Plant Breeding Reviews (Janick/Plant) || Breeding Soybeans Resistant to Diseases

7

Breeding Soybeans Resistant to Diseases

J. R. Wilcox1

U.S. Department of Agriculture, Agricultural Research Service, and Purdue University, West Lafayette, Indiana 47907

I. Introduction 184 II. Breeding Methods 185

A. Hybridization 185 B. Pedigree Method 186 C. Backcross Method 186 D. Single Seed Descent Method 187

III. Fungal Diseases 188 A. Phytophthora Rot 188 B. Brown Stem Rot 196 C. Stem Canker 197 D. Brown Spot 199 E. Frogeye Leafspot 200 F. Downy Mildew 201 G. Powdery Mildew 202 H. Target Spot 203 I. Soybean Rust 204 J. Pod and Stem Blight 206 K. Purple Seed Stain 208

IV. Bacterial Diseases 209 A. Bacterial Blight 209 B. Bacterial Pustule 210 C. Wildfire 211

V. Virus Diseases 212 A. Soybean Mosaic Virus 212 B. Bean Pod Mottle Virus 213

1 The author gratefully acknowledges the helpful suggestions of Dr. K.L. Athow, Dr. R.L. Bernard, and Dr. E.E. Hartwig in the preparation of this manuscript.

183

Plant Breeding Reviews Edited by Jules Janick

© Copyright 1983 The AVI Publishing Company, Inc.

184 PLANT BREEDING REVIEWS

C. Cowpea Chlorotic Mottle Virus D. Peanut Mottle Virus 214 E. Tobacco Ringspot Virus 215 F. Virus Methods 216

A. Soybean Cyst Nematode 217 B. Root-Knot Nematode 219 C. Reniform Nematode 220

VII. Summary and Conclusions 221 Literature Cited 222

214

VI. Nematodes 217

I. INTRODUCTION

The soybean is a member of the Leguminosae, subfamily Papilionoi- deae, and the genus Glycine. The cultivated form, Glycine max (L.) Merrill, is grown in most of the temperate and subtropical areas of the world as a source of oil and protein (Probst and Judd 1973). Mature soybean seeds contain about 20% oil and 40% protein that has a good balance of essential amino acids. The oil is used primarily for human consumption, and a small quantity goes into industrial uses. After the oil is extracted from the seed, the residual meal is used primarily as a livestock feed. The protein, however, is extracted from a small percentage of the meal and is used in various food products for human consumption.

World soybean production in 1979 totaled 96.5 million metric tons, which was grown on 53 million hectares. The United States produced 64%, Brazil 15%, mainland China 11%, and other countries the remain- ing 10% of the world’s production (USDA 1980).

Over 100 pathogens are known to attack soybeans; of these, 35 are of some economic importance. Generally, one or more soybean diseases can be found in fields wherever soybeans are grown. In specific areas where pathogens are endemic in the soil or where environmental conditions favorable for specific disease development commonly occur, losses due to diseases may occur with regularity. Where environmental conditions vary from one year to the next, diseases may be very destructive in one season, then not reappear the following season (Sinclair and Shurt- leff 1975).

Estimating total losses due to diseases is difficult because many factors influence disease prevalence and severity and have confounding effects on yield. Southern research and extension personnel have estimated yield losses due to diseases in 13 southern states in the United States for 1979. Estimated disease losses for the various pathogens were fungi, 11.9%; bacteria, 0.2%; viruses, 0.4%; and nematodes, 6.5%, for a

7 BREEDING SOYBEANS RESISTANT TO DISEASE 185

total loss due to all pathogens of 19% (R.V. Sturgeon, personal communication). Estimates of yield losses due to diseases obtained from a 1976 survey of Midwest pathologists were fungi, 9.0%; bacteria and viruses less than 1%, for a total loss of 9.5% in ten midwestern states. Average yield losses due to the soybean pathogens in 1979 probably averaged 14% of the crop, valued at 1.96 billion dollars.

Breeding soybeans for resistance to the most destructive pathogens has been an effective method of minimizing disease losses. Several articles are useful references for the breeder or pathologist interested in breeding for disease resistance. Reviews of fungal diseases (Athow 1973), bacterial diseases (Kennedy and Tachibana 19731, virus diseases (Dunleavy 19731, and nematodes (Good 1973) are included in the mon- ograph Soybeans: Improvement, Production, and Uses published by the American Society of Agronomy. The International Soybean Program (INTSOY) has published an annotated “Bibliography of Soybean Dis- eases” (Sinclair and Dhingra 1975) and “Sources of Resistance to Se- lected Fungal, Bacterial, Viral and Nematode Diseases of Soybeans” (Tisselli et al. 1980), both of which are useful references.

This review presents a current account of the genetics of disease resistance in soybeans and the methods used to breed soybeans for resistance to the major pathogens causing economic losses.

11. BREEDING METHODS

The soybean is a self-pollinated plant, and less than 1% outcrossing normally occurs. Methods of breeding self-pollinated crops, as given by Allard (19601, are applicable with this species; and pedigree, backcrossing, and single seed descent are the common methods used to incorporate disease resistance into soybean cultivars.

A. Hybridization

Techniques for hybridizing soybeans have been described and illus- trated by Paschal (1976) and Fehr (1980). Flowers used as “females” are prepared for pollination the day before they would normally open. The calyx and corolla are removed with fine tweezers, exposing the stigma and surrounding ring of immature anthers. Complete emasculation of the flower is unnecessary, but anthers just below the stigma are usually removed to facilitate pollination. The stamina1 column is removed from “male” flowers at anthesis, and pollen is brushed onto the stigma of the previously prepared female flower. In the northern United States, pollinations are usually made as soon as the female flowers have been prepared, using freshly collected flowers as males. In the southern


states, pollen flowers are usually collected in the morning and stored in a desiccator, and female flowers are prepared and immediately pollinated in the afternoon. It is not necessary to protect pollinated flowers from desiccation or stray pollen. Pollinations are identified with a tag attached to the internodes below the pollinated flower to identify the cross and to aid in locating the crossed seed when the plant is mature.

B. Pedigree Method

The pedigree method has been used to develop cultivars with new combinations of agronomic characteristics and disease resistance. One of the parents must be resistant to the disease or pathogen of interest. Crosses are made between the chosen parents, and the F1 generation is grown under conditions that will maximize seed production per plant. Initial disease evaluations may be made in the F2 generation, where one-fourth of the population will be homozygous resistant to the disease if resistance is controlled by a single recessive gene. Susceptible plants can be discarded, and selection for agronomic characteristics can be made in succeeding generations. If reaction to the pathogen is controlled by a single dominant gene, inoculation of F2 plants will identify the combined one-fourth homozygous resistant and one-half heterozygous resistant plants. Maintaining pedigrees of individual plants in succes- sive generations is essential. The pedigree method of breeding is also useful for genetic studies of disease resistance where the genotype of individual plants must be determined.

C. Backcross Method

This breeding method has been used to incorporate single-gene resistance to specific pathogens into many soybean cultivars. A soybean strain with a specific gene for resistance is used as a donor parent and crossed with a superior cultivar that lacks the gene for resistance to the pathogen. The heterozygous F1 is crossed back to the superior cultivar, and the seeds from this cross will be either heterozygous (resistant) or homozygous (susceptible) if resistance is controlled by a dominant gene. Seedling or preflowering inoculations may be used to identify the heterozygous resistant plants, which are again backcrossed to the superior, recurrent parent at the onset of flowering. The process is repeated until 4-7 backcrosses have been completed, at which time the backcross line will contain an average of 97-99% of the genes of the recurrent parent plus the gene for disease resistance from the donor parent. Heterozygous F, plants from the final backcross are self-pollinated, and their progeny are inoculated to identify the homozygous recessive (sus-


ceptible) individuals. The homozygous resistant F2 plants can be sepa- rated from the heterozygous F2 plants by inoculating 10-20 progeny from each F2 plant with the pathogen. If a recessive gene controls resistance to the pathogen, every other backcross must be followed by a generation of selfing to identify the homozygous recessive (resistant) plants.

Backcrossing to develop disease-resistant cultivars has advantages over other breeding methods. Success is assured, because the objective is to recover a superior genotype plus the gene for resistance, and 4-7 backcrosses are usually adequate. Public soybean breeders have agreed that strains derived from 4 or more backcrosses may be entered into the cooperative tests required before their release as new cultivars (Wilcox and Knapp 1980). A second advantage is that, because only a few plants are needed each generation, plants can be grown in greenhouses or growth chambers and three backcross generations can be evaluated each year. This reduces the time required for the development of a disease-resistant cultivar. Using the method as described, the name of the recurrent parent is retained and the year of release of the resistant form of the cultivar is added to the name, as in ‘Amsoy 71’ or ‘Williams 79.’

One disadvantage of backcrossing is that the recovered line is not expected to be superior to the recurrent parent in the absence of the disease. If improved cultivars have been developed and released concur- rently with a backcrossing program, the disease resistant cultivar will be lower yielding than the best recently developed cultivars. To minimize this problem, Hartwig has used one or two backcrosses to transfer resistance from non-adapted germplasm to a series of superior cultivars. The recurrent parent may change from a commonly grown cultivar to the most recently released superior cultivar during backcrossing. This tends to minimize yield differences between the disease resistant and the best cultivars in the absence of the disease (E.E. Hartwig, personal communication).

D. Single Seed Descent Method

Brim (1966) proposed a modified pedigree method of selection in soybeans that has been called single seed descent. One seed from each F2 plant is advanced to the next generation, and the process is repeated in succeeding generations until the desired level of inbreeding is attained.

This method of breeding is well adapted to the development of soybean lines that are homozygous for genes controlling disease resistance. Progenies from resistant x susceptible crosses are advanced to homo- zygosity by growing in each generation a single plant from each of


a large number of individuals in the preceding generation. Because no selection is practiced and only a single seed per plant is needed, 3 generations can be grown per year, 2 in greenhouses or in tropical areas during the temperate winters, to quickly increase the proportion of homozygous individuals in the population. The proportion of individuals homozygous for a given allele is (2”-1)/2”+l where n equals the number of generations of inbreeding. Therefore, by the F6 generation, after 5 generations of inbreeding, the proportion of homozygous dominant or recessive individuals would be 31/64 of the population, and only 2/64 of the population would be heterozygous for the alleles. Seedlings from individual F6 plants can be inoculated with the pathogen to determine the genotype of the F6 plants and those homozygous for resistance retained for agronomic evaluations.

