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Identification of QTL in soybean underlying resistance to herbivory by Japanese beetles (Popillia japonica, Newman)

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Abstract

Soybean [Glycine max (L.) Merr.] was one of the most important legume crops in the world in 2010. Japanese beetles (JB; Popillia japonica, Newman) in the US were an introduced and potentially damaging insect pest for soybean. JBs are likely to spread across the US if global warming occurs. Resistance to JB in soybean was previously reported only in plant introductions. The aims here were to identify loci underlying resistance to JB herbivory in recombinant inbred lines (RILs) derived from the cross of Essex × Forrest cultivars (EF94) and to correlate those with loci with factors that confer insect resistance in soybean cultivars. The RIL population was used to map 413 markers, 238 satellite markers and 177 other DNA markers. Field data were from two environments over 2 years. Pest severity (PS) measured defoliation on a 0–9 scale. Pest incidence (PI) was the percentage of plants within each RIL with beetles on them. Antibiosis and antixenosis data were from feeding assays with detached leaves in petri plates. Five QTL were detected for the mean PS field trait (16% < R 2 < 27%). The loci were within the intervals Satt632–A2D8 on linkage group (LG) A2 (chromosome 8); Satt583–Satt415 on LG B1 (11); Satt009–Satt530 on LG N (3); and close to two markers OB02_140 (LG E; 20 cM from Satt572) and OZ15_150 LG (19 cM from Satt291 C2). Two QTL were detected for the mean PI field trait (16% < R 2 < 18%) close to Satt385 on LG A1 and Satt440 on LG I. The no choice feeding studies detected three QTL that were significant; two for antixenosis (22% < R 2 < 24%) between Satt632–A2D8 on LG A2 (8) and Sat_039–Satt160 on LG F (13); and a major locus effect (R 2 = 54%) for antibiosis on LG D2 (17) between Satt464–Satt488. Therefore, loci underlying resistance to JB herbivory were a mixture of major and minor gene effects. Some loci were within regions underlying resistance to soybean cyst nematode (LGs A2 and I) and root knot nematode (LG F) but not other major loci underlying resistance to nematode or insect pests (LGs G, H and M).

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References

  • Abel CA, Wilson RL, Wiseman BR, White WH, Davis FM (2000) Conventional resistance of experimental maize lines to corn earworm (Lepidoptera: Noctuidae), fall armyworm (Lepidoptera: Noctuidae), southwestern corn borer (Lepidoptera: Crambidae), and sugarcane borer (Lepidoptera: Crambidae). J Econ Entomol 93:982–988

    Article  PubMed  CAS  Google Scholar 

  • Afzal AJ, Natarajan A, Saini N, Iqbal MJ, Geisler MA, El Shemy H, Mungur R, Willmitzer L, Lightfoot DA (2009) The nematode resistance allele at the rhg1 locus alters the proteome and metabolome of soybean roots. Plant Physiol 151:1264–1280

    Google Scholar 

  • Arahana VS, Eskridge KM, Graef GL, Specht JE, Steadman JR (2001) Identification of QTL for Resistance to Sclerotinia sclerotiorum in Soybean. Crop Sci 41:180–188

    Article  CAS  Google Scholar 

  • Ashley DA, Boerma HR, Carter TE Jr, Mian MAR, Wells R (1998) An additional QTL for water use efficiency in soybean. Crop Sci 38:390–393

    Article  Google Scholar 

  • Baur ME, Boethel D (2004) Host plant resistance in IPM and the advances and restraints on Bt engineered soybean/crops. In: Proceedings of the VII world soybean research conference; IV international soybean processing and utilization conference; III Congresso Mundial de Soja (Brazilian soybean congress)

  • Boerma HR, Hussey RS, Luzzi BM, Parrott WA, Tamulonis JP (1997) RFLP mapping of resistance to southern root-knot nematode in soybean. Crop Sci 37:1903–1909

    Article  Google Scholar 

  • Bohlen PJ, Barrett GW (1990) Dispersal of the Japanese beetle (Coleoptera: Scarabaeidae) in strip-cropped soybean agroecosystems. Environ Entomol 19:955–960

    Google Scholar 

  • Bradshaw JD, Rice ME, Hill JH (2008) Evaluation of management strategies for bean leaf beetles (Coleoptera: Chrysomelidae) and bean pod mottle virus (Comoviridae) in soybean. J Econ Entomol 101:1211–1227

