Soybean Cyst Nematode

8/13/2019 Soybean Cyst Nematode

1/8


2/8

26 CANADIAN JOURNAL OF PLANT SCIENCE

BIOLOGY OF SOYBEAN CYST NEMATODESoybean cyst nematodes are round microscopic worms of approximately 480 m in length (Ichinohe 1952). They livein the soil and are parasitic, infecting and reproducing in theroots of specific hosts in the Fabaceae family. Legumes suchas soybean, pea ( Pisum sativum L.), birdsfoot trefoil ( Lotuscorniculatus L.) and common bean ( Phaseolus vulgaris L.)are efficient hosts for SCN.

The life cycle of SCN is approximately 21 d at 25C(Lauritis et al. 1983), resulting in two to five generations peryear. Embryos develop into juveniles within the eggs, thenbecome dormant or hatch out and become infectious. Rootdiffusate from the host plant stimulates hatching and emer-gence (Tefft and Bone 1985; Schmitt and Riggs 1991).Depending on the origin of the egg, the juveniles may alsohave to emerge through the cyst or female body. Thesehatched juveniles, which are invasive for only 611 d(Robinson et al. 1987), migrate toward host roots in thewater film between soil particles (Wallace 1963); migrationis influenced by gradients in pH, amino acids, sugars or heat(Sharma and Sharma 1998).

Upon arrival at a host plant the juveniles travel along theroot, repeatedly pressing their lips against its surface andinitiating stylet probing in search of a suitable entry point(Doncaster and Seymour 1973). Identification of a success-ful entry point increases probing frequency until the cuticleof the root is penetrated. Sites of invasion attract other indi-viduals, initiating colony formation within the root.Juveniles preferentially migrate to zones of elongation andcommonly penetrate the vascular tissues of the root(Atkinson and Harris 1989). Once migration slows, achange in stylet activity occurs and a specialized feedingstructure known as the syncytium is induced. The syncytiumis a large distinctive metabolically active group of plantcells that surround the nematodes head and provides a foodsource of plant nutrients. Once the feeding process is initiat-ed, the juveniles become immobile (Sharma and Sharma1998) and then enlarge and differentiate sexually intofemale or male adults (Mankau and Linford 1960; Mller etal. 1981). Adult males, which become mobile and move outof the root to fertilize the females, are unable to feed onplant tissue, resulting in a lifespan of only a few weeks(Zunke and Eisenback 1998).

Adult female nematodes do not become mobile, andremain receptive for at least 2 mo (Triantaphyllou andHirschmann 1962). Upon fertilization, their bodies swellwith egg development, resulting in the rupture of the cortexand epidermis of the root while still attached to the feedingsite. The initial egg production results in the deposition of 50 to 200 eggs in an external gelatinous matrix, which pro-vides antimicrobial and desiccation protection (Riggs andNiblack 1999). Upon degeneration of the vaginal muscles, afurther 50 to 200 eggs are deposited within the body cavityuntil the adult female dies. The body cavity enlarges to alemon shape and turns from white to yellow to brown withdevelopment. Egg dormancy is initiated from mid-summerto October and is critical for winter survival (Yen et al.1995). The life cycle begins as dormancy is broken andhatching occurs usually from April to June. Dormancy is

dependent on several factors, including host phenology andsoil temperature (Hill and Schmitt 1989). A unique featureof cyst nematodes is the ability of the female to turn herbody into a protective case or cyst, in which her progenymay remain viable for more than 12 yr (Riggs and Niblack 1999). Cysts of SCN can spread easily via water, wind, soiland machinery.

Soil environment influences the biological success of SCN. For examples, the duration of the complete life cycleis 18, 22 and 37 d at constant temperatures of 31, 24 and17C, respectively (Alston and Schmitt 1988), temperaturesof 20 and 30C result in cyst counts that are 30% less thanthose at 27C (Palmateer et al. 2000), non-irrigated soilstend to have higher SCN populations than irrigated soils(Koenning and Barker 1995), and cyst counts are positivelycorrelated with percent sand (Avendao et al. 2004).

MANAGEMENT OF SOYBEAN CYST NEMATODEManagement of SCN is complicated by the prolonged via-bility of eggs within unique protective cysts (Riggs andNiblack 1999), combined with population variability (Riggset al. 1981; Young 1984; Leudders 1989; Colgrove et al.2002) and the numerous methods by which eggs are dis-persed (Riggs and Niblack 1999). In addition, high inputconditions that promote soybean growth also enhance theability of SCN to reproduce (Ishibashi et al. 1973). The nar-row host range of SCN, however, is a characteristic that canbe exploited.

The use of resistant soybean cultivars is the primarymethod for managing SCN in commercial production. Theyare effective tools, but their success depends on the geneticvariability of the SCN population. In infested soils, resistantcultivars can yield 1050% higher than susceptible cultivars(Epps et al. 1981; Hartwig 1981; Young and Hartwig 1992).The presence of identifiable SCN races facilitates the effec-tive use of resistant cultivars.

Crop rotation is also a valuable tool in managing SCNpopulations. In Arkansas, a 3-yr rotation consisting of 1 yrof a non-host crop, 1 yr of a resistant soybean cultivar, and1 yr of a susceptible soybean cultivar is effective (Slack etal. 1981). More northerly areas of soybean production oftenrequire longer rotations for equally effective results(Niblack 1993). The use of non-host crops places minimalselection pressure on nematode populations and stabilizespopulation growth. Many growers resist long crop rotationsbecause non-host crops might be less-profitable and mightrequire additional equipment (Riggs and Schuster 1998).