111. FUNGAL DISEASES

Diseases caused by fungi may be restricted to a single plant part: root, stem, leaf, or seed, or may be present on several parts of the plant. Most of the economic losses due to a single pathogen are restricted to a single part of the plant. Fungal diseases can cause poor emergence after planting, losses in seed yield due to low plant vigor or defoliation, and poor quality seed.

A. Phytophthora Rot

Phytophthora rot, caused by Phytophthora megasperma Drechs. f. sp. glycinea (Syn. P. megasperma Drecks. var. sojae A.A. Hildeb.), is one of the most destructive soybean diseases in the United States. The pathogen causes pre- and postemergence damping off of seedlings and a root and stem rot that results in wilting and death ofplants from the primary leaf stage to maturity (Kaufmann and Gerdemann 1958). The disease may also reduce the vigor of susceptible plants and thus reduce yields.

When the disease was first reported, the cultivars ‘A.K.,’ ‘Arksoy,’ ‘Blackhawk,’ ‘CNS,’ ‘Dorman,’ ‘Harly,’ ‘Illini,’ ‘Monroe,’ and ‘Mukden’ were all resistant and ‘Hawkeye,’ ‘Capital,’ and ‘Lincoln’ were susceptible to the pathogen. Inoculation of progenies from crosses between resistant and susceptible cultivars indicated resistance was controlled by a single dominant gene, Ps (Bernard et al. 19571, which was later changed to Rps (Hartwig et al. 1968).

A second race of the pathogen was identified based on different reactions of the soybean strain D60-9467 to two isolates (Morgan and Hartwig 1965). Inheritance studies indicated that resistance to race 2


was controlled by the gene rps2, which was part of an allelomorphic series with Rps dominant to rps2, which was dominant to rps (Hartwig et al. 19681.

Additional physiologic races of the pathogen reported include race 3 (Schmitthenner 19721, race 4 (Schwenk and Sim 19741, races 5 and 6 (Haas and Buzzell 1976), races 7,8, and 9 (Laviolette and Athow 1977) and races 10 through 16 (Keeling 1980). Reactions of soybean differentials, selected by soybean breeders and pathologists at a meeting a t Harrow, Ontario, in 1976 to the various races are shown in Table 7.1.

Additional genes have been reported that control resistance to specific races of the pathogen. Kilen et al. (1974) identified a dominant gene, designated Rps2, in the cultivar ‘CNS’ based on the reaction of progenies from crosses between ‘CNS-derived lines and susceptible strains to liquid cultures of the pathogen. They suggested changing the previously reported locus, Rps , rps’, rps to Rpsl , rps12, rpsl, t o distinguish it from the second locus. Mueller et al. (1978) identified the gene Rps‘ in P1 54615-1, and suggested changing the rps2 designation to Rps‘, forming the allelic series, in decreasing order of dominance, of Rps“, Rps’, and rps. They also identified in P1 86972- 1 the dominant allele Rps3 at a different locus from those previously reported. Laviolette et al. (1979) extended the number of physiologic races of the pathogen controlled by specific genes, showing that Rps‘ controlled resistance to races 1, 3, 4, and 5 through 9; Rps‘ controlled resistance to races 1 through 3 and 6 through 9. The independent gene Rps3 controlled resistance to races 1 through 4 and 5, 8, and 9. Athow et al. (1980) reported a gene at a new locus, Rps4, that controls resistance to races 1 through 4 of the pathogen. The gene Rps5, that resulted in resistance to races 1 through 5 and 8 and 9 but susceptibility to races 6 and 7, was identified by Buzzell and Anderson (1981). An additional gene at the rpsl locus, Rpskl , in the variety ‘Kingwa’ has been reported by Bernard and Cremeens (1981) that controls resistance to races 1 through 10’13, 14, and 15 but results in susceptibility to races 12 and 16. Genes for resistance to specific races of Phytophthora are summarized in Table 7.2.

When it was first determined that resistance to the pathogen was controlled by a readily identifiable dominant gene, backcrossing was used to transfer resistance into several good cultivars that lacked resistance. Resistant isolines developed by this method were released with the year of release appended to the original cultivar name: ‘Clark 63,’ ‘Harosoy 63,’ ‘Hawkeye 63,’ ‘Lindarin 63,’ ‘Chippewa 64,’ ‘Lee 68,’ ‘Amsoy 71,’ ‘Cutler 71,’ and ‘Pickett 71.’

Wilcox et al. (1971) evaluated the efficiency of backcrossing as a

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method of transferring a specific gene for phytophthora resistance into 5 soybean cultivars. They compared the performance of random resistant and susceptible lines selected after each backcross generation. Results varied among crosses but, in general, recovery of the recurrent parent phenotype was slower than predicted if we assume only additive genetic control of the agronomic characteristics being evaluated. By the 7th backcross, yields of the resistant and susceptible isolines were not significantly below those of the recurrent parent. Because 3 backcrosses can be made per year, the authors concluded that 7 backcrosses without selection for agronomic characteristics, followed by elimination of plant rows that did not conform to the phenotype of the recurrent parent, would be the most efficient way to add phytophthora rot resistance to susceptible cultivars. This procedure would eliminate costly and time- consuming yield trials for comparison of the performance of the resistant isoline with that of the recurrent parent. The method has been used to transfer genes for phytophthora resistance into the cultivars ‘Wells 11’ and ‘Beeson 80.’

The proportion of resistant plants in a heterogeneous population can be increased by growing the population on soils infested with P. megasperma f. sp. glycinea. Buzzell and Haas (1972) determined the relative fitness of the Rps Rps versus the rps rps gene pairs by growing composites of cultivars differing in these alleles and in pubescence color. The average fitness of the rps allele relative to the Rps allele decreased from 0.784 to 0.372 on soils infested with the pathogen during the 3 years of the study. Their results indicated that natural and mass selection could increase the proportion of resistant plants in segregating bulk-hybrid populations.

An alternative to incorporating a series of race-specific genes for resistance to phytophthora rot into new cultivars is breeding for tolerance to the pathogen (Wilcox 1976). Tolerance is defined here as the ability of plants lacking major genes for resistance to specific races of the pathogen to endure infection by the fungus without serious yield losses. Advantages are that tolerance is reported to be race nonspecific (Walker and Schmitthenner 1979); and there is evidence that transgres- sive segregation can occur for tolerance (Schmitthenner and Walker 1979), which indicates a polygenic system is involved in its control. A polygenic system suggests that it should be possible to develop higher levels of tolerance than are present in existing cultivars. Schmitthenner and Walker (1979) list 2 disadvantages of tolerance for phytophthora rot control. First, absolute control is not obtained, and under severe disease conditions cultivars that are resistant to the prevalent races of the pathogen will yield more than cultivars that are tolerant to the patho-


gen. Second, all known tolerant cultivars are susceptible to damping off. Because tolerance does not seem to be expressed until seedlings are 7 days old, preemergence damping-off due to Phytophthora could be a severe problem with tolerant cultivars.

Both field and greenhouse techniques have been developed to screen soybeans for tolerance to phytophthora rot. Schmitthenner and Walker (1979) evaluate experimental lines in a hill-plot nursery in which the soil is naturally infested with several races of the pathogen. Lines that survive and yield well are tested in the greenhouse for resistance to specific races, and those lines that are susceptible are assumed to be tolerant to the pathogen. Wilcox (1976) has evaluated F5 or F, lines, developed by single seed descent, for major gene resistance to phytophthora rot. Susceptible lines are then tested where the disease is prevalent, and lines that yield well under these conditions are selected as tolerant to the pathogen.

Two greenhouse methods for screening for tolerance have been developed (Franks and Schmitthenner 1978; Jimenez and Lockwood 1978). Both methods involve germinating soybean seeds in a sterile medium and allowing the roots to grow through media containing the pathogen. Roots of tolerant cultivars are rotted, but the infection does not progress beyond the upper tap root of the seedling from which healthy secondary roots develop. Tolerance is rated as the incidence of surviving seedlings and as height of surviving plants.

Phytophthora megasperma f. sp. glycinea can be isolated from infected soybean tissue and maintained on potato-dextrose agar (PDA), cornmeal (Kaufman and Gerdeneau 19581, or lima bean agar (Calvert et al. 1960). Several techniques have been used to screen soybeans for reaction to the pathogen. Hypocotyl inoculation techniques include inserting a 2 x 2 mm piece of mycelium into a longitudinal slit in 10-day- old soybean seedlings (Kaufman and Gerdeman 1958; Lam-Sanchez et al. 1968) or injecting 4-day-old seedlings with a suspension of zoospores (Eye et al. 1978; Schwenk et al. 1979). Desiccation of wounds is prevented by covering the wound with petroleum jelly or putting the plants in a moist chamber. Resistant (no external disease symptoms) and susceptible (dead) plants can be identified 6 days after inoculation with myceluim and 3 days after inoculation with zoospores.

Screening has also been done in a liquid culture medium of the pathogen (Kilen et al. 1974). Seeds are germinated in vermiculite, then transplanted to holes spaced 5 cm apart in sheets of polystyrene floated on a culture of modified Hoagland's solution. A cornmeal agar slush culture of the pathogen is added to the culture solution 3 days after transplanting. Ten days after adding the fungus to the culture solution,


the plants can be classified as susceptible (dead or having lesions on the hypoctyl) or resistant.

With the discovery of several genes controlling resistance to different races of the pathogen, methods have been needed to simultaneously screen populations for more than one gene. Separate groups of seedlings from individual parent plants can be inoculated with different races of the pathogen to screen for specific genes for resistance, and although the method is time-consuming, this procedure is necessary for genetic studies of resistance. Hypocotyls of individual plants can be inoculated at different sites with different races of the pathogen and screened simultaneously for reaction to at least two races. Ward et al. (1979) were able to evaluate reactions of up to four races on a single hypocotyl by placing droplets of zoospore suspensions on hypocotyls of etiolated seedlings. Plants were maintained in a moist chamber for 20 to 24 hours at 25°C before the type of reaction was recorded.

By knowing the specific genes in the parents used in a cross and with a judicious selection of races used for inoculations, the plant breeder can screen for genes that will give resistance to several races with a minimum of effort. For example, in progenies segregating for the Rps! and Rps4 genes (Table 7.2), simultaneous inoculations with race 2 to screen for Rps; and with race 7 to screen for Rps, will identify plants resistant to both races and consequently to all 16 races of the pathogen. This procedure has been used by pathologists and plant breeders at Pur- due University to develop, through backcrossing, isolines of currently grown soybean cultivars that are resistant to all reported races of the pathogen.

