Soyabean (Glycine max (L.) Merr.)

ELSEVIER

Field Crops Research 53 (1997) 171-186

Field Crops _ Research

Soyabean ( Glycine max(L.) Merr.) J o s e p h W . Burton * USDA-ARS, North Carolina State University, 3127 Ligon St., Box 7631, Raleigh, NC 27695-7631, USA

1. Origin Seeds of soybean (Glycine max (L.) Men'.) have been used in Asia for many centuries to prepare a variety of fresh, fermented and dried foods (Probst and Judd, 1973). Based on historical and geographical evidence, Hymowitz (1970) concluded that soybean was domesticated in the l lth century B.C. in northern China. To locate the likely point of origin, the similarity between soybean and Glycine soja, its nearest wild relative, was investigated with a survey of land races throughout China. The two species were most similar in seed protein content, frequency of Ti a (trypsin inhibitor) alleles and flowering date at 35°N latitude (Xu et al., 1989). They concluded that, the Yellow River Valley, which is the birthplace of ancient Chinese civilization, was the probable place of origin. From there, it spread into southern China and east through Korea into Japan (Probst and Judd, 1973). Both soybean and G. soja have 2 n = 40 chromosomes and are cross fertile. Because of the large number of chromosomes and a high frequency of duplicate gene loci (Palmer and Kilen, 1987); Zobel, 1983; Keim et al., 1990a), it is believed that soybean is a diploidized tetraploid (Van Raamsdonk, 1995).

* Tel.: + 1-919-515-2734; fax: + 1-919-856-4598.

2. General botany

2.1. Seeds and germination

Soybean seeds have a seed coat and embryo. The seed coat, which is maternal tissue, has three layers, epidermis, hypodermis, and inner parenchyma layer (Carlson, 1973). On the outside, the seed coat is covered with a cuticle. On the inside are remnants of the endosperm tissue which has been compressed by the developing embryo (Williams, 1950). The seed coat has pores which vary in size, shape and number (Calero et al., 1981). These pores form as ~ e seeds desiccates during maturation (Vaughn et al., 1987). There are also surface deposits of a waxy material derived from the endocarp of the podwall (Yaklich et al., 1986). Some genotypes have areas of the seed coat without pores, and in others, pores are located over the entire surface. The rate of water absorption by soybean seeds is dependent on pore size, distribution and the extent of the waxy surface deposit. If pores are smaller or occluded by the waxy material, J the seed may not imbibe water at all unless the seed coat is scarified. Seeds which do not imbibe or those which require several hours to imbibe are termed 'hard seeds'. Variation in the impermeable response within a hard seed line is associated with seed size, with smaller seeds being more impermeable (Hill et al., 1986). Colors of soybean seed coats are shades of black,

0378-4290/97/$17.00 © 1997 Elsevier Science B.V. All rights reserved. PII S0378-4290(97)00030-0

172

J. W. Burton~Field Crops Research 53 (1997) 171-186

brown, green or yellow (Williams, 1950). Pigmentation is controlled by two major gene pairs (T, t and R, r) and two modifying gene pairs (O, o and W1, Wl). Another locus with four alleles (I, i i, i k, i) controls pigment intensity (Bhatt and Torrie, 1968). Seed hilum, formed where the funiculus separates from the seed is also pigmented. Hilum color is determined by the I, R, T, and W1 genes (Taylor and Caviness, 1982; Palmer and Kilen, 1987). Distribution of pigment in the seed coat is affected by three k loci. Recessive alleles at these loci produce a 'saddle' pattern of pigmentation which begins at the hilum and continues down both sides of the seed (Palmer and Kilen, 1987). Another gene (G) causes chlorophyll retention in the seed coat and produces a green seed coat. The embryo of soybean seeds is either green or yellow. Green coloration, caused by chlorophyll retention, is conditioned by either two recessive nuclear genes ( d l / d 1, d2/d 2) or a cytoplasmic gene (cyt-G1). In the former, presence of at least one dominant allele ( D 1 or D 2) will result in a yellow seed embryo (Palmer and Kilen, 1987). Grain-type soybeans that are processed for oil and protein meal must have yellow seeds because darker pigments in the seed coat or embryo will cause discoloration of oil extracted from the seeds. While this dark color can be removed from the oil in processing, the procedure is costly and can be difficult. Soybean is a warm season legume and most production occurs in temperate zones of the northern and southern hemispheres. In the northern hemisphere, most planting for a full-season crop is done in May or early June. In the southern hemisphere, full-season crops are planted in November. In climates where winter crops, (e.g. wheat and barley) can be grown, soybeans are sometimes planted after the winter crop is harvested, and thus planting may be as late as July or December. After planting, the soybean germination proceeds through seven stages: seed imbibition, testa splitting, radicle emergence, hypocotyl-root axis development, root hair formation, lateral root primordial formation and emergence (Muthiah et al., 1994). The rate at which these processes occur is affected by both soil temperature and moisture. Rapid rates of seed hydration in wet soils cause cotyledon cracking (Knittle and Burris, 1979), an effect that is exacerbated as

temperatures increase (Sorrells and Pappelis, 1976). Hypocotyl elongation is inhibited by low temperatures (25 °, Grabe and Metzer, 1969) and compacted soils impede emergence (Howle and Caviness, 1988). There is evidence that genetic variation exists for both cold tolerance (germination at 10°C, Unander et al., 1986) and heat tolerance (germination at 38°C, Emerson and Minor, 1979) in the germplasm collection. Germination is also influenced by the environment in which the seeds developed. For instance, drought stress during seed development reduces viability (Dornbos et al., 1989; Heatherly, 1993). After emergence, cotyledons expand, turn green and become the first leaves of the plant. Storage lipids and protein in the cotyledons are important sources of carbon and nitrogen during very early plant development. At the seedling stage, hypocotyl coloration is a convenient and useful genetic marker. The W1 genotype which has purple flowers also has a purple hypocotyl. The double recessive genotype (WlW 1) has white flowers and a green hypocotyl (Palmer and Kilen, 1987). In addition, a bronze coloration of the hypocotyl is indicative of a tawny pubescent (T_Td_ or T__td) white flowered (WlW 1) genotype (Palmer and Payne, 1979).

2.2. Vegetative growth The first two leaves to develop, above the cotyledonary node are unifoliate. Thereafter, a trifoliate leaf is produced at each node that develops on the main stem or branches. Leaflets vary in size and shape but are typically oval or ovate. There is a single recessive gene (ln) which produces a narrow leaflet. Narrow leaflets may allow more light penetration into the crop canopy. Some cultivars have been developed with narrow leaflets. Research conducted to determine whether or not the narrow leaflet phenotype confers a productive advantage has been inconclusive (Cooper and Waranyuwat, 1985; Wells et al., 1993). There is also variation among germplasm for leaflet orientation in response to light and temperature (Wofford and Allen, 1982). Plant color varies from dark green to light green depending on chlorophyll concentration (Statues and Hadley, 1965). Pubescence, which develops in stems and leaves, may be tawny, light tawny or grey in color (Palmer and Kilen, 1987). Pubescence pheno-

J.W. Burton/Field Crops Research 53 (1997) 171-186

type may be glabrous, curly, erect, appressed, blunt, dense, sparse, and puberulent (Bernard and Singh, 1969; Palmer and Kilen, 1987). Pubescence phenotype influences overall plant coloration and appearance. Cultivated soybeans have an erect growth habit, but procumbency is not uncommon in germplasm sources. Wild soybeans (Glycine soja) tend to be viney, and many of the soybean types developed for forage use are also viney. Soybeans may have a single main stem with no branching or various degrees of branching. Branching response is strongly influenced by plant population density. More branching occurs at low plant densities. The soybean root system begins as a taproot developing from the radicle of the germinating seed. Secondary roots develop from the taproot and several orders of branch roots arise from the secondary roots (Carlson, 1973). Rooting depth and prominence of the taproot versus the more fibrous branching roots is influenced by soil type and moisture, cultural practices and plant population densities (Carlson, 1973; Barber, 1978; Robertson et al., 1980; Huck and Davis, 1976). For instance, in some soils, machinery traffic creates a hard-pan which is difficult for roots to penetrate, and consequently, root growth is more lateral than downward, (Koon-Hup, 1977). There is genetic variation for rooting pattem in germplasm resources (Cardwell and Poison, 1972; Pantalone et al., 1996). In a recent study, extent of root fibrosity appears to be quantitatively inherited, and an entry mean heritability estimate of a visual score for the trait was H = 0.35 (Pantalone et al., 1994). Nodulation of the soybean root system occurs after infection through root-hair cells by Bradyrhizobium japonicum. In the field or greenhouse culture, nodules are usually visible by the 10th day after infection and N 2 fixation begins within the next 8 days (Lersten and Carlson, 1987). There is a single recessive gene (rjl) which prevents nodulation, and there are dominant genes at other loci which prevent effective nodulation by particular strains of Bradyrhizobium (Palmer and Kilen, 1987). There are also super-nodulating mutants which have 2 to 4 times more nodules per plant root system than normal cultivars (Wu and Harper, 1991; Lee et al., 1991). Genotypic variation in nodule number and

