nodulate lupin, appear to be highly sensitive (Parker and Oakley, 1964). At pH > 8.5, the growth of most rhizobia is reduced. Bhardwaj (1975) found that the growth of R. leguminosarum and R. trifolii isolated from lentil and berseem (7: ulexundrinum), respectively, growing in various soils with acid, neutral, or alkaline reactions, was equally limited by pH 8.7; however, this does not preclude the possibility of genetic variation. Some strains of rhizobia are able to survive and even grow, though very slowly, at pH levels around 10 (Lakshmi-Kumari et al., 1974; Rao et al., 1994). A fast-growing strain of Bradyrhizobium sp. isolated from a native Lupinus species from the Sonoran Desert, Mexico, survived and grew in a soil with pH 8.2 (Miller and Pepper, 1988). The effects of soil alkalinity on nodulation may also vary in different cool season grain legumes. In chickpea, lentil, faba bean, and pea, nodulation is relatively unaffected by alkalinity up to about pH 8.0 (Fig. 2). In comparison, nodulation in lupins decreases dramatically with increasing alkalinity (Fig. 2, and Tang and Robson, 1993), and this response is independent of host plant growth (Tang and Robson, 1993). For lupins (L. angustifolius and L. albus) the optimum pH for nodulation is in the range of pH 5.0-6.0 (Tang and Thomson, 1996). The exact processes involved in reduced nodulation in alkaline soils are poorly understood

112

H. P. S. JAYASUNDARA ETAL.

but may relate to inhibitory effects on rhizobial-root recognition and attachment processes (Lakshmi-Kumari et al., 1974; Kijne et al., 1985). The optimum pH for attachment of R. leguminosarum to pea root hairs in YEM culture medium is 7.5 (Kijne et al., 1985); thus a higher pH may inhibit the attachment. Alkalinity appears more inhibitory than salinity to nodule formation. Nodulation in lucerne (Medicago sativa), for example, was completely inhibited by 0.2% NaHCO, in the medium but occurred, though delayed, at 0.6% NaCl (Lakshmi-Kumari et al., 1974). Micronutritional disorders, common in alkaline soils, may also affect the legume-rhizobium symbiosis (Robson, 1988). In particular, iron deficiency is an important factor affecting both nodulation and N, fixation (Rai et a/., 1982 and 1984; Tang et al., 1990). Plants reliant on N, fixation have a higher requirement for iron than those supplied with mineral nitrogen (Tang et al., 1992b). Generally, nodule initiation is more sensitive to iron deficiency than other phases of the symbiosis, whereas the division of cortical cells and bradyrhizobial proliferation in the developing nodule may also be affected (Tang et al., 1992b). In iron deficient lupin plants, nodule leghaemoglobin concentration is significantly decreased (Tang et al., 1990). Boron is another micronutrient that is important in the legume-rhizobium symbiosis (Bolanos et al., 1996) and is likely to be deficient in some alkaline soils. Nodule development in faba bean is reduced by B deficiency (Robson, 1988). Zinc application has also been reported to increase nodule dry weight of chickpea (Shukla and Yadav, 1982), but this may be due to increased host plant growth rather than a direct effect on nodule development. The growth of legumes dependent on N, fixation does not appear to be more sensitive to Zn deficiency than that of mineral N-fed legumes (Shukla and Yadav, 1982).

D. GENETIC VARIATION INRESPONSE TO SOILALKALINITY It is clear that some species are better adapted to alkaline soils than others and possess certain adaptive mechanisms to avoid or tolerate the adverse chemical factors. Also, adapted species are capable of obtaining nutrients with low availability, i.e., iron, phosphorus, zinc, and manganese from the soil for optimum growth, and their root extension growth is less affected by high concentrations of Ca2+, HCO;, or high pH (Tang ef al., 1996). Although it is recognized that the interspecific variation in response to soil alkalinity is important, what is more useful may be the extent of the intraspecific variation. Due to the complex nature of the causes for poor growth in alkaline soils and the differences in the response exhibited by species, it may be difficult to select common selection criteria in determining the extent of genetic variation in tolerance of different genotypes to soil alkalinity. This is particularly so for species such as lupin, for which iron deficiency is not the single cause for poor growth in alka-

GRAIN LEGUME RESPONSES T O SOIL ABIOTIC STRESSES

1 13

line soils. Also, in some instances, iron deficiency symptoms occur, but the loss of seed yield is not economically significant (Zaiter and Ghalayini, 1994). For most widely cultivated cool season grain legumes, however, where attempts have been made to determine the extent of intraspecific genetic variation, research has been focused mainly on “iron efficiency” of different cultivars or germplasms (Saxena and Sheldrake, 1980; Kannan, 1983; Kaur et al., 1984; Rai et al., 1984; Singh et al., 1986; Hamze et al., 1987; Saxena et al., 1990; Erskine et al., 1993; Zaiter and Ghalayini, 1994); for example, evaluation of 3267 lines of chickpea and 35 12 lines of lentil for iron deficiency chlorosis symptoms on a calcareous soil (CaCO, content 20%, pH 8.5) at the International Centre forAgricultura1 Research in Dry Areas (ICARDA) revealed a large intraspecific genetic variation in the development of lime-induced chlorosis symptoms in both species (Saxena etal., 1990; Erskine et al., 1993). The characteristic appearance of chlorosis in younger leaves in susceptible germplasm and lack of incipient deficiency in tolerant germplasm permits selection of tolerant germplasm on the basis of visual scoring (Hamze et al., 1987; Saxena et al., 1990). In chickpea, susceptibility to iron deficiency is governed by a single recessive gene (Gowda and Rao, 1986; Saxena et af., 1990); thus susceptible types can be identified easily in segregating populations in breeding problems. Since lime-induced chlorosis resistance is related to adaptive mechanisms in the root system of efficient genotypes, such genotypes may generally be efficient in obtaining other marginally available nutrients from calcareous soils (Marschner, 1995). For species in which iron deficiency often correlates poorly with shoot growth and seed yield in alkaline soils, iron chlorosis scores alone may not be useful as a selection criteria for intraspecific variation in tolerance to alkalinity. Tang et al. (1996) suggested that rate of tap-root elongation and shoot weight in plants growing in alkaline nutrient solutions might be useful selection criteria for lupin genotypes tolerant to alkaline soils. The early root elongation rate of 16 lupin genotypes (from six species) at pH 7.0 in a buffered nutrient solution was well correlated with shoot growth and seed yield of these genotypes in alkaline soils under field conditions (Tang et al., 1996). Using the same screening technique a large intraspecific variation in response to alkalinity has been found among 30 wild genotypes of L. angustifolius (C. Tang, unpublished data).

-

-

V. SOIL COMPACTION Soil structure can deteriorate as a result of a number of processes. Compaction from agricultural traffic is a common process of deterioration of the soil structure (Voorhees, 1992). Surface crusting and hard setting are other forms of physical degradation, particularly in soils with low-activity clays, low organic matter con-

114

H. P. S. JAYASUNDARA ETAL.

tents, and high exchangeable sodium percentage (Mullins et al., 1990). Some soils naturally have a relatively light-textured shallow top soil, overlying a heavier finetextured subsoil with a high bulk density and lower permeability (Dracup et d., 1992).All these conditions can severely limit the productivity of cool season grain legumes by poor seedling emergence and/or restricted root growth.

