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Mineral Nutrition and Yield Response
Mineral Nutrition and Yield Response
6.1
General
Various factors are required for plant growth such as light, CO2, water and mineral nutrients. Increasing the supply of any of these factors from the deficiency range increases the growth rate and yield, although the response diminishes as the supply of the growth factor is increased. This relationship was formulated mathematically for mineral nutrients by MitscherUch as a law of diminishing yield increment (Mitscherlich, 1954; Boguslawski, 1958). According to this formulation, the yield response curves for a particular mineral nutrient are asymptotic; when the supply of one mineral nutrient (or growth factor) is increased, other mineral nutrients (or growth factors) or the genetic potential of crop plants become limiting factors. Typical yield response curves for mineral nutrients are shown in Fig. 6.1. The slopes of the three curves differ. Micronutrients have the steepest and nitrogen the flattest slope, if the nutrient supply is expressed in the same mass units. The slopes reflect the different demands of plants for particular mineral nutrients. It is now established that some of the assumptions made by MitscherHch were incorrect. The slope of the yield response curve for a particular mineral nutrient cannot be described by a constant factor, nor is the curve asymptotic. Also when there is an abundant supply of nutrients, a point of inversion is obtained, as shown for micronutrients in Fig. 6.1. This inversion point also exists for other mineral nutrients such as nitrogen (e.g., in the case of grain yield depression by lodging in cereals) and is caused
C^100 g> 0)
50
> Nutrient supply (e.g., kg ha"^) Fig. 6.1 Yield-response curves for nitrogen, phosphorus, and micronutrients.
185
Mineral Nutrition and Yield Response
3 Grain
\
!
....••••** 5.0 K
i 2 >» ./,'-'
T3
S
1.25 K
1 /
°0
0.25
K \
5
10 15~^ ^0 5 10 15 Nitrogen supply (mM) Fig. 6.2 Effect of increasing nitrogen supply at three potassium levels (HIM) on grain and straw yield of barley grown in water culture. (Reproduced from MacLeod, 1969, by permission of the American Society of Agronomy.) by a number of factors such as the toxicity of a nutrient per se or the induced deficiency of another nutrient. The effects of high nitrogen supply on the phytohormone level and thus on development processes can also be the cause of yield depression. Furthermore, distinct deviations from typical yield response curves (Fig. 6.1) can be obtained when mineral nutrients such as copper are supplied in very low quantities to a severely deficient copper fixing soil. In this case seed set is either prevented or severely inhibited (Section 6.3). An example of the effect of interaction between mineral nutrients on yield is given in Fig. 6.2. At the lowest potassium level, the response to increasing nitrogen supply is small and at high nitrogen supply yield depression is severe. Under field conditions, however, yield depressions caused by excessive nutrient supply are usually less severe. Yield response curves differ between grain and straw, particularly at higher potassium levels (Fig. 6.2). In contrast to the straw yield, the grain yield levels off when the nitrogen supply is high, reflecting sink limitation (e.g., small grain number per ear), sink competition (e.g., enhanced formation of tillers), or source limitation (e.g., mutual shading of leaves). Yield response curves are strongly modulated by interactions between mineral nutrients and other growth factors. Under field conditions the interactions between water availability and nitrogen supply are of particular importance. In maize, for example, with increasing nitrogen supply and different soil moisture levels, the grain yield response curves obtained (Shimshi, 1969) are similar to those shown for different potassium levels (Fig. 6.2). The depressions in yield that accompany a large supply of nitrogen in combination with low soil moisture levels are presumably caused by several factors such as (a) delay in stomatal response to water deficiency (Chapter 5), (b) the higher water consumption of vegetative biomass and the correspondingly higher risk of drought stress in critical periods of grain formation, and (c) increase in shoot-root dry weight ratio with increasing nitrogen supply (Section 8.2.5), an effect which seems to be more prominent in C3 than in C4 plant species (Hocking and Meyer, 1991). Yield response curves can differ not only between vegetative and reproductive organs (Fig. 6.2) but also between the yield components of harvested products. In most
186
Mineral Nutrition of Higlier Plants
1
f
1
—
—
^ , /-
—
—
•-•••
---
0)
>
Fertilizer supply
Fig. 6.3 Schematic representation of yield response curves of harvested products. Key: , quantitative yield (e.g., dry matter per hectare); , qualitative yield (e.g., content of sugar, protein, and mineral elements; for examples (1) to (3) see following text). crops, both quantity (e.g., dry matter yield in tons per hectare) and quality (e.g., content of sugars or protein) are important yield components. As shown schematically in Fig. 6.3 maximum quality can be obtained either before [curve(l)] or after [curve(2)] the maximum dry matter yield has been reached, or both yield components can have a synchronous pattern [curve(3)]. Examples of the behaviour described by curve (1) are nitrate accumulation in spinach and sucrose accumulation in sugar beet with increasing levels of nitrogen fertilizer. Examples of curve (2) are the change in protein content of cereals, grains of forage plants with increasing supply of nitrogen fertilizer, or the change in content of certain mineral elements with increasing mineral nutrient supply, for example, magnesium and sodium in forage plants, or zinc and iron in cereal grains for human consumption. Examples of curve (3) are common under conditions where with increase in mineral nutrient supply the number of either reproductive sinks (e.g. grains) or vegetative storage sinks (e.g. tubers) is increased. 6.2
Leaf Area Index and Net Photosynthesis
Positive yield response curves are the result of different individual processes, such as an increase in leaf area and net photosynthesis per unit leaf area (i.e., effects at the source) or an increase in fruit and seed number (i.e., effects at the sink). In this section the main emphasis is put on processes that primarily affect the source site, although feedback regulation from the sink sites are often involved, and may even dominate the source processes. Generally, the density of a crop population is expressed in terms of the leaf area index (LAI), which is defined as the leaf area of plants per unit area of soil. For example, an LAI of 5 means that there is a 5 m^ leaf area of plants growing on a soil area of 1 m^. As a rule the crop yield increases until an optimal value in the range of 3-6 is reached, the exact value depending on plant species, light intensity, leaf shape, leaf angle and other factors. At a high LAI, mutual shading usually becomes the main limiting factor. When the water supply is limited, however, drought stress and corresponding negative effects, particularly at the sink sites (Section 6.3), can decrease the optimal LAI to values far below those resulting from mutual shading.
Mineral Nutrition and Yield Response
187
Table 6.1 Inhibition of Leaf Growth by Nitrogen Deficiency in Different Plant Species'" Average growth inhibition (%) Plant species Cereals (wheat, barley, maize, sorghum) Dicotyledons (sunflower, cotton, soybean, radish)
Day 16 53
Night 18 8
''Based on Radin (1983).
When the nutrient supply is suboptimal, the leaf growth rate, and thus the LAI, can be limited by low rates of net photosynthesis or insufficient cell expansion or both these factors. This is particularly evident with suboptimal supply of nitrogen and phosphorus. In plants suffering from nitrogen deficiency, elongation rates of leaves may decline before there is any reduction in net photosynthesis (Chapin et al., 1988), this decline being the result of decrease in both number and duration of extension of epidermal cells (MacAdam et al., 1989). Besides hormonal effects (Section 5.6) a decrease in root hydraulic conductivity might be involved, leading to a decrease in water availability in expanding leaf blades (Radin and Boyer, 1982). The effect of nitrogen deficiency on leaf expansion differs between plant species (Table 6.1). In cereals (monocotyledons) cell expansion is inhibited to the same extent during the day and night. In dicotyledons, however, the inhibition is much more severe during the daytime. This difference in response is related to morphological differences among species and corresponding differences in competition for the water available for transpiration and for cell expansion. In dicotyledons, cell expansion occurs in leaf blades which are exposed to the atmosphere and therefore experience a high rate of transpiration during the daytime. In cereals, however, cell expansion occurs at the base of the leaf blade. This zone is protected from the atmosphere by the sheath of the preceding leaf, so that little transpiration occurs from this zone of elongation. In contrast to leaf expansion, net photosynthesis per unit leaf area is depressed to a similar extent in both groups of plants by nitrogen deficiency. Similar results to those shown in Table 6.1 for the nitrogen effect in dicotyledons have been obtained for phosphorus in cotton plants (Radin and Eidenbock, 1984). It was found that phosphorus deficiency severely inhibited leaf growth rate only during the daytime, and had very Uttle effect at night. These day/night differences were primarily a response to limited water availability for cell expansion during the daytime, caused by low hydraulic conductance of the root system as a result of phosphorus deficiency. The small size and often dark-green color of the leaf blades in phosphorus deficient plants are the result of impaired cell expansion and a correspondingly larger number of cells per unit surface area (Hecht-Buchholz, 1967). In addition, particularly in dicots the number of leaves might be reduced through a lower number of nodes branching (Lynch et al., 1991). However, in many instances, a transient deficiency of phosphorus or nitrogen during the early growth of cereals or maize might reduce final yield not as a consequence of smaller leaf area but as the result of a lower number of spikelets per ear or grains per cob (Romer and Schilling, 1986; Barry and Miller, 1989).