173

weight is also found in germplasm collections (Sinclair et al., 1991; Hudak and Patterson, 1995). The vegetative and reproductive periods in the soybean life cycle are divided for descriptive purposes into sub-stages which correspond to the appearance in development of main stem nodes and reproductive structures (Fehr and Caviness, 1977). Hence, the plant is in stage V1 when the unifoliate leaves at node 1 are fully developed. This is followed by V2 when the first trifoliolate leaf has fully developed at node 2. This description continues until the last node (n) develops (stage Vn). The reproductive period is described from stage R1 (beginning bloom) when at least one flower opens on the main stem, through stage R4 (full pod) when a pod 2 cm long occurs at one of the four uppermost nodes on the main stem, to stage R8 (full maturity) when 95% of the pods have mature pod color. The vegetative and reproductive periods may overlap, the extent of which is influenced by stem termination type. In soybean, there are three stem termination types which are controlled by two major gene loci, Dt I and Dt 2. Indeterminate genotypes ( D t l D t 1 dt2dt a) tend to have one or two pods near the stem apex. Determinate genotypes (dt I dt l) have a well defined terminal raceme with several pods. Semi-determinate types ((DtlDt I Dt2Dt 2) are intermediate between these two in the abruptness with which the main stem terminates (Palmer and Kilen, 1987). The overlap of vegetative and reproductive periods is greatest in genotypes with indeterminate stem termination types and least in determinate genotypes. In one comparison, an indeterminate cultivar produced 58% of its total vegetative material prior to initial flowering (R1) while a determinate breeding line had 78% of its vegetative production at R1 (Egli and Leggett, 1973). All three stem types are represented in cultivars currently in use. In the northern hemisphere, most cultivars grown in northern latitudes ( ~ > 36 °) are indeterminate and those grown further south ( = < 36 °) are mostly determinate. Soybean breeders have used the Dt 1 and Dt 2 genes to modify plant architecture and alter the reproductive period (Cooper, 1976); Boerma et al., 1982; Hartung et al., 1981). In a comparison of stem termination isolines in Nebraska, USA (41 ° latitude), semi-determinate types had a reduced main stem length and node number

174

J. W. Burton~Field Crops Research 53 (1997) 171-186

(Hartung et al., 1981). This effect was even greater in the determinate types. Even so, attempts to demonstrate yield differences due specifically to stem termination type have generally failed except in particular environments (Hartung et al., 1981; Chang et al., 1982; Cooper, 1976; Ouattera and Weaver, 1994; Cober and Tanner, 1995).

2.3. Reproductive growth and maturity Flowering and maturity are generally influenced by photoperiod. This photoperiodic sensitivity limits adaptability of soybean as a full-season crop to relatively narrow latitudinal belts. Soybean breeders have developed cultivars with wide adaptation within these belts (Brim, 1973). In North America, cultivars adapted for each belt are designated a maturity grouping (MG). These maturity groups extend from MG000, MG00, MG00, MGI, in Canada and northern-most USA to MGVIII in the southern-most USA production areas. There are also MGIX and MGX germplasms which are adapted to sub-tropical and tropical production areas. The maturity groupings are also used in the Caribbean Basin, Central and South America and Europe, but maturity classification sometimes changes because seasonal temperature as well as photoperiod can affect flowering and maturity response (Ecochard, 1985; Tanasch and Gretzmacher, 1991). In China, soybeans have been bred for adaptation to five areas of production (Calkins and Ma, 1985). These production areas are related to the type of cropping system used, which may require spring, early summer, or mid-summer planting. Thus, photoperiod response is important in adaptation to these five growing regions, but the maturity grouping system used in the Americas and Europe is not used in China. There are four major gene pairs which affect time of flowering and maturity (El, E2, E3, E 4) (Palmer and Kilen, 1987). Bernard (1971) termed E 1 a gene for lateness and E 2 a gene for earliness in both flowering and maturity. E 3 is also a gene for lateness but is not additive in combination with E 2. Photoperiod insensitivity has been found (Criswell and Hume, 1972; Polson, 1972) and at least one major gene ( E 4) is involved. Within a single maturity grouping, there can be wide variation in flower response to extend-

ing the day length, (Nissly et al., 1981). Also, cooler temperatures and longer day length have been found to be additive in delaying flowering (Major et al., 1975). In controlled growth chambers, (Thomas and Raper, 1976, 1984) found that age did not affect sensitivity of the plants to flower induction with short day length, but delay of flowering induction, increased the number of main stem and axially nodes. This later response is also effected by the 'long juvenile trait', (controlled by a single recessive gene) which delays flowering under short day lengths (Hartwig and Kiihl, 1979; Ray et al., 1995; Hinson, 1989). This trait is being used by soybean breeders for cultivar adaptation to tropical environments and to very early spring plantings in the southern USA. It is also being used to delay maturity of early maturing cultivars, thus moving their adaptation further south. After pollination, pods begin to develop and are usually visible within five days. Pods reach an almost full width while the developing embryo is still very small. This period between R1 (beginning bloom) and R5 (beginning seed) can vary from 18 to 40 days depending on genotype and environment (Metz et al., 1985). After R5, seeds enter a period of rapid linear dry matter accumulation. In one study, the linear seed fill rate was between 79 and 98 kg ha -1 per day. The length of this period is also variable, between 18 and 57 days (Egli et al., 1984; Reicosky et al., 1982; Metz et al., 1985). Once rapid seed-fill begins, rate of photosynthesis begins to decline and photosynthate is used for seed development and very little is exported to the root system and nodules (Latimore et al., 1977; BoonLong et al., 1983). N 2 fixation rate declines as a result. The developing seeds are a strong sink for N which is needed for protein synthesis. In mid seedfill, N in leaves begins to be exported to the developing seeds (Wittenbach et al., 1980) and continues until leaf senescence at which time leaf N concentration is between 2 and 2.5%, an approximate 50 percent loss (Egli et al., 1987). Physiological maturity occurs between stages R7 and R8 when pods lose their green color and become yellow (Gibikpi and Crookston, 1981). Leaflets and petioles also turn yellow at this time and abscise. Pods reach their mature color (black, brown, or tan) about one week after physiological maturity.

J. W. Burton~Field Crops Research 53 (1997) 171-186

Soybeans are usually harvested after drying in the pod to 15% (or less) moisture. On a dry weight basis, mature soybean seeds are approximately 40% protein, 21% oil, 34% carbohydrate and 5% ash. In processing, oil is extracted from crushed beans and used in a variety of food and industrial products. The remaining protein meal is used primarily in animal feeds.

3. Floral biology and controlled pollination Soybean flowers have either 3 or 4 ovules, all of which reach maturity (and consequent full female fertility) prior to anthesis (Stelly and Palmer, 1985). This protogyny permits cross pollination without emasculation one day prior to anthesis. Flowers open and normally self-pollinate at anthesis. Between 26 and 76% of the flowers abscise prior to pod formation (Van Shaik and Probst, 1958). Because most ovules are fertilized and embryo development initiated prior to flower abscission (Abernathy et al., 1977), it is likely that the abortion is due to environmental effects on the physiological status of the plant. In field environments, flower shedding is observed during periods of drought and high temperature. Cool temperatures also effect fertilization and pod formation. Research with MG00 through MGIII germplasms, showed 15° days and between 15° to 9 ° nights to be the biological minimum for pod formation (Van Shaik and Probst, 1958; Hume and Jackson, 1981). Soybeans are almost entirely self-pollinated. Rates of natural outcrossing between.03% and 1.1% have been observed in field environments (Culter, 1934; Caviness, 1966). Caviness (1966) found rate of outcross to vary with environment and to be influenced by proximity with other plants. Insect vectors transfer pollen and both environment and genotype have been shown to influence the attractiveness of soybean flowers to honey bees, a primary insect pollen vector (Robacker et al., 1983). For controlled pollination, unopened flowers with petals protruding through the sepals are selected as females. Sepals and then petals are removed from the flower so that the stigma is exposed. Depending on genotype, flower, age, and technique, anthers may be

175

removed simultaneously with the petals. If not they may be carefully removed with tweezers, but they are often left in place. Emasculation is not considered to be necessary (Walker et al., 1979; Stelly and Palmer, 1985). For future identification, all other flowers on the raceme or at the node (if there is no raceme) are removed. This would include both immature flowers and those which had already opened. Flowers which are to be used as pollen donors may be newly opened, but they can also be collected in the morning just prior to opening. With forceps, sepals are removed first, followed by removal of the standard petal. The wing and keel petals are then removed to expose the anthers. Holding this flower with forceps, the anthers are brushed lightly over the stigma of the female flower. The pollinated flower is then tagged either on the raceme or on the stem below the node where the pollination was made. The tag contains all needed information, e.g. parentage of the cross, date of the pollination, etc. The dominant genetic markers, purple flower color or tawny pubescence, when carded by the pollen donor to a recessive female can be used to detect cross- vs. self-pollinations. Soybean breeders use a variety of pollination systems. Some emasculate flowers for pollination in the afternoon and pollinate them the next morning. Others, collect male pollen flowers in the morning and emasculate and pollinate female flowers in the afternoon. Others do both together in the morning or afternoon. There is no consensus on which system is best. Climatic factors often enter into the decision of which system to use, e.g. cool mornings or evenings are sometimes considered the best for pollination success. Successful pollination percentage varies widely depending on genotype, technique, climate, and unknown factors. Fifty percent is usually considered to be a good success rate, but lower and higher rates are not uncommon. There are several nuclear recessive genes which confer male-sterility. These are used by soybean breeders for insect mediated pollination. This is usually done for random mating purposes in recurrent selection population improvement programs (Brim and Stuber, 1973; Burton et al., 1990; Tinius et al., 1991). But controlled biparental pollinations are also possible (Nelson and Bernard, 1984; Lewers et al., 1996).