A. RESPONSESOF COOLSEASONGRA~N LEGUMES TO S o n COMPACTION 1. Seedling Emergence

Mechanical resistance to seedling emergence can be an important limiting factor for establishment of cool season grain legumes in soils prone to surface crusting (Sivaprasad and Sarma, 1987; White and Robson, 1989a). Surface crusts can be formed by beating action by rain followed by drying. When crusts are formed after sowing, seedlings attempting to penetrate the crust may be weakened or fail to emerge. A greater proportion of seed reserves may be utilized by seedlings emerging through a hard surface crust compared to seedlings emerging from a normal seed bed with optimum conditions (Goyal et al., 1980). Seedlings stressed at emergence may develop slowly and may be more susceptible to pests, diseases, and other environmental stresses (White, 1990). The adverse effects of surface crusts may vary depending on the pattern of seedling emergence. In species with an epigeal pattern of emergence (e.g., lupin), the relatively large cotyledons have to be pushed through the soil surface, and this process may face considerable resistance. Seedlings of these species initially rupture the soil surface with the hypocotyl hook while the cotyledons still remain in the soil, and further growth of the hypocotyl pulls the cotyledon out of the soil. If the strength of the soil crust is high, the cotyledons may become trapped in the soil, causing severe seedling damage (Rathore et al., 1981; White and Robson, 1989a). In contrast, species with a hypogeal pattern of emergence (e.g., faba bean and field pea) face less mechanical resistance because their cotyledons remain below the soil surface while the relatively small plumule emerges through the soil surface (Inouye el al., 1979; White and Robson, 1989a). Seed size has an effect on seedling emergence through surface crusts. The greater reserves in the larger cotyledons may produce a stronger seedling with a large emergence force (Inouye et al., 1979). In 12 leguminous species, including faba bean, pea, and lupin, the mean maximum emergence force of a species is strongly and positively correlated with the seed size and cross-sectional area of the stem (Inouye et al., 1979), with faba bean being highest, followed by lupin and pea. In lupin, total emergence and seedling vigour were more affected in the smaller seeded L. angust$olius than in larger seeded L. albus in a hard-setting soil

GRAIN LEGUME RESPONSES T O SOIL ABIOTIC STRESSES

1 15

(White and Robson, 1989a). Similar results have been reported for different cultivars of soybean with varying seed size (Longer e t a / . , 1986). The development of the maximum emergence force, however, is quicker in species with smaller seeds (Inouye et al., 1979), so these species may avoid the resistance from surface by emerging before surface crusts develop maximum hardness (White, 1990).

2. Plant Growth and Seed Yield Soil compaction may considerably reduce the growth of cool season grain legumes; for example, compaction reduced 20-30% of shoot dry matter in lupin (Henderson, 1991) and faba bean (Kahnt et al., 1986; Brereton et al., 1986) and more than 50% of shoot dry matter in field pea (Hebbelethwaite and McGowan, 1980; Whiteley and Dexter, 1982) and chickpea (Agrawal, 1985). Such reductions are usually associated with restricted growth and functioning of the root system. In faba bean, increasing bulk density from 1.25 to 1.65 Mg mp3 at 20 cm soil depth decreased the total root length by more than 55% and shoot dry matter by 30% (Kahnt et al., 1986). Plants growing in compacted soils often produce shallow roots. This is particularly so when the root-impeding layer is near the surface (Olsson et al., 1995). This can cause severe adverse effects on growth and yield when surface soils are dry. Under field conditions in Western Australia, deep ripping increased the yield of pea by 60% and that of lupin by 20%, indicating the limitations of soil compaction on the productivity of these species (Henderson, 1991). In pigeon pea, compaction at 5 cm depth reduced root penetration into the subsoil considerably, resulting in a 50% reduction in shoot dry weight and 65% reduction in seed yield in a dry year (Kirkegaard el a/., 1992), whereas compaction did not reduce yield in a wet year.

B. FACTORSRELATING TO POORGROWTH IN COMPACTED SOILS 1. Physical Resistance to Root Growth

Some degree of resistance is common for all roots growing in soil, but this is considerably higher in compacted soils (Voorhees, 1992). It has been shown that radicle elongation decreases with increasing soil resistance (Fig. 5). The values of soil resistance that limit root growth may range from 0.8 to 5 MPa penetrometer resistance or 1.4 to 1.8 Mg mp3 bulk density (Vepraskas, 1988). These values are largely influenced by soil water content (Eavis, 1972), soil texture (Jones, 1983), soil structure (Bennie, 1991),and plant species (Materechera et a/., 1991). In many crops, including grain legumes, commonly encountered mechanical impedance under field conditions, i.e., around 2 MPa penetrometer resistance (Atwell, 1993),

116

H. P. S. JAYASUNDARA ETAL. 807

70 - -

E E

.-z0a a

u

3

0

60 ~50

--

-Fa m - c)

0 0

0 0 0.

0 0

0

30.20

0

--

10 - -

07

-.. 0

.

0

0

0

0

O.

m

0

usually decreases the total root length by at least 50% (e.g., common bean, Asady and Smucker, 1989; pigeon pea, Kirkegaard et al., 1992; lupins, Patterson et al., 1995). For some soils, the interpretation of root elongation relative to penetrometer resistance may be complicated due to high gravel content (Hamblin, 1985), high spatial variability of texture, structure and water content of the soil (Bengough and Mullins, 1990), and the existence of biopores (Wang et al., 1986). Root elongation in some grain legumes can proceed slowly at soil strengths greater than 2 MPa (e.g., groundnuts, Taylor and Ratliff, 1969; L. angustifolius, Materechera, et al., 1991) (discussed in more detail in Sec. V.8.3). 2. Interactions with Soil Aeration Soil pore volumes are considerably decreased with compaction; thus the rate of gaseous diffusion is reduced in a compacted soil. Asady and Smucker (1989) found that the oxygen diffusion rate decreased by more than 50% when the soil bulk density increased from 1.1 to 1.4 Mg mP3 (0.43and 2.14 MPa penetrometer resis-

GRAIN LEGUME RESPONSES TO SOIL ABIOTIC STRESSES

117

tance at a constant moisture level). Therefore, inadequate aeration may exert adverse effects on root growth in addition to physical resistance in a compacted soil. These two limiting conditions are often synergistic and difficult to separate (Eavis, 1972). Using compressed artificial granules (ballotini) circulated with nutrient solutions containing different concentrations of 0,, Gill and Miller (1956) and Barley (1962) demonstrated the interactive effects of poor aeration with mechanical resistance on the rate of root elongation in maize. Increasing external pressure from 0 to 0.05 MPa at a high concentration of 0, (20%) decreased the root elongation by 31%, whereas the same increase of external pressure at a low concentration of 0, (5%) decreased root elongation by 50% (Barley, 1962). Although root penetration into subsoil can be restricted by high mechanical resistance or bulk density, proliferation of lateral roots in the topsoil may proceed (Asady and Smucker, 1989; Kirkegaard et al., 1992). In such situations, the normal activities of the root system and its associated rhizosphere microflora in the topsoil could exacerbate the problem of inadequate aeration down the soil profile. Consumption of oxygen may be faster than the rate of replenishment due to reduced diffusion rates. Asady and Smucker (1989), for example, measured the oxygen diffusion rates at different depths of soil columns compacted to three levels of bulk densities: 1.1, 1.4, and 1.7 Mg m p 3 (0.43, 2.14, and 5.50 MPa penetrometer resistance at a constant metric suction) and planted with common bean. The oxygen diffusion rate was below the critical level (02diffusion rate required for optimum root growth) at the bottom of soil columns with highest bulk density (1.7 Mg m-3) at all stages of plant growth, whereas it was not limiting at the other two levels of bulk densities at early stages of growth (0-20 days after planting). As root accumulations increased at the 0.10-0.25 m depths, oxygen diffusion rates dropped below critical levels for all bulk densities (Asady and Smucker, 1989).

