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Progress in genetics and mapping for resistance in soybean [Glycine max (L.) Merrill] to cyst nematode (Heterodera glycines Ichinohe).

Prakash R. Arelli1, Brian W. Diers2, Vergel C. Concibido3 and Lawrence D. Young4

USDA-ARS-MSA-CG & PRU, Jackson, TN 38301, USA. Email parelli@ars.usda.go
Dept. of Crop Sciences, University of Illinois, Urbana, IL 61801, USA. Email bdiers@uiuc.edu
Monsanto Co., 800 N. Lindbergh Blvd., St. Louis, MO 63167, USA. Email vergel.c.concibido@monsanto.com
USDA-ARS-MSA-CG & PRU, Stoneville, MS 28776, USA. Email ldyoung@ars.usda.gov

Abstract

Soybean [Glycine max (L.) Merrill] seed is a major source of protein for animal feed and oil for human consumption. It supplies approximately 65% of the world’s protein meal and 25% of the world’s edible oils. Worldwide, soybean cyst nematode (SCN: Heterodera glycines Ichinohe) is the most destructive pest on soybean crops. The annual yield losses due to SCN in 2002 are estimated to be nearly 9 million metric tons (2 Billion USD). Resistant cultivars reduce losses to SCN and are most cost effective and environmentally safe. Five major genes for resistance are designated and include rhg1, rhg2, rhg3, Rhg4 and Rhg5 from two different sources Peking and PI 88788. Widespread use of these resistance genes caused major shifts in nematode populations and produced more virulent types. Broad based resistance in soybean will reduce nematode shifts. Breeding for SCN resistance is tedious, time-consuming and inefficient. Genetic mapping and marker-assisted selection will improve the efficiency and provide durable resistance. Molecular markers have mapped several major resistance quantitative trait loci in soybean germplasm including rhg1, Rhg4 and Rhg5. Predominantly, QTL for SCN resistance are mapped to linkage Groups A, G and J. Additional sources of resistance have been reported. Unique QTL for SCN resistance are uncovered in diverse lines. These ongoing efforts should reduce yield losses in soybean to SCN. Progress will be discussed.

Media summary

Worldwide, soybean cyst nematode is the most destructive root-parasite on soybean crop. Genetic technologies will reduce yield losses caused by cyst nematode.

Keywords

Gene pyramiding, Syncytia, Plant Introductions.

Introduction

Worldwide, soybean seed is a major source of protein for animal feed and oil for human consumption. It supplies approximately 65% protein meal and 25% of the edible oil (Golbitz 2001). World soybean production in 2002 was 185 million metric tons. Diseases have suppressed soybean yield, especially soybean cyst nematode (SCN) continue to cause significant yield losses. Most recent estimates for SCN indicate losses of nearly 9 million metric tons worldwide in 1998 and 7.6 million metric tons in the USA (Wrather et al. 2003). Soybean cyst nematode causes yield reductions by feeding on plant nutrients, retarding root growth, and inhibiting Bradyrhizobium nodulation (Riggs and Schmidt 1987).

Primarily, genetic resistance in cultivars reduce yield losses to SCN. Development of productive cultivars with SCN resistance is a major goal of soybean breeding programs. These efforts are providing cultivars that may yield up to 56% more than susceptible cultivars in infested fields (Young and Hartwig 1988; Wheeler et al. 1997). Soybean growers in the USA have increased their profits by 400 million dollars merely from growing the resistant cultivar Forrest (Bradley and Duffy 1982).

Genetics of resistance

In soybean, inheritance of resistance to SCN is quantitative and complex. It involves three to four major genes and several minor genes (Diers and Arelli 1999). Caldwell et al. (1960) were the first to report that the inheritance of resistance to SCN in cv. Peking, an introduction from China, is conditioned by three recessive genes rhg1, rhg2 and rhg3. A fourth resistance gene Rhg4,is closely linked to the I locus which controls seed coat color, was reported by Matson and Williams (1965). A dominant gene, Rhg5 was identified in Plant Introduction (PI) 88788, and provides resistance to SCN populations found in MO, USA (Arelli et al. 1992; Arelli 1994). Further research has identified several common resistance genes among several PIs and several others that are different (Arelli and Anand 1988; Anand and Arelli 1989; Arelli et al. 1989; Young and Kilen 1994). In more recent studies, several new genes have been identified but have not been designated due to difficulties involved in conducting tests for allelism.