176

J. W. Burton~Field CropsResearch 53 (1997)171-186

4. Major breeding achievements At the beginning of this century, soybean production in the USA was primarily for forage. In 1929, 60% of the total soybean hectarage was harvested for forage. By 1945, this had changed so that only 15% of the hectarage was forage (Morse, 1950). At that time, 4.2 million hectares of soybeans were produced for beans. This increased steadily until 1979 when 28.5 million hectares were harvested in the USA for beans (Soya Bluebook Plus, 1995). Thus, the earliest breeding achievement in this century was the development of cultivars that permitted the transition from hay to grain production. Adaptation to the maturity zones (000-VIII) was a major part of this change. The regional testing program, organized in 1942 by the US Department of Agriculture in cooperation with the state Experiment Stations, was instrumental in identifying germplasm that was best suited for each growing region (Brim, 1973). In the southeastern states, pod dehiscence prior to harvest (shattering), poor seed quality and foliar diseases were early problems that needed to be overcome. The development of the cultivar, Lee (MGVI), by Dr. E.E. Hartwig was the first breakthrough (Hartwig, 1954). Lee did not shatter, so seed production was not lost prior to harvest. Seed quality and composition were excellent, and the cultivar was also resistant to the foliar disease bacterial pustule (Xanthomonos phaseoli vat. sojensis). Subsequently, Lee became the standard for cultivars released in the southeastern states and is an early ancestor of most current culfivars (Carter et al., 1993). The USDA regional testing program provided a means for cooperation and free exchange of germplasm among soybean breeders. Soybean breeders began meeting each winter to plan the next regional test, identify problems and potential solutions, and summarize their research. Soybean pathologists and entomologists met with the group periodically. This led to extensive cooperation and coordination of breeding efforts among soybean breeders and allied scientists which brought about another major achievement, genetic increases in seed yield potential. Soybean breeding in the USA has been viewed as a process of cyclical recurrent selection in which

superior cultivars are selected and released for production, then recombined and reselected (Burton, 1987). Luedders (1977) identified four such cycles in the selection of MGI-IV cultivars between 1933 and 1971. In simultaneous tests of sets of cultivars from those cycles, be provided estimates of yield increases of 1% and 0.6% per year (Luedders, 1977; Wilcox et al., 1979). From similar research, Specht and Williams (1984) placed yield gains of cultivars in MG00-IV released between 1902 and 1977 at 18.8 kg ha -1 per year. In the southeastern states (MGVI-VIII), the rate of progress between 1914 and 1973 has been estimated to be 0.7% per year (Boerma, 1979). Judging from results of state official variety tests and the fact that many cultivars released in the early 1980's have now been replaced by improved varieties, it is reasonable to conclude that progress in yield improvement continues. In the past 30 years, soybean production increased dramatically in Central and South America. Adaptation of the crop to new geographical areas has been another accomplishment of soybean breeding. Many of the germplasm resources that provided the foundation of breeding programs in Central and South America and in Europe were improved US and Canadian cultivars. Incorporation of genes for resistance to diseases and pests in cultivars has served to protect and maintain genetic increases in seed yield. In the U.S. development of cultivars with resistance to phytophthora rot (caused by Phytophthora sojae) a n d / o r nematodes both, soybean cyst (Heterodera glycine) and root-knot (Meloidogine species), have been important in this maintenance of 'genetic capital'. Cultivars were released in the early 1960s which carried the dominant Rps gene which conferred resistance to Phytophthora races 1 and 2. Thirty-two races are now recognized and breeding solutions involve combining multiple sources of resistance (Schmitthenner et al., 1994). The first soybean cyst nematode (SCN) resistant cultivar, Pickett (MGVI), released in 1965 was resistant to races 1 and 3 (Brim and Ross, 1966). Genes for resistance were found in a Chinese cultivar, Peking, which prevented nematode reproduction. Other germplasm resources have been used to provide resistance to other races (3, 4, 5, 6, and 14). The germplasm PI 437,654 from the former USSR was

J. W. Burton/Field Crops Research 53 (1997) 171-186

found to be resistant to all known races of SCN (Anand, 1991) The cultivar Hartwig (MGV), which carries the resistance genes of PI 437,654, was released in 1991. Root-knot nematode is a world-wide problem on soybean, particularly in warmer production areas (Good, 1973). While no cultivars have been developed that are completely free of infection by the nematodes, several cultivars have been developed which dramatically reduce yield losses on infested fields. A recent achievement that is expected to have a major impact on soybean production in the USA is the development of glyphosate tolerance in soybean (Padgette et al., 1995). A glyphosate tolerance gene was transferred to soybean using molecular genetic technology, and then bred into cultivars using standard plant breeding methodology. Because glyphosate is an effective herbicide against a broad spectrum of weeds, weed control in a glyphosate tolerant crop is expected to be more effective and less expensive than other weed control measures that rely on a combination of herbicidal and mechanical control measures.

5. Current goals of breeding programs 5.1. Seed characteristics

Because protein meal and oil are the two commodities produced from grain-type soybeans, increasing both protein and oil concentration in seeds are breeding goals. Most research in recent years has been directed at protein concentration (Wehrmann et al., 1987; Wilcox and Cavins, 1995). But protein and oil are negatively correlated, so there is the difficulty that increasing one usually results in a decrease in the other (Brim and Burton, 1979). Index selection has been used to simultaneously increase both (Openshaw and Hadley, 1984; Burton, 1991). About 10% of soybean oil is the polyunsaturated fatty acid linolenic acid and another 10% is the saturated fatty acid palmitic acid. Soybean oil for food uses would be improved if both were reduced. Linolenic acid is subject to autooxidation which gives the oil an undesirable odor and flavor (Chang et al., 1983). Palmitic acid is implicated as a contributor to coronary heart disease (Willett, 1994). Thus,

177

reduction of palmitic acid should make soybean oil more healthful. Germplasms have been developed through mutagenesis a n d / o r recombination which decrease one or the other and the traits are being bred into high yielding cultivars (Hammond and Fehr, 1983; Wilcox and Cavins, 1986; Burton et al., 1989; Wilcox et al., 1994). Also of some interest are mutants which increase the saturated fatty acids, palmitic and stearic. Protein quality is also receiving attention. Soy protein is low in the sulfur amino acids, methionine and cystine. These amino acids are routinely added to soy protein animal feeds to meet dietary requirements. Efforts to increase cystine and methionine in soy protein have been primarily aimed at increasing the concentration of protein subunits which are known to have higher levels of the two amino acids (Burton, 1984). In addition to seed composition, seed quality is an important consideration. Particularly in warmer production areas, weathering and disease organisms such as Phomopsis and Cercospora kikuchii lower seed quality which can result in price penalties when the damage is severe. Two breeding strategies have been followed. One is direct selection for genotypes which are resistant to seed diseases (Ross, 1986; Wilcox et al., 1975) and the second is breeding cultivars with the impermeable seed coat which protects the seed against weathering and disease infection (Hartwig and Potts, 1987). 5.2. Plant characteristics

Lodging resistance is the main plant characteristic that soybean cultivars need to have because an erect growth habit reduces mechanical harvest loss and is probably needed for maximum light penetration of the plant canopy. Severe lodging can result in yield losses (Cooper, 1976). There is no consensus on other plant characteristics that are needed. Soybean breeders have used several other traits with mixed results, these include, narrow leaflets, brachytic stem (short internode), stem termination change to alter height, and more fibrous rooting (Cooper and Waranyuwat, 1985; Chang et al., 1982; Wells et al., 1993; Pantalone et al., 1994). Alterations of length of reproductive period has been used for adaptation to specific environments

J.W. Burton/Field Crops Research 53 (1997) 171-186

178

(Hinson, 1989) and investigated as a general method for improving seed yield (Smith and Nelson, 1986a; Hanson, 1992). While positive correlations between seed yield and reproductive period traits have been observed, in practice yield improvements gained by lengthening the pod-filling period a n d / o r changing the rate of dry matter accumulation in pods have been minor (Smith and Nelson, 1986b; Hanson, 1992; Egli et al., 1984). There have also been attempts to increase the rate of N 2 fixation, total N accumulated, and N 2 fixation in high N03 environment which have met with some success (Graham and Rosas, 1984; Herridge and Rose, 1994; Ronis et al., 1985).