3. Changes in Root Characteristics Several anatomical and morphological changes may occur in mechanically impeded roots (Atwell, 1988; Bennie, 199 I). Both cell division and cell elongation in the root meristem may be reduced. In field pea, root penetration resistance of 0.34 MPa reduced the rate of cell division by 40% and the rate of root elongation by 70% (Eavis, 1969). The reduced cell elongation is, however, accompanied by a radial expansion of the cortical cells (Atwell, 1988; Bennie, 1991). This may lead to increased root diameter (Table 111). Mechanically impeded roots are, therefore, shorter and thicker compared with roots developed under unimpeded conditions. It has been suggested that the root penetration into compacted soils may be facilitated by the thickening of roots in response to mechanical impedance (Abdalla et al., 1969). An increase in radial root pressure resulting from root swelling may relieve the resistance at the root apex thereby permitting further axial growth until a

118

H. P. S. JAYASUNDARA ETAL.

limiting situation occurs again (Abdalla et al., 1969). Thicker roots may also have a greater resistance to bending (Materechera et al., 1992) and higher axial rootgrowth pressure (Misra et al., 1986), which may further facilitate elongation in a compacted soil. Roots of different species may vary in their ability to elongate in compacted soils (Taylor and Ratliff, 1969; Materechera et al., 1991, 1993). This variation is largely related to the thickness of the roots and the tendency of roots to swell in response to mechanical impedance (Taylor and Ratliff, 1969; Atwell, 1988; Materechera et al., 1991, 1992, 1993). Materachera et al. (1993) found that in a range of crop species, the proportion of roots that penetrated into a compacted soil layer was higher in dicotyledonous species (with thicker roots) than in mono-

Table 111 Rates of Root Elongation and Root Diameters of Some Cool Season Grain Legumes as Affected by Increasing Soil Bulk Density Species Faba bean (% faba)

Pea

(I? sativum)

Soil bulk density (Mg rn-.’)

Elongation rate (mm day-')

Root diameter

Low" 1.35

9.87 0.68

0.95 2.07

Materechera et a1 , 1991

Reference

I .25 1.57

ND" ND

0.81 1.52

Materechera efa/., 1992

Low" I .35

10.46 0.70

0.78 I .62

Materechera et a/.. 1991

I .25 1.57

ND ND

0.7 I I .28

Materechera et ul.. 1992

0.98 1.81

Materechera ef a/., 19Y1

Lupin Low" (L. ~rig~,~t~ffl;ffs) 1.35

Vetch (V. sativa)

(mm)

6.94 0.7 1

1.23 1.42 1.64

45.5 33.2 28. I

1.56 I .68 1.81

Atwell, 1988

1.3 1.7

22.9 5.7

1.7 2. I

Patterson e t a / . , 1995

Low" 1.35

11.27 0.65

0.74 1.33

Materechera et ul., 1991

"Roots grown in vermiculite. "ND = no data.

GRAIN LEGUME RESPONSES T O SOIL ABIOTIC STRESSES

119

cotyledonous species (with thinner roots). Results from a few experiments where several cool season grain legumes have been tested under uniform conditions show that root growth in lupin (L. angustifilius) was least affected by soil compaction (compared to that in deeply tilled soil), followed by the root growth in faba bean, pea (Materechera era/., 1992, 1993), and vetch (Vicia saliva) (Materechera e f al., 1991). Other morphological changes in roots growing in compacted soils are increased production of sclerified cells in the cortical and vescular tissues, thicker casparian strips, and ruptured epidermal cells (Beligar et a/., 1975). Tissues with such sclerified cells probably prevent the deformation of interior cells of the root (Prihar et a/., 1971). The growth of lateral roots may also be considerably inhibited due to the compression of surrounding soils resulting from root thickening (Dexter, 1987). In lupin growing through a layer of fine-textured sandy loam, there was little or no proliferation of lateral roots due to compaction (Atwell, 1988). The zone of lateral root growth is sometimes advanced nearer to the apex of the main axis due to compaction (Atwell, 1988). The mechanisms for root responses to mechanical impedance are complex. Greacen and Oh (1972) suggested that root cells may change their osmotic potential to exert more pressure on the surrounding soil. Atwell ( 1 988) found an increase of about 27% in the osmotic pressure of compacted root apices of lupin (L. angusrifolius). Many root morphological changes occumng in compacted soils, however, do not relate to osmotic adjustments alone (Bengough and Mullins, 1990). An involvement of ethylene has been implicated in the root response to mechanical impedance (Kays e t a / . , 1974; Veen, 1982). Applications of exogenous ethylene causes changes in root morphology similar to those of mechanically impeded roots (Kays et al., 1974). Moss ef a/. (1988), however, recently suggested that the increased ethylene evolution by mechanically impeded roots is not a direct effect of mechanical impedance but an effect of physical wounding of radially expanding roots. Thus, many physiological aspects of the root response to mechanical impedance still remain unclear.

4. Functioning of Roots Root functioning is also affected by soil compaction. Roots developed under high mechanical impedance are usually shorter and thicker with reduced proliferation in the subsoil; thus the amount of soil volume they explore is reduced (Bennie, 1991). As an example, field pea roots, which penetrate to around 1.5 m under well-drained deep sandy soils (Armstrong et ul., 1994), exhibit variable rooting depths (sometimes as low as 0.4 m) in soils with a compacted subsoil (Reid et al., 1987; Henderson, 1991). The demand for water and nutrients by the shoots may also lead to a rapid depletion of resources within the limited soil volume early in the plant growth (Bennie, 1991). In a number of grain legumes water uptake, depth of soil water ex-