188
Mineral Nutrition of Higlier Plants
(0 (Ov
20
2 ^ -C^, 4 ^ (M
i.E (0 T3
^o"io o ® E
20 30 40 Light intensity (klx) Fig. 6.4 Photosynthetic light response curves of a mature sugar beet leaf 1, 4, 7, 9 and 12 days after the plant was transferred to nitrogen-free nutrient solution. (Reproduced from Nevins and Loomis, 1970, by permission of the Crop Science Society of America.) Mineral nutrient deficiency can also delay plant development. For example, in barley the number of days to reach the booting stage is about twice as much for manganesedeficient as for manganese-sufficient plants (Longnecker et aL, 1991b). Mineral nutrition can also influence net photosynthesis in various ways (Natr, 1975; Barker, 1979). The direct involvement of some mineral nutrients in the electron transport chain in the thylakoid membranes, in detoxification of oxygen free radicals and in photophosphorylation has been summarized in Fig. 5.1 and discussed in Sections 5.2.1 and 5.2.2. Mineral nutrients are also required for chloroplast formation, either for synthesis of proteins, thylakoid membranes or chloroplast pigments. In green leaf cells, for example, up to 75% of the total organic nitrogen is located in the chloroplasts, mainly as enzyme protein. A deficiency of mineral nutrients that are directly involved in synthesis of protein or chloroplast pigments or electron transfer therefore results in the formation of chloroplasts with lower photosynthetic efficiency (Spencer and Possingham, 1960), and also in a change in the fine structure of chloroplasts in a more or less specific manner (Hecht-Buchholz, 1972). In leaves of spinach about 24% of the total nitrogen is allocated to thylakoid membranes; nitrogen nutrition therefore also affects the amount of thylakoids per unit leaf area (Terashima and Evans, 1988). A mineral nutrient deficiency can also depress net photosynthesis by influencing the CO2 fixation reaction and entry of CO2 through the stomata. Finally, starch synthesis in the chloroplasts and transport of sugars across the chloroplast envelope into the cytoplasm are directly controlled by the concentration of inorganic phosphate (Heldt et al., 1977). These functions of mineral nutrients in photosynthesis are discussed in more detail in Chapters 8 and 9. In the range between suboptimal and optimal nutrient supply, close positive correlations are often observed between mineral nutrient content of leaves and the rate of net photosynthesis (Natr, 1975). In principle, these correlations can also be indirectly demonstrated in mature leaf blades when the root supply of mineral nutrients such as nitrogen is withheld (Fig. 6.4). As nitrogen becomes increasingly deficient, the light response curve of net photosynthesis in the mature leaf declines to low levels (Fig. 6.4), and an increasing proportion of
Mineral Nutrition and Yield Response
^89
Table 6.2 Effect of Zinc Deficiency and Light Intensity on Shoot Growth and Content of Chlorophyll and Carbohydrates in Primary Leaves of Bean (Phaseolus vulgarisY Carbohydrates (mg glucose equiv. g~^ dry wt) Shoot dry wt. (g per plant)
Chlorophyll (mg g~Mry wt.)
Light intensity (/^Em'^s-i)
+Zn
-Zn
+Zn
-Zn
80 230 490
L24
1.13 1.13 1.16
19.2 16.6 11.2
17.3
2.38 3.80
7.8 4.5
Sucrose ~~~ +Zn -Zn 10 11 17
11 54 82
Total +Zn
-Zn
40 42 77
42 124 138
''Based on Marschner and Cakmak (1989). ^Sucrose, reducing sugars, starch.
the absorbed light energy which is not used in photochemical reactions is dissipated as heat (Demming and Winter, 1988). Nevertheless, the photosynthetic efficiency per unit chlorophyll can even increase under nitrogen deficiency (Khamis et al., 1990b), presumably reflecting a response to decrease in source-sink ratio. In contrast, in manganese-deficient leaves the photosynthetic efficiency per unit chlorophyll is drastically decreased and can be restored within two days after foliar application of manganese, indicating a direct effect on photosystem II (Fig. 5.1) rather than an indirect effect via source-sink relationships (Kriedemann et al., 1985). Similar changes in the light response curves shown for nitrogen deficiency (Fig. 6.4) are also found under phosphorus deficiency (Lauer et al., 1989a), and deficiency of a range of other mineral nutrients. In many instances in the deficient plants, however, despite poor utilization of higher light intensities, carbohydrates accumulate in leaves (Grabau et al. 1986a; Rao et al., 1990) and also in roots (Khamis et al., 1990a) of phosphorus-deficient plants. Thus, low photosynthetic efficiency of source leaves might often be the result of feedback regulation induced by a lower demand for photosynthates at the sink sites. An example for this is shown for zinc-deficiency in Table 6.2, With increasing light intensity plant dry weight increases in the zinc-sufficient plants but not in the zinc-deficient plants (Table 6.2). Although chlorophyll content drastically declines with increasing Ught intensities, particularly in the zinc deficient plants the carbohydrate content increases steeply, indicating that the lack of growth response to increasing light intensities reflects a sink and not source limitation. Accumulation of photosynthates under high light intensity in source leaves of deficient plants not only decreases utilization of light energy but also poses a stress. This high light stress is indicated, for example, by an increase in the antioxidative defense mechanisms in the deficient leaves (Cakmak and Marschner, 1992; Fig. 5.2), photooxidation of chloroplast pigments (Table 6.2) and enhanced leaf senescence. These side effects of mineral nutrient deficiency decrease not only current photosynthesis and LAI but also leaf area duration (LAD), that is the length of time in which the source leaves supply photosynthates to sink sites, an aspect that is discussed in Section 6.4.
190
6.3 6.3.1
Mineral Nutrition of Higher Plants
Mineral Nutrient Supply, Sink Formation, and Sink Activity General
In crop species where fruits, seeds, and tubers represent the yield, the effects of mineral nutrient supply on yield response curves are often a reflection of sink Umitations, imposed by either a deficiency or an excessive supply of mineral nutrients during certain critical periods of plant development, including flower induction, pollination, and tuber initiation. These effects can be either direct (as in the case of nutrient deficiency) or indirect (e.g., effects on the levels of photosynthates or phytohormones). 6.3.2
Flower Initiation
In apple trees, flower formation is affected to a much greater extent by the time or form of nitrogen application or both these factors than by the level of nitrogen supply. Compared with a continuous nitrate supply a short-term supply of ammonium to the roots was found to more than double both the percentage of buds developing inflorescences and the arginine content in the stem (Table 6.3). Arginine is a precursor of polyamines which also accumulate particularly in leaves of plants supplied with high levels of ammonium (Gerendas and Sattelmacher, 1990). The causal involvement of polyamines in the ammonium-induced enhanced development of inflorescences in apple trees is indicated by the similar effects obtained by infiltrating polyamines into the petioles (Table 6.3). These results on the flowerinducing effects of ammonium supply confirm earlier results of Grasmanis and Edwards (1974). Since the apple trees in this study were amply supplied with nitrogen throughout the growing season, it is unlikely that these effects on flower initiation (i.e. on developmental processes) are related to a general nutritional role of nitrogen. It appears more probable that some nitrogen compounds such as polyamines may function as second messenger in flower initiation (Section 5.6.3). Table 6.3 Effect of Ammonium-N or Polyamines on Flower Initiation and Arginine Content in Apple Trees'"
Treatment Control, nitrate continuously NH4-N for 24 h^ NH4-N for 1 week Putrescine"^ Spermine*^ NH4-N for 24h^ ""Based on Rohozinski et al. (1986). ^8 mM N H ^ in the nutrient solution. ^8 mM petiole infiltration.
Percentage flowering
Stem arginine content (i"gg~^ dry wt)
15 37 40 51 47 50
1120 2570 2330 — — —
Mineral Nutrition and Yield Response
191
Table 6.4 Shoot Growth, Flower Induction and CYT in Xylem Exudate of Apple Root Stock M7 as Affected by the Form of Nitrogen Supply" Form of Shoot length N-supply (cm) NOs-N NH4NO3 NH4-N
No. lateral CYT_ shoots Flowering buds (nmol (100 g) ^ shoot (spurs) (% of emerged) fresh wt)
326 268 209
6.4 6.0 8.9
7.4 8.2 20.7
0.002 0.373 0.830
'Based on Gao et al. (1992). Most probably, changes in the phytohormone level in general and of CYT in particular are involved in this enhancing effect of ammonium supply on flowering (Buban et ah, 1978). In apple root stocks, ammonium supply as compared with nitrate, not only increased flower bud formation but also CYT concentration in the xylem exudate and the number of flower-bearing lateral branches (spurs), whereas the total shoot length was depressed (Table 6.4). Promotion offlowermorphogenesis by CYT is weU documented for various other plant species (Bruinsma, 1977; Herzog, 1981). Flower formation in apple trees (Bould and Parfitt, 1973), tomato (Menary and Van Staden, 1976), and wheat (Rahman and Wilson, 1977) is also positively correlated with phosphorus supply. The positive correlations between the number offlowersand CYT level in tomato (Menary and Van Staden, 1976), on the one hand, and between the phosphorus supply and the CYT level on the other (Horgan and Wareing, 1980), provide additional evidence that CYT also contributes to the enhancing effect of phosphorus on flower formation. Basically similar conclusions were drawn from the effects of potassium on flower formation in Solarium sisymbrifolium (Wakhloo, 1975a,b). Low potassium levels in the leaves were correlated with a high proportion of sterile female flowers. This sterility did not occur in plants of either high or low potassium status when the plants had been sprayed with CYT. These various results strongly confirm the supposition that the effects of mineral nutrient supply on flower formation are brought about by changes in phytohormone level. This is also true for the beneficial effects of nitrogen fertilizer appUcation before anthesis in increasing grain number per ear in wheat (Herzog, 1981) or seed number per plant in sunflower (Steer et al., 1984). However, seed number per plant can also be increased by high concentrations of sucrose prior to flower initiation (Waters et al., 1984), high light intensity (Stockman et al,, 1983) or stem injection of sucrose under drought stress conditions (Boyle et al., 1991; Section 5.7). The possibility can not be ignored, therefore, that mineral nutritional status may also affect flower initiation and seed set by increasing the supply of photosynthates during critical periods of the reproductive phase. 6.3.3
Pollination and Seed Development
The number of seeds or fruits or both per plant can also be directly affected by mineral nutrient supply. This is clearly the case with various micronutrients. In cereals in
192
Mineral Nutrition of Higher Plants
Table 6.5 Effect of Increasing Copper Supply in Wheat (cv. Chatilerma) Grown on Copper-Deficient SoiP Copper supply (mg per pot)
Number of tillers Straw yield (g) Grain yield (g)
0
0.1
0.4
2.0
22 7.7 0.0
15 9.0 0.5
13 10.3 3.5
10 10.9 11.8
''Total number of plants per pot: 4. Based on Nambiar (1976c).