5.3. Disease resistance There are many diseases associated with soybean production. Some cause limited economic loss and others are only a problem in certain geographical areas. Breeding research on a particular disease is usually done in areas where the disease is predictable in occurrence so that field screening and selection of resistant genotypes is possible. The following is a summary of those diseases which cause economic loss and countries or regions where they are most prevalent. The information was obtained from the Proceedings of the World Soybean Research Confer-

ence IV in Buenos Aires, Argentina (1989), World Soybean Research Conference V in Chang Mai, Thailand (1994) and the Soybean Breeders Workshop in St. Louis, USA (1995). Fungal diseases which are currently receiving the most research attention are frogeye leafspot caused by Cercospora sojina, sudden death syndrome caused by Fusarium solani, anthracnose caused by Colletotrichum truneatum, phytophthora rot caused by Phytophthora sojae, brown stem rot caused by Philalophora gregata, white mold caused by Sclerotinia sclerotiorum, stem canker caused by Diaporthe phaseolorum var. caulivora, red crown rot caused by Cylindrocladium crotalariae, purple seed stain caused by Cercospora kikuchii and phomopsis seed decay caused by Phomopsis spp. and Diaporthe phaseolorum var. sojae (Athow, 1987). Genetic resistance to most of these diseases can be found in soybean germplasm collections. Countries with active programs for breeding cultivars resistant to these diseases are presented in Table 1.

5.4. Insect resistance Resistance to insects has been a difficult objective to achieve through conventional plant breeding methodology. In the USA, three germplasms, PI

Table 1 Important soybeandiseases and regions where they are most prevalent and where breeding for resistance is a controlmeasure Diseases Regions Fungal Frogeyeleafspot Southeastern USA, Brazil, India, China Sudden death syndrome USA, Argentina Anthracnose Argentina, Thailand Phytophthora USA, Canada, Yugoslavia Brown stem rot USA Whitemold USA, China, Argentina, France Stem canker USA, Argentina, France Rust China, Taiwan, India Red crownrot China Purple seed stain USA, India Phomopsis seed decay USA, Argentina Bacterial

Blight

USA

Viral

Soybeanmosaic virus Bud blight

USA, China, France Argentina

Nematodes

Soybeancyst Root-knot

USA, China, France USA, Argentina

J.W. Burton/Field CropsResearch 53 (1997)171-186 229358, PI 171451 and PI 227687, have been the source of resistance genes for most breeding programs. But, it has been difficult to transfer the resistance to high yielding cultivars without losing yielding ability. Without high yield potential, farmers are unwilling to grow an insect-resistant cultivar, given the unpredictability of severe insect infestations. In the USA, research on a biotechnological solution is being conducted at the University of Georgia (H.R. Boerma, personal communication). This involves incorporation of genes from Bacillus thuringensis which produce a toxin that can kill many insect species. In the USA, serious insect infestations occur mainly in warmer production areas; those south of 40 ° latitude. The species which cause the greatest economic loss and for which there are active programs breeding for resistance are the following: Mexican bean beetle (Epilachna varivestes Mulsant), corn earworm (Helicoverpa zea), soybean looper (Pseudoplusia includens Walker), and velvetbean catterpillar ( Anticarsia gemmatalis Hiibner) (Turnipseed and Kogan, 1987). Green stink bug (Acrosternum hilare Say), a pod sucking insect which can cause serious damage to seed quality and some yield loss, are identified as a serious problem in Japan (Panizzi and Shiga, 1994), Brazil (Rossetto et al., 1994) and intermittently in the USA (Gilman et al., 1982). In China, Japan, India, and some other Asian countries, the beanfly (Melenagromyza sojae) causes severe loss of seed yield. Finding sources of resistance to beanfly and breeding resistant cultivars is a high priority in those countries (Rahman and Bhattacharya, 1994; Talekar, 1994; Gai et al., 1989).

5.5. Environmental stress tolerance Environmental stresses on the soybean crop can be subdivided into categories, those due primarily to climate and weather and those due to nutrition resulting from poor soil fertility. In the first instance, drought is the most serious stress worldwide. Soybeans are grown in many areas where rainfall is marginal or where drought stress is intermittent throughout the growing season because soils have a low water holding capacity. It has been shown that over the past 30 years, lack of water during reproductive development has been the factor most limit-

179

ing seed yields in the southeastern states in the USA (Carter, 1989). Thus, in most countries where soybeans are produced and where there are active soybean breeding programs, breeding cultivars with drought tolerance is a research objective. In practice, tolerance to drought is difficult to define in terms of varietal characteristics because degree of tolerance is always related to severity of the stress. Thus, very few cultivars have been released with a claim of tolerance to drought. Several strategies for improving drought tolerance are used. Probably the most common is field screening where the selection criterion is yielding ability under droughty conditions (Carter and Rufty, 1993). Sometimes, irrigated production is compared with non-irrigated production (Specht et al., 1986; Carter and Rufty, 1993). Drought is also induced artificially in growth chambers or field 'rain-out' shelters (Sammons et al., 1978; Sloane et al., 1990). Traits that have been associated with tolerance to drought and thus subject to selection are deeper a n d / o r more diffuse rooting (Kasper et al., 1984; Hudak and Patterson, 1995), leaflet orientation a n d / o r wilting during stress (Oosterhuis et al., 1985; Carter and Rufty, 1993), and aluminum tolerance (Hanson and Kamprath, 1979; Campbell and Carter, 1990). Another climatic stress often associated with drought is heat. Genetic variation for heat tolerance has been investigated at germination (Emerson and Minor, 1979; Bouslama and Schapaugh, 1986) and early in the reproductive period (Martineau et al., 1979). In the latter case, cellular membrane thermostability was evaluated. Low temperature stress is also a problem for germination and seedling growth of cultivars planted in early spring and for reproductive development in regions where low night temperatures are common during the growth stage. Genetic variation for tolerance to both has been investigated (Unander et al., 1986; Seddigh et al., 1988). Genetic variation for tolerance to a fourth weather related stress, flooding, has also been reported. It was a tolerance that was independent of phytophthora rot resistance (Van Toai et al., 1994). In soybeans, nutritional stresses are usually a result of low soil pH and fertility. Most of these can be solved with soil amendments. Exceptions are toxic levels of micro-nutrients, such as zinc and manganese, and problems which arise because of

180

J. W. Burton/Field Crops Research 53 (1997) 171-186

high soil pH, such as iron deficiency chlorosis. Differences in susceptibility among soybean cultivars to toxic levels of manganese and zinc have been reported (Heenan and Carter, 1976; White et al., 1979). In midwestern states of the USA, iron deficiency chlorosis is common in soybeans produced on calcareous soils. There has been intensive breeding for resistance to this stress in those areas (Byron and Lambert, 1983; Hintz et al., 1987; Cianzio and Voss, 1994).

6. Selection techniques Breeding populations are often developed by 2way, 3-way or 4-way crosses of cultivars a n d / o r breeding lines. If it is desirable to use unadapted germplasm, then at least one backcross to the adapted parent is often used. Populations are advanced through generations of inbreeding in several ways, including pedigree selection, modified pedigree selection (single seed or pod descent) (Brim, 1966), or bulk selfing. In the latter two, pure-line identification, evaluation, and selection take place in later (Fs-F7) generations. With pedigree selection, desirable families are selected (often visually) in each generation and one or more plants from within each family are advanced through selfing to the next generation. Selection in early generations can be shown to be desirable provided the genotypic worth of single F 2 plants, F 3 a n d / o r F4 lines can be successfully determined. Research to compare the relative efficiency of pedigree selection (PS), single-seed descent (SSD) and early generation testing (EGT), for seed yield has generally found the three to be similar in terms of the final outcome (Boerma and Cooper, 1975; Snape and Riggs, 1975). Sometimes SSD is recommended as being least costly of the three. More recently, Cooper (1990) has described a modified version of his earlier EGT method which he has found to be both efficient and successful. Various recurrent selection methods have been used or proposed for use with soybean. These include mass selection for oil (Burton and Brim, 1981) and seed weight (Tinius et al., 1991), among selfed half-sib family selection for seed yield (Burton and Carver, 1993), within half-sib family selection for

seed oil quality (Carver et al., 1986), and S 1 (or S z) family selection for yield (Kenworthy and Brim, 1979; Rose et al., 1992) and protein (Brim and Burton, 1979). Nuclear male sterility has been used for insect mediated random mating of selected materials in recurrent selection programs. It worked well in the previously cited mass selection programs and in one example of S 1 family selection for yield (Burton et al., 1990). Even though all of the above were used successfully to improve population performance for single traits, most soybean breeding efforts are still concentrated in traditional PS and SSD methodologies and very few cultivars have been derived from recurrent selection programs. The multiplicity of breeding goals often requires simultaneous consideration of more than one trait during the selection process either to improve the total phenotype or prevent an unwanted change in phenotypes due to correlated responses. Tandem selection has been used to improve traits of high heritability in early generations (e.g. protein and maturity) followed by selection for yield in later generations (Sebern and Lambert, 1984; Byron and Orf, 1991). Several types of selection indexes have also been used. Base indexes have been used to increase yield, protein and oil using various protein to oil price ratios (Brim et al., 1959; 0 i f and Helms, 1994). Restricted or expected gain indexes have been used to increase yield while holding protein constant (Holbrook et al., 1989) and to increase protein without changing maturity (Miller and Fehr, 1979). Finally, DNA markers are being examined as a means to enhance soybean breeding in several ways including pedigree tracing and genotype identification in backcross breeding. Their use in marker assisted selection is beginning as knowledge about the soybean genome accumulates and molecular maps are constructed. In a population derived from a G. m a x X G. s o j a cross, quantitative trait loci (QTLs) have been identified which affect iron efficiency, hard seededness, protein, oil, maturity, height, lodging, days to R1, days to R8, seed-filling period, stem diameter, stem length, canopy height, leaf width, and leaf length (Graef et al., 1989; Keim et al., 1990a; Keim et al., 1990b; Diets et al., 1992a; Diets et al., 1992b). Similar research has been conducted using a population derived from a G. max × G. max cross (Mansur et al., 1993). Information about cosegrega-

J.w. Burton / Field Crops Research 53 (1997) 171-186

tion of DNA markers and QTLs should eventually lead to marker assisted selection of quantitative traits.