120

H. P. S. JAYASUNDARA ETAL.

traction, and crop transpiration rates were decreased significantly by soil compaction (e.g. faba bean, Brereton et al., 1986; field pea, Reid et at., 1987; field pea and L. angustifolius, Henderson, 1991; pigeon pea, Kirkegaard et al., 1992). In pigeon pea compaction at 5 cm below the surface decreased the maximum depth of water extraction at flowering by approximately 30% relative to that in deep-tilled soils with a lower bulk density (Kirkegaard et al., 1992). Low oxygen diffusion in compacted soils may also reduce water and nutrient uptake by roots. Roots may sometimes penetrate into the compacted subsoil by extending through biopores or cracks (Wang et al., 1986), but their ability to extract marginally available water may be considerably limited because they are often clumped in pores (Passioura, 1991). Moreover, the usually low water storage capacity and restricted movement of water in compacted soils may further exacerbate limitations in water uptake by roots (Olsson et al., 1995). Many studies with various crop species, including cool season grain legumes, have shown that if the limitations to root growth are alleviated by soil management practices such as deep tilling, root growth can proceed into the subsoil, and plant growth and yield are increased, presumably due to improved uptake of water (Hamblin, 1985). The effects of soil compaction on the uptake of nutrients may vary depending on differences in their availability and mobility in the bulk soil (Cornish et al., 1984) and possibly on plant species (Castillo et al., 1982). Generally, the reduced root-length density and decreased root-length-root-weight ratio of plants grown in compacted soils decrease both the availability of nutrients to the root system as a whole and the rate of nutrient absorption per unit length of root (Bennie, 1991). Conversely, a higher bulk density can sometimes improve the ability of roots to extract relatively immobile or poorly soluble nutrients, possibly due to the increased contract between roots and soil and increased mobility of the nutrient (Passioura and Leeper, 1963; Cornish et al., 1984). For cool season grain legumes, information is limited on these aspects. Castillo et al. (1982) investigated the effects of mechanical stress on root growth and nutrient uptake by field pea grown in soil cores under controlled environmental conditions. Application of an external pressure of 0.18 MPa to a soil core (initial bulk density = 1.16 Mg m-3) decreased root length and root-length-root-weight ratio by 86% and 76%, respectively, resulting in a 25-40% decrease in the uptake of K, Ca, and Mg. Similar decreases in the uptake of nutrients resulting from increased bulk density have been reported for field pea (Grath and Hakansson, 1992) and faba bean (Rowse and Stone, 1980) under field conditions and for soybean under glasshouse conditions (Hallmark and Barber, 1981). 5. Shoot Responses

Depressions in plant height, number of branches per plant, leaf area index, leaf area duration, and shoot dry matter resulting from compaction are common with

GRAIN LEGUME RESPONSES T O SOIL ABIOTIC STRESSES

12 1

many cool season grain legumes (Hebblethwaite and McGowan, 1980; Agrawal, 1985; Brereton et al., 1986; Kahnt ef a/.. 1986). Limitations of nutrient and water uptake resulting from restricted root growth are thought to be the main reason for these responses. Brereton et al. (1986) and Passioura (1991), however, have suggested that the restricted root growth or distorted roots do not necessarily impair shoot growth because in some situations shoot growth is slow even when roots are able to supply adequate amounts of water and nutrients. Hormonal mechanisms have been proposed through which roots “sense” the physical impedance of the soil or possibly the restricted water supply and communicate these to the shoot to modify water relations and lower the leaf expansion rates and growth of shoots (Masle and Passioura, 1987). Contradictory results have been reported, however, for some grain legumes, especially in nonuniformly compacted soils. In pigeon pea, for example, growing in soil columns with different subsoil bulk densities (0.95-1.46 Mg m p 3 or 0.5 1-3.47 MPa penetrometer resistance) under optimum supply of water and nutrients, root growth (root length and weight) and root distribution in the compacted subsoil were inhibited with increasing mechanical strength, but the proliferation of lateral roots in the top soil was unaffected (Kirkegaard et al., 1992). As a result the total root length per plant was not affected, and plant height, leaf area, and shoot dry weight were not significantly different. Under field conditions a similar proliferation of roots in the topsoil and a reduced penetration in the subsoil may still be disadvantages, particularly under suboptimal conditions (i.e., in a dry year).

C. EFFECTSOF SOILCOMPACTION ON NODUTION AND N, FIXATION Among soil factors affecting nodulation and nitrogen fixation in cool season grain legumes, soil compaction is probably the least studied. Since soil compaction can modify several aspects of the soil physical environment, such as soil aeration and soil water relations, which influence both nodule formation and functioning (Sprint, 1971),biological nitrogen fixation is likely to be adversely affected by soil compaction. In addition, soil strength may directly affect nodule development, as it does root elongation (Kirkegaard et al., 1992). Grath and Hakansson (1992) studying the relationship between poor growth of field pea and several soil parameters under field conditions in Sweden, found that decreases of about 40% in total plant dry matter, 52% in shoot N concentration, and 60% in number of nodules in the main roots of pea were associated with soil compaction resulting from agricultural traffic and its accompanied indirect effects, i.e., poor aeration and low hydraulic conductivity. In soybean and common bean, increasing soil bulk density from 1.2 to 1.6 Mg m-3 resulted in a 30-50% reduction in nodule number and a 25-30% reduction in nodule fresh weight per plant (Tu and Buttery, 1988). The

122

H. P. S. JAYASUNDARA ETAL.

corresponding reductions in N, fixation (measured as acetylene-reduction activity) for both species were about 60% in total nitrogenase activity and about 50% in specific nitrogenase activity (Tu and Buttery, 1988). That nodule functioning (nitrogenase activity) was more affected than number of nodules and nodule growth in soybean and common bean suggests that the N, fixation was particularly sensitive to changes in the soil environment.

D. GENETIC VARIATION IN RESPONSETO SOILCOMPACTION To some extent interspecific variation in root responses to mechanical impedance has been demonstrated for a number of cool season grain legumes (e.g., lupins, field pea, faba bean, and vetch, Materecheraet al., 1991, 1992, 1993); however, the extent of intraspecific variation in these species is still not known. Although soil management practices play an important role in optimizing soil conditions for crop growth in poorly structured soils, selection of genotypes tolerant to soil compaction may still be valuable. In experiments where interspecific variation has been demonstrated, a significant positive correlation exists between root thickening and rate of root elongation in stressed plants both under controlled environment conditions and in the field (Materechera et al., 1991, 1992, 1993). Knowledge based on these studies may now be used in identifying the extent of such genetic variability within a species. A similar approach for common bean has demonstrated the possibility of selecting cultivars better adapted to soils with high bulk densities (Asady et at., 1985).

VI. WATERLOGGING Waterlogging is defined as saturation of the soil root zone with water. Waterlogging is harmful to plant growth because it prevents the diffusion of gases between the soil system and the atmosphere. As the soil becomes saturated with water, airfilled pore space gradually decreases. The concentration of 0, in the soil also decreases because it is used by microorganisms and plant roots. The depletion of 0, can range from partial depletion (hypoxia) to complete depletion (anoxia) depending upon several factors, including soil temperature, plant and microbial biomass, and the length of the waterlogging period. Once depleted, 0, concentrations remain low in a soil saturated with water because of low solubility and low diffusivity of 0, in water. As the 0, concentration depletes, the soil aerobic microorganisms are replaced sequentially by facultative anaerobic and then obligatory, anaerobic microorganisms. Anaerobic microorganisms use other substances from the environment for terminal electron acceptors instead of 0,, and the soil becomes increas-

GRAIN LEGUME RESPONSES T O SOIL ABIOTIC STRESSES

123

ingly reduced. Under these conditions a number of chemical changes, such as denitrification and reduction of manganese, iron, and sulphates, can occur in the soil (Ponnamperuma, 1984). At the same time various toxic end-products of anaerobic respiration, such as lactic acid, ethanol, acetic acid, butyric acid, and amines, may accumulate. Ethylene, a physiologically active organic substance (Jackson and Drew, 1984), increases in concentration in waterlogged soils through production by both soil microorganisms and plant roots. The chemical processes occurring in waterlogged soils have been comprehensively reviewed by Ponnamperuma ( 1984).

