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J o u r n a l o f Nematology 30(2):184-191. 1998. © T h e Society of Nematologists 1998.

Variation in Resistance of Soybean Lines to Races of

Heterodera glycines D. G. KIM, 2 R. D. RtGGS,3 AND A. ~xAUROMOUSTAKOS 4 Abstract: T h e objective o f this study was to d e t e r m i n e the interrelationships of Heterodera glycines races based o n their resistance to soybean (Glycine max) cultivars a n d lines against which they were tested. G r e e n h o u s e tests d e t e r m i n e d the n u m b e r s of females of each of eight races of H. glycines that developed on 277 to 522 soybean cultivars a n d lines. A Female I n d e x ( n u m b e r of females on a test cultivar as a percentage of the n u m b e r o n 'Lee 74') was calculated a n d used in frequency distributions, correlations, a n d d u s t e r analyses o f the resistance reactions to the different races in an a t t e m p t to d e t e r m i n e relationships a m o n g cultivars. Frequency distribution patterns o f all cultivars a n d lines tested against each race were skewed in favor of resistance, a n d in s o m e cases bimodality was observed. T h e majority o f correlations between pairs o f races were highly significant. Cluster analyses based on the correlations divided eight races into f o u r clusters that explained 73% of the variation in resistance. Cluster 1 was c o m p r i s e d of races 2, 4, a n d 14; Cluster 2 was c o m p r i s e d of races 6 a n d 9; Cluster 3 was c o m p r i s e d of races 1 a n d 3; a n d Cluster 4 was comprised of race 5. T h e information obtained in this study could increase the efficiency of testing resistant soybean b r e e d i n g lines for resistance to I-1. glycines. Key words: Cluster analysis, Glycine max, Heterodera glycines, n e m a t o d e , resistance, soybean, soybean cyst n e m a t o d e , virulence group.

Soybean cyst n e m a t o d e (SCN), Heterodera glycines Ichinohe, causes m o r e yield reduction of soybean, Glycine max (L.) Merr., in the U n i t e d States t h a n any o t h e r disease (Doupnik, 1993; Z h a n g et al., 1992). Use of genetic resistance is the m a j o r m e t h o d for limiting yield losses due to this n e m a t o d e (Epps et al., 1981). Selection pressure results in d e v e l o p m e n t of virulent races of SCN a n d often c o m p r o mises cultivars with race-specific resistance within a few years. Riggs a n d Schmitt (t988) identified 16 possible races of SCN based on relative female m a t u r a t i o n on four differential soybean lines. However, b r e e d i n g resistant cultivars for all 16 races is n o t necessary because some races occur m u c h m o r e frequently than others in the U n i t e d States (Anand et al., 1994; Kim et al., 1997); eight

Received for publication 6 May 1997. 1 Approved for publication by the Director, Arkansas Agricultural Experiment Station, Fayenevine, AR 72701. This research was supported by funds provided by the soybean producers of Arkansas through the Arkansas Soybean Promotion Board. 2 Formerly, Department of Plant Pathology, University of Arkansas, Fayetteville, AR 72701. Currently, Department of Crop Protection, Agricultural Science and Technology, Institute, Rural Development Administration, Suweon, South Korea. s Department of Plant Pathology, University of Arkansas, Fayetteville, AR 72701. 4 Agricultural Statistics Laboratory, University of Arkansas, Fayetteville, AR 72701. E-mail: [email protected]