181

generation. Seeds from the F4 or F5 plants are bulked to produce F4:5 or F5:6 lines. 7.3. Line evaluation and selection

7. A comprehensive breeding plan 7.1. Parental choice

Choice of parents for a breeding population is crucial to successful plant breeding. Parents should be chosen to maximize the chances that the breeding populations will be genetically variable for whatever traits are being selected. Thus, breeding objectives will dictate the germplasm pool from which parents can be selected. It is usually best to choose parents which are as unrelated as possible from that germplasm pool. If the breeding objective is high productivity, then usually one would select highyielding unrelated breeding lines or cultivars as parents. If other traits such as disease resistance or special seed composition are desired, then the most productive breeding lines or cultivars which carry those traits are chosen as parents. If it is necessary to choose unadapted parents in order to find genes for a particular trait, then one should use unadapted germplasm with the least number of undesirable traits (e.g. seed shattering, green seeds, lodging). 7.2. Inbreeding and line development

The S o progeny from the mating can be evaluated themselves (Burton and Brim, 1981; Tinius et al., 1991), but usually they are allowed to self-pollinate one or more generations prior to evaluation. Generations of selfing provide a seed increase needed for field plot testing. When backcrossing is needed in order to transfer particular genes to another genetic background, this can be done with S O progeny prior to screening for the gene or in one of the later inbred generations after individuals carrying the genes have been identified. When standard pedigree selection methods are applied early generation selection within lines is done, often visually. In other early generation methods, selection is practised among lines. With modified pedigree (or bulk) selection, inbreeding proceeds from the F 2 through the F4 or F5 generation by taking only a single seed or pod from each plant in each

Lines are evaluated by various laboratory, greenhouse, and field screening procedures, but suitability for farm growers requires testing in a standard field production system. This is done in small plots usually 3- or 4-row plots (between 3 and 5 m in length and 1.5-3 m in width). In yield evaluations, bordering and 'end trimming' is standard practice because of potential competitive effects from adjacent plots. Thus, seed yield is measured on only the center one or two rows which are harvested after a small portion at the end of the rows have been removed (trimmed). Potential cultivars are evaluated throughout the region in which they will be grown. This permits evaluation in a number of different soil types and environmental conditions. Comparisons are always made with standard high performing cultivars of similar maturity already in production and which have a proven value. 7.4. Cultivar release

Breeding lines with good performance relative to other standard cultivars may be released as a new cultivar. If the breeding line has a trait other cultivars do not have, such as resistance to a problem disease, then the need and importance of its release is obvious. Elite breeding lines which do not become cultivars are often used as parents in a new cycle of breeding.

8. Summary The past 50 years of breeding grain-type soybeans has produced many cultivars with good yield potential that are adapted to modem cultural practices and resistant to important diseases. Genetic improvement throughout this period has been gradual but continuous, and there is no evidence that a true breeding plateau has been reached. The progress has been due, at least partially, to a large number of soybean breeding programs, and until recent years, a free exchange of germplasm among those programs. In the United States, there are both publicly and pri-

182

J. W. Burton~Field Crops Research 53 (1997) 171-186

vately funded soybean breeding programs that develop and release cultivars. In 1994, soybean cultivars were being developed by 37 private companies with one or more breeding programs each and by 26 public breeding programs supported by Universities and the US Department of Agriculture. There are many more privately developed soybean cultivars available to farmers than publicly developed cultivars and private company cultivars are planted on about 80% of the total US soybean aceage. In the long term, continued soybean improvement requires that adequate genetic variation exists in breeding populations. In North America, there is some cause for concern in this regard because most soybean varietal development populations in use originated from a relatively small number of plant introductions. Eighty ancestors contributed all foundational germplasm to 258 North American cultivars released between 1947 and 1988 by public breeding programs and more than half of this genetic base was contributed by only 6 of the 80 ancestors (Gizlice et al., 1994). Thus, attention to genetic diversity and deliberate actions to widen the genetic base of breeding populations are needed. Future research should continue to focus on ways to improved breeding method efficiency and ways to increase the rate of improvement. These include the following: (i) the development of breeding populations, taking into account the genetic origin of the parents, their overall phenotype, and their performance in diverse environments; (ii) the development of single and multiple trait selection schemes which incorporate a more rapid cycling of elite line identification, selection, and recombination; (iii) the development of ways to manage genotype X environment interactions so that heritabilities are increased; (iv) the allocation of resources with respect to preliminary vs. advanced testing; and (v) cost effective ways to apply molecular genetic technology to quantitative trait improvements.

Acknowledgements The author wishes to thank Mrs. Connie D. Bryant for skilled assistance in preparation of this manuscript and Drs. C.A. Brim, S.R. Cianzio, and T.C. Kilen for their helpful comments and suggestions.

References Soya Bluebook Plus, 1995. Soyatech, Inc., Bar Harbor, ME, pp. 226-229. Abernathy, R.N., Palmer, R.G., Shibles, R. and Anderson, I.C., 1977. Histologicalobservationon abscising and retained soybean flowers. Can. J. Plant Sci., 57: 713-716. Anand, S.C., 1991. Registration of soybean germplasm line $882036 having multiple-raceresistance. Crop Sci., 31: 856. Athow, K.L., 1987. Fungal diseases. In: ed. J.R. Wilcox, Soybeans: Improvement,Production,and Uses. Agron. Mongr. 16, 2nd ed. ASA, CSSA, and SSSA, Madison, WI, pp. 687-727. Barber, S.A., 1978. Growth and nutrient uptake of soybean roots under field conditions.Agron. J., 70: 457-461. Bernard, R.L., 1971. Two major genes for time of flowering and maturity in soybean.Crop Sci., 11: 242-244. Bernard, R.L. and Singh, B.B., 1969. Inheritance of pubescence type in soybeans: Glabrous, curly, dense, sparse, and puberulent. Crop Sci., 9: 192-197. Bhatt, G.M. and Torfie, J.H., 1968. Inheritanceof pigment color in the soybean. Crop Sci., 8: 617-619. Boerma, H.R., 1979. Comparisonof past and recently developed soybean cultivars in maturity groups VI, VII, and VIII. Crop Sci., 19: 611-613. Boerma, H.R. and Cooper, R.L., 1975. Comparison of three selection procedures for yield in soybeans. Crop Sci., 15: 225-229. Boerma, H.R., Wood, E.D. and Barrett, G.B., 1982. Registration of duocrop soybean. Crop Sci., 22: 448-449. Boon-Long, P., Egli, D.B. and Leggett, J.E., 1983. Leaf N and photosynthesis during reproductive growth in soybean. Crop Sci., 23: 617-620. Bouslama, M. and Schapaugh Jr., W.T., 1986. Stress tolerance in soybeans. I. Evaluationof three screeningtechniquesfor heat and drought tolerance. Crop Sci., 26: 933-937. Brim, C.A., 1966. A modified pedigree method of selection in soybeans. Crop Sci., 6: 220. Brim, C.A., 1973. Quantitativegenetics and breeding.In: ed. B.S. Caldwell, Soybeans: Improvement, Production, and Uses. Agron. Mongr. 16, 1st ed. ASA, CSSA, and SSSA, Madison, WI, pp. 155-186. Brim, C.A., Johnson, H.W. and Cockerham, C.C., 1959. Multiple selection criteria in soybeans. Agron. J., 51: 42-46. Brim, C.A. and Burton, J.W., 1979. Recurrent selection in soybeans. II. Selection for increased percent protein in seeds. Crop Sci., 19: 494-498. Brim, C.A. and Ross, J.P., 1966. Relative resistance of Pickett soybeans to various strains of Heterodera glycines Phytopath., 56: 451-454. Brim, C.A. and Stuber, C.W., 1973. Applicationof genetic male sterility to recurrent selection schemes in soybeans.Crop Sci., 13: 528-530. Burton, J.W., 1984. Breeding soybeans for improved protein quantity and quality. In: ed. R. Shibles, Proc. of the World Soybean Res. Conf. III., Westview Press, Inc., Boulder, CO, pp. 361-367. Burton, J.W., 1987. Quantitative genetics: results relevant to