Kilen and Keeling (1977) used the hydroponic inoculation technique to simultaneously screen soybeans for reaction to three races of the pathogen. Any genotype that showed susceptibility to one or more races of the pathogen when tested individually was also susceptible when tested with the mixture of the 3 races. No antagonistic effects among races were found. Kilen (1979) reported that hydroponic screening with only 2 races of the pathogen would be an efficient screening method to select families that were segregating for reaction to 4 or more races of the pathogen.

Morrison and Thorne (1978) inoculated detached soybean cotyledons to screen for reaction to two races of the pathogen. Cotyledons from seedlings were placed on moist filter paper and inoculated with a homogenate of an agar culture of the pathogen by using a hypodermic needle. Cotyledons of resistant genotypes showed only a slight discoloration at the inoculation site, whereas cotyledons of susceptible genotypes became severely necrotic 72 - 96 hours after inoculation. Results


of cotyledon inoculations were similar to those of hypocotyl inoculations when genotypes differing in their reaction to races 1 and 3 were tested. An advantage of the system is that it is nondestructive so that germplasm susceptible to specific races can be conserved.

B. Brown Stem Rot

Brown stem rot occurs frequently in the north central United States and Canada and has been reported in Mexico and Egypt (Athow, 1973; Sinclair and Shurtleff, 1975). Symptoms of the diseases, caused by Phialophora gregata (Allington & Chamberl.) W. Gams. (Syn. Cephalo- sporium gregatum Allington & Chamberl.), appear in July or early August as a brown discoloration of the pith and vascular elements extending from the base of the stem. There are no external symptoms of the disease at this time. Under conditions favorable for disease development, the brown discoloration becomes continuous throughout the stem. External symptoms appear in late August or September as an interveinal blighting and drying of the leaves, a result of a shortage of water (Allington and Chamberlain, 1948). A review of the disease, its pathogenic history, epidemiology, and methods of control has been written by Abel (1977). In years in which conditions are favorable for disease development the pathogen can cause significant yield reductions. Dunleavy and Weber (1967) showed yield reductions of 44% from growing soybeans on land planted continuously to soybeans for 10 years. Tachibana (1979) reported that the brown stem rot-resistant cultivar ‘BSR 301’ yielded 30% more than brown stem rot-susceptible cultivars of similar maturity when grown on fields where the disease has been a problem.

Gray (1971) identified 2 types of pathogenic isolates, Type I, which caused typical leaf symptoms and defoliation in addition to vascular discoloration, and Type 11, which caused only a less extreme vascular discoloration than Type I.

Resistance to the disease was identified in PI 84946-2. This strain had a high incidence of disease-free plants in 12 years of testing and transmitted the resistance to its progeny in crosses with susceptible cultivars (Chamberlain and Bernard 1968).

The resistance of PI 84946-2 was incorporated into two moderately resistant cultivars, ‘BSR 301’ and ‘BSR 302,’ through a breeding program at Iowa State University (W.R. Fehr and H. Tachibana, personal communication). Lines with this source of resistance were crossed with high yielding cultivars or breeding lines, and the populations were advanced to the F4 generation by single seed descent. The F4 plants were


grown in a field heavily infested with the pathogen, and plants with little or no internal stem browning were saved. Progeny rows from selected F4 plants were again grown on pathogen-infested soil and plants with adequate resistance, as determined by extent of internal stem browning, were evaluated in yield tests in the F6 and F7 generations, then evaluated in the Uniform Soybean Tests Northern States. The best line from this program was released as ‘BSR 301’ in 1979. A similar procedure was followed in the development of ‘BSR 302.’ Both varieties are recommended specifically for production on fields in which 75% or more of the plants were infected with the disease the previous year (Tachibana et ul. 1980, 1981).

A modification of the breeding method is now in use at Iowa State University in which F4 plants are evaluated in infested fields and 1000 plants with the best resistance available are selected. The F5 generation is yield-tested in replicated hill plots on infested soils, and the highest yielding lines are selected. The high yielding F6 lines are evaluated in replicated yield tests on both infested and noninfested soils before their entry into the Uniform Soybean Tests for final evaluations (W.R. Fehr, personal communication). Yield tests on infested and noninfested land permit the simultaneous evaluation of genetic potential for yield and for brown stem rot resistance.

The causal organism can be isolated from infested stems and maintained on PDA at 20°C. Sporulation is best on soybean stem agar (adding an extract of 25 g macerated green soybean stems in 100 ml water to 1 liter of 2% agar). Individual plants are inoculated by making stem punctures near the base of the stem and inserting small pieces of mycelium (Allington and Chamberlain 1948) or spore suspensions (Tachibana and Card 1972) into the wound. Disease severity evaluation is based on length of discoloration of the pith and vascular tissue after 5 weeks.

Extensive screening for resistance is commonly done by growing plants in fields containing soil infested with fungus, splitting the stems at physiological maturity, and evaluating the extent of internal stem browning.

Additional sources of resistance to brown stem rot that have been reported are PI 86150, PI 88820N, PI 90138, and PI 95769 (Tachibana and Card 1972).

C. Stem Canker

This disease, caused by Diuporthephuseolorum (Cke & Ell.) Sacc. var. cuulzuoru, Athow and Caldwell, has been very destructive on specific


cultivars of soybeans. Natural infection occurs when plants are at least 70 days old, during the time of pod fill, and the opportunity for adjacent, noninfected plants to compensate for the yield of killed plants is limited (Athow 1957, 1973; Athow and Caldwell 1954).

The disease was common throughout the north central United States and in Ontario, Canada, with the widespread production of the very susceptible cultivars ‘Hawkeye’ and ‘Blackhawk‘ (Athow 1969, 1973; Hildebrand 1952). In the late 1940s and early 1950s, when these cultivars were widely grown, fields with 30 to 75% infected plants were reported, and yield losses were estimated as high as 50% (Andrews 1950; Athow 1969; Crall 1949, 1951).

The pathogen is borne in the seed, in the soil, and on soybean debris from previous crops. Infection takes place through either the leaf blade or the juncture of the leaflets and petiole. The fungus grows through the petiole and into the main stem, causing a slightly shrunken lesion that girdles the stem and kills the plant. Green plant tissue above and below the lesion at the time the plant is killed is a diagnostic characteristic of this disease (Athow 1957, 1973).

Most currently grown cultivars are moderately resistant to stem canker, and it is unusual to find more than 1 to 5% infected plants in commercial fields of soybeans. There is some evidence that resistance has been derived from ‘Mandarin,’ which is in the ancestry of most of these cultivars (Athow 1969,1973). Soybean breeders neither evaluate plants for their reaction to this pathogen nor select for a high level of resistance to the disease. Breeding lines that are highly susceptible are discarded, which has resulted in the development of cultivars with adequate resistance to the disease.

The pathogen can be isolated from the green tissue adjacent to the stem lesion when symptoms first appear. Stems from killed plants can be put into a moist chamber where the fungus will produce perithecia on the stems. Ascospores can be collected from the beaks of perithecia protruding from the soybean stems. The fungus can be cultured on PDA (Athow, personal communication).

Soybean plants can be inoculated by inserting toothpicks overgrown with fungus into wounds made with an awl in stems of 26-84-day-old plants. However, this method of inoculation overcomes any morphological resistance of the plant (Athow 1954; Crall 1952; Hildebrand 1953). Dunleavy (1956) has suggested inserting toothpicks overgrown with the fungus into the top of the main stem after the distal portion, above the third node from the top, had been removed. Dunleavy was able to differentiate among resistant and susceptible cultivars based on the rate of growth and of symptom development down the stem.


D. Brown Spot

Brown spot, caused by Septoria glycines Hemmi is one of the most prevalent soybean diseases where the crop is grown in temperate areas of the world. The disease has been reported in the southern United States, but is not usually a problem there (Athow 1973).

The first symptoms of the disease are irregular dark-brown patches, up to 4 mm in size, on the cotyledons. Then, conspicuous, reddish-brown lesions, angular in outline and 1-5 mm in diameter appear on the unifoliolate leaves. Tissues surrounding the lesions are pale green, becoming chlorotic, after which the leaves drop off the plants. Under favorable weather conditions, the disease may move progressively up the plant, causing premature defoliation. Symptoms may also appear on stems, branches, and petioles of the plant (Wolf and Lehman 1926).

Yield reductions of 17- 18% (Williams and Nyvalll980; Young and Ross 1978a) have resulted from inoculating soybean plants with the pathogen at various growth stages.

No soybean strains have been identified that have a high level of resistance to the pathogen. Young and Ross (1978b) reported that PI 79609 produced abnormal lesions, which were black, and surrounding leaf tissue was not chlorotic, when inoculated with S. glycines. Mature seeds of this strain have green cotyledons, a characteristic which is controlled by two recessive genes, dl and d2. Progeny from crosses with this plant introduction segregated 15 susceptible: 1 resistant in reaction to the pathogen, and all resistant plants had green cotyledons. Apparently the nonchlorotic resistant reaction of PI 79609 is either a manifestation of, or closely linked to, chlorophyll retention in the cotyledons. Lim (1979) reported the same nonchlorotic lesion on isolines of ‘Clark‘ with green cotyledons. Because Lim did not observe any difference in the amount of defoliation or in the number and rate of pycnidia formation between plants grown from yellow and green seeds, he concluded the reaction of green cotyledon plants was not a resistant reaction to the pathogen. Athow (personal communication) has used PI 65338, PI 68708, and PI 79609 as sources of resistance to this disease.

S. glycines can be isolated from infested soybean plants and maintained on PDA. Inoculum is prepared from 2- to 3-week-old cultures of the pathogen by blending them in tap water for 2-3 minutes and filtering the homogenate through several layers of cheesecloth. Spore suspensions containing about 2 x lo5 spores/ml are sprayed on plants until run-off. A second inoculation method has been used in which 100 ml of the spore suspension was added to 1-liter flasks filled to one-third capacity with sterlized sorghum grain. After 4-5 weeks’ incubation at


22-24”C, the grain from individual flasks was mixed, dried, and spread uniformly within rows of field-grown soybeans (Lim 1979).

E. Frogeye Leafspot

Frogeye leafspot occurs worldwide on soybeans and is common in the southern United States, particularly during warm, humid weather (Sinclair and Shurtleff 1975). The pathogen Cercospora sojina Hara. causes gray or light tan lesions with a narrow, reddish-brown border on soybean leaves. The absence of yellowing around the spot is a distin- guishing symptom. Large lesions may coalesce to form irregular spots on the leaves, and when the lesions are numerous the leaves become dry and drop prematurely. Although frogeye leafspot is primarily a foliar disease, infections also occur on stems, pods, and seeds (Athow 1973).