A. RESPONSESOF COOLSEASON GRAINLEGUMES TO WATERLOGGING 1. Germination and Seedling Emergence Seed germination is very susceptible to waterlogging at least partly because at this stage of growth the whole organism is subjected to the stress. Germination is also an intensely energy-dependent process in which energy is provided by respiration. Thus, both anoxic and hypoxic conditions may inhibit germination of nonwetland species, including cool season grain legumes (Crawford, 1977; Rowland and Gusta, 1977; Sarlistyaningsih, et al., 1995, 1996). In addition, the leakage of nutrients from germinating seeds can create favorable conditions for microbial growth, and this may also affect the germination and survival of seeds (Rowland and Gusta, 1977). Poor crop establishment is a common problem when waterlogging occurs at seedling emergence. Waterlogging 6 days after the germination of pea, for example, delayed seedling emergence for 2 4 days and reduced the final plant density by 80% relative to plant density in freely drained soil (Belford and Thornson, 1979). In lupin (L. angustifolius) seed germination was also completely inhibited after 4 days of waterlogging, and seed survival (assessed 5 days after the recovery of waterlogging) was decreased to 0% (Sarlistyaningsih et al., 1995, 1996). In faba bean and pea, soaking seeds for 4 hours in nonaerated water decreased germination by about 50% (Rowland and Gusta, 1977). Crawford (1977) found that in faba bean and field pea alcoholic fermentation resulting from excess water reduced both germination and survival of seeds. In comparison with cereals, grain legumes are intolerant to waterlogging at germination (Crawford, 1977). Information is scarce on comparative responses of different cool season grain legumes to waterlogging at germination. Limited data suggest that faba bean is relatively tolerant to waterlogging at germination compared with field pea (Crawford, 1977) and L. ungustifalius (Sarlistyaningsih, 1993). Viability of pea seeds is completely lost within 72 hours after exposure to excess water, whereas faba bean was able to maintain over 50% germination after soaking 72 hours in water (Crawford,

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1977). Sarlistyaningsih (1993) recorded 60% seed germination in faba bean even after 6 days waterlogging. We are not aware of any studies on the comparative response to waterlogging at seed germination in other cool season grain legumes.

2. Plant Growth and Seed Yield Waterlogging severely depresses vegetative growth of plants. Generally, root growth is more affected than shoot growth (Fig. 6.; B. Thomson, unpublished data; Gallacher and Sprent, 1978; Ashraf and Chisti, 1993). The initial response to waterlogging is reduced rate of root elongation (Jackson and Drew, 1984). Thus, a significant reduction in root growth may occur before any significant change in the shoot growth. Hanbury (1988), for example, found that root dry weight of L. albus decreased within 5 days of imposing waterlogging, but shoot dry weight did not significantly decrease for 10 days. Similar observations have been made by Broue et al. (1976) with a range of lupin species subjected to waterlogging. The capacity of roots to tolerate waterlogging may vary among different cool season grain legumes. Roots of L. luteus and L. angustifolius exhibited a greater tolerance (based on the relative growth rate) to waterlogging between 35 and 42 days after sowing than did the roots of faba bean, which in turn exhibited a greater tolerance than did the roots of chickpea, lentil, and field pea (Fig. 6). In many plants tolerant of waterlogging, including grain legumes, adventitious roots are formed from the base of the submerged stem while original roots are dying (e.g., lupin, Hanbury, 1988; Dracup er al., 1992; Davies et al., 1996; lentil, Alcalde and Summerfield, 1994; soybean, Singh, 1988a; K sinensis, Nawata et al., 1991). The development of an adventitious root system relates to the capacity of these species to adapt to waterlogged conditions because these are normally distributed closer to soil surface where 0, concentration is relatively high. In L. luteus and L. angustifolius waterlogged at 8-10 weeks after sowing, original root dry weights measured at 12 weeks were reduced by 70-94%, but the adventitious root dry weights were increased by 200% in waterlogging-tolerant L. luteus compared with only 20% in waterlogging-sensitive L. angustifolius (C. Davies, unpublished data). Waterlogging-sensitive species, such as pea, fail to form adventitious roots (Jackson, 1979). In plants adapted to wetlands, roots usually have aerenchyma (tissues with large intercellular spaces), facilitating continuous gas diffusion from shoots to roots (Jackson and Drew, 1984). Such tissues may also form in newly developed adventitious roots and old roots in some legume species in response to waterlogging (e.g., L. ulbus, Hanbury, 1988; Vigna sinerzsis, Nawata et ul., 1991; Trifolium spp., Rogers and West, 1993; cowpea, Takele and McDavid, 1994), and this may greatly contribute to the waterlogging tolerance of these species. Waterlogging decreases stem elongation, leaf orientation, leaf expansion, and dry matter accumulation (Jackson and Drew, 1984). Many of these responses are common to cool season grain legume species (e.g., chickpea, Cowie et al., 1996;

GRAIN LEGUME RESPONSES TO SOIL ABIOTIC STRESSES

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Figure 6 Effects of waterlogging at between 3.5 and 42 days after sowing on relative growth rates of two lupin species and four widely cultivated cool season grain legumes grown in soils under glasshouse conditions (from B. D. Thornson, unpublished data). Solid bars represent nonwaterlogged controls, and open bars represent waterlogged treatments.

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lentil, Alcalde and Summerfield, 1994; field pea, Belford et al., 1980; Jackson, 1979; lupin, Davies et al., 1996). In species relatively tolerant to waterlogging, however, such as L. luteus (Broue et al., 1976) and faba bean (Fig. 6), a slight to moderate reduction in root growth in response to waterlogging is sometimes accompanied by an increase in shoot growth, particularly when waterlogging stress is of relatively short duration. Such “compensatory” interactions between root and shoot growth during short-term waterlogging have been attributed to the inhibition of root respiration and the consequent “removal” of the root sink for assimilates (Luxmoore et al., 1973). With prolonged waterlogging shoot growth is drastically decreased in many grain legumes (Broue et al., 1976; Ashraf and Christi, 1993; Davies e f al., 1996). Reduced shoot growth under waterlogging is generally associated with reduced leaf growth. Alcalede and Summerfield (1994) found about 60% reduction in total leaf area of lentil at flowering when the plants were waterlogged for 6 days between 16 and 22 days after sowing. The reduction in leaf area per plant was due to inhibition of leaf expansion as well as a reduction in number of leaves per plant. Similar results have been reported for field pea (Jackson, 1979; Belford ef al, 1980) and chickpea (Cowie et al., 1996). In L. luteus and L. angustifolius, waterlogging between 8 and 10 weeks reduced leaf expansion more than leaf dry matter, causing a 38-60% reduction in specific leaf area (C. Davies, 1996, unpublished data). Development of leaf chlorosis, necrosis, and premature senescence are common symptoms of waterlogging stress in grain legumes (e.g., field pea, Jackson, 1979; Belford et al., 1980; lentil, Alcalde and Summerfield, 1993; chickpea, Cowie et al., 1996; lupin, Broue et al., 1976; faba bean, Younis et al., 1993). The adverse effects of waterlogging increase with the length of the period of waterlogging (Belford et al., 1980; Alcalde and Summerfield, 1994) and are decreased if waterlogging is only intermittent (Broue et al., 1976). For field pea at the 6-7 leaf stage, complete saturation of the root zone for 2 days or partial saturation for 5 days had little adverse effects relative to complete saturation of the root zone for 5 days (Belford et al., 1980). Thus, the greater the proportion of the pea root system in saturated soil and the longer this occurred, the greater the adverse effect. Furthermore, once seedlings are established, the sensitivity of plants to waterlogging stress is generally increased with increasing age (Broue et ul., 1976; Jackson, 1979; Belford et al., 1980; Cowie er al., 1996). Thus, the ability to survive and recover following waterlogging is dependent on timing of waterlogging relative to the stage of growth and generally declines sharply as reproductive growth approaches (Jackson, 1979; Cowie et al., 1996). High temperatures during waterlogging usually increase the severity of waterlogging damage compared to moderate or low temperatures (Cowie et al., 1995). Therefore, the potential confounding factors of plant age, duration of waterlogging, the extent of the root zone saturated, and soil temperature should not be ignored when comparing the waterlogging tolerance of different plant genotypes.