J. W. Burton~Field Crops Research 53 (1997) 171-186 soybean breeding. In: ed. J.R. Wilcox, Soybean: Improvement, Production, and Uses, Agron. Mongr. 16, 2nd ed. ASA, CSSA, and SSSA, Madison, WI, pp. 211-247. Burton, J.W., 1991. Development of high-yielding, high protein soybean germplasm. In: ed. R.F. Wilson, Designing ValueAdded Soybeans for Markets of the Future. AOCS, Champaign, IL, pp. 109-117. Burton, J.W. and Brim, C.A., 1981. Recurrent selection in soybeans. III. Selection for increased percent oil in seeds. Crop Sci., 21: 31-34. Burton, J.W. and Carver, B.F., 1993. Selection among S t families vs. selfed half-sib or full-sib fanailies in autagamous crops. Crop Sci., 33: 21-28. Burton, J.W., Koinange, E.M.K. and Brim, C.A., 1990. Recurrent selfed progeny selection for yield in soybean using male sterility. Crop Sci., 30: 1222-1226. Burton, J.W., Wilson, R.F., Brim, C.A. and Rinne, R.W., 1989. Registration of soybean germplasm with modified fatty acid composition of seed oil. Crop Sci., 29: 1583. Byron, D.F. and Lambert, J.W., 1983. Screening soybeans for iron efficiency in the growth chamber. Crop Sci., 23: 885-888. Byron, D.F. and Off, J.H., 1991. Comparison of three selection procedures for development of early-maturing soybean lines. Crop Sci., 31: 656-660. Calero, E., West, S.H. and Hinson, K., 1981. Water absorption of soybean seeds and associated causal factors. Crop Sci., 21: 926-933. Calkins, P.H. and Ma, J.C., 1985. Soybeans and cropping patterns in China. In: ed. R. Shibles, World Soybean Res+ Conf. III: Proceedings. Westview Press, Boulder, CO, pp. 67-77. Campbell, K.A. and Carter Jr., T.E., 1990. Aluminum tolerance in soybean: Genotypic correlation and repeatability of solution culture and greenhouse screening methods. Crop Sci., 30: 1049-1054. Cardwell, V.B. and Polson, D.E., 1972. Response of 'Chippewa 64' soybean scions to roots of different genotypes. Crop Sci., 12: 217-219. Carlson, J.B., 1973. Morphology. In: ed. B.E. Caldwell, Soybeans: Improvement, Production, and Uses. Agron. Mongr. 16, 1st ed. ASA, CSSA, and SSSA, Madison, WI, pp. 17-95. Carter Jr., T.E. and Rufty, T.W., 1993. Soybean plant introductions exhibiting drought and aluminum tolerance. In: ed. C.G. Kuo, Adaptation of Food Crops to Temperature and Water Stress: International Symposium Proceedings, AVRDC, Talpei, Taiwan, pp. 335-346. Carter Jr., T.E., 1989. Breeding for drought tolerance in soybean: Where do we stand? In: ed. A.J. Pascale, Proc. World Soybean Res. Conf. IV, Assoc. Argentina de la Soja, Buenos Aires, Argentina, pp. 1001-1008. Carter Jr., T.E., Gizlice, Z. and Burton, J.W., 1993. Coefficient of parentage and genetic similarity estimates for 258 North American soybean cultivars released by public agencies during 1945-1988. US Dept. of Agric., Tech. Bull. No. 1814, 169 pp. Carver, B.F., Burton, J.W., Wilson, R.F. and Carter Jr., T.E., 1986. Cumulative response to various recurrent selection

183

schemes in soybean: Oil quality and correlated agronomic traits. Crop Sci., 26: 853-858. Caviness, C.E., 1966. Estimates of natural cross-pollination in Jackson soybeans in Arkansas. Crop Sci., 6:211-212. Chang, J.F., Green, D.E. and Shibles, R., 1982. Yield and agronomic performance of semideterminate and indeterminate soybean stem types. Crop Sci., 22: 97-101. Chang, S.S., Shen, G.-H., Tang, J., Jin, Q.Z., Shi, H., Carbin, J.T. and Ho, C.T., 1983. Isolation and identification of 2pentenyl-furans in the reversion flavor of soybean oil. J. Am. Oil Chem. Soc., 60: 553-557. Cianzio, S.R. and Voss, B.K., 1994. Three strategies for population development in breeding high-yielding soybean cultivars with improved iron efficiency. Crop Sci., 34: 355-360. Cober, E.R. and Tanner, J.W., 1995. Performance of related indeterminate and tall determinate soybean lines in short-season areas. Crop Sci., 35: 361-364. Cooper, R.L., 1976. Modifying morphological and physiological characteristics of soybeans to maximize yield. In: ed. L.D. Hill, World Soybean Research: Proc. of the World Soybean Res. Conf., Interstate Printers and Publishers, Danville, IL, pp. 230-236. Cooper, R.L., 1990. Modified early generation testing procedure for yield selection in soybean. Crop Sci., 30: 417-419. Cooper, R.L. and Waranyuwat, A., 1985. Effect of three genes (Pd, Rps~, In) on plant height, lodging, and seed yield in indeterminate and determinate near isogenic lines of soybean. Crop Sci., 25: 90-92. Criswell, J.R. and Hume, D.J., 1972. Variation in sensitivity to photoperiod among early maturing soybean strains. Crop Sci., 12: 657-660. Culter, G.H., 1934. A simple method for making soybean hybrids. J. Am. Soc. Agron., 26: 252-253. Diers, B.W., Cianzio, S.R. and Shoemaker, R.C., 1992a. Possible identification of quantitative trait loci affecting iron efficiency in soybean. J. Plant Nurt., 15: 2127-2136. Diers, B.W., Keim, P., Fehr, W.R. and Shoemaker, R.C., 1992b. RFLP analysis of soybean seed protein and oil content. T.A.G., 83: 608-612. Dombos Jr., D.L., Mullen, R.E. and Shibles, R.M., 1989. Drought stress effects during seed fill on soybean seed germination and vigor. Crop Sci., 29: 476-480. Ecochard, R., 1985. La sensibilit6 de soja h la photoptriode et h la thermoptriode. Eurosoya, 3: 30-34. Egli, D.B. and Leggett, J.E., 1973. Dry matter accumulation patterns in determinate and indeterminate soybean. Crop Sci., 13: 220-222. Egli, D.B., Off, J.H. and Pfeiffer, T.W., 1984. Genotypic variation for duration of seed fill in soybean. Crop Sci., 24: 587-592. Egli, D.B., Swank, J.C. and Pfeiffer, T.W., 1987. Mobilization of leaf N in soybean genotypes with varying duration of seed fill. Field Crops Res., 15: 251-258. Emerson, B.W. and Minor, H.C., 1979. Response of soybeans to high temperature during germination. Crop Sci., 19: 553-556. Fehr, W.E. and Caviness, C.E., 1977. Stages of Soybean Development. Cooperative Extension Service and Agriculture and

184

J. W. Burton~Field Crops Research 53 (1997) 171-186

Home Economics Experiment Station. Special Report 80. Iowa State University, Ames, IA. Gal, J., Xia, J.K., Cui, Z.L., Ren, Z.J., Pu, F.H. and Ji, D.F., 1989. A study on resistance of soybean from southern China to beanfly. In: ed. A.J. Pascale, Proc. of World Soybean Res. Conf. IV, Assoc. Argentina de la Soja, Buenos Aires, Argentina, pp. 1241-1245. Gibikpi, P.J. and Crookston, R.K., 1981. A whole-plant indicator of soybean physiology maturity. Crop Sci., 21: 469-472. Gilman, D.F., McPherson, R.M., Newsom, L.D., Herzog, D.C. and Williams, C., 1982. Resistance in soybeans to the southern green stink bug. Crop Sci., 22: 573-576. Gizlice, Z., Carter Jr., T.E. and Burton, J.W., 1994. Genetic base for North American public soybean cultivars released between 1947 and 1988. Crop Sci., 34: 1143-1151. Good, J.M., 1973. Nematodes. In: ed. B.E. Caldwell, Soybeans: Improvement, Production and Uses. Agron. Mongr. 16, 1st ed. ASA, CSSA, and SSSA, Madison, WI, pp. 527-543. Grabe, D.F. and Metzer, R.B., 1969. Temperature inhibition of soybean hypocotyl elongation and seedling emergence. Crop Sci., 9: 331-333. Graef, G.L., Fehr, W.R. and Cianzio, S.R., 1989. Relation of isozyme genotypes to quantitative characters in soybean. Crop Sci., 29: 683-688. Graham, P.H. and Rosas, J.C., 1984. Selection for improved nitrogen fixation in Glycine max (L.) and Phaseolus vulgaris L. Plant and Soil, 82: 315-327. Hammond, E.G. and Fehr, W.R., 1983. Registration of A5 germplasm line of soybean. Crop Sci., 23: 192. Hanson, W.D., 1992. Phenotypic recurrent selection for modified reproductive period in soybean. Crop Sci., 32: 968-972. Hanson, W.D. and Kamprath, E.J., 1979. Selection for aluminum tolerance in soybean based on seedling-root growth. Agron. J., 71: 581-586. Hartung, R.C., Specht, J.E. and Williams, J.H., 1981. Modification of soybean plant architecture by genes for stem growth habit and maturity. Crop Sci., 21: 51-56. Hartwig, E.E., 1954. Lee, a superior soybean for the mid-south. Soybean Dig., 14: 14-15. Hartwig, E.E. and Kiihl, R.A.S., 1979. Identification and utilization of a delayed flowering character in soybeans for short-day conditions. Field Crops Res., 2: 145-151. Hartwig, E.E. and Potts, H.C., 1987. Development and evaluation of impermeable seed coats for preserving soybean seed quality. Crop Sci., 27: 506-508. Heatherly, L.G., 1993. Drought stress and irrigation effects on germination of harvested soybean seeds. Crop Sci., 33: 777781. Heenan, D.P. and Carter, O.G., 1976. Tolerance of soybean cultivars to manganese toxicity. Crop Sci., 16: 389-391. Herridge, D.F. and Rose, I.A., 1994. Heritability and repeatability of enhanced N 2 fixation in early and late inbreeding generations of soybean. Crop Sci., 34: 360-367. Hill, H.J., West, S.H. and Hinson, K., 1986. Soybean seed size influences expression of the impermeable seed-coat trait. Crop Sci., 26: 634-637. Hinson, K., 1989. Use of a long juvenile trait in cultivar develop-