The disease was of minor importance in Indiana until 1947, when it occurred in epiphytotic proportions in the large soybean growing area of southwestern Indiana (Athow and Probst 1952). ‘Gibson’ and ‘Patoka,’ cultivars highly susceptible to the disease, had been recently released and were grown widely in southwestern Indiana at the time. The disease was found on the cultivar ‘Hawkeye’ as far north as the northern third of Indiana in 1950.

Laviolette et al. (1970) reported yield reduction of 17% and 21% in a 2-year study in which the susceptible cultivar ‘Clark’ was inoculated 2 or 3 times with the pathogen. The authors suggested the continued use of resistant cultivars to prevent reestablishment of the disease in Indi- ana.

Races of the pathogen that have been reported are 1 and 2 (Athow et al. 19621, 3 and 4 (Ross 1968a), and 5 (Phillips and Boerma 1980). Yorinori and Homechin (1978) identified 6 races of the fungus in Brazil. The cultivars ‘Davis,’ ‘Kanrich,’ and ‘Ogden’ are resistant to all races that have been reported. Two dominant genes, Rcsl (formerly Csl) (Athow and Probst 1952) and Rcs2 (Probst et al. 1965) have been reported that control resistance to races 1 and 2. Genes for resistance can be readily incorporated into cultivars by backcrossing or, more commonly, by selecting for resistance in segregating progenies from crosses between resistant and susceptible cultivars.

Cercospora sojina can be isolated from lesions on the soybean plant and maintained on PDA. Inoculum is obtained by seeding solidified V-8 juice agar in petri plates with mycelium from PDA slant cultures. After 10 days the contents of several petri plates are macerated in a blender with water, diluted to the desired concentration, and sprayed on young, expanding trifoliolate leaves of the soybean plants. Individual plants may be incubated in mist chambers for 3 to 4 days. Successful


infections have been obtained on field grown soybeans by inoculating in the early evening when humidity is high (Probst et al. 1965; Ross 1968a). Plants with no lesions or a few small lesions are considered resistant whereas those with medium-sized and large, spreading lesions are considered susceptible.

F. Downy Mildew

This disease, caused by Peronospora manshurica (Naum) Syd. ex Gaum. is widespread on soybeans in the United States and occurs worldwide where soybeans are grown (Athow 1973). In the early stages of disease development the pathogen produces yellowish-green, irreg- ularly shaped areas on the upper leaf surface of susceptible cultivars. Later, a fluffy, gray, mold-like growth develops on lesions on the lower leaf surface. Infested seeds have a dull-white powdery encrustation on the seed coat. Tests have shown yield reductions of up to 8%, but measurable yield losses due to downy mildew are rare in the United States. Hartwig (personal communication) has measured no significant difference in yield between the susceptible cultivar ‘Lee’ and a resistant isoline D 49-2491 in 6 years of tests in which ‘Lee’ developed disease lesions.

Thirty-two physiologic races of the pathogen have been reported, based on their reaction on 11 soybean differentials (Dunleavy 1970, 1971,1977; Geeseman 1950; Grabe and Dunleavy 1959; Lehman 1953, 1958). Five cultivars or plant introductions, Kanrich, ‘Mendota,’ ‘Pine Dell Perfection,’ PI 171443, and PI 201422 have been reported to be immune or highly resistant to all known races of the pathogen (Dun- leavy 1970; Dunleavy and Hartwig 1970). Resistance in ‘Kanrich’ and ‘Pine Dell Perfection’ is due to a single dominant gene, R p m (Bernard and Cremeens 1971).

The gene R p m has been backcrossed into the cultivars ‘Chippewa,’ ‘Corsoy,’ and ‘Wayne’ (Bernard and Cremeens 1971). Several backcrosses were used to incorporate the gene into the cultivar ‘Williams,’ one of these backcross lines was named ‘Union’ and is the only cultivar with the R p m gene currently in commercial production.

Because Peronospora manshurica is an obligate parasite, the fungus can be maintained only in uiuo. Isolates of the fungus are usually obtained from soybean seeds encrusted with oospores. Infected seeds are planted in moist, sterile soil, and maintained at temperatures of 10” to 16°C to ensure slow germination and seedling growth. Ten to 40% of the seedlings develop systemic infection by the fungus. Sporulation can be induced by putting seedlings exhibiting foliar symptoms into a moist


chamber at 10" to 16°C overnight. Abundant conidia are formed on the lower leaf surface. Conidial suspensions are sprayed on the foliage of plants to be inoculated, and the plants are kept in a moist chamber at 15-18°C for 24 hours. After a 10- to 14-day incubation period, inoculated plants can be evaluated for disease symptoms (Lehman 1958).

Pederson (1958) has obtained systemic infection by pulverizing air- dried leaves infested with downy mildew and depositing the powder on soaked seeds, either between the cotyledons or on the surface of cotyledons after removing the seedcoats. Seeds are then planted in steamed soil as indicated. With this technique, infested leaves can be collected from fields when symptoms are apparent, preserved, and used to obtain systemic infections rather than by attempting to locate oospore-encrusted seeds as a source of inoculum.

G. Powdery Mildew

The causal organism of this disease was first described as Erysiphe polygoni DC. ex St.-Amans, and several reports ascribe the disease to this organism. The causal organism was correctly identified later as Microsphaeru diffusa Cke. & Pk. (Lehman 1931, 1947; Paxton and Rogers 1974).

The disease occurs frequently on greenhouse-grown plants and occa- sionally on field-grown soybeans. Initial symptoms are leaf spots having a dirty gray color, slightly duller than the surrounding green of normal tissue. Within a few days the diseased areas assume a white, powdery appearance that may cover all of the upper leaf surface. Underlying tissues range from pale pink to dark red in color, which is clearly visible on the lower leaf surface (Lehman 1931).

The disease was common on field-grown soybeans in the north central United States from 1975 through 1977. In Iowa, the disease was present in 19% of the fields examined in 1975. The high incidence of the disease was partially attributed to the widespread use of the susceptible cultivars 'Corsoy' and 'Hark' (Dunleavy 1980). Dunleavy (1978, 1980) has measured yield losses as high as 26% on field-grown susceptible cultivars as compared with yields of the same cultivars protected with fungicide sprays.

Because of the sporadic occurrence of powdery mildew on field-grown soybeans, little attention has been given to breeding for resistance to the disease. Resistant and susceptible cultivars occur at random in most of the maturity groups grown in North America.

Grau and Laurence (1975) reported that resistance to powdery mildew was controlled by a single dominant gene. This may be the same gene, designated R m d by Buzzell and Haas (19781, for adult plant


resistance in the cultivar ‘Blackhawk’. The recessive allele, rmd, results in susceptibility at all stages of plant development. There are indica- tions that a second gene is involved in powdery mildew resistance.

The pathogen is an obligate parasite and cannot be maintained in culture. Spores or infected leaves must be stored as a source of inoculum. Plants to be evaluated for their reaction to the pathogen are dusted with conidia by shaking diseased leaves over the plants (Demski and Phillips 1974; Dunleavy 1977a). Dunleavy (1977a) evaluated reactions of soybean cultivars to the pathogen by growing hill plots in the field. An adjacent planting of the susceptible cultivar ‘Harosoy,’ supplied inoculum that naturally infected plants in the test area.

H. Target Spot

Target spot, caused by Corynesporu cussiicolu (Berk. & Curt.) Wei is generally distributed throughout the southern United States. The disease occurs primarily on the leaves, but stems, pods, seeds, and roots may be affected. On the leaves the symptoms are reddish-brown, circu- lar to irregular lesions that vary in size from specks to 10 to 15 mm in diameter. Severely infected leaves may shed prematurely. Infected areas on petioles and stems are dark brown in color and range from specks to elongated, spindle-shaped lesions (Athow 1973). Lesions on roots are dark reddish-brown, changing to violet brown with age. Plants with severely infected roots are characteristically stunted (Boosalis and Hamilton 1957).

Hartwig (1959) reported yield losses of 18-32% on susceptible cultivars that were naturally infected in the Delta area of Mississippi.

Resistance to target spot does not appear to be simply inherited. All soybean strains appear susceptible to early-infection lesions; however, on the more resistant strains the lesions fail to develop. On the susceptible strains, there is extensive development of the lesions, and there appears to be sensitivity to a toxin produced by the fungus. On these susceptible strains, a large chlorotic area develops around the lesion and leaves drop off the plant rather rapidly (E.E. Hartwig, personal communication).

Corynesporu cussiicolu can be isolated readily from lesions on the soybean plant and cultured on PDA, Difco cornmeal agar, or malt agar. Inoculum has been prepared by comminuting 14-day-old cultures of the pathogen in 200 ml distilled water and spraying the inoculum on upper and lower leaf surfaces until wet. Inoculated plants were placed in a moist chamber for 45 hours, then transferred to a greenhouse bench where symptoms appeared 2 weeks after inoculation. Field-grown susceptible soybean plants showed typical lesions 15-20 days after in-


oculation (Seaman and Shoemaker 1965; Spencer and Walters 1969). Hartwig (personal communication) reported difficulty in consistently obtaining adequate infections in the field for studies on the genetics of resistance. As a result of selection for resistance in the field, virtually all high-yielding cultivars grown in the South are resistant to the disease.

I. Soybean Rust

This disease, caused by Phakopsorapachyrhizi Sydow, is probably the most economically important fungus disease of soybeans in the Eastern Hemisphere. It has been reported in the eastern USSR, China, Japan, Taiwan, The Philippines, Malaysia, the Indonesian peninsula, India, Equatorial Africa, and Australia. In the Western Hemisphere, the disease has been reported in Brazil, Colombia, Venezuela, Central Ameri- ca, and several islands of the Caribbean, but the rust in these areas does not appear to be pathogenic on soybeans (E. E. Hartwig, personal communication). There are no reports of soybean rust in Europe or in North America. Because U.S. southern coastal areas have temperature and rainfall conditions similar to those areas where the rust is prevalent in China, the disease is a potential threat to soybean production in the southern United States (Bromfield 1976, 1980).

Initial symptoms of the disease on soybeans are chlorotic or gray- brown spots on the leaves and less frequently on the petioles and stems. On leaves, the spots enlarge, attaining sizes of about 1 mm2, and become brown or tan in color. Pycnidium-like uredia, or pustules, differentiate within the lesion, more commonly on the lower than on the upper leaf surface. The disease causes premature defoliation of plants and losses in yield due to reduced pod formation, seed number, and seed weight (Bromfield 1976; Sinclair and Shurtleff 1975). Yield losses due to rust in Taiwan may be as high as 70-80% in individual fields with annual losses estimated at 20-30%. In southeastern China, losses of 10-30% are common, and yield losses of over 50% occur in years with severe rust (Bromfield 1980).