Mapping and marker technology

Recent genetic marker technology in soybean has facilitated the identification, localization, and characterization of QTL associated with SCN resistance. Weisemann et al. (1992) used molecular markers to map SCN resistance gene in cv. Peking. Two molecular markers, pbLT24 and pbLT65 were found to be associated with the SCN resistance gene Rhg4 on Linkage Group (LG) A2. Concibido et al. (1994) found three RFLP markers A85, B32 and K69 associated with SCN resistance in PI 209332. These were located on LGs A, J and G, respectively. Several studies confirmed SCN resistance on LG A2 (Mahalingam and Skorupska 1995; Chang et al. 1997; Webb et al., 1995; Cregan et al. 1999a). Recently, simple sequence repeats (SSRs) have mapped close to rhg1 on LG G with SSR309 (Mudge et al. 1997; Cregan et al. 1999b). However, there are some inconsistencies in reports. Qui et al. (1999) and Vierling et al. (1996) have reported QTL on different locations. Most recently, Meksem et al. (2001) confirmed the importance of both genes rhg1 and Rhg4 and proposed a bigenic model in cv. Forrest for resistance to the SCN (PA3) population.

Current mapping efforts for SCN resistance include Yue et al. (2001a; 2001b) and Schuster et al., (2001). New LGs Dla , D2 and E were identified in PIs 89772 and 438489B. Mapping in Glycine soja ((PI 468916) has identified a new major QTL region (near Satt 288) on LG G (Wang et al., 2001). Glover et al. (2004, in press) confirmed a QTL on LG J in Near isogenic line populations from PI 88788 and designated as cq SCN-003. Two research groups using positional cloning claimed to have cloned and patented rhg1 and Rhg4 candidate alleles (Hauge et al. 2001; Meksem et al. 2001). Their use in marker assisted selection (MAS) programs is an infringement of the patents. These legal issues compel researchers to identify new sources of SCN resistance, and seek new research directions. Most recently, Lu et al. (2003) reported new QTL in PI 467312 for nematode populations PA5 and PA14. These need to be confirmed.

Resistance to emerging nematode isolates or races that are more aggressive in virulence

There are over a hundred sources of resistance in G. max to the soybean cyst nematode populations (Arelli et al. 2000). Early searches identified sources of resistance in cv. Peking, PI 90763, cv. Ilsoy, and PI209332 (Ross and Brim 1957), PI 88788 (Hartwig and Epps 1970), PI 437654 (Anand et al. 1985) that are currently used for developing resistant cultivars. Other sources of resistance to soybean cyst nematode have been identified in the USA (Young 1990; 1995). Cultivar LongKang 792 from PR China was found to have resistance to several nematode populations (Liu et al. 1985). Arelli et al. (1997; 2000) reported 118 lines as having varying levels of resistance to nematodes and identified those that are especially resistant to SCN Races 1 and 2. Of all the sources of resistance, soybean PI 437654 has the most comprehensive resistance (Arelli et al. 1997). Most recently, two nematode populations that reproduce on PI 437654 have been identified (Young 1999) and soybean PI 567516C was found to be resistant to LY1 nematode population (Young 1999).

Cluster analyses

Information on the genetic relationships of the PIs at the molecular level could provide clues for identifying unique sources. In general, genetically unrelated PIs are likely to have fewer resistance genes in common than closely related PIs. Several soybean lines including PIs 507354, 467312, 567516C, 567328, Cloud, and 438503A are found to be unrelated, and therefore may have novel genes for SCN resistance (Diers et al. 1997; Xie et al. 1998; Zhang et al. 1999).

Conclusions

In soybean, resistant cultivars reduce yield losses to SCN. Newly identified genes, unrelated to rhg1 , Rhg4 and Rhg5 will be more effective for durable resistance and will not infringe existing patents. Additional studies are also needed to confirm newly identified QTL for SCN resistance. Phenotyping soybean with several isolates of nematode populations will identify QTL for broader resistance. Selecting QTL with high regression values will improve the efficiency of MAS. Finally, effective management practices will also enhance durable resistance in soybean.

References

Anand SC, Wrather JA and Shumway CR (1985). Soybean genotypes with resistance to races of soybean cyst nematode. Crop Science 25, 1073-1075.

Anand SC and Arelli PR (1989). Genetic analyses of soybean genotypes resistant to soybean cyst nematode race 5. Crop Science 29,1181-1184.

Arelli PR (1994). Inheritance of resistance to Heterodera glycines Race 3 in soybean accessions. Plant Disease 78, 298-900.