Chemicals are costly, but have been effective in control-ling SCN in the past. The efficacy of nematicides can bevariable due to environmental conditions and improperapplication (Smith et al. 1991). Recent environmental andhealth concerns have resulted in the discontinuation of manyhighly successful nematicides (Roberts 1993), and controlof SCN using these chemicals is no longer widely recom-mended (Riggs and Schuster 1998).

Biological control theoretically provides an additionalSCN management tool. An unknown fungus, ArkansasFungus 18 (ARF18), develops on cysts, eggs and juvenilesof H. glycines and causes 2060% reduction in nematode


3/8

WINTER ET AL. SOYBEAN CYST NEMATODE RESISTANCE 27

numbers in infested soils (Kim and Riggs 1991). Currently,the amount required for field application is not economicalor practical for commercial use.

VIRULENCE OF SOYBEAN CYSTNEMATODE POPULATIONS

Variation in the virulence of SCN populations was identified a

few years after the development of the first commerciallyavailable SCN-resistant soybean cultivars (Ross 1962). Thisvariation together with the biological diversity within popula-tions resulted in the need for a classification scheme.

To characterize the heterogeneous populations of SCN, arace scheme was developed (Golden et al. 1970) and laterexpanded (Riggs and Schmitt 1988). A female index (FI),defined as the ratio of the number of females that develop ondifferential lines (different sources of resistance) to thosethat develop on the standard susceptible cultivar Lee, multi-plied by 100, is used to determine the race identity of SCNpopulations; an arbitrary value of < 10% is designated asresistant (Golden et al. 1970). The race characterizationscheme describes SCN populations in broad terms, and per-

mits intra-race variability (Riggs et al. 1981; Riggs andSchmitt 1988; Riggs and Schmitt 1991; Riggs et al. 1991;Rao-Arelli et al. 1992).

Several concerns have been expressed with the race clas-sification scheme. Ambiguity about race designation of aSCN population is common and may be attributed to the useof differential host plants from different sources, variabilityin inoculum preparation, and the inability to completelyrecover all cysts (Riggs et al. 1988). Other factors such asthe time of sampling and the temperature during testinggreatly influence race designations (Palmateer et al. 2000;Colgove et al. 2002). Directional selection studies usingresistant cultivars revealed unpredictable frequency changesin virulent individuals within SCN populations (Riggs et al.

1981; Young 1984; Leudders 1989; Anand et al. 1995; Noeland Edwards 1996; Colgrove et al. 2002). The race schemeonly considers the average phenotype and not the geneticdiversity of the population (Niblack et al. 2002).

The HG (named after Heterodera glycines ) Type test is aclassification scheme with enhanced flexibility to describeSCN population variation (Niblack et al. 2002). The abilityof a population to infect seven different indicator lines (i.e.,1. PI 548402, 2. PI 88788, 3. PI 90763, 4. PI 437654, 5. PI309332, 6. PI 89772 and 7. PI 548316), as well as the stan-dard susceptible line Lee 74, is evaluated under standardizedbioassay conditions. If fewer than 100 females are observedon Lee 74, the test is discarded and repeated. The populationtype is then based on the identifier numbers of the indicator

lines that exhibit a FI 10. For example, a population thatproduces FI 10 on PI 548402, PI 88788 and PI 89772 is anHG Type 1.2.6. The HG Type test does not identify geno-types within a population, and SCN populations with thesame HG designation may not behave in the same waybecause they can easily differ in characteristics not mea-sured by the test. HG Type testing does permit more accu-rate management recommendations than the Race schemedescribed above because of the additional resistantgermplasm used in the test, and the test is easily expandedas new soybean germplasm is released and deployed.

SOYBEAN CYST NEMATODE RESISTANTSOYBEAN CULTIVARS

The first SCN-resistant soybean sources identified in themid 1950s were plant introductions PI 90763 and PI 84751and cultivars Ilsoy and Peking (Ross and Brim 1957). Thesesources of resistant germplasm were undesirable for com-mercial use due to the presence of a black seed coat. Amajor resistance gene ( Rhg4 ) was later identified as closelylinked with the seed coat colour gene (Matson and Williams1965). This linkage made it difficult for breeders to developSCN-resistant cultivars with a desirable yellow seed coat.Peking was chosen as the initial parental source of resis-tance due to its agronomic characteristics, and after onecycle of breeding, three SCN-resistant cultivars, Custer,Pickett and Dyer were released in 1965, 1967 and 1968,respectively (Brim and Ross 1966; Hartwig and Epps 1968;Leudders et al. 1968). These cultivars were not widelygrown due to their relatively low yields, but they providedthe parentage base for future cultivars resistant to Races 1and 3 (Anand et al. 1998).

In the 1970s, a second cycle of breeding resulted in threemore cultivars from each of Custer, Pickett and Dyer.Shortly after their release a new SCN race, Race 4, wasidentified (Hartwig 1981), prompting another germplasmevaluation, which identified resistance to Race 4 in PI88788, PI 89772, PI 87631-1, Cloud, Columbia, Peking, PI84751 and PI 90763 (Epps and Hartwig 1972).Subsequently, breeding with PI 88788 as a resistant parentresulted in the release of the first cultivar, Bedford, withresistance to SCN Race 4 (Hartwig and Epps 1978). Laterrevisions to the race classification scheme classified PI88788 as resistant to Race 14. Forrest, the most widelygrown cultivar in the southern United States in the 1970s,derived SCN resistance to Races 1 and 3 from Dyer, andwas estimated to prevent US$405M in crop losses from1975 to 1980 (Bradley and Duffy 1982). However, repeateduse of resistant germplasm sources resulted in the develop-ment of new races of SCN (Riggs et al. 1981). An addition-al germplasm screen identified PI 437654 as resistant to allSCN races (Anand et al. 1988; Diers et al. 1997) and it wasused in the development of the resistant cultivar Hartwig(Anand 1992).