ment. In: ed. A.J. Pascale, Proc. World Soybean Res. Conf. IV. Assoc. Argentina de la Soja, Buenos Aires, pp. 983-987. Hintz, R.W., Fehr, W.R. and Cianzio, S.R., 1987. Population development for selection of high-yielding soybean cultivars with resistance to iron-deficiency chlorosis. Crop Sci., 22: 433-434. Holbrook, C.C., Burton, J.W. and Carter Jr., T.E., 1989. Evaluation of recurrent restricted index selection for increasing yield while holding seed protein constant in soybean. Crop Sci., 29: 324-329. Howle, D.S. and Caviness, C.E., 1988. Influence of cultivar and seed characteristics on vertical weight displacement by soybean seedlings. Crop Sci., 28: 321-324. Huck, M.G. and Davis, J.M., 1976. Water requirements and root growth. In: ed. L.D. Hill, World Soybean Reserach. Interstate Printers and Publishing, Danville, IL, pp. 16-27. Hudak, C.M. and Patterson, R.P., 1995. Vegetative growth analysis of a drought-resistant soybean plant introduction. Crop Sci., 35: 464-471. Hume, D.J. and Jackson, A.K.H., 1981. Pod formation in soybeans at low temperatures. Crop Sci., 21: 933-937. Hymowitz, T., 1970. On the domestication of the soybean. Econ. Bot., 24: 408-421. Kasper, T.C., Taylor, H.M. and Shibles, R.M., 1984. Tap root elongation rates of soybean cultivars in the glasshouse and their relation to field rooting depth. Crop Sci., 24: 916-920. Keim, P., Diers, V.W., Olsen, T.C. and Shoemaker, R.C., 1990a. RFLP mapping in soybean: Association between marker loci and variation in quantitative traits. Genetics, 126: 735-742. Keim, P., Diers, B.W. and Shoemaker, R.C., 1990b. Genetic analysis of soybean hard seededness with molecular markers. T.A.G., 79: 465-469. Kenworthy, W.J. and Brim, C.A., 1979. Recurrent selection in soybeans. I. Seed yield. Crop Sci., 19: 315-318. Knittle, K.H. and Burris, J.S., 1979. Hypocotyl growth under field conditions. Crop Sci., 19: 37-41. Koon-Hup, L., 1977. Sampling design for determining quantitative distribution of roots. M.Sc. Thesis, North Carolina State University, Raleigh, NC. Latimore, M.A., Giddens, J. and Ashley, D.A., 1977. Effect of ammonium and nitrate nitrogen upon photosynthate supply and nitrogen fixation by soybeans. Crop Sci., 17: 399-403. Lee, S.H., Ashley, D.A. and Boerma, H.R., 1991. Regulation of nodule development in supernodulating mutants and wild-type soybeans. Crop Sci., 31: 688-693. Lersten, N.R. and Carlson, J.B., 1987. Vegetative morphology. In: ed. J.R. Wilcox, Soybeans: Improvement, Production and Uses, Agron. Mongr. 16, 2nd ed. ASA, CSSA, and SSSA, Madison, WI, pp. 49-94. Lewers, K.S., St. Martin, S.K., Hedges, D.R., Widflechmer, M.P. and Palmer, R.G., 1996. Hybrid seed production: Comparison of three methods. Crop Sci., 36. Luedders, V.D., 1977. Genetic improvement of yield in soybeans. Crop Sci., 17: 971-972. Major, D.J., Johnson, D.R., Tanner, J.W. and Anderson, I.C., 1975. Effects of day length and temperature on soybean development. Crop Sci., 15: 174-179.

J.W. Burton~Field Crops Research 53 (1997) 171-186 Mansur, L.M., Lark, K.G., Kross, H. and Oliveira, A., 1993. Interval mapping of quantitative trait loci for reproductive, morphological, and seed traits of soybean (Glycine max L.). T.A.G., 86: 907-913. Martineau, J.R., Williams, J.H. and Specht, J.E., 1979. Temperature tolerance in soybeans. II. Evaluation of segregating populations for membrane thermostability. Crop Sci., 19: 79-81. Metz, G.L., Green, D.E. and Shibles, R.M., 1985. Reproductive duration and date of maturity in populations of three wide soybean crosses. Crop Sci., 25: 171-176. Miller, J.E. and Fehr, W.R., 1979. Direct and indirect recurrent selection for protein in soybeans. Crop Sci., 19: 101-106. Morse, W.J., 1950. History of soybean production. In: ed. K.S. Markley, Soybeans and Soybean Products. Interscience Publishers, New York, pp. 3-59. Muthiah, S., Langer, D.E. and Harris, W.M.., 1994. Staging soybean seedling growth from germination to emergence. Crop Sci., 34: 289-291. Nelson, R.L. and Bernard, R.L., 1984. Production and performance of hybrid soybeans. Crop Sci., 23: 549-553. Nissly, C.R., Bernard, R.L. and Hittle, C.N., 1981. Variation in photoperiod sensitivity for time of flowering and maturity among soybean strains of maturity group III. Crop Sci., 21: 833-836. Oosterhuis, D.M., Walker, S. and Eastham, J., 1985. Soybean leaflet movements as an indicator of crop water stress. Crop Sci., 25: 1101-1106. Openshaw, S.J. and Hadley, H.H., 1984. Selection indexes to modify protein concentration of soybean seeds. Crop Sci., 24: 1-4. Off, J.H. and Helms, T.C., 1994. Selection to maximize gross value per hectare within three separate soybean populations. Crop Sci., 34: 1163-1167. Ouattera, S. and Weaver, D.B., 1994. Effect of growth habit on yield and agronomic characteristics of late-planted soybean. Crop Sci., 34: 870-873. Padgette, S.R., Kolacz, K.H., Delanney, X., Re, D.B., LaValee, B.J., Tinius, C.N., Rhodes, W.K., Otero, Y.I., Barry, G.F., Eicholtz, D.A., Peschke, V.M., Nida, D.L., Taylor, N.B. and Kishore, G.M., 1995. Development, identification, and characterization of a glyphosate-tolerant soybean line. Crop Sci., 35: 1451-1461. Palmer, R.G. and Kilen, T.C., 1987. Qualitative genetics and cytogenetics. In: ed. J.R. Wilcox, Soybeans: Improvement, Production, and Uses. Agron. Mongr. 16, 2nd ed. ASA, CSSA, and SSSA, Madison, WI, pp. 135-209. Palmer, R.G. and Payne, R.C., 1979. Genetic control of hypocotyl pigmentation among white-flowered soybeans grown in continuous light. Crop Sci., 19: 124-126. Panizzi, A.R. and Shiga, M., 1994. Feeding frequency and duration of nymphal and adult southern green stink bug, Nezara Viridula (L.) on soybean seed. World Soybean Res. Conf. V: Abstracts of Papers, p. 13. Pantalone, V.R., Burton, J.W. and Carter Jr., T.E., 1994. Heritability of a fibrous root trait in soybean. Agron. Abstr., p. 109. Pantalone, V.R., Rebetzke, G.J., Burton, J.W. and Carter Jr., T.E.,