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Seed yield loss resulting from waterlogging can be substantial. Limited data available for lupin, field pea, and chickpea show that reductions in yield can vary from negligible to almost loo%, depending on the species, stage of growth when waterlogged, duration, and the extent of root zone affected by waterlogging. Some species are very sensitive to waterlogging; thus, a significant loss of seed yield may occur in response to only a brief inundation, such as excess irrigation, particularly in poorly drained soils (e.g., field pea, Greenwood and McNamara, 1987; chickpea, Cowie et al., 1995). On the other hand, some species can withstand waterlogging for up to 2 weeks without significant loss of seed yield (e.g., L. luteus, Fig. 7). At its most severe level of damage, waterlogging can kill plants (e.g., field pea, Cannell, 1979; chickpea, Cowie et d.,1996). Generally, the loss of seed yield is more severe when waterlogging occurs at the reproductive stage (flowering or pod filling) than at vegetative growth. Waterlogging for 10 days starting at 21 days after sowing, for example, reduced the seed yield of chickpea by 35% compared with 53 and 67% loss of seed yield if waterlogging occurred at flowering (48 days after sowing) and pod filling (75 days after sowing), respectively (Cowie et a/., 1996). The loss of seed yield in chickpea due to waterlogging at vegetative growth was mainly due to a decreased number of pods per plant, whereas the number of seeds per pod, hundred seed weight, and the harvest index were not significantly

1

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NARROW-LEAFED LUPIN

Figure 7 Effects of waterlogging for 14 days between 56 and 70 days after sowing on seed yield of L. lureus (yellow lupin) and L. clngrr.rtifiJius (narrow-leafed lupin) grown in hydraulically isolated

plots (2.25 mZ)in a duplex soil near Beverly, Western Australia (from C. L. Davies, unpublished data).

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affected. In contrast, the majority of plants died when waterlogging occurred at flowering or pod filling, and in surviving plants all the yield components were severely affected (Cowie et al., 1996a). In the field, seed yield of pea was reduced by 60-70% by waterlogging for 4 days at reproductive growth (Cannell, 1979). The severity of yield loss also varies with the duration of waterlogging. Thus, in field pea, 2 days waterlogging at the 6-7 leaf stage had little effect on seed yield, whereas 4 days of waterlogging reduced the yield by 42% (Belford et af., 1980).

B. PHYSIOLOGY OF WATERLOGGING STRESS 1. Root Growth

The adverse effects of waterlogging on roots may arise for a number of reasons; for example, inhibition of aerobic respiration may deprive the root system of energy required for physiological functions, such as cell division, cell elongation, and nutrient uptake (Jackson and Drew, 1984). The accumulation of various end products of chemical and biochemical reducing reactions resulting from waterlogging may also be responsible for root injury (e.g., nitrous oxide and CO,, Jackson, 1979). Moreover, anaerobic metabolism in the root system may also generate toxic end products. As an example, in many plants, including grain legumes, endogenous ethylene accumulates under waterlogging (e.g., faba bean, El-Beltagy and Hall, 1974; lupin, Young and Newhook, 1977; field pea, Huber ef aL, 1979), and this has been implicated in the reduction of root extension in field pea (Goodlass and Smith, 1979). The relative importance of each of these factors in causing waterlogging injury has not been quantified, however. Under prolonged waterlogging, roots start to degenerate, first at the tips, which have high energy requirements relative to fully expanded tissues (Jackson, 1979). The duration of root survival approximately corresponds to the period over which mitochondria1 structure undergoes no irreversible structural degeneration (Jackson and Drew, 1984), and this may vary between plant species. Roots of pumpkin (Cucurbitu pepo), for example, can survive for 12 hours in an anaerobic environment at 25"C, whereas roots of pea can only survive for 6 hours (Webb and Amstrong, 1983). Roots of faba bean appear relatively tolerant and are able to survive 12-48 hours under anaerobic conditions at 23°C (Williamson, 1968). Physiological reasons for such differences in the survival of roots in the absence of 0, are complex and may include both avoidance of accumulation of toxic compounds and maintenance of a continuous supply of energy (Jackson and Drew, 1984; Pezeshki, 1994). Root primordia have a greater resistance to waterlogging relative to root apices possibly because of the low energy requirement for cell maintenance (Jackson and Drew, 1984).Thus, the recovery of the root system after death of root apices main-

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ly relies on the recovery of root primordia. The new roots, mostly adventitious, formed during and after waterlogging tend to concentrate near the soil surface, leading to a shallower root system compared with nonwaterlogged plants (e.g., lupin, Dracup et al., 1992; Davies et al., 1996; V sinensis var. sesquipedalis, Nawata et al., 1991; soybean, Singh, 1988). Development of adventitious roots may be related to better 0, supply near the soil surface or through the stem tissues (Jackson and Drew, 1984). These roots may take over the functions of the original root system, although they would presumably be vulnerable to surface drying when the waterlogging stress ceases. The functioning of these roots during waterlogging is facilitated by the development of aerenchyma (Pezeshki, 1994). The formation of aerenchyma involves partial breakdown of the cortex with cell lysis, which in many plants is mediated through endogenous ethylene (Kawase and Whitmoyer, 1980; He et al., 1996).

2. IonUptake Waterlogging markedly reduces the nutrient uptake, particularly the uptake of nitrogen (e.g., field pea, Belford et al.. 1980; lentil, chickpea, and faba bean, B. Thomson, unpublished data). Jackson ( 1979) found that 4 days waterlogging at the 8-1 0 leaf stage decreased the concentrations of nitrogen, phosphorous, and potassium in the shoots of field pea, with greater inhibition in N uptake (82%) than in P (41%) and K (46%) uptake. This inhibition of N uptake appears at least partly responsible for the premature chlorosis and leaf senescence of waterlogged plants. As an example, following 2 weeks of waterlogging of 4-week old L. luteus and L. angustifolius supplied with inorganic N, Davies (unpublished data) found that N content was reduced by 30% in relatively waterlogging-tolerant L. luteus and by 60% in waterlogging-sensitive L. angustifolius compared to control plants. Furthermore, premature chlorosis and leaf senescence occurred earlier in L. angustifolius than in L. luteus. In several cool season grain legumes, waterloggingintolerant species or cultivars exhibited a greater decrease in leaf chlorophyll concentration compared with relatively waterlogging-tolerant species or cultivars (e.g., lupin and field pea, Phuphak, 1989; lentil, Ashraf and Chisti, 1993). The physiological reasons for the differences in N uptake by different grain legume species during waterlogging are not well understood, however. In contrast to the essential nutrients, shoot concentrations of Na and C1 are increased drastically under waterlogging (Rogers and West, 1993). The mechanisms for the exclusion of these ions are generally energy dependent (Greenway and Munns, 1980); thus, under waterlogging, these mechanisms may be disrupted. In I? vulgaris exposed to 40 mM NaCl under waterlogged conditions, leaf Na and C1 concentrations increased substantially relative to those in plants grown under welldrained conditions (West and Taylor, 1980). Similar observations have been made with Trifolium species grown under saline waterlogging (Rogers and West, 1993).