Cyst X, the most recent addition to the list of SCN-resistant cultivars, was derived from a cross betweenWilliams 82 and Hartwig (Vierling et al. 2000). It was madeavailable to public and private breeding programs in 1997and patent protected in 2000. The locus responsible for CystX resistance is on linkage group (LG) B1 and explainsmore than 90% of the total phenotypic variation to Race 3SCN (Vierling et al. 1996).

Peking, PI 88788 and PI 209332 were used extensively assources for SCN resistance in breeding programs, resultingin a narrow resistant germplasm base (Diers and Arelli1999). In the mid-western United States, 80% of publicSCN-resistant cultivars released during the 1990s and 93%of private industry cultivars available in 1998 derived SCNresistance from PI 88788 (Diers and Arelli 1999), whereasin Ontario, Canada, all cultivars available in 2005 derivedresistance from PI 88788 (Ontario Oil and Protein Seed


4/8


Crop Committee 2005). Genetic diversity studies suggestedthat many sources of resistance are genetically similar andcluster into two major groups (Diers et al. 1997). However,a more recent study identified that the resistant differentialsused in the race test are indeed genetically diverse (Zhang etal. 1999), a result that could be explained by specific alleliccomposition at the resistant loci, as described recently for

Rhg1 (Brucker et al. 2005). The presence of such allelic dif-ferences at resistance loci provides impetus for usingGlycine soja Sieb. and Zucc. as a source of novel resistancegenes and alleles since allelic differences between G. sojaand G. max are common and well established (Maughan etal. 1995; Powell et al. 1996).

MOLECULAR MARKERS ASSOCIATED WITHSOYBEAN CYST NEMATODE RESISTANCE

Molecular markers allow traits of interest to be identified,mapped and identified in subsequent generations. Linkagegroups (LG) reflect the nature of the relationships amongmolecular markers within and among individual chromo-somes. The use of molecular markers in combination withphenotypic data enables regions on the chromosome to beassociated with a particular trait. If many genes control thetrait of interest, the associated region identified is termed aquantitative trait locus (QTL). A recent genetic linkage mapof soybean, which has over 1000 SSR markers saturating 20linkage groups (Song et al. 2004), allows researchers toaccurately assign specific genetic markers associated withtraits of interest or QTL to LGs.

Breeding for SCN resistance using either the classicalapproach or molecular markers has been complicated by thelength of time for screening plant material and control of thetrait by multiple genes. Previous research indicates that SCNresistance QTL are located on 17 of the 20 LG within thesoybean genome, and explain 191% of the total phenotyp-ic variation [for a review, see Concibido et al. (2004)].

A major QTL, designated as rhg1 , is located on LG Gassociated with the RFLP marker C006V (Concibido et al.1994) and explains 54% of the total phenotypic variation indisease response in PI 209332 to Race 6, 50% to Race 3 and35% to Race 1 (Concibido et al. 1996). This multiple-race(non-race specific) response suggests that the gene-for-genetheory does not apply to SCN resistance, and that despite thecommon use of the term resistance, it is more likely a caseof genes/loci carrying either partial resistance or tolerance toSCN, which are terms rarely used in the SCN literature.Separate studies indicated that Peking (Chang et al. 1997;Concibido et al. 1997; Meksem et al. 2001), PI 90763(Concibido et al. 1997), PI 88788 (Concibido et al. 1997), PI209332 (Concibido et al. 1994), PI 89772 (Yue et al.2001b), PI 437654 (Webb et al. 1995), Peking + PI 437654(Prabhu et al. 1999) and Peking + PI 88788 + PI 90763(Heer et al. 1998) have the major QTL on LG G near rhg1 .The resistance conferred by rhg1 to multiple SCN races ledto extensive mapping of this region, with the SSR, Satt309,being identified only 0.4 cM from the rhg1 gene (Cregan etal. 1999).

A second major QTL for SCN resistance on LG A2 hasbeen designated as the Rhg4 gene. It is closely linked to the

i locus controlling seed coat colour (Matson and Williams1965). This region was the first SCN-resistant locus to bemapped using molecular markers (Weisemann et al. 1992).In PI 209332, LG A2 explains 15% of the total phenotypicvariation to SCN Race 3 (Concibido et al. 1994) and a sig-nificant portion of the variation in Peking (Mahalingam andSkorupska 1995; Chang et al. 1997; Meksem et al. 2001), PI437654 (Webb et al. 1995) and Peking + PI 88788 + PI90763 (Heer et al. 1998). Although two additional recessivegenes, rhg2 and rgh3 , have been named and hypothesised aspart of a three recessive gene model (Caldwell et al. 1960),they are yet to be assigned to a linkage group on the soybeangenome map. It is conceivable that some of the identifiedQTL are located at or near one of these two genes.

Many minor QTL have been identified on LG A1, B1,B2, C1, C2, D1a, D2, E, F, G, H, I, J, L, M and N(Concibido et al. 2004). The total number of QTL per LGrange from one (e.g., LG H and I) to four (LG G)(Concibido et al. 2004). The position of each QTL on thesoybean genetic map, however, can be considered tentativeat best due to differences in size and structure of mappingpopulations, DNA marker platforms and limited number of DNA markers at the time of publication of each report(Concibido et al. 2004). Perhaps not surprisingly, the great-est number of resistant QTL are identified in Peking (nineindependent QTL) as the oldest and most frequently studiedsource of SCN resistance, whereas low numbers are identi-fied in recent sources such as PI 88788 or PI 90763 (one andtwo QTL, respectively) (Concibido et al. 2004). The allelicdiversity found at the minor QTL is similar to that found atmajor QTL, but the amount of variation explained tends tobe smaller for the minor QTL. The existence of most minorQTL has often been reported only once and requires inde-pendent confirmation; this is a common deficiency withQTL mapping. The most consistent reports are those for therhg1 and Rhg4 loci (Concibido et al. 2004).