185

1996. Phenotypic evaluation of root traits in soybean and applicability to plant breeding. Crop Sci., 36. Poison, D.E., 1972. Day neutrality in soybeans. Crop Sci., 12: 773-776. Probst, A.H. and Judd, R.W., 1973. Origin, US History and Development, and World Distribution. In: ed. B.E. Caldwell, Soybeans: Improvement, Production, and Uses. Agron. Mongr. 16, 1st ed. ASA, CSSA, and SSSA, Madison, WI, pp. 1-15. Rahman, S.M.A.S. and Bhattacharya, A.H., 1994. Sources of resistance in soybean to stem fly. World Soybean Res. Conf. V: Abstracts of Papers, p. 13. Ray, J.D., Hinson, K., Mankono, J.E.B. and Malt, M.F., 1995. Genetic control of a long-juvenile trait in soybean. Crop Sci., 35: 1001-1006. Reicosky, D.A., Off, J.H. and Poneleit, C., 1982. Soybean germplasm evaluation for length of seed filling period. Crop Sci., 22: 319-322. Robacker, D.C., Flottum, P.K., Sammataro and Erickson, E.H., 1983. Effects of climatic and edaphic factors on soybean flowers and on the subsequent attractiveness of the plants to honey bees. Field Crops Res., 6: 267-278. Robertson, W.K., Hammond, L.C., Johnson, J.T. and Boote, K.J., 1980. Effects of plant-water stress on root distribution of corn, soybeans, and peanuts in sandy soil. Agron. J., 72: 548-550. Ronis, D.H., Sammons, D.J., Kenworthy, W.J. and Meisinger, J.J., 1985. Heritability of total and fixed N content of seed in two soybean populations. Crop Sci., 25: 1-4. Rose, J.L., Butler, D.G. and Ryley, M.J., 1992. Yield improvement in soybeans using recurrent selection. Aust. J. Ag. Res., 43: 135-144. Ross, J.P., 1986. Registration of eight soybean germplasm lines resistant to seed infection by Phomopsis ssp. Crop Sci., 26: 210-211. Rossetto, C.J., Razera, L.F., Tisselli, O., Gallo, P.B., Bortoletto, N., Medina, P.F. and Pinheino, J.B., 1994. Mechanisms of resistance to stink bug complex in the soybean cultivar IAC 100. World Soybean Res. Conf. V: Abstracts of Papers, p. 26. Sammons, D.J., Peters, D.B. and Hymowitz, T., 1978. Screening soybeans for drought resistance. I. Growth Chamber Procedure. Crop Sci., 18: 1050-1055. Schmitthenner, A.F., Hobe, M. and Bhat, R.G., 1994. Phytophthora sojae races in Ohio over a 10-year intemai. Plant Disease, 78: 269-276. Sebem, N.A. and Lambert, J.W., 1984. Effect of stratification for percent protein in two soybean populations. Crop Sci., 24: 225-228. Seddigh, M., Joliff, G.D. and Off, J.H., 1988. Field evaluation of early maturing soybean genotypes for differential adaptation to low night temperatures. Crop Sci., 28: 639-643. Sinclair, T.R., Soffes, A.R., Hinson, K., Albrecht, S.L. and Pfahler, P.L., 1991. Genotypic variation in soybean nodule number and weight. Crop Sci., 31: 301-304. Sloane, R.J., Patterson, R.P. and Carter Jr., T.E., 1990. Field drought tolerance of a soybean plant introduction. Crop Sci., 30: 118-123. Smith, J.R. and Nelson, R.L., 1986a. Selection for seed-filling period in soybean. Crop Sci., 26: 466-469.

186

J. W. Burton/Field Crops Research 53 (1997) 171-186

Smith, J.R. and Nelson, R.L., 1986b. Relationship between seedfilling period and yield among soybean breeding lines. Crop Sci., 26: 469-472. Snape, J.W. and Riggs, T.J., 1975. Genetical consequences of Jingle seed descent in the breeding of self-pollinated crops. Heredity, 35: 211-219. So-rrells, M.E. and Pappelis, A.J., 1976. Effect of temperature and osmotic concentration on cotyledon cracking during imbibition of soybean. Crop Sci., 16: 413-415. Specht, J.E. and Williams, J.H., 1984. Contribution of genetic technology to soybean productivity - - retrospect and prospect, In: ed. W.R. Fehr, Genetic Contribution to Yield Gains of Five Major Crop Plants. Spec. Pub. 7. CSSA and ASA, Madison, WI, pp. 49-74. ~pecht, J.E., Williams, J.H. and Weidenbenner, C.J., 1986. Differential responses of soybean genotypes subjected to a seasonal soil water gradient. Crop Sci., 26: 922-934. Starnes, W.J. and Hadley, H.H., 1965. Chlorophyll content of various strains of soybeans, Glycine max (L.) Merrill. Crop Sci., 5: 9-11. Stelly, D.M. and Palmer, R.G., 1985. Relative development of basal, medial, and apical ovules in soybean. Crop Sci., 25: 877-879. Talekar, N.S., 1994. Sources of resistance to insect pests of soybean in Asia. Word Soybean Res. Conf. V: Abstracts of Papers, p. 12. Tanasch, L. and Gretzmacher, R., 1991. Influence of photoperiod and temperature on flower induction of soybeans. Eurosoya, 7/8: 10-15. Taylor, B.H. and Caviness, C.E., 1982. Hilum color variation in soybean seed with imperfect black genotype. Crop Sci., 22: 682-683. Thomas, J.F. and Raper, C.D., 1976. Photoperiodic control of seed filling for soybeans. Crop Sci., 16: 667-672. Thomas, J,F. and Raper, C.D., 1984. Photoperiod regulation of floral initiation for soybean plants at different ages. Crop Sci., 24: 611-614. Tinius, C.N., Burton, J.W. and Carter Jr., T.E., 1991. Recurrent selection for seed size in soybean, I. Response to selection in replicate populations. Crop Sci., 31: 1137-1141. Turnipseed, S.G. and Kogan, M., 1987. Integrated control of insect pests. In: ed. J.R. Wilcox, Soybeans: Improvement, Production, and Uses. Agron. Mongr. 16, 2nd ed. ASA, CSSA, and SSA, Madison, WI, pp. 779-817. Unander, D.W., Off, J.H. and Lambert, J.W., 1986. Early season cold tolerance in soybean. Crop Sci., 26: 676-680. Van Shaik, P.H. and Probst, A.H., 1958. Effect of some environmental factors on flower and reproductive efficiency in soybeans. Agron. J., 50: 192-197. Van Toai, T.T., Beuerlein, J.E., Schmitthenner, A.F. and St. Martin, S.K., 1994. Genetic variability for flooding tolerance in soybean. Crop Sci., 34: 1112-1115. Van Raamsdonk, L.W.D., 1995. The cytological and genetical

mechanisms of plant domestication exemplified by four crop models. Bot. Rev., 61: 367-399. Vaughn, D.A., Bernard, R.L., Sinclair, J.B. and Kunwar, I.K., 1987. Soybean seed coat development. Crop Sci., 27: 759-765. Walker, A.K., Cianzio, S.R., Bravo, J.A. and Fehr, W.R., 1979. Comparison of emasculation and nonemasculation for artificial hybridization of soybeans. Crop Sci., 19: 285-286. Wehrmann, V.K., Fehr, W.R., Cianzio, S.R. and Cavins, J.F., 1987. Transfer of high seed protein to high-yielding soybean cultivars. Crop Sci., 27: 927-931. Wells, R., Burton, J.W. and Kilen, T.C., 1993. Soybean growth and light interception: Response to differing leaf and stem morphology. Crop Sci., 33: 520-524. White, M.C., Chaney, R.L. and Decker, A.M., 1979. Role of roots and shoots of soybean in tolerance to excess soil zinc. Crop Sci., 19: 126-128. Wilcox, J.R., Burton, J.W., Rebetzke, G.J. and Wilson, R.F., 1994. Transgressive segregation for palmitic acid in seed oil of soybean. Crop Sci., 34: 1248-1250. Wilcox, J.R. and Cavins, J.F., 1986. Registration of C1640 soybean germplasm. Crop Sci., 26: 209-210. Wilcox, J.R. and Cavins, J.F., 1995. Backcrossing high seed protein to a soybean cultivar. Crop Sci., 35: 1036-1041. Wilcox, J.R., Laviolette, F.A. and Martin, R.J., 1975. Heritability of purple seed strain resistance in soybean. Crop Sci., 15: 525-526. Wilcox, J.R., Schapaugh Jr., W.T., Bernard, R.L., Cooper, R.L., Fehr, W.R. and Niehaus, M.H., 1979. Genetic improvement of soybeans in the midwest. Crop Sci., 19: 803-805. Williams, L.F., 1950. Structure and genetic characteristics of the soybean. In: ed. K.S. Markley, Soybeans and Soybean Products. Interscience Publishers, New York. Willett, W.C., 1994. Diet and health: What should we eat? Science, 274: 532-537. Wittenbach, V.A., Ackerson, R.C., Giaquinta, R.T. and Hebert, R.R., 1980. Changes in photosynthesis, ribulose phosphate carboxylase, proteolytic activity and ultra structure of soybean leaves during senescence. Crop Sci., 20: 225-231. Wofford, T.J. and Allen, F.L., 1982. Variation in leaflet orientation among soybean cultivars. Crop Sci., 22: 999-1004. Wu, S. and Harper, J.E., 1991. Dinitrogen fixation potential and yield of hyper-nodulating soybean mutants: A field evaluation. Crop Sci., 31: 1233-1240. Xu Ban, Zhen Huiyu, Lu Qinhua, Zhao Shuwen and Hu Ziang, 1989. Three evidences of the original area of soybean. In: Proc. of World Soybean Res. Conf. IV. Assoc. Argentina de la Soja, Buenos Aires, Argentina, pp. 124-128. Yaklich, R.W., Virgil, E.L. and Wergin, W.P., 1986. Pore development and seed coat permeability in soybean. Crop Sci., 26: 616-624. Zobel, R.W., 1983. Genic duplication: A significant constraint to molecular and cellular genetic manipulation in plants. Comments Mol. Cell. Biophys., 1: 355-364.