The entire U.S. soybean germplasm collection was subjected to natural epidemics of soybean rust in Taiwan in 1961 and in northern India in 1970. Two accessions, PI 200490 and PI 200492, were rated as resistant in both tests. Accession PI 200492 was used as a parent in a breeding program for rust resistance in Taiwan that produced the cultivars ‘Tainung 3,’ ‘Tainung 4,’ and ‘Kaohsiung 3,’ all of which possess a degree of rust resistance in the field. This accession has also been used in various crosses in Australia that have resulted in progenies


with detectable degrees of rust resistance. Studies in Australia indicated that the resistance of PI 200490 and PI 200492 to certain races of P. pachyrhzzz is controlled by a single dominant gene (Bromfield 1976,1980; Singh et al. 1974). Data of McLean and Byth (1980) suggest that PI 200492 and Tainung 3 contain the same single dominant gene, Rpp,, for resistance to soybean rust. Subsequent research has shown that components of the pathogen population in Taiwan capable of at- tacking PI 200492 and cultivars derived from it have increased in prevalence. In Australia, 2 races of the pathogen have been identified, one of which is virulent on PI 200492 (Bromfield et al. 1980).

The Southern germplasm collection was evaluated for reaction to rust in Taiwan in 1975. Seven or 8 accessions that appeared most resistant were screened in greenhouses by Bromfield; PI 230970 and PI 230971 produced lesions with no sporulation (Hartwig, personal communication).

Bromfield and Hartwig (1980) inoculated F2 plants from the crosses ‘Centennial’ x PI 230970 and D75-10169 x PI 230971 with rust isolates from Australia, India, Taiwan, and the Philippines. Both accessions were reported to be moderately resistant to soybean rust in inoculated field plots in Taiwan. Results indicated that the two accessions have a single gene that governed resistance to all four isolates of the pathogen. Whether the gene is at the same locus as that reported in PI 200490, PI 200492, and ‘Ankar’ is unknown.

Breeding for rust resistance in the Philippines has been based on ‘TK - 5,’ ‘Wayne,’ ‘Kaohsiung 3,’ ‘Tainung 3,’ and ‘Tainung 4’ as sources of rust tolerance. Crosses were made among these cultivars, and segregating populations were evaluated for reaction to the pathogen for 3 seasons. The best selections were intercrossed in an attempt to recover higher levels of resistance to the pathogen. Recurrent selection will be used to further increase the level of resistance in the populations. Evaluations have been complicated by the changing reactions of cultivars to the pathogens, due to changes in the population of the rust organism (Lantican 1977).

Breeding programs for rust resistance in Australia, India, and Indo- nesia have emphasized screening populations for sources of resistance to the pathogen. The inheritance of resistance was studied in segregating progenies from crosses between resistant lines and adapted, high- yielding cultivars (McLean and Byth 1977; Singh and Thaplujal 1977; Sumarno and Sudjadi 1977).

Inoculum of P. pachyrhizi, an obligate parasite, must be obtained from sporulating uredia on soybean plants. Populations are usually evaluated in areas where epidemics of rust are severe and adequate


moisture is present for natural rust infections. For artificial inoculations, leaves were seeded with urediospores and plants were incubated in a moist chamber at 20°C in the dark for 16-22 hours. Plants were then moved to a greenhouse with daylnight temperatures and relative humidities of 25"-29"/20"-24"C and 45-46%152-67%, respectively. Lesions were counted 10 days after inoculation and sporulation evaluated starting 13 days after inoculation (Melching et al. 1979).

Several systems have been used to rate reactions to P. pachyrhizi. Singh et al. (1974) rated lines that were completely free of rust as resistant. Lines rated as moderately resistant developed a pink spot at the point of contact with the fungal spore, indicating a hypersensitive reaction, and there was very little or no further development of the fungus on the spots.

McLean (1979) described 3 reaction types to the fungus. Type 1, with no visible symptoms of infection, was considered immune. Type 3, where sporulating uredia were surrounded by necrotic host tissue, was considered susceptible. Type 2, which was intermediate between 1 and 3, consisted of necrotic lesions with no uredia formed and was considered a resistant reaction.

Bromfield et al. (1980) characterized the interactions of the pathogen- host combinations into 3 infection types: TAN, RB, and 0. The tan reaction on the lower leaf surface was characterized by a tan lesion about 0.4 mm2 in the area in which 2 to 5 uredia were present and sporulation was abundant. This was considered a susceptible reaction by the host. The RB infection type was characterized by a reddish-brown lesion about 0.4 mm2 in area in which 0,1, or 2 uredia were present and sporulation was sparse. This was considered a resistant reaction and corresponded to the moderately resistant reaction described by Singh et al. (1974). The 0 reaction exhibited no macroscopic evidence of rust and would be equivalent to the resistant reaction of Singh et al. (1974) and the Type 1 reaction of McLean (1979).

The International Working Group on Rust proposed a 3-digit rating system in an effort to standardize soybean rust evaluations (Shan- mugasundaram 1977). The first digit, 1 ,2 , or 3, designates the bottom, middle, or upper third of the plant evaluated. The second digit, 1 to 4, designates density of rust lesions from none to heavy. The third digit, 1, 2, or 3, denotes the reaction to the rust as no pustules, nonsporulating pustules, or sporulating pustules.

J. Pod and Stem Blight

Pod and stem blight, caused by Diaporthe phaseolorum (Cke. & Ell.) Sacc. var. sojae (Lehman) Wehm.; imperfect stage Phomopsis sojae


Lehman, is a common and serious disease of soybeans in many of the soybean-producing areas of the world (Athow 1973). The most noticea- ble symptom of the disease is the linear rows of pycnidia on stems, petioles, and pods of plants at maturity. The most important aspect of the disease is its effect on seed quality. Severely infected seeds may be cracked, shrivelled, and partially or completely covered with a white mold. Less severely infected seeds may not exhibit external symptoms of the fungus, but the seeds often do not germinate or, if they do, produce weak seedlings.

Because of its effect on seeds, pod and stem blight disease is particularly harmful where it occurs in seedlots designated for planting, especially where seedlots must meet minimum germination standards for certification.

Soybean seeds with visible symptoms of the disease contained more oil and protein and were smaller in size, lower in density, and had lower quality oil and flour than symptomless seeds (Hepperly and Sinclair 1978).

Moldy seeds contribute to the damaged-seed content in U S . grain grading standards. Symptomatic seed could lower grade directly if the incidence of moldy beans exceeds 2% or indirectly by lowering test weight or by increasing the number of split seeds (Sinclair 1978). Seedlots with a very high incidence of moldy seed may not be accepted in commercial trade.

There are differences in susceptibility to this disease among soybean strains and cultivars. The cultivar ‘Delmar’ and PI 80837 and PI 181550 exhibit a high degree of resistance to pod and stem blight and have been used in breeding programs to improve seed quality (Athow 1973). Three cultivars released by Delaware, ‘Emerald,’ ‘James,’ and ‘Verde’ are reported to be resistant to pod and stem blight.

Disease development is favored by warm, moist, humid conditions, particularly during and after the time of pod ripening (Kmetz et al. 1979; Lehman 1923; Nedrow and Harmon 1980; Shortt et al. 1981). Progressive delays in harvesting soybeans after maturity frequently result in increased incidence of pod and stem blight (Athow and Lavio- lette 1973; Kmetz et al. 1978; Wilcox et al. 1974).

These observations have led to the use of a “delayed harvest” technique for evaluating, soybeans for resistance to pod and stem blight. Duplicate one-meter rows of lines to be evaluated are grown; one row is harvested at maturity and the other row harvested 3 to 4 weeks after maturity. Seeds from both samples are plated on PDA to determine the prevalence of the pathogen and are evaluated for emergence in sand- bench germination tests. A comparison of the data from the two samples is used as an indication of which lines have resistance to the pathogen


and superior seed quality. One limitation to the technique is that seed quality tends to be associated with time of maturity. Early maturing lines tend to have the poorest seed quality, and late maturing lines have the best seed quality.

The pathogen can be isolated from infected stems, pods, and seeds and cultured on PDA (Athow and Laviolette 1973; Sinclair 1978). Tooth- picks overgrown with the fungus have been inserted in soybean stems and pods to inoculate plants (Athow and Laviolette 1973; Kmetz et ul. 1979). This technique provides an entrance for the pathogen, however, and may circumvent natural barriers to infection. The method is not as effective as is the delayed harvest technique in screening for resistance to pod and stem blight.

K. Purple-Seed Stain

Purple-seed stain, caused by Cercosporu Kikuchii (T. Matsumoto & Tomoyasu) Gardner, occurs worldwide on soybeans. As the name im- plies, the disease causes a pink to dark purple discoloration on the seed ranging in size from a small spot to the entire area of the seedcoat. The fungus also attacks the leaves, stems, and pods. Foliar symptoms are angular, reddish-brown spots, approximately 2 mm in diameter, that may coalesce to form areas up to 15 mm in diameter. When the infection is severe, leaves may turn yellow and drop prematurely (Athow 1973; Walters 1980).

Severely purple-stained seed may reduce germination by 10- 15% but agronomic characteristics of plants developing from purple-stained seeds are not affected (Wilcox and Abney 1973). The amount of purple discoloration in seedlots is important because it may reduce the grade and hence the value of the seed. The discoloration is not important on soybeans for processing because the color disappears when the seed is heated.

The amount of purple stain varies among locations where soybeans are grown and among cultivars. Natural infections have resulted in nearly 100% purple-stained seeds on susceptible cultivars at a given location (Lehman 1950). Inoculations of the very susceptible cultivar Amsoy 71 have resulted in 85% purple-stained seeds (Roy and Abney 1976; Wilcox et al. 1975).

Cultivar differences in susceptibility have been observed, and many currently grown cultivars have a moderate level of resistance to the disease. Accession PI 80837 has a high level of resistance when grown in the midwestern United States, averaging less than 3% compared to 85% purple-stained seed of Amsoy when inoculated with the pathogen. Wil-


cox et al. (1975) evaluated progenies from crosses between ‘Asmoy’ x PI 80837 and obtained heritability estimates of 0.91 in the F2 generation and 0.51 in the F3 generation for incidence of purple-stained seed. Selection for resistance to purple seed stain resulted in a reduced incidence of the disease. Because the disease does not seriously affect seed germination or agronomic characteristics of soybeans, the authors suggested selecting against extreme susceptibility to the disease rather than an intensive breeding effort to develop highly resistant cultivars.