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Therefore, under a combination of salt and waterlogging stress, plant growth may be more depressed than under either stress separately. There is no published information on the response of cool season grain legumes to combined salt and waterlogging stress. Under waterlogging, transfer of ions from the rooting medium to the shoots may take place passively, ions moving with little selectivity across damaged cell membranes by mass flow with the transpiration steam (Trought and Drew, 1980). Increased concentrations of Fe and Mn in shoots under waterlogging (e.g., lentil, Ashraf and Chishti, 1993) may be related to such passive uptake, since the solubility of Fe and Mn increases considerably under waterlogged conditions (Ponnamperuma, 1984). Conversely, the provision of greater concentrations of essential nutrients in the external medium may partially offset waterlogging-induced inhibition of nutrient transport to the shoot; for example, application of nitrogen fertilizer has been reported to reduce waterlogging damage in pea (Jackson, 1979), soybean (Buttery, 1987), and cowpea (Minchin and Summerfield, 1976).

3. Shoot Responses Shoot responses to waterlogging may primarily arise from the modifications to the internal flow of substances between root and shoot (Jackson and Kowalewska, 1983). Stomata1 closure is an early response to waterlogging (e.g., field pea, Jackson and Hall, 1987), perhaps due to increased resistance to water flow in flooded roots soon after waterlogging (Pezeshki, 1994; Zhang and Zhang, 1994). Stomata may remain closed until the waterlogging stress is removed or new adventitious roots or aerenchyma are formed (Pezeshki, 1994). The causes for the flood-induced stomatal closure are not fully understood, but both nutritional (particularly potassium nutrition) and hormonal (abscisic acid and ethylene) imbalances have been implicated (Pezeshki, 1994). Generally, stomatal closure in response to environmental stress is associated with increase in abscisic acid (ABA) concentration in response to a leaf water deficit. In many plants, however, including grain legumes, the concentration of endogenous ABA increases following waterlogging without significant change in the leaf water potential (Jackson and Kowelewska, 1983; Zhang and Davies, 1987; Jackson and Hall, 1987). In the absence of a leaf water deficit, an accumulation (due to waterlogging-induced inhibition of translocation from shoots to roots) rather than increased synthesis of ABA in leaves has been implicated as the cause for stomatal closure (Jackson and Hall, 1987). More recently, Zhang and Zhang (1994) have shown that under waterlogging ABA is produced due to loss of turgor in the older leaves and translocated to younger leaves, thus leading to stomatal closure. Wilting in response to waterlogging is common in many plants (Pezeshki, 1994), and in most cases this is alleviated by the closure of stomata (Pezeshki, 1994).Therefore, stomatal closure may be an important adaptive response to conserve water during the initial few days of water-

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logging stress. Under prolonged waterlogging the resumption of normal stomatal functioning may occur depending on the plants’ adaptive mechanisms (Pezeshki, 1994). In waterlogging intolerant plants, however, a drastic loss of leaf water content may occur a few days after waterlogging followed by leaf desiccation (e.g., field pea, Jackson and Kowalewska, 1983). This severe loss of water from leaves also coincides with increased leakiness of nutrients and large molecular organic compounds from leaves, suggesting membrane damage (e.g., field pea, Jackson and Kowaleska, 1983). Ion leakage, loss of water, and leaf desiccation under extended waterlogging have been attributed to injurious substances, but the exact nature of such substances is not known (Jackson and Kowalewska, 1983). The rate of photosynthesis may be decreased in response to waterlogging; for example, waterlogging (four alternative cycles of 6 days of waterlogging and 6 days of drainage) decreased average net photosynthesis in cowpea by about 45% relative to that of control plants (Takele and McDavid, 1994). In common bean, rate of photosynthesis was reduced by 17% within 24 hours after waterlogging and reached near zero 7 days after waterlogging (Singh et al., 1991). The reduction in photosynthesis may be due to inhibition of metabolic processes (Pezeshki, 1994) as well as stomatal closure (Younis et a/., 1993). The rate of photosynthesis may recover in waterlogging-tolerant species following the initial reduction, whereas it progressively declines in intolerant species (Pezeshki, 1994).

C. EFFECTSOF WATERLOGGING ON NODULATION AND N, FIXATION Apart from a few studies with field pea and faba bean, relatively little information is available on nodulation and N, fixation in cool season grain legumes in response to Waterlogging. In many instances where the effects of waterlogging on legume growth have been studied, the adverse effects on the performance of symbiosis have not been investigated. The reduced root growth, particularly loss of root hairs under waterlogging, may inevitably reduce nodule initiation (Minchin et al., 1978). In cowpea, waterlogging during early vegetative growth (16 days of waterlogging starting from 8 days after sowing), reduced the nodule dry weight by about 70%, relative to that of plants grown at field capacity (Minchin and Summerfield, 1976). In the absence of 0, supply in field pea, nodulation was completely inhibited and only very small nodules were formed with limited 0, supply (Virtanen and von Hausen, 1936).Nitrogen accumulation in these plants was much lower, and their growth was improved by the supply of chemical N (Virtanen and von Hausen, 1936). A later study with field pea has also shown that accumulation of nitrogen was severely inhibited by waterlogging in plants dependent on N, fixation, but nitrate-fed plants showed relatively smaller reduction in nitrogen accumulation (Minchin and Pate, 1975). These results suggest that nodule formation

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and functioning may be more sensitive than the growth of the host plant to waterlogging. Oxygen is required for bacteriodes in root nodules; thus limited 0, supply may depress N, fixation by inhibiting the energy supply to the bacteroides (Schwinghamer et al., 1970; Trinick et al., 1976).Furthermore, the respiratory quotient (RQ) increases with declining PO,, so that N, fixation is much less efficient in terms of carbohydrate consumed at low 0, tensions (Smith, 1987). In most grain legumes the nitrogenase activity reduces drastically under waterlogging (e.g., faba bean, Sprent, 1972; field pea, Minchin and Pate, 1975; cowpea, Minchin and Summerfield, 1976; soybean, Sung, 1993). In soybean, the imposition of waterlogging either at anthesis or the commencement of seed filling suppressed the nitrogenase activity by more than 60% relative to the controls (Sung, 1993). When a 10-day waterlogging stress at anthesis was removed, nitrogenase activity recovered to some extent, but there was irreversible damage to the nitrogenase system by a 4-day waterlogging stress at seed filling (Sung, 1993).The inhibitory effects of low 0, on N, fixation may arise from (1) restricted supply of ATP and other intermediates from aerobic pathways of carbohydrate metabolism (Sprent, 197I), ( 2 ) direct effects of ethylene (Grobbelaar et al., 1971; Goodlass and Smith, 1979; Smith, 1987), and (3) decreased synthesis of the nitrogenase enzyme (Bisseling et al., 1980). The nodules already formed when waterlogging stress was imposed may exhibit certain adaptive mechanisms to the stress depending on the species. Enhanced production of lenticels and/or aerenchyma, increases in the ratio of uninfected cells to infected cells, and increases in the size of intercellular spaces in both cortex and the infected region are some examples of adaptation shown in root nodules in response to waterlogging (e.g., soybean, Pankhurst and Sprent, 1975; cowpea, Minchin and Summerfield, 1976; faba bean, Gallacher and Sprent, 1978). A substantial enlargement of infected cell vacuoles has been observed in nodules of waterlogged white clover (Pugh et ul., 1995). These enlarged vacuoles push the cell contents outwards toward the cell walls, thus increasing the surface-volume ratio of the protoplast, and this may result in 0, within the intercellular spaces between infected cells becoming more accessible to the bacteroids (Pugh et al., 1995). The presence of bacteriods in the center of anatomically adapted nodules of cowpea, even after 32 days of waterlogging, provides strong evidence of a continued 0, supply to these tissues (Minchin et al., 1978). Nodules with such anatomical adaptations have relatively high nitrogenase activity under waterlogging compared with more compact nodules developed under better aerated conditions (Smith, 1987). In contrast, legumes intolerant to waterlogging exhibit pronounced degeneration of nodules soon after waterlogging (e.g., field pea, Minchin and Pate, 1975; lupin, Farrington eral. 1977).The recovery of symbiosis in these species may well depend on the formation of new nodules after waterlogging is relieved, and may occur at the expense of the recovery of shoot growth (Hong et al., 1977; Minchin et al., 1978).