particular, copper deficiency affects the reproductive phase (Table 6.5). The critical period in copper-deficient plants is the early booting stage at the onset of pollen formation (microsporogenesis). When the copper deficiency is severe, no grains are produced even though the straw yield is quite high owing to enhanced tiller formation (loss of apical dominance of the main stem). As the copper supply is increased, grain yield rises sharply, whereas the straw yield is only sHghtly enhanced. These results provide an informative example of both sink limitation on yield and deviation from the typical response curve (Fig. 6.1) between grain yield and mineral nutrient supply. Under field conditions, in copper deficient soils, especially when the top soil is dry, copper application to the soil is often much less effective than foliar application at the early vegetative growth stage in increasing the grain yield (Section 4.3). The primary causes of failure in grain set in copper-deficient plants are inhibition of anther formation, the production of a much smaller number of pollen grains per anther, and particularly the nonviability of the pollen (Graham, 1975), in part because of lack of supply of carbohydrates to the developing pollen grains (Jewell et al., 1988). In principle, similar results as those found for copper deficiency (Table 6.5) are obtained with zinc or manganese deficiency. In maize, zinc deficiency prior to microsporogenesis (—35 days after germination) did not significantly affect vegetative growth and ovule fertility but decreased pollen viability and cob dry weight by about 75% (Sharma et al., 1990). Also under manganese deficiency vegetative growth of maize is much less depressed than grain yield (Table 6.6). In the deficient plants anther
Table 6.6 Effect of Manganese ]Deficiency on Growth, Fertilization and Grain Yield in Maize"
(/^gr^)
Shoot dry wt. (g per plant)
Grain wt (g per plan t)
Single grain wt (mg)
Pollen (no. per anther)
Pollen germination (%)
550 5.5
82.5 57.8
69.3 11.8
302 358
2770 1060
85.6 9.4
Mn supply
'^Sharma et al. (1991). Reprinted by permission of Kluwer Academic Publishers.
193
Mineral Nutrition and Yield Response
250 f S 200
Grain
Q.
3 150
*- Silks + cob sheaths ^ Stalk + leaves
I 100 Q
50 0.5
1.0 2.0 5.0 10.0 20.0 Boron supply (mg planf^) Fig. 6.5 Effect of boron supply on the production and distribution of dry matter in maize plants. (Based on Vaughan, 1977.)
development is delayed and fewer and smaller pollen grains are produced with very low germination rates. In contrast, ovule fertility was not significantly affected by manganese deficiency (Sharma et al., 1991), a result, which is in agreement with the effect of copper deficiency in wheat (Graham, 1975). The production and viability of pollen are also affected by molybdenum. In maize, a decrease in the molybdenum content of pollen was correlated with a decrease in the number of pollen grains per anther as well as a decrease in the size and viability of the pollen grains (Section 9.6). As yet no information is available as to the extent to which molybdenum deficiency also depresses fertilization and grain set. However, it is well documented that preharvest sprouting in maize (Section 9.6) and wheat (Cairns and Kritzinger, 1992), causing severe yield losses in certain areas, is very high in seeds with low molybdenum content and can be effectively decreased by molybdenum supply to the soil or as a foUar spray. Boron is another mineral nutrient that affects fertilization. Boron is essential for pollen tube growth (Section 9.7), a role reflected under conditions of boron deficiency by a decrease in the number of grains per head in rice (Garg et al., 1979) or even a total lack of fertilization in barley and rice (Ambak and Tadano, 1991). The failure of seed formation in maize suffering from boron deficiency is caused by the nonreceptiveness of the silks to the pollen (Vaughan, 1977). As the level of boron nutrition increases, vegetative growth, including the structural growth of the silks, is either not affected or is even somewhat depressed (Fig. 6.5). In contrast, grain formation is absent in severely deficient plants but increases dramatically when the boron supply is adequate. Obviously there is a minimum boron requirement, which is in the range of 3 mg boron per maize plant for fertilization and grain set. Figure 6.5 provides another example of both a strict sink limitation induced by mineral nutrient deficiency and a yield response curve quite different from the typical curve. Low boron supply not only inhibits flowering and seed development but may also produce seeds with low boron content in plants even without visual symptoms of boron
194
Mineral Nutrition of Higher Plants
Table 6.7 Effect of Potassium Supply to Wheat on ABA Content and Weight of Grains'" ABA content (ng per grain) days after anthesis K Supply
28
35
38
44
Days from anthesis to full ripening
Low (deficient) High
7.7 3.7
13.4 4.4
16.5 ND^
2.2 9.4
46 75
Weight of a single grain (mg) 16.0 34.4
''Based on Haeder and Beringer (1981). ^ND, Not determined.
deficiency. These low boron seeds have a low germination rate and produce a high percentage of abnormal seedlings (Bell etal, 1989). In lowland rice, grain yield might be considerably decreased by spikelet sterility induced by low temperatures (below 20°C) during anthesis. This temperature sensitivity can be drastically decreased by high supply of potassium (Haque, 1988). Increasing potassium contents in the panicles from 0.61% to 2.36% in the dry matter decreased spikelet sterihty after three days at 15°C from 75% to 11%. The reasons for this protecting effect of potassium are not known, high nitrogen contents in the low potassium plants are probably involved (Haque, 1988). In certain plant species, such as soybean, drop of flowers and developing pods is a major yield-Umiting factor. Nitrogen or phosphorus deficiency during the flowering period enhances flower and pod drop and depresses seed yield correspondingly (Streeter, 1978; Lauer and Blevins, 1989). Supplying ample amounts of nitrogen or phosphorus during this critical phase is therefore quite effective in reducing flower and pod drop and in increasing final seed yield in soybean (Brevedan et al., 1978; Lauer and Blevins, 1989). Although the physiological reasons for both the flower and pod drop and the decline in drop produced by nitrogen application are not yet known in detail, it is certain that phytohormones, especially CYT and ABA, are involved. An ample nitrogen supply both increases CYT and decreases ABA (Section 5.6.4) and hence decreases flower and pod drop, as would be expected from the specific role of ABA in the formation of abscission layers. Accordingly, maize kernel abortion can be reduced by either foHar application of CYT or supplying the roots with ammonium-N (Smiciklas and Below, 1992), the latter treatment being particularly effective in increasing the CYT contents in the plants (Table 6.4). Premature ripening of fruits and seeds imposed by water or nutrient deficiency is another yield-Hmiting factor. In this case it is not the number of grains but the weight (size) of a single grain or fruit that is low. There is substantial evidence that elevated ABA levels are also involved in premature ripening. An example of this is shown in Table 6.7 for potassium-deficient wheat plants. In these plants, and particularly 4-6 weeks after anthesis, the levels of ABA in the grains are much higher than those in the grains of plants well supplied with potassium. Correspondingly, the grain-filling period in potassium-deficient plants is much shorter and the weight of a single grain at maturity is lower than that in control plants. As has been shown before (Section 5.6.5), high
Mineral Nutrition and Yield Response
195
ABA levels in grains coincide with a sharp decline in the sink activity of grains. It is quite Ukely that the elevated ABA levels in the flag leaves of potassium-deficient wheat plants (Haeder and Beringer, 1981), and a correspondingly higher ABA import to the developing grains, are responsible for the premature ripening and not the source limitation of a mineral nutrient per se (Section 6.4). 6.3.4
Tuberization and Tuber Growth Rate
In root and tuber crops such as sugar beet or potato, the induction and growth rate of the storage organ are strongly influenced by the environmental factors. In contrast to crop species in which seeds and fruits are the main storage sinks, root and tuber crops often exhibit a distinct sink competition between vegetative shoot growth and storage tissue growth for fairly long periods after the onset of storage growth. This competition is particularly evident in so-called indeterminate genotypes of crop species, for example, in potato (Kleinkopf et al., 1981). In general, environmental factors (e.g., high nitrogen supply) with pronounced favorable effects on vegetative shoot growth delay the initiation of the storage process and decrease growth rate and photosynthate accumulation in storage organs - for example, of sugar beet (Forster, 1970) and potato (Ivins and Bremner, 1964; Gunasena and Harris, 1971). A large and continuous supply of nitrogen to the roots of potatoes delays or even prevents tuberization (Krauss and Marschner, 1971). After tuberization the tuber growth rate is also drastically reduced by high nitrogen supply, whereas the growth rate of the vegetative shoot is enhanced. The effect of nitrogen supply on tuber growth rate is illustrated in Table 6.8. Resumption of the tuber growth rate to normal levels after interruption of the nitrogen supply indicates that sink competition between the vegetative shoot and tubers can readily be manipulated by means of the nitrogen supply. In potato, cessation of tuber growth caused by a sudden increase in nitrogen supply to the roots induces 'regrowth' of the tubers, that is, the formation of stolons on the tuber apex (Krauss and Marschner, 1976, 1982). Interruption and resupply of nitrogen, therefore, can result in the production of chain-Uke tubers or so-called secondary growth (Fig. 6.6). After a temporary cessation of growth, resumption of the normal
Table 6.8 Growth Rate of Potato Tubers in Relation to Nitrate Supply to the Roots of Potato Plants^ Nitrate concentration (mn)
Nitrate uptake (meq per day per plant)
Tubei • growth rate (cm^ pel• day per plant)
1.18 2.10 6.04 —
3.24 4.06 0.44 3.89
1.5 3.5 7.0 Nitrogen supply withheld for 6 days ''From Krauss and Marschner (1971).