The pathogen can be isolated from purple-stained seed and cultured on PDA or V-8 juice agar. The fungus does not sporulate well on PDA cultures in continuous darkness. Abundant sporulation occurs when the fungus is grown on an agar medium containing senescent soybean plant tissue and is grown under 8- to 12-hour photoperiods. (Vathakos and Walters 1979; Yeh and Sinclair 1980).

Inoculum has been prepared by allowing the fungus to overgrow petri plates containing V-8 juice agar, macerating the entire contents of 40 plates in a blender with 2 liters ofwater, straining the contents through a double layer of cheesecloth, and diluting with 11 liters of water. Field-grown plants were sprayed with the inoculum until runoff in the late afternoon or evening to delay drying of the inoculum (Wilcox et al. 1975). The highest incidence of infected seed was observed when plants were inoculated at the full bloom stage of development (Laviolette and Athow 1972; Roy and Abney 1976).

IV. BACTERIAL DISEASES

Bacterial diseases are widespread on soybeans but generally do not seriously limit production. This is due in part to the widespread use of resistant cultivars where the disease is a potential problem. Leaf spots are the most prevalent disease caused by these pathogens.

A. Bacterial Blight

This disease, caused by Pseudomonas glycinea Coerper, occurs throughout soybean growing areas of the world and is especially prevalent during cool, wet weather (Sinclair and Shurtleff 1975). Symptoms of the disease are first, small angular lesions, surrounded by a yellow-green halo, that gradually become black or brown and coalesce, resulting in a shredded appearance of the leaves (Kennedy and Tachibana 1973). Yield reductions from inoculating plots of susceptible cultivars have been as high as 46-62% (Williams and Nyvall 1980).

At least 8 races of the pathogen have been reported, but more than


this number probably exist (Cross et al. 1966; Thomas and Leary 1980). Tisselli et al. (1980) list cultivars that are resistant to specific races of the pathogen. Mukherjee et al. (1966) reported that resistance to a single colony isolate of the organism was controlled by the dominant gene Rpg, in the cultivars ‘Norchief,’ ‘Harosoy,’ and PI 132207.

Soybean breeders have not put as much emphasis on breeding for a high level of resistance to bacterial blight as they have on eliminating soybean strains that are extremely susceptible to the disease. Evidence for this is that currently grown cultivars are relatively free of bacterial blight during most growing seasons, whereas unselected accessions in the same nurseries are often heavily infected with the disease. The moderate level of resistance of most soybean cultivars and the complica- tions of breeding for resistance to changing races of the pathogen have been deterrents to breeding cultivars with a high level of resistance to the disease.

P. glycinea can be isolated from infected soybean leaves and maintained on agar media. It is easier to maintain the pathogen by collecting infected leaves and storing them in plastic containers in a refrigerator or a freezer at -18°C. Viable bacteria can be maintained for several years with this procedure (Chamberlain 1957; Frosheiser 1956). Inocu- lum can be prepared by comminuting a few leaves in a blender, filtering out the coarse fragments with cheesecloth, and spraying a suspension of the bacteria onto 4- to 6-week-old soybean seedlings. Kennedy and Cross (1966) reported that atomizing the bacterial suspension with an airbrush sprayer on unifoliolate leaves of 10- to 14-day-old seedlings was a rapid and effective method of inoculating plants. Resistant and susceptible plants could be differentiated within 3 to 5 days after inoculation.

B. Bacterial Pustule

Bacterial pustule is a common disease in those soybean-growing areas where warm temperatures and frequent showers prevail during the growing season (Sinclair and Shurtleff 1975). The bacterium, Xan- thomonasphaseoli (E. F. Smith) Dowson var. sojensis (Hedges) Starr & Burkholder, enters the leaf through the stomata, producing light green elevated areas on either leaf surface. These small elevations enlarge to form prominent pustules, which eventually collapse and turn brown, varying in size from minute flecks to large irregular spots (Wolf 1924).

Hartwig and Johnson (1953) evaluated the peformance of 18 resistant and 18 susceptible soybean lines at 2 southern United States locations where moderate but uniform bacterial pustules developed on susceptible lines. Susceptible lines yielded 11% and 8% less than their resistant


counterparts at the two locations. Most of the yield reduction was attributed to fewer seeds produced on the susceptible than on the resistant lines. As a result of this study, nearly all soybean cultivars grown in the southern United States have resistance to bacterial pustule bred into them.

In Iowa, Weber et al. (1966) reported only a 4.4% yield reduction due to bacterial pustule on inoculated susceptible cultivars. Most of the yield reduction was associated with reduced seed number rather than seed size. In Indiana tests, where susceptible cultivars were repeatedly inoculated with bacterial pustule, no yield reductions associated with the disease were observed (Laviolette et al. 1970a, 1970b). These studies demonstrated that this disease was not a severe problem in the north- central United States and that incorporating resistance into cultivars adapted to this area was of questionable value and should be given minor consideration. Consequently, most soybean breeders in the Mid- west are not conscientiously incorporating resistance to this disease into new cultivars.

Resistance to bacterial pustule is controlled by a single recessive gene (Feaster 1951; Hartwig and Lehman 1951) designated rxp (Bernard and Weiss 1973). The gene, originally found in the cultivar ‘CNS’ introduced from Nanjing, China, can be readily incorporated into cultivars by backcrossing or by selecting for resistance among segregating lines from a cross between resistant and susceptible parents.

The bacterium can be isolated from infected soybean leaves and maintained on Wernham’s potato-dextrose agar. Inoculum is prepared by multiplying the bacteria on agar, suspending the bacteria in distilled water, and forcibly spraying the inoculum against the underside of soybean leaves until water-soaking of the leaf is visible (Chamberlain 1962). Disease ratings can be made approximately 10 days after inoculation. Resistant cultivars have few lesions with no pustule outgrowths, susceptible plants have pustules developing from the lesions (Feaster 1951).

C. Wildfire

Wildfire, caused by Pseudomonas tabaci (Wolf & Foster) F. L. Ste- vens, is a worldwide disease of tobacco that has been reported on soybeans in the United States and in Brazil (Sinclair and Shurtleff 1975). On soybeans, the pathogen causes brown, necrotic spots of varying size that are almost always surrounded by a wide yellow halo. Under favorable weather conditions the lesions enlarge and coalesce, and defoliation, starting with the lower leaves, is common and may progress until few leaves remain (Allington 1945).


Studies by Graham (1953) and Chamberlain (1956) demonstrated that pustules caused by Xanthomonas phaseoli var. sojensis are the primary avenues of entry for P. tabaci. Therefore, breeding for resistance to bacterial pustule effectively controls wildfire in soybeans. Since virtually all cultivars grown in the southern United States are resistant to bacterial pustule, the wildfire disease is effectively controlled. There are no reported sources of resistance for T. tabaci alone.

V. VIRUS DISEASES

Soybeans are susceptible to about 50 viruses, but fewer than 12 are important on the crop (Ford and Goodman 1976). The genetics of resistance is known for very few virus diseases, and limited efforts are underway to incorporate this resistance into improved cultivars.

A. Soybean Mosaic Virus

Soybean mosaic virus (SMV) is worldwide in its distribution and is one of the most important diseases of soybeans in many areas of the world (Sinclair and Shurtleff 1975).

Plants infected early in the season are usually stunted with shortened internodes and petioles. Leaflets are puckered, generally asymmetric, twisted, and curled downward at the margins. Pods on diseased plants may be stunted, flattened, less pubescent, and more acutely curved than those on normal plants (Gardner and Kendrick 1921; Sinclair and Shurtleff 1975). Mottling of the seedcoat, sometimes referred to as hilum bleeding or hilum extension, is a symptom of SMV on seed (Kennedy and Cooper 1967; Koshimizur and Iizuka 1963). Wilcox and Laviolette (1968) found that the appearance of mottled seeds resulting from SMV infection suggested that the virus modified the normal expression of the Z and iz alleles that restrict color to the hilum, permit- ting pigmentation in the seedcoat outside the hilum. In general, the ealier infection occurs, the more severe the symptoms on plants. The disease also reduces the number, size, and weight of nodules on infected plants. (Tu et al. 1970). Yield reductions as high as 86% due to the virus have been reported (Goodman and Oard 1980; Ross 1968b, 1977; Kend- rick and Gardner 1924).

Isolates of SMV differ in their pathogenicity on soybean cultivars (Ross 1969). Cho and Goodman (1979) classified isolates of SMV into 7 groups based on disease reactions of inoculated, differential soybean cultivars. No cultivars were identified that were resistant to all strains of the virus.


There are several kinds of resistance to SMV or SMV symptoms in soybeans. Cooper (1966) reported that ‘Merit’ was immune to seed coat mottling, due to a single gene Im, that exhibited partial to complete dominance in an environment that favored expression of mottling. Subsequent studies have shown that Merit is not immune to SMV because infectious virus could be detected in immature but not in mature embryos ofthis cultivar (Bowers and Goodman 1979). Several other strains have been identified that are susceptible to SMV but have a very low incidence of transmission through the seed. (Goodman et al. 1979, Goodman and Oard 1980). Resistance to seed transmission could be useful in reducing the incidence of this disease because SMV-infected seed is an important source for transmitting the virus from one crop to another .

Plant resistance to SMV was reported due to both dominant and recessive alleles, depending upon the SMV stain used. In crosses between immune and susceptible cultivars in Japan, immunity was dominant in the F1 of some crosses and the F2 segregated in a ratio of 3 immune: 1 susceptible plant. In other crosses, susceptibility was dominant and the F2 segregated in a ratio of 9 susceptible: 7 immune plants (Koshimizu and Iizuka 1963). Kwon and Oh (1980) reported that resistance to a necrotic strain of soybean mosaic virus (SMV-N) was controlled by a single recessive gene. In crosses between cultivars resistant and susceptible to SMV- 1, Kiihl and Hartwig (1979) recognized 2 types of resistance. The highest level of resistance gave complete protection against SMV- 1 and a variant of the strain, SMV- 1 -B. A lesser level of resistance gave protection against SMV- 1 in the homozygous condi- tion, but all homozygous plants became necrotic after inoculation with SMV-1-B. They proposed the gene symbols Rsu Rsu for the highest level of resistance from PI 96983, rsut rsut for the lesser level of resistance from ‘Tokyo,’ and rsu rsu for the susceptible reaction. The 3 alleles formed an allelomorphic series with Rsu dominant to rsd, and rsut dominant to rsu.