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D. GENETICVARIATION r~ TOLERANCE TO WATERLOGGING Published results have shown a range of interspecific variation in waterlogging tolerance in different cool season grain legumes, from greatest tolerance of faba bean and L. lureus to intolerance of field pea and lentil. For the selection of cultivars for soils prone to transient waterlogging, it is also useful if intraspecific variation in response to waterlogging can be exploited. Such intraspecific variation in response to waterlogging has been observed in soybean (Hartley et a/., 1993) and cowpea (Takele and David, 1994). Very few studies, however, have explored the intraspecific variation for tolerance to waterlogging within cool season grain legumes. Results from limited studies with chickpea have indicated a substantial variation in the waterlogging tolerance among different cultivars or assessions. Begiga and Anbessa (1995), for example, recorded a large genotypic variation in the ability of 100 chickpea lines to survive a 50-day waterlogging period imposed at 30 days after sowing. Of 100 lines tested about 30 lines were able to survive more than 40 days of waterlogging. Considerable variation in the mortality rate (10-65%) of ten chickpea lines in response to 10 days of waterlogging during the vegetative growth has also been recorded by Cowie et al. (1995). In these studies comparative responses of different genotypes have been made by comparing their growth and development under waterlogged conditions without any attempt to relate the observed differences to physiological parameters. Although these observations are valuable in terms of recognizing the existing variation among different assessions within a species, in view of compounding effects of plant age and other environmental factors, such as soil temperature and organic matter content in the development of waterlogging damage, it would be useful if morphological, anatomical, or physiological parameters associated with the observed responses were identified (Smith, 19887).

VII. CONCLUSIONS Cool season grain legumes are a major source of protein for both humans and animals in many parts of the world. These crops play a key role in sustaining longterm soil fertility in cereal production systems, particularly in temperate, mediterranean, and subtropical environments. With a contribution of more than 50% to the world’s current total pulse production (FAO, 1994), cool season grain legumes already play a major role in world food supply, and this is likely to increase with time. The production and expansion of cool season grain legumes on a worldwide scale are limited by major abiotic stresses such as drought, heat, and cold (Buddenhagen and Richards, 1988; Saxena, 1993), but they are also limited by soil abiotic stresses such as acidity, salinity and sodicity, alkalinity, poor soil structure,

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and waterlogging. Considerable interaction is likely to occur between soil abiotic stresses and drought (and nutrient) stress through effects on root growth. Management practices that reduce the effects of abiotic stresses on cool season grain legumes will play a significant role in overcoming the barriers for increased production and expansion of these crops; however, the selection of species or cultivars better adapted to soil stresses is also likely to have an important role in improving crop growth on marginal soils. The success of both approaches for increasing production of cool season grain legumes, will depend on an improved understanding of physiological and biochemical processes involved in tolerance to these stress conditions. Historically, for cool season grain legumes, a large proportion of research has concentrated on responses to soil salinity, with relatively little research concerning the responses to other soil abiotic stresses. The knowledge base for research on responses of tropical grain legumes to soil stresses such as acidity, alkalinity, soil compaction, and waterlogging has some relevance to improving the understanding of physiological and biochemical aspects of adaptation; however, these responses need to be confirmed for cool season grain legumes. Responses to soil abiotic stresses also need to be tested for a wider range of species and genotypes than have been tested in the past and under uniform experimental conditions. Furthermore, in defining species adaptation to a particular soil condition, results obtained under controlled conditions need to be verified under field conditions. Cool season grain legumes are generally more sensitive to soil abiotic stresses than are cereals, although considerable variation exists among species in their sensitivity. Faba bean, for example, appears relatively better adapted to salinity, alkalinity, and transient waterlogging compared to chickpea and lentil. Field pea also appears relatively more tolerant to salinity and alkalinity than chickpea and lentil but is very sensitive to waterlogging. Lupins are the most well-adapted cool season grain legume to acidic soils, whereas faba bean and field pea are moderately sensitive, and chickpea and lentil are very sensitive to acidity. Considerable variation also exists within species in their response to a given soil stress. In this context also, a large amount of research has considered intraspecific variation in response to soil salinity (particularly with chickpea and lentil), with relatively little research concerning other species or stress factors. In some instances the extent of intraspecific variation appears too narrow (e.g., chickpea for soil salinity) to be of any practical significance in terms of conventional breeding purposes, whereas for others intraspecific variation appears considerable (e.g., lentil for salinity and chickpea and lentil for iron chlorosis). A major limitation of studies looking at intraspecific variation is the limited number of genotypes that have been tested. In only a few instances has a broadscale evaluation of genotypes to a particular stress been undertaken, e.g., chickpea and lentil for iron deficiency (Saxena et al., 1990; Erskine et al., 1993).Thus, the existing intraspecific variation in response to aparticular stress has not been fully explored. Future studies of the intraspecific varia-

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tion in cool season grain legumes should concentrate on defining practical selection criteria that can be used in screening programs. Responses of the legume-(brady)rhizobium symbiosis to soil abiotic stresses have received insufficient attention in the past. The symbiosis appears more sensitive than host plant growth to some stresses, e.g., soil acidity, and this implies that under these conditions the performance of the symbiosis is limiting grain legume growth. In situations where the poor performance of the symbiosis is due to the intolerance of the microsymbiont it may be necessary to select nodule bacterial strains adapted to the abiotic stress. For most grain legume species, however, the symbiosis appears particularly sensitive to soil abiotic stresses at the infection stage. In such situations the selection of host cultivars capable of nodulating under stress conditions may also be an important requirement in the selection of adapted cultivars. There appears to be substantial intraspecific variation in the response of the legume-(brady)rhizobium symbiosis to major soil abiotic stresses in different cool season grain legumes, but this variation has not been fully explored.

ACKNOWLEDGMENTS The authors thank the Grains Research and Development Corporation (Australia) for financial assistance; Mike Perry for valuable discussions throughout the review, and Nancy Longnecker, Miles Dracup, and Tim Setter for constructive comments on the manuscript.

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