196
Mineral Nutrition of Higher Plants
Fig. 6.6 Secondary growth and malformation of potato tubers induced by alternating high and low nitrogen supply to the roots. (Krauss, 1980.) growth rate is usually restricted to a certain area of the tubers (meristems or 'eyes'), leading to typical malformations and knobby tubers, which are often observed under field conditions after transient drought periods. Similar effects on cessation of tuber growth and 'regrowth' can be achieved by exposing growing tubers to high temperatures, which instantly inhibit starch synthesis and lead to the accumulation of sugars in the tubers (Krauss and Marschner, 1984; Van den Berg et al., 1991), followed by a decrease in ABA levels in the tubers and 'regrowth'. The effects of nitrogen supply on tuber growth rate and 'regrowth' are brought about by nitrogen-induced changes in the phytohormone balance both in the vegetative shoots and in the tubers. As already shown (Section 5.6.4), an interruption of the nitrogen supply results in a decrease both in CYT export from roots to shoots and in the sink strength and growth rate of the vegetative shoot. A corresponding increase in the ABA/GA ratio of the shoots seems to trigger tuberization. In agreement with this, tuberization can also be induced by the application of either ABA or the GA antagonist CCC (Krauss and Marschner, 1976) or by the removal of the shoot apices, the main sites of GA synthesis (Hammes and Beyers, 1973). On the other hand, after cessation of growth the regrowth of tubers induced by a sudden increase in the nitrogen supply is correlated with a decrease in the ABA/GA ratio not only in the vegetative shoots but also in the tubers, where the GA level increases by a factor of 2 but the ABA level drops to less than 5% of that in normal growing tubers (Krauss, 1978b).
6.4
Mineral Nutrition and the Sini(-Source Relationships
In root and tuber crops, unUke grain crops, the sink-source relationship is quite labile even after the onset of the storage process. This has to be considered, for example, in the application of nitrogen fertilizer to potato. On the one hand, a high nitrogen supply is important for rapid leaf expansion and for obtaining an LAI between 4 and 6, a value considered necessary for high tuber yields (Kleinkopf et al., 1981; Dwelle et al., 1981). On the other hand, a high supply of nitrogen delays either tuberization or the onset of the linear phase of tuber growth. The principles of these interactions are demonstrated in Fig. 6.7. The advantage of earlier tuberization obtained by supplying a low level of nitrogen is offset by a low LAI and earUer leaf senescence, that is a short LAD and a
197
Mineral Nutrition and Yield Response l^yi
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75 100 125 Days after planting Fig. 6.7 Time course of leaf area index and fresh weight of potato tubers at two levels of nitrogen supply. (Based on Ivins and Bremner, 1964, and Kleinkopf et al., 1981.) correspondingly lower tuber yield. When the nitrogen supply is high, both LAI and LAD, and thus final tuber yield, are much higher. However, higher tuber yield induced by a large nitrogen supply can be realized only when the vegetation period is sufficiently long, that is, in the absence of early frost (Clutterbuck and Simpson, 1978) or in the absence of severe drought stress. The early decHne in LAI when the supply of nitrogen is low (Fig. 6.7) indicates that the final tuber yield is limited by the source. The question arises as to the reasons for this source limitation. In potato plants at maturity, between 60% and 80% of the total nitrogen is located in the tubers (Kleinkopf et al., 1981). Therefore, when the nitrogen supply is low, exhaustion of nitrogen in the source leaves presumably plays a key role in leaf senescence and in the termination of tuber growth. However, these simple relationships between nitrogen supply, LAI, LAD and tuber yield (Fig. 6.7) are not only modified by the length of the growing period but also the mineralization rate of soil nitrogen and temperature during tuber growth. At high nitrogen supply and high LAI, mutual shading of the basal leaves may not only drastically decrease their net photosynthesis but also the LAD by rapid leaf senescence (Firman and Allen, 1988), a process which is further enhanced at high ambient temperatures (Manrique and Bartholomew, 1991). Thus, a lower, but more continuous supply of nitrogen which allows an earlier tuberization and continuous root growth and CYT production, and which is more effective on LAD than on LAI, might often lead to higher tuber yields than a rapid establishment of a high LAI by high nitrogen supply during early growth. Interestingly, an increase in LAD is one of the major characteristics of the new, high-yielding varieties in maize and wheat developed during the last 30 years (Austin, 1989; Tollenaar, 1991). Competition for nitrogen rather than for carbohydrates supplied from the source leaves can also be the main limiting factor for seed yield in mustard and rape plants (Trobisch and Schilling, 1969; Schilling and Trobisch, 1970). In mustard plants the developing seeds and leaves compete for nitrogen, and seed set, seed growth, and final seed yield are determined primarily by the size of the nitrogen pool in the vegetative parts. In crucifers, the flower differentiation at the auxiliary stems occurs after the onset
198
Mineral Nutrition of Higher Plants
Control
0.9
1.9 (g N pot')
Nitrogen addition
Fig. 6.8 Effect of addition of 0.9 and 1.9 g nitrogen at the onset offloweringon total dry weight and dry weight distribution in shoots of white mustard plants. (Based on Trobisch and Schilling, 1970.)
offloweringof the main stem and is strongly dependent on the availability of nitrogen during this period. Additional application of nitrogen at the onset of flowering therefore leads to an increase in seed number and yield (Fig. 6.8). The example with mustard plants in Fig. 6.8 demonstrates that source limitation can be imposed by nitrogen rather than carbohydrates. This aspect has also to be considered in source-sink manipulations. Removing source leaves from a plant is a common procedure for evaluating source limitation in photosynthesis (Section 5.7). Of course, when source leaves are removed, nitrogen and other mineral nutrients are also removed. Therefore, shading of source leaves may have a different effect on the reduction of seed yield from that of leaf removal. Shading the source leaves of mustard plants reduced the seed yield by only 20%, whereas removal of these same leaves reduced the seed yield by 50% (Trobisch and Schilling, 1969). In plant species like mustard and rape, mutual shading of source leaves is usually much less detrimental on yield than, for example, in cereals and tuber crops, as in the crucifers after the onset of flowering the stems and pods provide a high proportion of the photosynthates required in the developing seeds (Section 5.7.1). In principle, each of the mineral nutrients can become the dominant factor inducing source limitation onfinalyield of seeds, fruits and tubers, provided that it can be readily retranslocated from the source (Section 3.5). Whether such a limitation exists depends on such factors as the availabihty of the given nutrient in the soil, its concentration and amount (source size) in the vegetative shoot, the specific demand of the sink for the nutrient, and the growth rate of the sink. For example, in fleshy fruits or tubers, the potassium content is very high (2-3% of the dry weight), and at maturity most of the potassium is located in the fruits or tubers. Potassium-induced source Hmitation is therefore more Ukely in this type of crop. An example of this has been given in Section 5.7 for tomato genotypes. In contrast, in mature cereal plants, as much as 80% of the total amount of nitrogen or phosphorus is located in the grains, compared with less than 20% of the total potassium (see also Section 3.5.4). Thus, in cereal plants where there is a suboptimal supply of the three mineral nutrients during the vegetative stage, source limitation during grainfillingis most likely induced by nitrogen or phosphorus, but not
Mineral Nutrition and Yield Response
199
A
10 20 30 40 50 60 70 80 Days after anthesis Fig. 6,9 Time course of chlorophyll content inflagleaf and dry weight accumulation in spikelet grains of phosphorus-sufficient (•, A) and phosphorus-deficient (O, A) wheat plants. (Modified from Batten and Wardlaw, 1987a.)
by potassium. The importance of export of mineral nutrients to developing seeds for senescence of source leaves has been discussed in Section 5.7. In soybean, for example, enhanced leaf senescence and also premature pod drop could be counteracted not only by an increase in phosphorus supply to the roots but also by stem infusion of phosphorus (Grabau et al., 1986a), indicating that in this case phosphorus deficiency limited seed yield by decreasing LAD. In moderately phosphorus-deficient cereal plants source limitation may also become the dominant factor for grain yield. In wheat these relationships are particularly prominent for the flag leaf blade which may deliver between 5 1 % and 89% of the phosphorus found in the grains at harvest (Batten et al., 1986). As shown in Fig. 6.9, in phosphorus-deficient plants the flag leaf senesced rapidly and its photosynthetic activity approached zero by the time the grains were only 60% of their final potential dry weight, leading to a reduction in final grain yield by 40% and in phosphorus content by 75%. The results shown in Fig. 6.9 reflect source Umitation of either phosphorus or photosynthates. Evidence against limitation by photosynthates had been presented by additional experiments where shading of ears increased the rate of net photosynthesis severalfold in the deficient flag leaf and also substantially delayed its senescence (Chapin and Wardlaw, 1988). In contrast, in the phosphorus-sufficient plants shading of the ear was without significant effects on flag leaf net photosynthesis. Thus, enhanced leaf senescence in the phosphorus-deficient plants is most likely caused by accumulation of photosynthates in the flag leaf and a subsequent photooxidation of the chloroplast
200
Mineral Nutrition of Higher Plants
pigments and destruction of membranes (Section 5.2.2) which, in turn, enhances remobihzation and re translocation of phosphorus from source to sink. These examples illustrate the role of mineral nutrients as yield-limiting factors when fruits, seeds, or other organs are the dominant sink sites and mineral nutrient uptake by the roots is declining. Progress in selecting and breeding for genotypes with a high harvest index (ratio of economic yield to total dry matter) and short periods of fruit growth or ripening (e.g., thefillingperiod in cereals) might be severely restricted, not because of the limited capacity of the source to supply carbohydrates, but rather because of the limited amount of mineral nutrients such as potassium, nitrogen, phosphorus, and magnesium that are available for retranslocation from source to sink.