Crosses have revealed significant resistance not identifiedin either parent. For example, in the cross Peking by PI437654, two resistant QTL to SCN Race 3 were located onLG B1 (Vierling et al. 1996). These QTL on LG B1, identi-fiable by RFLP markers A006 and A567, explained 91 and1% of the total phenotypic variation, respectively. If thesources of resistance are considered independently, a resis-tant QTL is only identified on LG B1 at A567 in PI437654,and it explains 27% of the total phenotypic variation(Webb 2003). The QTL on LG B1 is not derived fromPeking (Concibido et al. 2004). However, it is known to bepresent in resistant source PI 89772, but it only explains717% of the resistance to SCN Races 1, 2 and 5 (Yue et al.2001b). On the other hand, the number of races showing sig-nificant response at a QTL ranges from one to five (LG G,rhg1 locus for races 1, 2, 3, 5 and 14) per locus (Concibidoet al., 2004).

Resistant QTL can be found in several regions on an indi-vidual linkage group. For example, on LG G, three loci areassociated with SCN resistance in addition to the majorgene, rhg1 (Concibido et al. 2004). The SCN resistantsources Peking (Concibido et al. 1997), PI 438489B (Yue etal. 2001a) and PI 468916 (Wang et al. 2001) have resistant


5/8


QTL at other locations on LG G. Of the three additionalregions of SCN resistance on LG G, all are associated withresistance to Race 3 SCN, suggesting a possible rearrange-ment of the resistant genes on LG G. Multiple QTL for SCNresistance have been identified on LGs A1, B1, B2, C2,D1a, D2, E, G and M [for a review, see Concibido et al.(2004)].

Minor loci for SCN resistance vary with regards to racespecificity. For example, a minor locus for resistance to SCNRace 3 occurs on LG J in resistant sources PI 209332(Concibido et al. 1996) and PI 90763 (Concibido et al. 1997).A minor QTL is also present on LG E in P438489B and PI468916 and associated with resistance to SCN Races 2 and14, and 3, respectively (Wang et al. 2001;Yue et al. 2001a).

Significant interaction between major and minor markersassociated with SCN resistance has been previously identi-fied (Mahalingam and Skorupska 1995; Webb et al. 1995;Chang et al. 1997; Kilo et al. 1997; Heer et al. 1998; Prabhuet al. 1999; Meksem et al. 2001; Wang et al. 2001; Yue etal. 2001b). For example, single factor ANOVA does not sig-nificantly associate either Rhg4 or rhg1 with SCN resistanceto Race 3 in a Flyer Hartwig population; however, theirinteraction accounts for 16% of the total phenotypic varia-tion (Prabhu et al. 1999). Interaction between significantmarkers has been attributed to epistasis (Heer et al. 1998;Yue et al. 2001a; Concibido et al. 2004).

INTERSPECIFIC BREEDING WITH GLYCINE SOJARecently, soybean breeders and geneticists began to use G.soja as an alternative source of SCN resistance for theimprovement of elite cultivars. This wild ancestor of thedomesticated soybean enables many common interspecificobstacles such as infertility and pod abortion to be circum-vented. In G. max G. soja populations, three backcrossesto G. max are required to attain a reasonable number of agronomically suitable lines (Junyi et al. 1982; Ertl and Fehr1985; Carpenter and Fehr 1986).

Loci associated with SCN resistance have been docu-mented in a cross between G. max (A81-356022) and G.soja (PI 468916) (Wang et al. 2001). Significant QTL,which derive resistance from G. soja , are located on LG Gand E, and respectively, explain 27 and 23% of the total phe-notypic variation to SCN Race 3. The region on LG G is notbelieved to be a major SCN resistance gene as the QTL islocated 230 cM away from the rhg1 gene. Therefore, thisQTL may be unique as it has not previously been associatedwith SCN resistance. By contrast, the QTL on LG E may ormay not be unique to G. soja as this region has previouslybeen associated with SCN resistance in G. max (Yue et al.2001a). G. soja -specific QTL could represent unique genesfor broadening SCN resistance in G. max cultivars, but littleinformation on their use is available. The development andrelease of the first cultivars incorporating such QTL maytake some years due to the backcrossing and linkage dragissues. In addition to the preliminary efforts describedabove, it is reasonable to believe that the more than 1000plant introductions of G. soja available at the USDA soy-bean germplasm collection in Urbana-Champaign, IL, carryunutilized genes and alleles for SCN resistance.

CLONING OF CANDIDATE SOYBEAN CYSTNEMATODE RESISTANCE GENES

In recent years, the ability to genetically engineer plants hasrevolutionized the possibilities for nematode control(Williamson 1999; Atkinson et al. 2003; McLean et al.2003). This approach typically involves the manipulationand incorporation of various genes that could directly inter-fere with feeding cells or the nematode. However, this couldalso involve genes of uncertain function. For example, thereare claims that candidate genes for rhg1 and Rhg4 have beencloned, and that both genes are receptor kinases (seeConcibido et al. 2004). However, it is unclear if these can-didate genes are associated with SCN resistance, and com-plementation studies to confirm the identity of the geneshave not been reported. Another gene known as Hs1 pro-1reportedly provides resistance against the beet cyst nema-tode, H. schachtii Schmidt (Cai et al. 1997), and interspe-cific hybridizations between H. schachtii and H . glycinesare fertile, with the cross being successfully taken through tothe F 2 generation (Potter and Fox 1965). This lack of areproductive barrier between these two species of cystnematode demonstrates an extremely high genetic related-ness, and although different plant hosts are parasitized, themolecular mechanisms employed are likely similar. Thus,the mechanism of resistance provided by the Hs1 pro-1 geneagainst H. schachtii may also be effective against H.glycines. Interestingly, the presence of an Hs1 pro-1 homo-logue in soybean fails to distinguish between susceptibleand tolerant germplasm, but complementation studies toconfirm the identity of the gene have not been conducted(see Concibido et al. 2004). Further analysis of these candi-date resistance genes is necessary to provide insights intothe genetic mechanisms involved.