R. L. Bernard (personal communication) has backcrossed resistance to the Illinois severe strain of SMV (SMV-11-S) from PI 96983 (Rsu Rsu) into the cultivar Williams, and the backcross line has been released as germplasm.

B. Bean Pod Mottle Virus

Bean pod mottle virus (BPMV) causes green to yellow mottling on young leaves near the top of the soybean plant. Under cool greenhouse conditions, leaves produce a chlorotic mottling after inoculation (Sin-


clair and Shurtleff 1975). A green stem syndrome due to BPMV was reported by Schwenk and Nickel1 (1980). Symptoms were thin, brown, dried pods with small seeds on maturing plants and stems that re- mained green after maturity.

Naturally occurring infections of BPMV have reduced seed yields by 29% and in combination with moisture stress by 45% (Myhre et al. 1973). Bean pod mottle and soybean mosaic virus appear to exert synergistic effects when they occur together in plants. Ross (1968b) reported that SMV alone reduced soybean yields by 8-25%; but in combination with BPMV, yields were reduced up to 80%. Yields of the cultivar ‘Lee’ inoculated with SMV, BPMV, and both viruses were reduced 18%, 26%, and 73%, respectively. Yields of ‘Hill’ similarly inoculated were reduced 43%, 14% and 81%, respectively (Ross 1963). Mean seed yield of the cultivars Amsoy, Corsoy, and Wayne was reduced 18% by SMV, 1 0 9 by BPMV, and 66% by both SMV and BPMV (Quiniones et al. 1971).

No cultivars have been identified that are immune to BPMV. Some cultivars such as ‘Marshall’ have displayed a high level of resistance to the virus (Schwenk and Nickel1 1980). Incorporating resistance to SMV into cultivars should reduce the synergistic effects of BPMV and SMV in reducing soybean yields.

C. Cowpea Chlorotic Mottle Virus

A distinct strain of cowpea chlorotic mottle virus, designated CCMV- S, was reported on soybeans by Kuhn (1968). Symptoms following inoculation were a mild mottle on the first trifoliolates that became more intense on newer growth, reduced plant height and vigor, and slightly crinkled leaves that tend to be more upright than normal (Harris and Kuhn 1971). Yields of inoculated plants have been reduced as much as 31% compared with uninoculated controls. The virus also reduces the oil content of the seed and slightly alters the fatty acid composition of the oil (Harris et al. 1970).

Boerma et al. (1975) determined that resistance to CCMV-S was controlled by a single dominant gene, designated Rcm, in the cultivars ‘Lee’, ‘Bragg’, and ‘Hill.’ They suggested the gene for resistance could be easily transferred into susceptible cultivars by the backcross method of breeding.

D. Peanut Mottle Virus

Peanut mottle virus (PMV) on soybeans causes leaf mottling, an upward curling of leaflets, and depression of the interveinal tissue (Kuhn 1965). Inoculation of susceptible soybean cultivars in the field


resulted in reduced plant height and seed yield by 6% and 20%, respectively. Resistant cultivars were unaffected by inoculation, and aphids could not transmit PMV to them (Demski and Kuhn 1975).

Boerma and Kuhn (1976) determined that resistance to a mild strain, M-2, of PMV in the cultivars ‘Dorman’ and ‘CNS’ was controlled by a single dominant gene, designated Rpu. A second gene, rpuz, has been identified in the cultivar ‘Peking’ that, as a recessive gene, controls resistance to the peanut mottle virus isolate PMV-SIV 745 (Shipe et ul. 1979).

E. Tobacco Ringspot Virus

Tobacco ringspot virus (TRSV) causes a characteristic curving and necrosis of the tip of the stem and the terminal bud of infected soybean plants, hence the term “bud blight” to describe the disease. Additional symptoms include stunted plants, due to shortened internodes or reduced number of nodes, a proliferation of cupped or rugose leaves, and of floral buds, a reddish-brown discoloration of the pith, particularly a t the nodes, and green or distorted seeds (Allington 1966; Hildebrand and Koch 1947; Kahn and Latterell 1955; Melhus 1942). The number and size of roots and nodules may be reduced by the virus (Orellana and Sloger 1978). The virus is seed transmitted, which may account for the common occurrence of the disease at very low incidences in soybean fields (Athow and Bancroft 1959; Athow and Laviolette 1962; Des- jardins et al. 1954; Hildebrand and Koch 1947). Serious epiphytotics of the disease are usually associated with soybeans adjacent to fields of legume-grass mixtures or weedy pastures (Athow and Bancroft 1959). The virus is transmitted from several weed hosts to soybeans by insect vectors including thrips, Thrips tubaci (Dysart and Chamberlain 1960; Messieha 1969; Tuite 1960). Grasshoppers, Melanophes spp. have been shown to transmit TRSV to soybeans but probably are not an important vector (Dunleavy 1957).

The author has observed a 5-hectare field of soybeans in which plants in the hectare adjacent to a weedy pasture were severely stunted and almost devoid of pods. Symptom severity decreased as distance from the weedy pasture increased until plants in the hectare most distant from the weedy pasture were free of disease symptoms. Athow and Laviolette (1961) reported a significant decrease in seed yield when the incidence of infected plants exceeded. 30%.

K. L. Athow and F. A. Laviolette (personal communication) have identified resistance to TRSV in the cultivar UFV- 1, released in Brazil in 1973. They crossed this cultivar with susceptible Group 11,111, and IV


cultivars adapted to production in the Midwest. Segregation of the F2 populations of 5 crosses inoculated in the greenhouse suggested that resistance was controlled by a single, recessive gene. Progenies from these crosses are being evaluated for resistance using a paired-row technique. Two 1-m rows are planted of each selected progeny. One row of the pair is inoculated with TRSV at the unifoliolate or first trifoliolate stage of growth. The difference between the inoculated plot and the uninoculated plot with respect to virus symptoms, particularly plant height and seed yield, is used as a measure of resistance to TRSV.

F. Virus Methods

Inoculum for infecting soybeans with all the viruses discussed is obtained by macerating infected tissue, usually leaves, in a blender with a potassium phosphate buffer to adjust PH to 6.5 or 7.0. The macerated material is filtered through 60- to 120- mesh sieves or cheesecloth, and an abrasive, usually carborundum, is added to break leaf surfaces during inoculation. The inoculum is rubbed on primary or first trifoliolate leaves with gauze pads dipped into the suspension. Inoculum may be sprayed on exposed parts of young plants with an atomizer at about 90 psi air pressure (Kiihl and Hartwig 1979; Schwenk and Nickel1 1980; Boerma et al. 1975). Ross (1978) has developed a pad applicator mounted on wheels that can be pushed over rows of plants to inoculate large populations of soybeans in the field. In a field trial, two inoculations 1 week apart produced 60% and 72% infection of soybean seedlings with SMV and BPMV, respectively.

Viruses can be detected in soybean seeds by germinating the seeds and observing the seedlings for symptoms. Viruses can also be detected by infectivity tests, in which extracts from plants or seeds to be tested are used to inoculate an indicator plant that shows a characteristic lesion if the virus is present. Lister (1978) reported that the enzyme- linked immunosorbent assay (ELISA) test easily detected tobacco ringspot and soybean mosaic virus in both leaf tissue and seeds of infected soybeans. He suggested that in breeding for resistance to virus infection or resistance to the passage of virus through seed to progeny plants, ELISA could aid in rapid, accurate comparisons of the virus content of selected plants and seeds. The precision of the assay might detect degrees of resistance that would pass unnoticed in evaluating progeny of plants for seedling symptoms or in infectivity tests.

Most of the viruses that attack soybeans are transmitted by known insect vectors. Ford and Goodman (1976) have speculated that it may be easier to breed soybeans for resistance to general insect feeding than to


incorporate specific resistance for each of the several viruses transmitted by only one or two insects.

VI. NEMATODES

As many as 50 species representing about 20 genera of plant-parasitic nematodes have been reported to feed on soybeans (Caviness and Riggs 1976). The genetics of resistance, however, is known for only 3 species and breeding for resistance is concentrated here.

A. Soybean Cyst Nematode

The soybean cyst nematode, Heterodera glycines Ichinohe, has been reported in China, Japan, and Korea and in 22 states in the United States. Infected plants may become severely stunted and chlorotic. These symptoms, however, appear only when the nematode population is very high and environmental conditions, including low soil fertility, light textured soils, and limited available moisture, are ideal for symptom expression (Tisselli et al. 1980). These symptoms are the result of damage to the roots including root pruning and stubby or coarse roots caused by the nematodes and general root decay caused by other pathogens that attack the root system through wounds produced by the nematode (Good 1973). An identifying characteristic of the pathogen is the presence of white to yellow cysts, about the size of a pinhead, on roots of infected plants. Yield losses due to the soybean cyst nematode range from a slight loss in plant vigor to 90% of possible production depending upon degree of infestation.

Golden et al. (1970) described 4 races of the nematode based on their ability to reproduce on differential cultivars and on their morphological characteristics.

Resistance to the cyst nematode was discovered in the blackseeded cultivar ‘Peking’ (Ross and Brim 1957). Caldwell et al. (1960) reported that resistance was controlled by 3 independently inherited recessive genes, rhgl, rhg2, and rhg,. Later, Matson and Williams (1965) found that an additional dominant gene, Rhg,, was also necessary for resistance. Breeding for resistance was complicated by a close linkage between Rhg, and the recessive allele i , which allows complete expression of dark-colored pigments throughout the seedcoat, an unacceptable characteristic in the soybean processing industry. The linkage was eventually broken after 3 backcrosses to ‘Lee’ in a program to transfer resistance from Peking to a line approaching ‘Lee’ in performance, and the yellow-seeded cultivar ‘Pickett’ was released (Brim and Ross 1966).


Sugiyama and Heronia (1966) reported linkage also between the i allele and the rhg, gene in ‘Peking.’

Hartwig and Epps (1970) reported that resistance to race 2 of the soybean cyst nematode was controlled by an additional recessive gene in PI 90763. Resistance to race 4 is apparently controlled by one dominant and two recessive genes, one of which was identified in PI 88788 (Thomas et al. 1975).