6.1
General
Various factors are required for plant growth such as light, CO2, water and mineral nutrients. Increasing the supply of any of these factors from the deficiency range increases the growth rate and yield, although the response diminishes as the supply of the growth factor is increased. This relationship was formulated mathematically for mineral nutrients by MitscherUch as a law of diminishing yield increment (Mitscherlich, 1954; Boguslawski, 1958). According to this formulation, the yield response curves for a particular mineral nutrient are asymptotic; when the supply of one mineral nutrient (or growth factor) is increased, other mineral nutrients (or growth factors) or the genetic potential of crop plants become limiting factors. Typical yield response curves for mineral nutrients are shown in Fig. 6.1. The slopes of the three curves differ. Micronutrients have the steepest and nitrogen the flattest slope, if the nutrient supply is expressed in the same mass units. The slopes reflect the different demands of plants for particular mineral nutrients. It is now established that some of the assumptions made by MitscherHch were incorrect. The slope of the yield response curve for a particular mineral nutrient cannot be described by a constant factor, nor is the curve asymptotic. Also when there is an abundant supply of nutrients, a point of inversion is obtained, as shown for micronutrients in Fig. 6.1. This inversion point also exists for other mineral nutrients such as nitrogen (e.g., in the case of grain yield depression by lodging in cereals) and is caused
C^100 g> 0)
50
> Nutrient supply (e.g., kg ha"^) Fig. 6.1 Yield-response curves for nitrogen, phosphorus, and micronutrients.
185
Mineral Nutrition and Yield Response
3 Grain
\
!
....••••** 5.0 K
i 2 >» ./,'-'
T3
S
1.25 K
1 /
°0
0.25
K \
5
10 15~^ ^0 5 10 15 Nitrogen supply (mM) Fig. 6.2 Effect of increasing nitrogen supply at three potassium levels (HIM) on grain and straw yield of barley grown in water culture. (Reproduced from MacLeod, 1969, by permission of the American Society of Agronomy.) by a number of factors such as the toxicity of a nutrient per se or the induced deficiency of another nutrient. The effects of high nitrogen supply on the phytohormone level and thus on development processes can also be the cause of yield depression. Furthermore, distinct deviations from typical yield response curves (Fig. 6.1) can be obtained when mineral nutrients such as copper are supplied in very low quantities to a severely deficient copper fixing soil. In this case seed set is either prevented or severely inhibited (Section 6.3). An example of the effect of interaction between mineral nutrients on yield is given in Fig. 6.2. At the lowest potassium level, the response to increasing nitrogen supply is small and at high nitrogen supply yield depression is severe. Under field conditions, however, yield depressions caused by excessive nutrient supply are usually less severe. Yield response curves differ between grain and straw, particularly at higher potassium levels (Fig. 6.2). In contrast to the straw yield, the grain yield levels off when the nitrogen supply is high, reflecting sink limitation (e.g., small grain number per ear), sink competition (e.g., enhanced formation of tillers), or source limitation (e.g., mutual shading of leaves). Yield response curves are strongly modulated by interactions between mineral nutrients and other growth factors. Under field conditions the interactions between water availability and nitrogen supply are of particular importance. In maize, for example, with increasing nitrogen supply and different soil moisture levels, the grain yield response curves obtained (Shimshi, 1969) are similar to those shown for different potassium levels (Fig. 6.2). The depressions in yield that accompany a large supply of nitrogen in combination with low soil moisture levels are presumably caused by several factors such as (a) delay in stomatal response to water deficiency (Chapter 5), (b) the higher water consumption of vegetative biomass and the correspondingly higher risk of drought stress in critical periods of grain formation, and (c) increase in shoot-root dry weight ratio with increasing nitrogen supply (Section 8.2.5), an effect which seems to be more prominent in C3 than in C4 plant species (Hocking and Meyer, 1991). Yield response curves can differ not only between vegetative and reproductive organs (Fig. 6.2) but also between the yield components of harvested products. In most
186
Mineral Nutrition of Higlier Plants
1
f
1
—
—
^ , /-
—
—
•-•••
---
0)
>
Fertilizer supply
Fig. 6.3 Schematic representation of yield response curves of harvested products. Key: , quantitative yield (e.g., dry matter per hectare); , qualitative yield (e.g., content of sugar, protein, and mineral elements; for examples (1) to (3) see following text). crops, both quantity (e.g., dry matter yield in tons per hectare) and quality (e.g., content of sugars or protein) are important yield components. As shown schematically in Fig. 6.3 maximum quality can be obtained either before [curve(l)] or after [curve(2)] the maximum dry matter yield has been reached, or both yield components can have a synchronous pattern [curve(3)]. Examples of the behaviour described by curve (1) are nitrate accumulation in spinach and sucrose accumulation in sugar beet with increasing levels of nitrogen fertilizer. Examples of curve (2) are the change in protein content of cereals, grains of forage plants with increasing supply of nitrogen fertilizer, or the change in content of certain mineral elements with increasing mineral nutrient supply, for example, magnesium and sodium in forage plants, or zinc and iron in cereal grains for human consumption. Examples of curve (3) are common under conditions where with increase in mineral nutrient supply the number of either reproductive sinks (e.g. grains) or vegetative storage sinks (e.g. tubers) is increased. 6.2
Leaf Area Index and Net Photosynthesis
Positive yield response curves are the result of different individual processes, such as an increase in leaf area and net photosynthesis per unit leaf area (i.e., effects at the source) or an increase in fruit and seed number (i.e., effects at the sink). In this section the main emphasis is put on processes that primarily affect the source site, although feedback regulation from the sink sites are often involved, and may even dominate the source processes. Generally, the density of a crop population is expressed in terms of the leaf area index (LAI), which is defined as the leaf area of plants per unit area of soil. For example, an LAI of 5 means that there is a 5 m^ leaf area of plants growing on a soil area of 1 m^. As a rule the crop yield increases until an optimal value in the range of 3-6 is reached, the exact value depending on plant species, light intensity, leaf shape, leaf angle and other factors. At a high LAI, mutual shading usually becomes the main limiting factor. When the water supply is limited, however, drought stress and corresponding negative effects, particularly at the sink sites (Section 6.3), can decrease the optimal LAI to values far below those resulting from mutual shading.
Mineral Nutrition and Yield Response
187
Table 6.1 Inhibition of Leaf Growth by Nitrogen Deficiency in Different Plant Species'" Average growth inhibition (%) Plant species Cereals (wheat, barley, maize, sorghum) Dicotyledons (sunflower, cotton, soybean, radish)
Day 16 53
Night 18 8
''Based on Radin (1983).
When the nutrient supply is suboptimal, the leaf growth rate, and thus the LAI, can be limited by low rates of net photosynthesis or insufficient cell expansion or both these factors. This is particularly evident with suboptimal supply of nitrogen and phosphorus. In plants suffering from nitrogen deficiency, elongation rates of leaves may decline before there is any reduction in net photosynthesis (Chapin et al., 1988), this decline being the result of decrease in both number and duration of extension of epidermal cells (MacAdam et al., 1989). Besides hormonal effects (Section 5.6) a decrease in root hydraulic conductivity might be involved, leading to a decrease in water availability in expanding leaf blades (Radin and Boyer, 1982). The effect of nitrogen deficiency on leaf expansion differs between plant species (Table 6.1). In cereals (monocotyledons) cell expansion is inhibited to the same extent during the day and night. In dicotyledons, however, the inhibition is much more severe during the daytime. This difference in response is related to morphological differences among species and corresponding differences in competition for the water available for transpiration and for cell expansion. In dicotyledons, cell expansion occurs in leaf blades which are exposed to the atmosphere and therefore experience a high rate of transpiration during the daytime. In cereals, however, cell expansion occurs at the base of the leaf blade. This zone is protected from the atmosphere by the sheath of the preceding leaf, so that little transpiration occurs from this zone of elongation. In contrast to leaf expansion, net photosynthesis per unit leaf area is depressed to a similar extent in both groups of plants by nitrogen deficiency. Similar results to those shown in Table 6.1 for the nitrogen effect in dicotyledons have been obtained for phosphorus in cotton plants (Radin and Eidenbock, 1984). It was found that phosphorus deficiency severely inhibited leaf growth rate only during the daytime, and had very Uttle effect at night. These day/night differences were primarily a response to limited water availability for cell expansion during the daytime, caused by low hydraulic conductance of the root system as a result of phosphorus deficiency. The small size and often dark-green color of the leaf blades in phosphorus deficient plants are the result of impaired cell expansion and a correspondingly larger number of cells per unit surface area (Hecht-Buchholz, 1967). In addition, particularly in dicots the number of leaves might be reduced through a lower number of nodes branching (Lynch et al., 1991). However, in many instances, a transient deficiency of phosphorus or nitrogen during the early growth of cereals or maize might reduce final yield not as a consequence of smaller leaf area but as the result of a lower number of spikelets per ear or grains per cob (Romer and Schilling, 1986; Barry and Miller, 1989).