CONCLUSIONSThe SCN is a serious pest of the soybean crop. The repro-duction of SCN is very dependent on soil environment, andsoil variables such as temperature need to be considered inresearch on SCN resistance. Management of SCN is primar-ily dependent upon a combination of crop rotation and resis-tant cultivars, which minimize selection pressure on SCNpopulations and reduce soil populations. It has been difficultto separate SCN populations that differ in reproductive abil-ity on known sources of resistance. The Race scheme andHG Type test are common methods of characterizing popu-lations with respect to known resistant soybean germplasmand can be used as tools in the management of SCN. SCNpopulations often display broad variation in virulence, andcan rapidly overcome resistance in commercially availablesoybean cultivars, which are derived from a limited geneticbase. A number of different resistance genes in a single cul-tivar may be necessary to ensure long-term resistance.Recently, molecular markers have become important foridentifying QTL for SCN resistance and predicting plantphenotype within experimental populations. This ability,combined with marker-assisted selection, is an invaluabletool for plant breeders. Wild soybean germplasm representsan alternative source of SCN resistance for breeding intoelite cultivars, but its use is often avoided because of possi-


6/8


ble linkage drag of deleterious traits. The development anduse of molecular markers for identifying desirable DNAregions has made, and will continue to make, the use of wildgermplasm more efficient. Several candidate SCN resis-tance genes have reportedly been cloned, but further analy-sis is necessary to provide insights into the mechanisms of genetic resistance.

ACKNOWLEDGEMENTSS.M.J.W. was supported by funds to I.R. and B.J.S. from theFood Systems Biotechnology Center at the University of Guelph, the Ontario Soybean Growers, and the OntarioMinistry of Agriculture and Food.

Alston, D. G. and Schmitt, D. P. 1988. Development of Heterodera glycines life stages as influenced by temperature. J.Nematol. 20: 366372.Anand, S. C. 1992. Registration of Hartwig soybean. Crop Sci.32 : 10691070.Anand, S. C., Cook, R. and Dale, M. F. B. 1998. Development of resistant and tolerant varieties. Pages 293321 in S. B. Sharma, ed.

The cyst nematodes. Kluwer Academic Publishers, London, UK.Anand, S. C., Koenning, S. R. and Sharma, S. B. 1995. Effect of temporal deployment of different sources of resistance to soybeancyst nematode. J. Prod. Agric. 8: 119123.Anand, S. C., Gallo, K. M., Baker, I. A. and Hartwig, E. E.1988. Soybean plant introductions with resistance to races 4 or 5 of soybean cyst nematode. Crop Sci. 28: 563564.Anderson, T. R., Welacky, T. W., Olechowski, H. T., Ablett, G.and Ebsary, B. A. 1988. First report of Heterodera glycines onsoybeans in Ontario, Canada. Plant Dis. 72 : 453.Atkinson, H. J. and Harris, P. D. 1989. Changes in nematodeantigens recognized by monoclonal antibodies during early infec-tions of soya beans with the cyst nematode Heterodera glycines .Parasitology 98 : 479487.Atkinson, H. J., Urwin, P. E. and McPherson, M. J. 2003.

Engineering plants for nematode resistance. Annu. Rev. Phytopathol.41: 26.126.25.Avendao, F., Pierce, F. J., Schabenberger, O. andMelakeberhan, H. 2004. The spatial distribution of soybean cystnematode in relation to soil texture and soil map unit. Agron. J. 96 :181194.Bradley, E. B. and Duffy, M. 1982. The value of plant resistanceto soybean cyst nematodes: A case study of forrest soybeans. NRSstaff report. US Department of Agriculture, Washington, DC.Brim, C. A. and Ross, J. P. 1966. Registration of Pickett soy-beans. Crop Sci. 6: 305.Brucker, E., Carlson, S., Wright, E., Niblack, T. and Diers, B.2005. Rhg1 alleles from soybean PI437654 and PI 88788 responddifferentially to isolates of Heterodera glycines in the greenhouse.Theor. Appl. Genet. 111 : 4449.Cai, D., Kleine M., Kifle, S., Harloff, H.-J., Sandal, N. N.,Marcker K. A., Klein-Lankhorst, R. M., Salentijn, E. M. J.,Lange, W., Stiekema, W. J., Wyss, U., Grundler, F. M. W. andJung, C. 1997. Positional cloning of a gene for nematode resis-tance in sugar beet. Science 275 : 832834.Caldwell, B. E., Brim, C. A. and Ross, J. P. 1960. Inheritance of resistance of soybeans to the cyst nematode, Heterodera glycines .Agron. J. 52 : 635636.Carpenter, J. A. and Fehr, W. R. 1986. Genetic variability fordesirable agronomic traits in populations containing Glycine sojagermplasm. Crop Sci. 26 : 681686.