Resistance from ‘Peking’ was incorporated into the cultivars ‘Custer’ and ‘Dyer’ in addition to ‘Pickett’. These 3 cultivars, of maturity groups IV, V, and VI, provided growers with protection against the nematode in infested areas, but they did not yield as well as the best susceptible cultivars of comparable maturity on noninfested soils (Hartwig 1981). A second cycle of resistant cultivars, ‘Centennial,’ ‘Forrest,’ and ‘Mack,’ were released with resistance to races 1 and 3 of the cyst nematode and are either equal or superior in yield to the best susceptible cultivars when grown on noninfested soils. Resistance to race 4 from PI 88788 was added to previous sources of resistance with the release of ‘Bedford’ and ‘Nathan.’

Because the genetics of resistance is complex and multiple race resistance requires several recessive genes, modified backcrossing methods have been used to develop cultivars with resistance to known races of the cyst nematode (Caviness and Riggs 1976; Hartwig 1981). These methods involved crossing cultivars or strains with good agronomic characteristics and resistance to races 1 and 3 of the cyst nematode with a source of resistance to race 4. Several hundred F2 plants were evaluated for reaction to race 4, and resistant plants were backcrossed to the agronomically desirable recurrent parent. Resistant plants were also progeny-tested for their reaction to race 4, and those backcrosses from the plant with the highest level of resistance, based on the progeny test, were retained. The process was repeated until good agronomic strains could be selected that were resistant to races 1, 3, and 4 of the cyst nematode. Several different sources of resistance have been used in breeding programs; combining the best lines from each of these will offer possibilities of new genetic combinations if new economically important races of the pathogen are recognized.

Screening for resistance to the cyst nematode can be done in the field or in the greenhouse. Luedders and Duclos (1978) reported that resistant cultivars had a reproductive advantage over susceptible cultivars when the two types were grown as a blend on infested soils. The data suggested that growing segregating populations for several generations on heavily infested land should increase the frequency of resistant plants. This kind of inexpensive screening would be particularly useful


if it would increase the very low frequency of resistant lines that occur when 3 recessive genes and 1 dominant gene are required for resistance.

Screening in the greenhouse requires growing plants in pots of sterilized soil into which crushed cysts have been placed near the root area or growing seedlings in naturally infested soil. After 30 days, soil is washed from the roots and screened through a 60-mesh sieve. Cysts in the residue and on the roots are counted. Caldwell et al. (1960) classified plants with 0 or 1 cyst as resistant and those with more than one cyst as susceptible. Epps and Hartwig (1972) rated root systems on a scale of 0 to 4 where 0 indicated none and 4 indicated more than 30 white cysts on plant roots. Plants were considered resistant if there were 10 or fewer cysts on roots and susceptible if there were more than 10 cysts on roots.

B. Root-Knot Nematode

Root-knot nematodes (Meloidogyne spp.) that attack soybeans include M . arenaria (Neal) Chitwood, M. hapla Chitwood, M . incognita (Kofoid & White) Chitwood, M . incognita acrita Chitwood, M. incognita war- tellei (Golden & Birchfield), M.jauanica (Treub) Chitwood, and M . naasi Franklin (Tisseli et al. 1980). The disease occurs in most soybean- growing areas of the world and is particularly severe in warm climates on sandy, light textured soils. '

Infected plants may show various degrees of stunting and yellowing and have a tendency to wilt or die under moisture stress. The disease can be identified by the presence of galls or knots on soybean roots that vary from the size of a pinhead on small roots to 20 mm on large roots. Nematode feeding within the knots disrupts the internal structure of the roots and decreases the efficiency of water and nutrient transport within the plant (Tisseli et al. 1980; Dropkin and Nelson 1960).

In addition to different species of root-knot nematodes, several different races have been identified in M. incognita based on extent of galling and number of egg masses in roots of different soybean cultivars (Boquet et al. 1975; Dropkin 1959; Williams et al. 1973).

Sources of resistance have been reported to M. arenaria (Maxwell and Musen 1979) and to M. incognita (Boquet et al. 1975; Crittenden 1955; Holston and Crittenden 1951; Kinloch and Hinson 1973; Williams et al. 1973). Cultivars'resistant to one species are not necessarily resistant to other species of Meloidogyne. The highest levels of resistance in breeding lines appear to result from recombination of genes for resistance from several sources (Williams et al. 19731, which can result in an immune reaction to the nematode (Maxwell and Musen 1979).

Breeding for resistance usually involves evaluating segregating pop-


ulations on fields heavily infested with root-knot nematodes. In Florida, breeding lines are evaluated in two-replicate tests of one-row plots. Plants are pulled several weeks before maturity and scored on a 0 to 5 scale in which 0 indicates roots entirely free of galls and 5 indicates 75- 100% of the root surface galled. Lines with ratings less than 3 are reevaluated for resistance in similar tests (Kinloch and Hinson 1973). A similar system was used by Williams et al. (19731, in which the ratings ranged from 0, no roots with galls, to 6,50- 100% of the roots with galls. Vigorous, high-yielding plants were associated with a low incidence or the absence of galls; therefore, plant vigor could be useful as a rapid method of screening for resistance.

Greenhouse screening requires planting soybeans in pots of sterilized soil infested with a known nematode population, usually 300 to 700 nemasi500 ml soil. Pots are placed in sand to within 1.5 cm of the top to minimize soil temperature changes. After 25-75 days, plants are removed from the soil and extent of galling scored from 0 to 6 (Boquet et al. 1975; Saichuk et al. 1976; Williams et al. 1973).

C. Reniform Nematode

The reniform nematode, Rotylenchulus reniformis, occurs most frequently on soybeans in the Gulf Coast states and the coastal plains of the southeastern United States (Good 1973). The nematode causes root decay and poor growth; and yields of susceptible cultivars have been 20% below those of resistant cultivars on infested soils (Williams and Birchfield 1974).

Resistance to the reniform nematode was identified in the cultivars ‘Pickett’ and ‘Dyer.’ The resistance apparently was derived from ‘Peking’ (Rebois et al. 1968). Additional studies showed that all cultivars with resistance to the soybean cyst nematode derived from ‘Peking’ were resistant to the reniform nematode, but not to the root-knot nematode (Rebois et al. 1970). Subsequent research suggested that separate, but probably linked, genes control resistance to the two species of nematodes because not all soybean breeding lines were resistant to both species (Birchfield et al. 1971). Williams et al. (1981) reported that resistance to the reniform nematode was controlled by a single recessive gene, designated rrn. The relationship between this gene and those for resistance to the soybean cyst nematode is not known.

Greenhouse screening techniques for the reniform nematode are similar to those used for the root-knot nematode. Soybean plants are grown in pots of sterilized soil to which a known population of nematodes has been added. After 21 to 31 days, roots are removed from the soil, and egg

7 BREEDING SOYBEANS RESISTANT TO DISEASE 22 1

masses on the roots are counted or the percentage of roots with egg masses is scored. Roots may be stained with lactophenol acid fuchsin, then destained in lactophenol to aid in identifying egg masses (Birch- field and Brister 1979; Birchfield et a1 1971; Williams et al. 1979).

VII. SUMMARY AND CONCLUSIONS

Soybean breeders and pathologists have been extremely effective in developing cultivars that minimize losses due to diseases. Virtually all cultivars released in the southern United States are resistant to bacterial pustule, wildfire, and target spot. Cultivars are available to soybean growers in the South that are resistant to phytophthora rot, to the root-knot nematode, and to prevalent races of the soybean cyst nematode. Current research efforts are directed toward combining resistance to several pathogens, from somewhat independent breeding programs, into cultivars with multiple pest resistance (Hartwig 1981).

The time between the appearance of pathogenic problems and the release of resistant cultivars to overcome these problems has been very short in soybeans. Race 1 of frogeye leafspot, which occurred in epiphytotic proportions in southern Indiana in the late 1940s, was essentially eliminated with the release of ‘Wabash’ in 1950 and ‘Clark’ in 1953. The soybean cyst nematode was first found in North Carolina in 1954 and in Tennessee in 1957, and the resistant cultivar ‘Pickett’ was released in 1966. New races of phytophthora rot, first reported in Ohio in 1972, were controlled with the release of ‘Vickery’ in 1978.

The prompt control of pathogens in soybeans has been due, in large part, to anticipation of problems and direction of breeding efforts accord- ingly. Long before the soybean cyst nematode became a problem in the north central United States, soybean breeders began incorporating resistance into adapted breeding lines. When races 1 and 3 of the nematode were recognized in Central Illinois in 1976, ‘Franklin,’ a resistant cultivar adapted to the area, was available for release in 1977. Soybean breeders and pathologists met at a work-planning conference in 1972 to plan strategy for dealing with new races of Phytophthora megasperma f. sp. glycinea. Teams of breeders and pathologists agreed to utilize different sources of resistance to known races of the pathogen; then, if additional races were recognized, some breeding lines would have the potential of carrying resistance to the additional races. Results of this effort were the discovery of RpsCl in PI 54615-1, rps3 in PI 86972- 1, Rps4 in PI 86050, and Rps? in ‘Kingwa’ that control resistance to different races of the pathogen. Although soybean rust has not been reported in the United States, the United States germplasm collection


was screened for resistance in 1961, in 1970, and 1975; subsequently, identified genes for resistance are being incorporated into breeding lines adapted to the southern United States.

The U.S. soybean germplasm collection has been a reservoir from which breeders and pathologists have been able to select genes for resistance to pathogenic problems. Effective sources of resistance have been identified whenever problems have arisen. An expanded germplasm collection and the continued careful maintenance and evaluation of the collection will be critical to successfully controlling new pathogenic problems on soybeans.

Before 1970, nearly all of the soybean cultivars grown in the United States were developed by soybean breeders in cooperation with plant pathologists, employed by the United States Department of Agriculture and State Agricultural Experiment Stations. At present, the number of cultivars developed and merchandised by soybean breeders employed by private companies far exceed the number developed and merchandised by breeders employed by public agencies. Privately developed cultivars, however, currently occupy only about 15% of the United States soybean acreage. Virtually all privately developed cultivars have, as their parents, publicly developed cultivars and therefore frequently have the disease resistance of these cultivars. Because very few privately supported soybean breeders work cooperatively with plant pathologists, there is a potential problem of many newly developed cultivars being marketed and grown that do not have adequate pest resistance. Continued diligence will be required by both publicly and privately supported soybean breeders to incorporate into new cultivars resistance to pathogens that have the greatest potential for reducing soybean yields.

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NOTE ADDED IN PROOF

An additional gene for resistance to Phytophthora megasperma f. sp. glycinea has been

Rps, was identified in the cultivar ‘Altona’ as the gene that controls resistance to races identified since this manuscript went to press.

1-4, 10, 12, 14-16. Athow and Laviolette, 1982. Personal communication.

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