188
Mineral Nutrition of Higlier Plants
(0 (Ov
20
2 ^ -C^, 4 ^ (M
i.E (0 T3
^o"io o ® E
20 30 40 Light intensity (klx) Fig. 6.4 Photosynthetic light response curves of a mature sugar beet leaf 1, 4, 7, 9 and 12 days after the plant was transferred to nitrogen-free nutrient solution. (Reproduced from Nevins and Loomis, 1970, by permission of the Crop Science Society of America.) Mineral nutrient deficiency can also delay plant development. For example, in barley the number of days to reach the booting stage is about twice as much for manganesedeficient as for manganese-sufficient plants (Longnecker et aL, 1991b). Mineral nutrition can also influence net photosynthesis in various ways (Natr, 1975; Barker, 1979). The direct involvement of some mineral nutrients in the electron transport chain in the thylakoid membranes, in detoxification of oxygen free radicals and in photophosphorylation has been summarized in Fig. 5.1 and discussed in Sections 5.2.1 and 5.2.2. Mineral nutrients are also required for chloroplast formation, either for synthesis of proteins, thylakoid membranes or chloroplast pigments. In green leaf cells, for example, up to 75% of the total organic nitrogen is located in the chloroplasts, mainly as enzyme protein. A deficiency of mineral nutrients that are directly involved in synthesis of protein or chloroplast pigments or electron transfer therefore results in the formation of chloroplasts with lower photosynthetic efficiency (Spencer and Possingham, 1960), and also in a change in the fine structure of chloroplasts in a more or less specific manner (Hecht-Buchholz, 1972). In leaves of spinach about 24% of the total nitrogen is allocated to thylakoid membranes; nitrogen nutrition therefore also affects the amount of thylakoids per unit leaf area (Terashima and Evans, 1988). A mineral nutrient deficiency can also depress net photosynthesis by influencing the CO2 fixation reaction and entry of CO2 through the stomata. Finally, starch synthesis in the chloroplasts and transport of sugars across the chloroplast envelope into the cytoplasm are directly controlled by the concentration of inorganic phosphate (Heldt et al., 1977). These functions of mineral nutrients in photosynthesis are discussed in more detail in Chapters 8 and 9. In the range between suboptimal and optimal nutrient supply, close positive correlations are often observed between mineral nutrient content of leaves and the rate of net photosynthesis (Natr, 1975). In principle, these correlations can also be indirectly demonstrated in mature leaf blades when the root supply of mineral nutrients such as nitrogen is withheld (Fig. 6.4). As nitrogen becomes increasingly deficient, the light response curve of net photosynthesis in the mature leaf declines to low levels (Fig. 6.4), and an increasing proportion of
Mineral Nutrition and Yield Response
^89
Table 6.2 Effect of Zinc Deficiency and Light Intensity on Shoot Growth and Content of Chlorophyll and Carbohydrates in Primary Leaves of Bean (Phaseolus vulgarisY Carbohydrates (mg glucose equiv. g~^ dry wt) Shoot dry wt. (g per plant)
Chlorophyll (mg g~Mry wt.)
Light intensity (/^Em'^s-i)
+Zn
-Zn
+Zn
-Zn
80 230 490
L24
1.13 1.13 1.16
19.2 16.6 11.2
17.3
2.38 3.80
7.8 4.5
Sucrose ~~~ +Zn -Zn 10 11 17
11 54 82
Total +Zn
-Zn
40 42 77
42 124 138
''Based on Marschner and Cakmak (1989). ^Sucrose, reducing sugars, starch.
the absorbed light energy which is not used in photochemical reactions is dissipated as heat (Demming and Winter, 1988). Nevertheless, the photosynthetic efficiency per unit chlorophyll can even increase under nitrogen deficiency (Khamis et al., 1990b), presumably reflecting a response to decrease in source-sink ratio. In contrast, in manganese-deficient leaves the photosynthetic efficiency per unit chlorophyll is drastically decreased and can be restored within two days after foliar application of manganese, indicating a direct effect on photosystem II (Fig. 5.1) rather than an indirect effect via source-sink relationships (Kriedemann et al., 1985). Similar changes in the light response curves shown for nitrogen deficiency (Fig. 6.4) are also found under phosphorus deficiency (Lauer et al., 1989a), and deficiency of a range of other mineral nutrients. In many instances in the deficient plants, however, despite poor utilization of higher light intensities, carbohydrates accumulate in leaves (Grabau et al. 1986a; Rao et al., 1990) and also in roots (Khamis et al., 1990a) of phosphorus-deficient plants. Thus, low photosynthetic efficiency of source leaves might often be the result of feedback regulation induced by a lower demand for photosynthates at the sink sites. An example for this is shown for zinc-deficiency in Table 6.2, With increasing light intensity plant dry weight increases in the zinc-sufficient plants but not in the zinc-deficient plants (Table 6.2). Although chlorophyll content drastically declines with increasing Ught intensities, particularly in the zinc deficient plants the carbohydrate content increases steeply, indicating that the lack of growth response to increasing light intensities reflects a sink and not source limitation. Accumulation of photosynthates under high light intensity in source leaves of deficient plants not only decreases utilization of light energy but also poses a stress. This high light stress is indicated, for example, by an increase in the antioxidative defense mechanisms in the deficient leaves (Cakmak and Marschner, 1992; Fig. 5.2), photooxidation of chloroplast pigments (Table 6.2) and enhanced leaf senescence. These side effects of mineral nutrient deficiency decrease not only current photosynthesis and LAI but also leaf area duration (LAD), that is the length of time in which the source leaves supply photosynthates to sink sites, an aspect that is discussed in Section 6.4.
190
6.3 6.3.1
Mineral Nutrition of Higher Plants
Mineral Nutrient Supply, Sink Formation, and Sink Activity General
In crop species where fruits, seeds, and tubers represent the yield, the effects of mineral nutrient supply on yield response curves are often a reflection of sink Umitations, imposed by either a deficiency or an excessive supply of mineral nutrients during certain critical periods of plant development, including flower induction, pollination, and tuber initiation. These effects can be either direct (as in the case of nutrient deficiency) or indirect (e.g., effects on the levels of photosynthates or phytohormones). 6.3.2
Flower Initiation
In apple trees, flower formation is affected to a much greater extent by the time or form of nitrogen application or both these factors than by the level of nitrogen supply. Compared with a continuous nitrate supply a short-term supply of ammonium to the roots was found to more than double both the percentage of buds developing inflorescences and the arginine content in the stem (Table 6.3). Arginine is a precursor of polyamines which also accumulate particularly in leaves of plants supplied with high levels of ammonium (Gerendas and Sattelmacher, 1990). The causal involvement of polyamines in the ammonium-induced enhanced development of inflorescences in apple trees is indicated by the similar effects obtained by infiltrating polyamines into the petioles (Table 6.3). These results on the flowerinducing effects of ammonium supply confirm earlier results of Grasmanis and Edwards (1974). Since the apple trees in this study were amply supplied with nitrogen throughout the growing season, it is unlikely that these effects on flower initiation (i.e. on developmental processes) are related to a general nutritional role of nitrogen. It appears more probable that some nitrogen compounds such as polyamines may function as second messenger in flower initiation (Section 5.6.3). Table 6.3 Effect of Ammonium-N or Polyamines on Flower Initiation and Arginine Content in Apple Trees'"
Treatment Control, nitrate continuously NH4-N for 24 h^ NH4-N for 1 week Putrescine"^ Spermine*^ NH4-N for 24h^ ""Based on Rohozinski et al. (1986). ^8 mM N H ^ in the nutrient solution. ^8 mM petiole infiltration.
Percentage flowering
Stem arginine content (i"gg~^ dry wt)
15 37 40 51 47 50
1120 2570 2330 — — —
Mineral Nutrition and Yield Response
191
Table 6.4 Shoot Growth, Flower Induction and CYT in Xylem Exudate of Apple Root Stock M7 as Affected by the Form of Nitrogen Supply" Form of Shoot length N-supply (cm) NOs-N NH4NO3 NH4-N
No. lateral CYT_ shoots Flowering buds (nmol (100 g) ^ shoot (spurs) (% of emerged) fresh wt)
326 268 209
6.4 6.0 8.9
7.4 8.2 20.7
0.002 0.373 0.830
'Based on Gao et al. (1992). Most probably, changes in the phytohormone level in general and of CYT in particular are involved in this enhancing effect of ammonium supply on flowering (Buban et ah, 1978). In apple root stocks, ammonium supply as compared with nitrate, not only increased flower bud formation but also CYT concentration in the xylem exudate and the number of flower-bearing lateral branches (spurs), whereas the total shoot length was depressed (Table 6.4). Promotion offlowermorphogenesis by CYT is weU documented for various other plant species (Bruinsma, 1977; Herzog, 1981). Flower formation in apple trees (Bould and Parfitt, 1973), tomato (Menary and Van Staden, 1976), and wheat (Rahman and Wilson, 1977) is also positively correlated with phosphorus supply. The positive correlations between the number offlowersand CYT level in tomato (Menary and Van Staden, 1976), on the one hand, and between the phosphorus supply and the CYT level on the other (Horgan and Wareing, 1980), provide additional evidence that CYT also contributes to the enhancing effect of phosphorus on flower formation. Basically similar conclusions were drawn from the effects of potassium on flower formation in Solarium sisymbrifolium (Wakhloo, 1975a,b). Low potassium levels in the leaves were correlated with a high proportion of sterile female flowers. This sterility did not occur in plants of either high or low potassium status when the plants had been sprayed with CYT. These various results strongly confirm the supposition that the effects of mineral nutrient supply on flower formation are brought about by changes in phytohormone level. This is also true for the beneficial effects of nitrogen fertilizer appUcation before anthesis in increasing grain number per ear in wheat (Herzog, 1981) or seed number per plant in sunflower (Steer et al., 1984). However, seed number per plant can also be increased by high concentrations of sucrose prior to flower initiation (Waters et al., 1984), high light intensity (Stockman et al,, 1983) or stem injection of sucrose under drought stress conditions (Boyle et al., 1991; Section 5.7). The possibility can not be ignored, therefore, that mineral nutritional status may also affect flower initiation and seed set by increasing the supply of photosynthates during critical periods of the reproductive phase. 6.3.3
Pollination and Seed Development
The number of seeds or fruits or both per plant can also be directly affected by mineral nutrient supply. This is clearly the case with various micronutrients. In cereals in
192
Mineral Nutrition of Higher Plants
Table 6.5 Effect of Increasing Copper Supply in Wheat (cv. Chatilerma) Grown on Copper-Deficient SoiP Copper supply (mg per pot)
Number of tillers Straw yield (g) Grain yield (g)
0
0.1
0.4
2.0
22 7.7 0.0
15 9.0 0.5
13 10.3 3.5
10 10.9 11.8
''Total number of plants per pot: 4. Based on Nambiar (1976c).