Chang, S. J. C., Doubler, T. W., Kilo, V. Y., Abu-Thredeih, J.,Prabhu, R., Freire, V., Suttner, R., Klein, J., Schmidt, M. E.,Gibson, P. T. and Lightfoot, D. A. 1997. Association of lociunderlying field resistance to soybean sudden death syndrome(SDS) and cyst nematode (SCN) race 3. Crop Sci. 37 : 965971.Colgrove, A. L., Smith, G. S., Wrather, J. A., Heinz, R. D. andNiblack, T. L. 2002. Lack of predictable race shift in Heteroderaglycines Infested field plots. Plant Dis. 86: 11011108.Concibido, V. C., Denny, R. L., Boutin, S. R., Hautea, R., Orf,J. H. and Young, N. D. 1994. DNA marker analysis of loci under-lying resistance to soybean cyst nematode ( Heterodera glycinesIchinohe). Crop Sci. 34 : 240246.Concibido, V. C., Denny, R. L., Lange, D. A., Orf, J. H. andYoung, N. D. 1996. RFLP mapping and marker-assisted selectionof soybean cyst nematode resistance in PI 209332. Crop Sci. 36:16431650.Concibido, V. C., Diers, B. W. and Arelli, P. R. 2004. A decadeof QTL mapping for cyst nematode resistance in soybean. CropSci. 44 : 11211131.Concibido, V. C., Lange, D. A., Denny, R. L., Orf, J. H. andYoung, N. D. 1997. Genome mapping of soybean cyst nematoderesistance genes in Peking, PI 90763, and PI 88788 using DNAmarkers. Crop Sci. 37: 258264.

Cregan, P. B., Mudge, J., Fickus, E. W., Danesh, D., Denny, R.and Young, N. D. 1999. Two simple sequence repeat markers toselect for soybean cyst nematode resistance coditioned by the rhg1locus. Theor. Appl. Genet. 99: 811818.Diers, B. W. and Arelli, P. R. 1999. Management of parasitic nema-todes of soybean through genetic resistance. Pages 300306 in H. E.Kauffman, ed. Proc. of the World Soybean Research Conference. 6th.Chicago, Illinois. Superior Printing, Champaign, IL.Diers, B. W., Skorupska, H. T., Rao-Arelli, A. P. and Cianzio,S. R. 1997. Genetic relationships among soybean plant introduc-tions with resistance to soybean cyst nematodes. Crop Sci. 37 :19661972.Doncaster, C. C. and Seymour, M. K. 1973. Exploration andselection of penetration site by Tylenchida. Nematologica 19 :137145.

Epps, J. M. and Hartwig, E. E. 1972. Reaction of soybean vari-eties and strains to race 4 of the soybean cyst nematode. J.Nematol. 4: 222 (Abstr.).Epps, J. M., Young, L. D. and Hartwig, E. E. 1981. Evaluationof nematicides and resistant cultivar for control of soybean cystnematode race 4. Plant Dis. 65: 665666.Ertl, D. S. and Fehr, W. R. 1985. Agronomic performance of soy-bean genotypes from Glycine max ( Glycine soja crosses. Crop Sci.25: 589592.Golden, A. M., Epps, J. M., Riggs, R. D., Duclos, L. A., Fox, J.A. and Bernard, R. L. 1970. Terminology and identity of infra-specific forms of the soybean cyst nematode ( Heteroderaglycines ). Plant Dis. Rep. 54 : 544546.Hartwig, E. E. 1981. Breeding productive soybean cultivars resis-tant to the soybean cyst nematode for the southern United States.Plant Dis. 65 : 303307.Hartwig, E. E. and Epps, J. M. 1968. Dyer soybeans. Crop Sci. 8:402.Hartwig, E. E. and Epps, J. M. 1978. Registration of Bedfordsoybeans. Crop Sci. 18 : 915.Heer, J. A., Knap, H. T., Mahalingam, R., Shipe, E. R., Arelli,P. R. and Matthews, B. F. 1998. Molecular markers for resistanceto Heterodera glycines in advanced soybean germplasm. Mol.Breed. 4: 359367.Hill, N. S. and Schmitt, D. P. 1989. Influence of temperature andsoybean phenology on dormancy induction of Heteroderaglycines . J. Nematol. 21: 361369.


7/8


Ichinohe, M. 1952. On the soybean nematode, Heteroderaglycines n. sp. from Japan. Oyo-Dobutsugaka-Zasshi [Mag. Appl.Zool.] 17: 14. [in Japanese.]Ishibashi, N., Kondo, E., Muraoka, M. and Yokoo, T. 1973.Ecological significance of dormancy in plant parasitic nematodes.I. Ecological difference between eggs in gelatinous matrix and cystof Heterodera glycines Ichinohe (Tylenchida: Heteroderidae).Appl. Entomol. Zool. 8: 5363.Junyi, G., Fehr, W. R. and Palmer, R. G. 1982. Genetic perfor-mance of some agronomic characters in four generations of a back-crossing program involving Glycine max and Glycine soja . ActaGenet. Sin. 9: 4456. [in Japanese, English abstract.]Kilo, V. Y., Abu-Thredeih, J., Suttner, B., Chang, S. J. C.,Gibson, P. C. and Lightfoot, D. A. 1997. Co-inheritance of resis-tance to SCN and SDS in Pyramid x Douglas. Soybean Genet.Newsl. 24: 126127.Kim, D. G. and Riggs, R. D. 1991. Characteristics and efficacy of a sterile Hyphomycete (ARF18), a new biocontrol agent for