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o f the races are seldom f o u n d in soybean fields in the United States. D e v e l o p m e n t of race-specific resistant soyb e a n cultivars is a labor-intensive a n d timec o n s u m i n g process. Many p r o g e n y derived f r o m a cross must be screened to obtain a few resistant plants. These resistant plants can be identified only by a bioassay in which they are grown in soil infested with SCN. After ca. 30 days, females a n d cysts are ext r a c t e d f r o m t h e r o o t s a n d soil, a n d counted. H u n d r e d s of soybean plants must be screened to find one that is resistant to just one race, a n d the process must be rep e a t e d for each race. A soybean field is infested with only one race of H. glycines, even t h o u g h multiple parasitic g e n o t y p e s are present. If m o r e than one sample is taken f r o m a field, the n e m a t o d e population in each sample may be a different race, but the race in the field is a composite of all the genotypes in all the samples. Planting cultivars with different sources of resistance in different areas o f the field is n o t practical. Therefore, a race test of the composite p o p u l a t i o n f r o m the field provides a guide to the type of resistance n e e d e d to suppress d a m a g e by the nematodes present. The race o f SCN in a field s h o u l d be d e t e r m i n e d before a race-specific resistant cultivar is r e c o m m e n d e d . Cultivars with resistance to several races may reduce

Variation in Resistance to H. glycines: Kim et al. 185 eluded in each experiment, and when a test required m o r e than one g r e e n h o u s e b e n c h they were included on each bench, to confirm race identity. Each soybean line was replicated five times for each race with o n e plant p e r replication. T h e n u m b e r o f females p r o d u c e d on each soybean line was converted to a Female I n d e x (FI), defined as the n u m b e r of females that developed o n a soybean line expressed as a p e r c e n t a g e of the n u m b e r that developed on the susceptible cultivar, Lee 74. T h e average FI of each soybean line was used in statistical comparisons. Analysis: T h e f r e q u e n c y distributions o f FIs of all races tested on all cultivars and lines were depicted with n o t c h e d boxplots (McGill et al., 1978) (Fig. 1). T h e n o t c h e d b o x p l o t shows the m e a n (asterisk) a n d the m e d i a n with an a p p r o x i m a t e 95% confid e n c e interval a n d mild a n d e x t r e m e oufliers. T h e b o x width is p r o p o r t i o n a l to the MATERIALS AND METHODS sample size. T h e n o t c h e d b o x p l o t is used Screening procedure: During 1991-94, 524 instead o f the regular b o x p l o t to show an soybean cultivars and b r e e d i n g lines, mainly a p p r o x i m a t e 95% c o n f i d e n c e interval for the location of the p o p u l a t i o n m e d i a n by in Maturity Groups V-VII, were e x a m i n e d for resistance to H. glycines. Although a total notches on the side of the box. Two races, the notches of which do not overlap, are o f 524 cultivars a n d b r e e d i n g lines were c o n s i d e r e d significantly different in their tested, not all were tested against every race. central values. T h e notches are calculated as N o t all races were tested at the same time, the m e d i a n _+ 1.58 ( I n t e r Q u a r t i l e R a n g e and, in any given test, seeds of a particular [ I Q R ] / ~ n , where I Q R is the middle 50% o f cultivar or line either m i g h t not have germinated or seed n u m b e r s may have b e e n in- the range a n d n is the n u m b e r of entries) to sufficient for all tests. Races 1-6, 9, a n d 14, give an a p p r o x i m a t e 95% c o m p a r i s o n o f the which are f o u n d most frequently in soybean m e d i a n (Velleman and Hoaglin, 1981). A correlation matrix between pairs of the fields in the central United States (Anand a n d Rao-Arelli, 1989; Luedders, 1989), were e i g h t races was g e n e r a t e d with the SAS used in these experiments. Race 6 was the C O R R p r o c e d u r e (SAS version 6.12, SAS Inmost difficult race to maintain, a n d the few- stitute, Cary, NC). These correlations were est cultivars a n d lines were tested against it. used in the SAS VARCLUS p r o c e d u r e to diSeeds o f soybean lines were received f r o m vide races into groups in a tree diagram. various sources, g e r m i n a t e d in vermiculite, and transplanted into fine sandy soil in pots. RESULTS AND DISCUSSION T h e soil then was infested with eggs and secFrequency distribution: T h e frequency distriond-stage juveniles (J2) of the a p p r o p r i a t e race (Riggs et al., 1991). Eggs and J2 were bution patterns for FI differed a m o n g races (Table 1). Lines resistant (FI

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