particular, copper deficiency affects the reproductive phase (Table 6.5). The critical period in copper-deficient plants is the early booting stage at the onset of pollen formation (microsporogenesis). When the copper deficiency is severe, no grains are produced even though the straw yield is quite high owing to enhanced tiller formation (loss of apical dominance of the main stem). As the copper supply is increased, grain yield rises sharply, whereas the straw yield is only sHghtly enhanced. These results provide an informative example of both sink limitation on yield and deviation from the typical response curve (Fig. 6.1) between grain yield and mineral nutrient supply. Under field conditions, in copper deficient soils, especially when the top soil is dry, copper application to the soil is often much less effective than foliar application at the early vegetative growth stage in increasing the grain yield (Section 4.3). The primary causes of failure in grain set in copper-deficient plants are inhibition of anther formation, the production of a much smaller number of pollen grains per anther, and particularly the nonviability of the pollen (Graham, 1975), in part because of lack of supply of carbohydrates to the developing pollen grains (Jewell et al., 1988). In principle, similar results as those found for copper deficiency (Table 6.5) are obtained with zinc or manganese deficiency. In maize, zinc deficiency prior to microsporogenesis (—35 days after germination) did not significantly affect vegetative growth and ovule fertility but decreased pollen viability and cob dry weight by about 75% (Sharma et al., 1990). Also under manganese deficiency vegetative growth of maize is much less depressed than grain yield (Table 6.6). In the deficient plants anther
Table 6.6 Effect of Manganese ]Deficiency on Growth, Fertilization and Grain Yield in Maize"
(/^gr^)
Shoot dry wt. (g per plant)
Grain wt (g per plan t)
Single grain wt (mg)
Pollen (no. per anther)
Pollen germination (%)
550 5.5
82.5 57.8
69.3 11.8
302 358
2770 1060
85.6 9.4
Mn supply
'^Sharma et al. (1991). Reprinted by permission of Kluwer Academic Publishers.
193
Mineral Nutrition and Yield Response
250 f S 200
Grain
Q.
3 150
*- Silks + cob sheaths ^ Stalk + leaves
I 100 Q
50 0.5
1.0 2.0 5.0 10.0 20.0 Boron supply (mg planf^) Fig. 6.5 Effect of boron supply on the production and distribution of dry matter in maize plants. (Based on Vaughan, 1977.)
development is delayed and fewer and smaller pollen grains are produced with very low germination rates. In contrast, ovule fertility was not significantly affected by manganese deficiency (Sharma et al., 1991), a result, which is in agreement with the effect of copper deficiency in wheat (Graham, 1975). The production and viability of pollen are also affected by molybdenum. In maize, a decrease in the molybdenum content of pollen was correlated with a decrease in the number of pollen grains per anther as well as a decrease in the size and viability of the pollen grains (Section 9.6). As yet no information is available as to the extent to which molybdenum deficiency also depresses fertilization and grain set. However, it is well documented that preharvest sprouting in maize (Section 9.6) and wheat (Cairns and Kritzinger, 1992), causing severe yield losses in certain areas, is very high in seeds with low molybdenum content and can be effectively decreased by molybdenum supply to the soil or as a foUar spray. Boron is another mineral nutrient that affects fertilization. Boron is essential for pollen tube growth (Section 9.7), a role reflected under conditions of boron deficiency by a decrease in the number of grains per head in rice (Garg et al., 1979) or even a total lack of fertilization in barley and rice (Ambak and Tadano, 1991). The failure of seed formation in maize suffering from boron deficiency is caused by the nonreceptiveness of the silks to the pollen (Vaughan, 1977). As the level of boron nutrition increases, vegetative growth, including the structural growth of the silks, is either not affected or is even somewhat depressed (Fig. 6.5). In contrast, grain formation is absent in severely deficient plants but increases dramatically when the boron supply is adequate. Obviously there is a minimum boron requirement, which is in the range of 3 mg boron per maize plant for fertilization and grain set. Figure 6.5 provides another example of both a strict sink limitation induced by mineral nutrient deficiency and a yield response curve quite different from the typical curve. Low boron supply not only inhibits flowering and seed development but may also produce seeds with low boron content in plants even without visual symptoms of boron
194
Mineral Nutrition of Higher Plants
Table 6.7 Effect of Potassium Supply to Wheat on ABA Content and Weight of Grains'" ABA content (ng per grain) days after anthesis K Supply
28
35
38
44
Days from anthesis to full ripening
Low (deficient) High
7.7 3.7
13.4 4.4
16.5 ND^
2.2 9.4
46 75
Weight of a single grain (mg) 16.0 34.4
''Based on Haeder and Beringer (1981). ^ND, Not determined.
deficiency. These low boron seeds have a low germination rate and produce a high percentage of abnormal seedlings (Bell etal, 1989). In lowland rice, grain yield might be considerably decreased by spikelet sterility induced by low temperatures (below 20°C) during anthesis. This temperature sensitivity can be drastically decreased by high supply of potassium (Haque, 1988). Increasing potassium contents in the panicles from 0.61% to 2.36% in the dry matter decreased spikelet sterihty after three days at 15°C from 75% to 11%. The reasons for this protecting effect of potassium are not known, high nitrogen contents in the low potassium plants are probably involved (Haque, 1988). In certain plant species, such as soybean, drop of flowers and developing pods is a major yield-Umiting factor. Nitrogen or phosphorus deficiency during the flowering period enhances flower and pod drop and depresses seed yield correspondingly (Streeter, 1978; Lauer and Blevins, 1989). Supplying ample amounts of nitrogen or phosphorus during this critical phase is therefore quite effective in reducing flower and pod drop and in increasing final seed yield in soybean (Brevedan et al., 1978; Lauer and Blevins, 1989). Although the physiological reasons for both the flower and pod drop and the decline in drop produced by nitrogen application are not yet known in detail, it is certain that phytohormones, especially CYT and ABA, are involved. An ample nitrogen supply both increases CYT and decreases ABA (Section 5.6.4) and hence decreases flower and pod drop, as would be expected from the specific role of ABA in the formation of abscission layers. Accordingly, maize kernel abortion can be reduced by either foHar application of CYT or supplying the roots with ammonium-N (Smiciklas and Below, 1992), the latter treatment being particularly effective in increasing the CYT contents in the plants (Table 6.4). Premature ripening of fruits and seeds imposed by water or nutrient deficiency is another yield-Hmiting factor. In this case it is not the number of grains but the weight (size) of a single grain or fruit that is low. There is substantial evidence that elevated ABA levels are also involved in premature ripening. An example of this is shown in Table 6.7 for potassium-deficient wheat plants. In these plants, and particularly 4-6 weeks after anthesis, the levels of ABA in the grains are much higher than those in the grains of plants well supplied with potassium. Correspondingly, the grain-filling period in potassium-deficient plants is much shorter and the weight of a single grain at maturity is lower than that in control plants. As has been shown before (Section 5.6.5), high
Mineral Nutrition and Yield Response
195
ABA levels in grains coincide with a sharp decline in the sink activity of grains. It is quite Ukely that the elevated ABA levels in the flag leaves of potassium-deficient wheat plants (Haeder and Beringer, 1981), and a correspondingly higher ABA import to the developing grains, are responsible for the premature ripening and not the source limitation of a mineral nutrient per se (Section 6.4). 6.3.4
Tuberization and Tuber Growth Rate
In root and tuber crops such as sugar beet or potato, the induction and growth rate of the storage organ are strongly influenced by the environmental factors. In contrast to crop species in which seeds and fruits are the main storage sinks, root and tuber crops often exhibit a distinct sink competition between vegetative shoot growth and storage tissue growth for fairly long periods after the onset of storage growth. This competition is particularly evident in so-called indeterminate genotypes of crop species, for example, in potato (Kleinkopf et al., 1981). In general, environmental factors (e.g., high nitrogen supply) with pronounced favorable effects on vegetative shoot growth delay the initiation of the storage process and decrease growth rate and photosynthate accumulation in storage organs - for example, of sugar beet (Forster, 1970) and potato (Ivins and Bremner, 1964; Gunasena and Harris, 1971). A large and continuous supply of nitrogen to the roots of potatoes delays or even prevents tuberization (Krauss and Marschner, 1971). After tuberization the tuber growth rate is also drastically reduced by high nitrogen supply, whereas the growth rate of the vegetative shoot is enhanced. The effect of nitrogen supply on tuber growth rate is illustrated in Table 6.8. Resumption of the tuber growth rate to normal levels after interruption of the nitrogen supply indicates that sink competition between the vegetative shoot and tubers can readily be manipulated by means of the nitrogen supply. In potato, cessation of tuber growth caused by a sudden increase in nitrogen supply to the roots induces 'regrowth' of the tubers, that is, the formation of stolons on the tuber apex (Krauss and Marschner, 1976, 1982). Interruption and resupply of nitrogen, therefore, can result in the production of chain-Uke tubers or so-called secondary growth (Fig. 6.6). After a temporary cessation of growth, resumption of the normal
Table 6.8 Growth Rate of Potato Tubers in Relation to Nitrate Supply to the Roots of Potato Plants^ Nitrate concentration (mn)
Nitrate uptake (meq per day per plant)
Tubei • growth rate (cm^ pel• day per plant)
1.18 2.10 6.04 —
3.24 4.06 0.44 3.89
1.5 3.5 7.0 Nitrogen supply withheld for 6 days ''From Krauss and Marschner (1971).