Heterodera glycines and other nematodes. J. Nematol. 23 :275282.Koenning, R. R. and Barker, K. R. 1995. Soybean photosynthe-sis and yield as influenced by Heterodera glycines , soil type andirrigation. J. Nematol. 27: 5162.Lauritis, J. A., Rebois, R. V. and Graney, L. S. 1983.Development of Heterodera glycines Ichinohe on soybean,Glycine max (L.) Merr., under gnotobiotic conditions. J. Nematol.15 : 272281.Leudders, V. D. 1989. Variable transfer of soybean genes forresistance to soybean cyst nematode. Crop Sci. 29: 933936.Leudders, V. D., Williams, L. F. and Matson, A. 1968.Registration of Custer soybeans. Crop Sci. 8: 402.Mahalingam, R. and Skorupska, H. T. 1995. DNA markers forresistance to Heterodera glycines I. race 3 in soybean cultivarPeking. Breed. Sci. 45 : 435443.Mankau, R. and Linford, M. B. 1960. Host-parasite relationshipsof clover cyst nematode, Heterodera trifolii Goffart. AgriculturalExperimental Station, University of Illinois, Bulletin 667. 50 pp.Matson, A. L. and Williams, L. F. 1965. Evidence of a fourthgene for resistance to the soybean cyst nematode. Crop Sci. 5: 477.Maughan, P. J., Saghai Maroof, M. A. and Buss, G. R. 1995.Microsatellite and amplified sequence length polymorphisms incultivated and wild soybean. Genome 38 : 715723.McLean, M. D., Yevtushenko, D. P., Deschene, A., VanCauwenberghe, O. R., Makhmoudova, A., Potter, J. W., Bown,A. W. and Shelp, B. J. 2003. Overexpression of glutamate decar-boxylase in transgenic tobacco plants confers resistance to thenorthern root-knot nematode. Mol. Breed. 11 : 277285.Meksem, K., Pantazopoulos, P., Njiti, V. N., Hyten, L. D.,Arelli, P. R. and Lightfoot, D. A. 2001. Forrest resistance to thesoybean cyst nematode is bigenic: saturation mapping of the Rhg1and Rhg4 loci. Theor. Appl. Genet. 103 : 710717.Mller, J., Rehbock, K. and Wyss, U. 1981. Growth of

Heterodera schachtii with remarks on amounts of foods consumed.Rev. Nmatol. 4: 227234.Niblack, T. L. (ed.) 1993. Protect your soybean profits: Managesoybean cyst nematode. University of Missouri Printing Services,Columbia, MO. 20 pp.Niblack, T. L., Arelli, P. R., Noel, G. R., Opperman, C. H., Orf,J. H., Schmitt, D. P., Shannon, J. G. and Tylka, G. L. 2002. Arevised classification scheme for genetically diverse populations of

Heterodera glycines . J. Nematol. 34 : 279288.Noel, G. R. and Edwards, D. I. 1996. Population development of

Heterodera glycines and soybean yield in soybean-maize rotations fol-lowing introduction into a noninfested field. J. Nematol. 28: 335342.

Ontario Oil and Protein Seed Crop Committee. 2005. Resistantvariety performance in SCN infested fields. [Online] Available:http://www.oopscc.org/table7.html [Undated].Palmateer, A. J., Schmidt, M. E., Stetina, S. R. and Russin, J.S. 2000. Temperature effects on race determination in Heteroderaglycines . J. Nematol. 32: 349355.Potter, J. W. and Fox, J. A. 1965 . Hybridization of Heteroderaschachtii and H. glycines . Phytopathology 55: 800801.Powell, W., Morgante, M., Doyle, J. J., McNicol, J. W., Tngey,S. V. and Rafalski, A. J. 1996. Genepool variation in genusGlycine subgenus Soja revealed by polymorphic nuclear andchloroplast microsatellites. Genetics 144 : 793803.Prabhu, R. R., Njiti, V. N., Bell-Johnson, B., Johnson, J. E.,Schmidt, M. E., Klein, J. H. and Lightfoot, D. A. 1999. Selectingsoybean cultivars for dual resistance to soybean cyst nematode andsudden death syndrome using two DNA markers. Crop Sci. 39 :982987.Rao-Arelli, A. P., Wrather, J. A. and Anand, S. C. 1992.Genetic diversity among isolates of Heterodera glycines andsources of resistance in soybeans. Plant Dis. 76 : 894896.Riggs, R. D. and Niblack, T. L. 1999. Soybean cyst nematode.Pages 5253 in G. L. Hartman, J. B. Sinclair, and J. C. Rupe, eds.Compendium of soybean diseases. 4th ed. APS Press, St. Paul,

MN.Riggs, R. D. and Schmitt, D. P. 1988. Complete characterizationof the race scheme for Heterodera glycines . J. Nematol. 20 :392395.Riggs, R. D. and Schmitt, D. P. 1991. Optimization of the

Heterodera glycines race test procedure. J. Nematol. 23 : 149154.Riggs, R. D. and Schuster, R. P. 1998. Management. Pages388416 in S. B. Sharma, ed. The cyst nematodes. KluwerAcademic Publishers, London, UK.Riggs, R. D., Hamblen, M. L. and Rakes, L. 1981. Infra-speciesvariation in reactions to hosts in Heterodera glycines populations.J. Nematol. 13: 171179.Riggs, R. D., Rakes, L. and Elkins, R. 1991. Soybean cultivarsresistant and susceptible to Heterodera glycines . J. Nematol. 23:584592.

Riggs, R. D., Schmitt, D. P. and Noel, G. R. 1988. Variability inrace tests with Heterodera glycines . J. Nematol. 20: 565572.Roberts, P. A. 1993. The future of nematology: Integration of newand improved management strategies. J. Nematol. 25 : 383394.Robinson, M. P., Atkinson, H. J. and Perry, R. N. 1987. Theinfluence of soil moisture and storage time on the motility, infec-tivity and lipid utilization of second stage juveniles of the potatocyst nematodes Globodera rostochiensis and G. pallida . Rev.Nmatol. 10: 343348.Ross, J. P. 1962. Physiological strains of Heterodera glycines .Plant Dis. Rep. 46: 766769.Ross, J. P. and Brim, C. A. 1957. Resistance of soybeans to thesoybean cyst nematode as determined by a double-row method.Plant Dis. Rep. 41: 923924.Schmitt, D. P. and Riggs, R. D. 1991. Influence of selected plantspecies on hatching of eggs and development of larvae of

Heterodera glycines . J. Nematol. 23: 16.Sharma, S. B. and Sharma, R. 1998. Hatch and emergence.Pages 191216 in S.B. Sharma, ed. The cyst nematodes. KluwerAcademic Publishers, London, UK.Slack, D. A., Riggs, R. D. and Hamblen, M. L. 1981. Nematodecontrol in soybeans: Rotation and population dynamics of soybeancyst and other nematodes. Report Series 263 : 136. Arkan.Agric.Exp. Sta.Smith, G. S., Niblack, T. L. and Minor, M. C. 1991. Responseof soybean cultivars to aldicarb in Heterodera glycines -infestedsoils in Missouri. J. Nematol. 23 (Suppl.): 693698.