Arelli PR, Sleper DA, Yue P and Wilcox JA (2000). Soybean reaction to Races 1 and 2 of Heterodera glycines. Crop Science 40, 824-826.

Arelli PR and Anand SC (1988). Genetic relationships among soybean plant introductions for resistance to Race 3 of soybean cyst nematode. Crop Science 28, 650-652.

Arelli PR, Anand SC and Myers GO (1989). Partial dominance of susceptibility in soybean to soybean cyst nematode Races 3, 4, and 5. Crop Science 29, 1562-1564.

Arelli PR, Anand SC and Wrather JA (1992). Soybean resistance to soybean cyst nematode race 3 is conditioned by an additional dominant gene. Crop Science 32, 862-866.

Arelli PR, Wilcox JA, Myers Jr. O and Gibson PT (1997). Soybean germplasm resistant to races 1 and 2 of Heterodera glycines. Crop Science 37, 1367-1369.

Bradley EB and Duffy M (1982). The value of plant resistance to soybean cyst nematode: A case study of Forrest soybeans. (National Resource Economics Staff Report No. AGES820929, USDA. U.S. Govt. Print. Office, Washington, DC).

Caldwell BE, Brim CA and Ross JP (1960). Inheritance of resistance of soybeans to the cyst nematode, Heterodera glycines. Agronomy Journal 52, 635-636.

Chang SJC, Doubler TW, Kilo V, Suttner R, Klein J, Schmidt ME, Gibson PT and Lightfoot DA (1997). Association of field resistance to Soybean Sudden Death Syndrome (SDS) and Cyst Nematode (SCN). Crop Science 37, 965-971.

Concibido VC, Denny RL, Boutin SR, Hautea R, Orf JH and Young ND (1994). DNA marker analysis of loci underlying resistance to soybean cyst nematode (Heterodera glycines Ichinohe). Crop Science 34, 240-246.

Cregan PB, Jarvik T, Bush AL, Shoemaker RC, Lark KG, Kahler AL, Vantoai TT, Lohnes DG, Chung J and Specht JE (1999a). An integrated genetic linkage map of the soybean genome. Crop Science 39, 1464-1490.

Cregan PB, Mudge J, Fickus EW, Danesh D, Denny R and Young ND (1999b). Two simple sequence repeat markers to select for soybean cyst nematode resistance conditioned by the rhg1 locus. Theoretical and Applied Genetics 99, 811-818.

Diers BW and Arelli PR (1999). Management of parasitic nematodes of soybean through genetic resistance. In ‘Proc. World Soybean Res. Conf.’ (H.E. Kauffman) 6th Chicago, IL. 4-7 Aug, 300-306.

Diers BW, Skorupska HT, Arelli PR and Cianzio SR (1997). Genetic relationships among soybean plant introductions with resistance to soybean cyst nematodes. Crop Science 37, 1966-1972.

Glover K, Wang D, Arelli PR, Carlson SR, Cianzio SR and Diers B (2004). Near isogenic lines confirm a soybean cyst nematode resistance gene from PI 88788 on linkage group J. Crop Science (In press).

Golbitz P (2001). 2001 Soya & oil seed Bluebook. (Soya-Tech, Inc., Bar Harbor, ME).

Hartwig EE and Epps JM (1970). An additional gene for resistance to the soybean cyst nematode, Heterodera glycines. Phytopathology 60, 584 (Abstract).

Hauge BM, Wang ML, Parsons JD and Parnell LD (2001). Nucleic acid molecules and other molecules associated with soybean cyst nematode resistance. U.S. Pat. 2003005491.

Liu H, Shang Shaogang, Huo Hong, Wu Heli, Yao Zhenchun and Li Xiulan (1985). Study on physiological race of soybean cyst nematode Heterodera glycines. Soybean Science 4, 136 (Abstract).

Lu P, Shannon JG, Sleper DA, Nguyen HT and Arelli PR (2003). Molecular mapping of resistance to soybean cyst nematode in PI 467312 soybean. In 2003 Agronomy Abstracts. ASA, Madison, WI.

Mahalingam R and Skorupska HT (1995). DNA markers for resistance to Heterodera glycines Race 3 in soybean cultivar Peking. Breeding Science 45, 435-443.

Matson AL and Williams LF (1965). Evidence of four genes for resistance to the Soybean cyst nematode. Crop Science 5, 477.

Meksem K, and Lightfoot D (2001). Novel polynucleotides and polypeptides relating to loci underlying resistance to soybean cyst nematode and methods of use thereof U.S. Patent 09772134.