196
Mineral Nutrition of Higher Plants
Fig. 6.6 Secondary growth and malformation of potato tubers induced by alternating high and low nitrogen supply to the roots. (Krauss, 1980.) growth rate is usually restricted to a certain area of the tubers (meristems or 'eyes'), leading to typical malformations and knobby tubers, which are often observed under field conditions after transient drought periods. Similar effects on cessation of tuber growth and 'regrowth' can be achieved by exposing growing tubers to high temperatures, which instantly inhibit starch synthesis and lead to the accumulation of sugars in the tubers (Krauss and Marschner, 1984; Van den Berg et al., 1991), followed by a decrease in ABA levels in the tubers and 'regrowth'. The effects of nitrogen supply on tuber growth rate and 'regrowth' are brought about by nitrogen-induced changes in the phytohormone balance both in the vegetative shoots and in the tubers. As already shown (Section 5.6.4), an interruption of the nitrogen supply results in a decrease both in CYT export from roots to shoots and in the sink strength and growth rate of the vegetative shoot. A corresponding increase in the ABA/GA ratio of the shoots seems to trigger tuberization. In agreement with this, tuberization can also be induced by the application of either ABA or the GA antagonist CCC (Krauss and Marschner, 1976) or by the removal of the shoot apices, the main sites of GA synthesis (Hammes and Beyers, 1973). On the other hand, after cessation of growth the regrowth of tubers induced by a sudden increase in the nitrogen supply is correlated with a decrease in the ABA/GA ratio not only in the vegetative shoots but also in the tubers, where the GA level increases by a factor of 2 but the ABA level drops to less than 5% of that in normal growing tubers (Krauss, 1978b).
6.4
Mineral Nutrition and the Sini(-Source Relationships
In root and tuber crops, unUke grain crops, the sink-source relationship is quite labile even after the onset of the storage process. This has to be considered, for example, in the application of nitrogen fertilizer to potato. On the one hand, a high nitrogen supply is important for rapid leaf expansion and for obtaining an LAI between 4 and 6, a value considered necessary for high tuber yields (Kleinkopf et al., 1981; Dwelle et al., 1981). On the other hand, a high supply of nitrogen delays either tuberization or the onset of the linear phase of tuber growth. The principles of these interactions are demonstrated in Fig. 6.7. The advantage of earlier tuberization obtained by supplying a low level of nitrogen is offset by a low LAI and earUer leaf senescence, that is a short LAD and a
197
Mineral Nutrition and Yield Response l^yi
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y /t-\
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75 100 125 Days after planting Fig. 6.7 Time course of leaf area index and fresh weight of potato tubers at two levels of nitrogen supply. (Based on Ivins and Bremner, 1964, and Kleinkopf et al., 1981.) correspondingly lower tuber yield. When the nitrogen supply is high, both LAI and LAD, and thus final tuber yield, are much higher. However, higher tuber yield induced by a large nitrogen supply can be realized only when the vegetation period is sufficiently long, that is, in the absence of early frost (Clutterbuck and Simpson, 1978) or in the absence of severe drought stress. The early decHne in LAI when the supply of nitrogen is low (Fig. 6.7) indicates that the final tuber yield is limited by the source. The question arises as to the reasons for this source limitation. In potato plants at maturity, between 60% and 80% of the total nitrogen is located in the tubers (Kleinkopf et al., 1981). Therefore, when the nitrogen supply is low, exhaustion of nitrogen in the source leaves presumably plays a key role in leaf senescence and in the termination of tuber growth. However, these simple relationships between nitrogen supply, LAI, LAD and tuber yield (Fig. 6.7) are not only modified by the length of the growing period but also the mineralization rate of soil nitrogen and temperature during tuber growth. At high nitrogen supply and high LAI, mutual shading of the basal leaves may not only drastically decrease their net photosynthesis but also the LAD by rapid leaf senescence (Firman and Allen, 1988), a process which is further enhanced at high ambient temperatures (Manrique and Bartholomew, 1991). Thus, a lower, but more continuous supply of nitrogen which allows an earlier tuberization and continuous root growth and CYT production, and which is more effective on LAD than on LAI, might often lead to higher tuber yields than a rapid establishment of a high LAI by high nitrogen supply during early growth. Interestingly, an increase in LAD is one of the major characteristics of the new, high-yielding varieties in maize and wheat developed during the last 30 years (Austin, 1989; Tollenaar, 1991). Competition for nitrogen rather than for carbohydrates supplied from the source leaves can also be the main limiting factor for seed yield in mustard and rape plants (Trobisch and Schilling, 1969; Schilling and Trobisch, 1970). In mustard plants the developing seeds and leaves compete for nitrogen, and seed set, seed growth, and final seed yield are determined primarily by the size of the nitrogen pool in the vegetative parts. In crucifers, the flower differentiation at the auxiliary stems occurs after the onset
198
Mineral Nutrition of Higher Plants
Control
0.9
1.9 (g N pot')
Nitrogen addition
Fig. 6.8 Effect of addition of 0.9 and 1.9 g nitrogen at the onset offloweringon total dry weight and dry weight distribution in shoots of white mustard plants. (Based on Trobisch and Schilling, 1970.)
offloweringof the main stem and is strongly dependent on the availability of nitrogen during this period. Additional application of nitrogen at the onset of flowering therefore leads to an increase in seed number and yield (Fig. 6.8). The example with mustard plants in Fig. 6.8 demonstrates that source limitation can be imposed by nitrogen rather than carbohydrates. This aspect has also to be considered in source-sink manipulations. Removing source leaves from a plant is a common procedure for evaluating source limitation in photosynthesis (Section 5.7). Of course, when source leaves are removed, nitrogen and other mineral nutrients are also removed. Therefore, shading of source leaves may have a different effect on the reduction of seed yield from that of leaf removal. Shading the source leaves of mustard plants reduced the seed yield by only 20%, whereas removal of these same leaves reduced the seed yield by 50% (Trobisch and Schilling, 1969). In plant species like mustard and rape, mutual shading of source leaves is usually much less detrimental on yield than, for example, in cereals and tuber crops, as in the crucifers after the onset of flowering the stems and pods provide a high proportion of the photosynthates required in the developing seeds (Section 5.7.1). In principle, each of the mineral nutrients can become the dominant factor inducing source limitation onfinalyield of seeds, fruits and tubers, provided that it can be readily retranslocated from the source (Section 3.5). Whether such a limitation exists depends on such factors as the availabihty of the given nutrient in the soil, its concentration and amount (source size) in the vegetative shoot, the specific demand of the sink for the nutrient, and the growth rate of the sink. For example, in fleshy fruits or tubers, the potassium content is very high (2-3% of the dry weight), and at maturity most of the potassium is located in the fruits or tubers. Potassium-induced source Hmitation is therefore more Ukely in this type of crop. An example of this has been given in Section 5.7 for tomato genotypes. In contrast, in mature cereal plants, as much as 80% of the total amount of nitrogen or phosphorus is located in the grains, compared with less than 20% of the total potassium (see also Section 3.5.4). Thus, in cereal plants where there is a suboptimal supply of the three mineral nutrients during the vegetative stage, source limitation during grainfillingis most likely induced by nitrogen or phosphorus, but not
Mineral Nutrition and Yield Response
199
A
10 20 30 40 50 60 70 80 Days after anthesis Fig. 6,9 Time course of chlorophyll content inflagleaf and dry weight accumulation in spikelet grains of phosphorus-sufficient (•, A) and phosphorus-deficient (O, A) wheat plants. (Modified from Batten and Wardlaw, 1987a.)
by potassium. The importance of export of mineral nutrients to developing seeds for senescence of source leaves has been discussed in Section 5.7. In soybean, for example, enhanced leaf senescence and also premature pod drop could be counteracted not only by an increase in phosphorus supply to the roots but also by stem infusion of phosphorus (Grabau et al., 1986a), indicating that in this case phosphorus deficiency limited seed yield by decreasing LAD. In moderately phosphorus-deficient cereal plants source limitation may also become the dominant factor for grain yield. In wheat these relationships are particularly prominent for the flag leaf blade which may deliver between 5 1 % and 89% of the phosphorus found in the grains at harvest (Batten et al., 1986). As shown in Fig. 6.9, in phosphorus-deficient plants the flag leaf senesced rapidly and its photosynthetic activity approached zero by the time the grains were only 60% of their final potential dry weight, leading to a reduction in final grain yield by 40% and in phosphorus content by 75%. The results shown in Fig. 6.9 reflect source Umitation of either phosphorus or photosynthates. Evidence against limitation by photosynthates had been presented by additional experiments where shading of ears increased the rate of net photosynthesis severalfold in the deficient flag leaf and also substantially delayed its senescence (Chapin and Wardlaw, 1988). In contrast, in the phosphorus-sufficient plants shading of the ear was without significant effects on flag leaf net photosynthesis. Thus, enhanced leaf senescence in the phosphorus-deficient plants is most likely caused by accumulation of photosynthates in the flag leaf and a subsequent photooxidation of the chloroplast
200
Mineral Nutrition of Higher Plants
pigments and destruction of membranes (Section 5.2.2) which, in turn, enhances remobihzation and re translocation of phosphorus from source to sink. These examples illustrate the role of mineral nutrients as yield-limiting factors when fruits, seeds, or other organs are the dominant sink sites and mineral nutrient uptake by the roots is declining. Progress in selecting and breeding for genotypes with a high harvest index (ratio of economic yield to total dry matter) and short periods of fruit growth or ripening (e.g., thefillingperiod in cereals) might be severely restricted, not because of the limited capacity of the source to supply carbohydrates, but rather because of the limited amount of mineral nutrients such as potassium, nitrogen, phosphorus, and magnesium that are available for retranslocation from source to sink.