8/8


Song, Q. J., Marek, L. F., Shoemaker, R. C., Lark, K. G.,Concibido, V. C., Delannay, X., Specht, J. E. and Cregan, P. B.2004. A new integrated genetic linkage map of the soybean, Theor.Appl. Genet 109 : 122128.Statistics Canada. 2004. Field crop reporting series, no. 8, 2003.Statistics Canada, Ottawa, ON.Tamulonis, J. P., Luzzi, B. M., Hussey, R. S., Parrott, W. A.and Boerma, H. R. 1997a. DNA markers associated with resis-tance to Javanese root-knot nematode in soybean. Crop Sci. 37 :783788.Tefft, P. M. and Bone, L. W. 1985. Plant-induced hatching of eggs of the soybean cyst nematode Heterodera glycines . J.Nematol. 17: 275279.Triantaphyllou, A. C. and Hirschmann, H. 1962. Oogenesis andmode of reproduction in the soybean cyst nematode, Heteroderaglycines . Nematologica 7: 235241.United States Department of Agriculture. 2004. Soybeans:world supply and distribution. Foreign Agricultural Service,Washington, DC. [Online] Available: http://www.fas.usda.gov/ oilseeds/circular/2004/04-08/table5t7.pdf [2004 Aug. 18].Vierling, R. A., Faghihi, J., Ferris, V. R. and Ferris, J. M. 1996.Association of RFLP markers with loci conferring broad-basedresistance to the soybean cyst nematode ( Heterodera glycines ).

Theor. Appl. Genet. 92 : 8386.Vierling, R. A., Faghihi, J., Ferris, V. R. and Ferris, J. M.,inventors; Purdue Research Foundation, assignee. 2000.Methods for conferring broad-based soybean cyst nematode resis-tance in a soybean line. US patent 6,096,944. Date issued: 2000Aug. 01.Wallace, H. R. 1963. The biology of plant parasitic nematodes.Edward Arnold, London, UK. 280 pp.Wang, D., Arelli, P. R., Shoemaker, R. C. and Diers, B. W.2001. Loci underlying resistance to Race 3 of soybean cyst nema-tode in Glycine soja plant introduction 468916. Theor. Appl.Genet. 103 : 561566.Webb, D. M. inventor; Pioneer Hi-Bred International, Inc.,assignee. 2003. Quantitative trait loci associated with cyst nema-tode resistance and use thereof. US patent 6,538,175. Date issued:

2003 Mar. 25 .

Webb, D. M., Baltazar, B. M., Rao-Arelli, A. P., Schupp, J.,Clayton, K., Keim, P. and Beavis, W. D. 1995. Genetic mappingof soybean cyst nematode race-3 resistance loci in soybeanPI437.654. Theor. Appl. Genet. 91: 574581.Weisemann, J. M., Matthews, B. F. and Devine, T. E. 1992.Molecular markers located proximal to the soybean cyst nematoderesistance gene, Rhg4 . Theor. Appl. Genet. 85 : 136138.Williamson, V. M. 1999. Plant nematode resistance genes. Curr.Opin. Plant Biol. 2: 327331.Winstead, N. N., Skotland, C. B. and Sasser, J. N. 1955.Soybean cyst nematode in North Carolina. Plant Dis. Rep. 39 :911.Wrather, J. A., Anderson, T. R., Arsyad, D. M., Tan, Y.,Ploper, L. D., Porto-Puglia, A., Ram, H. H. and Yorinori, J. T.2001. Soybean disease loss estimates for the top ten soybean-pro-ducing countries in 1998. Can. J. Plant Pathol. 23 : 115121.Yen, J. H., Niblack, T. L. and Wiebold, W. J. 1995. Dormancyof Heterodera glycines in Missouri. J. Nematol. 27: 153163.Young, L. D. 1984. Changes in the reproduction of Heteroderaglycines on different lines of Glycine max . J. Nematol. 16 :304309.Young, L. D. and Hartwig, E. E. 1992. Evaluation of soybeansresistant to Heterodera glycines race 5 for yield and nematode

reproduction. J. Nematol. 20 (Suppl.): 3840.Yue, P., Arelli, P. R. and Sleper, D. A. 2001a. Molecular charac-terization of resistance to Heterodera glycines in soybean PI438489B. Theor. Appl. Genet. 102 : 921928.Yue, P., Sleper, D. A. and Arelli, P. R. 2001b. Mapping resis-tance to multiple races of Heterodera glycines in soybean PI89772. Crop Sci. 41: 15891595.Zhang, J., Arelli, P. R., Sleper, D. A., Qiu, B. X. and Ellersieck,M. R. 1999. Genetic diversity of soybean germplasm resistant to

Heterodera glycines . Euphytica 107 : 205216.Zunke, U. and Eisenback, J. D. 1998. Morphology and ultra-structure. Pages 3156 in S. B. Sharma, ed. The cyst nematodes.Kluwer Academic Publishers, London, UK.

Soybean Cyst Nematode

Documents

Transcript of Soybean Cyst Nematode