Meksem K, Pantazopoulos P, Njiti VN, Hyten LD, Arelli PR and Lightfoot DA (2001). Forrest resistance to soybean cyst nematode is bigenic: saturation mapping of the Rhg1 and Rhg4 loci. Theoretical and Applied Genetics 103, 710-717.

Mudge J, Cregan PB, Kenworthy JP, Kenworthy WJ, Orf JH and Young ND (1997). Two microsatellite markers that flank the major soybean cyst nematode resistance locus. Crop Science 37, 1611-1615.

Qiu BX, Arelli PR and Sleper DA (1999). RFLP markers associated with soybean cyst nematode resistance and seed composition in a ‘Peking’ x ‘Essex’ population. Theoretical and Applied Genetics 98, 356-364.

Riggs RD and Schmitt DP (1987). Nematodes. In ‘Soybeans: Improvement, Production, and Uses’ (J.R. Wilcox) 2nd ed. Agron. Mongr. 16., 757-778, (ASA, CSSA, and SSSA, Madison, WI).

Ross JP and Brim CA (1957). Resistance of soybean to the soybean cyst nematode as determined by a double-row method. Plant Disease Reported 46, 766-769.

Schuster I, Abdelnoor RV, Marin SRR, Carvalho VP, Kiihl RAS, Silva JFV, Sediyama CS, Barros EG and Moreira MA (2001). Identification of a new major QTL associated with resistance to soybean cyst nematode (Heterodera glycines). Theoretical and Applied Genetics 102, 91-96.

Vierling RA, Faghihi J, Ferris VR and Ferris JM (1996). Association of RFLP markers with loci conferring broad-based resistance to the soybean cyst nematode (Heterodera glycines). Theoretical and Applied Genetics 92, 83-86.

Wang D, Arelli PR, Shoemaker RC and Diers BW (2001). Loci underlying resistance to Race 3 of soybean cyst nematode in Glycine soja plant introduction 468916. Theoretical and Applied Genetics 103, 561-566.

Webb DM, Baltazar BM, Arelli PR, Schupp J, Clayton K, Keim P and Beavis WD (1995). Genetic mapping of soybean cyst nematode race-3 resistance loci in soybean PI 437.654. Theoretical and Applied Genetics 91, 574-581.

Weisemann JM, Matthews BF and Devine TE (1992). Molecular markers located proximal to the soybean cyst nematode resistance gene, Rhg4. Theoretical and Applied Genetics 85, 136-138.

Wheeler TA, Pierson PE, Young CE, Reidel RM, Wilson HR, Eisley JB, Schimtthenner AF and Lipps PE (1997). Effect of soybean cyst nematode (Heterodera glycines) on yield of resistant and susceptible soybean cultivars grown in Ohio. Supplement to the Journal of Nematology 29, 703-709.

Wrather JA, Koenning SR and Anderson TR (2003). Effect of diseases on soybean yields in the United States and Ontario (1999-2002). Online. Plant Health Progress doi:10.1094/PHP-2003-0325-01-RV.

Xie M, Arelli PR and Sleper DA (1998). Genetic relationships among soybean plant introductions with resistance to Heterodera glycines using RFLPs. Soybean Genetics Newsletter 25, 157-159.

Young LD (1999). Soybeans resistant to Heterodera glycines populations attacking Hartwig soybean. Journal of Nematology 31, 583 (Abstract).

Young LD (1995). Soybean germplasm resistant to races, 3, 5, or 14 of soybean cyst nematode. Crop Science 35, 895-896.

Young LD (1990). Soybean germplasm evaluated for resistance to races 3, 5 and 14 of the soybean cyst nematode. Crop Science 30, 735-736.

Young LD and Kilen TC (1994). Genetic relationships among plant introduction for resistance to soybean cyst nematode race 5. Crop Science 34, 936-939.

Young LD and Hartwig EE (1988). Selection pressure on soybean cyst nematode from soybean cropping sequences. Crop Science 28, 845-847.

Yue P, Sleper DA and Arelli PR (2001a). Mapping resistance to multiple races of Heterodera glycines in soybean PI 89772. Crop Science 41, 1589-1595.

Yue P, Arelli PR and Sleper DA (2001b). Molecular characterization of resistance to Heterodera glycines in soybean PI 438489B. Theoretical and Applied Genetics 102, 921-928.

Zhang J, Arelli PR, Sleper DA, Qiu BX and Ellersieck MR (1999). Genetic diversity of soybean germplasm resistant to Heterodera glycines. Euphytica 107, 205-216.

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