    Article  PubMed  CAS  Google Scholar 

  • Campbell N, Warner AL, Lightfoot DA, Matthews BF, Knap HT (2009) Duplication of a chromosomal region from linkage group A2 involved in cyst nematode resistance in soybean. Mol Gen Genet (in press)

  • Casteel CL, O’Neill BF, Zavala JA, Bilgin DD, Berenbaum MR, Delucia EH (2008) Transcriptional profiling reveals elevated CO2 and elevated O3 alter resistance of soybean (Glycine max) to Japanese beetles (Popillia japonica). Plant Cell Environ 31:419–434

    Article  PubMed  CAS  Google Scholar 

  • Chang SJC, Doubler TW, Kilo V, Suttner RJ, Klein III JH, Schmidt ME, Gibson PT, Lightfoot DA (1997) Association of field resistance to soybean sudden death syndrome (SDS) and cyst nematode (SCN). Crop Sci 37:965–971

    Google Scholar 

  • Chase K, Jarvik T, Lark KG, Mansur LM, Orf JH, Terry LI (2001) Soybean quantitative trait loci for resistance to insects. Crop Sci 40:375–382

    Google Scholar 

  • Chiari L, Piovesan ND, Naoe LK, Jose IC, Viana JMS, Moreira MA, De Barros EG (2004) Genetic parameters relating isoflavone and protein content in soybean seeds. Euphytica 138:55–60

    Google Scholar 

  • de Bruxelles GL, Roberts MR (2001) Signals regulating multiple responses to wounding and herbivores. Crit Rev Plant Sci 20:487–521

    Google Scholar 

  • DeLucia EH, Casteel CL, Nabity PD, O’Neill BF (2008) Insects take a bigger bite out of plants in a warmer, higher carbon dioxide world. Proc Natl Acad Sci USA 105:1781–1782

    Article  PubMed  CAS  Google Scholar 

  • Gebhardt JS, Wadsworth GJ, Matthews BF (1998) Characterization of a soybean aspartate aminotransferase cDNA encoding isozymes that are differentially targeted to two subcellular compartments. Plant Mol Biol 37:99–108

    Article  PubMed  CAS  Google Scholar 

  • Gould GE (1963) Japanese beetle damage to soybeans and corn. J Econ Entomol 56:776–781

    Google Scholar 

  • Hammond RB, Cooper RL (1989) Development and antibiosis of released soybean germplasm lines resistant to Mexican bean beetle (Coleoptera: Coccinellidae). J Econ Entomol 82:259–263

    Google Scholar 

  • Hammond RB, Bierman P, Levine E, Cooper RL (2001) Field resistance of two soybean germplasm lines, HC95–24 MB, against bean leaf beetle (Coleoptera: Chrysomelidae), western corn rootworm (Coleoptera: Chrysomelidae), and Japanese beetles (Coleoptera: Scarabaidae). J Econ Entomol 94:1594–1601

    Article  PubMed  CAS  Google Scholar 

  • Iqbal MJ, Yaegashi S, Ahsan R, Shopinski KL, Lightfoot DA (2005) Root response to Fusarium solani f. sp. glycines: temporal accumulation of transcripts in partially resistant and susceptible soybean. Theor Appl Genet 110:1429–1438

    Google Scholar 

  • Kassem A, Meksem K, Njiti V, Iqbal MJ, Banz WJ, Winters TA, Wood AJ, Lightfoot DA (2004) Definition of soybean genomic regions that control seed phytoestrogen amounts. J Biotech Biomed 2:52–60

    Google Scholar 

  • Kassem MA, Shultz J, Meksem K, Cho Y, Wood AJ, Iqbal MJ, Lightfoot DA (2006) An updated ‘Essex’ by ‘Forrest’ linkage map and first composite interval map of QTL underlying six soybean traits. Theor Appl Genet 113:1015–1026

    Google Scholar 

  • Kazi S, Shultz J, Bashir R, Afzal J, Njiti V, Lightfoot DA (2008) Separate loci underlie resistance to soybean sudden death syndrome in ‘Hartwig’ by ‘Flyer’. Theor Appl Genet 116:967–977

    Article  PubMed  CAS  Google Scholar 

  • Kazi S, Shultz J, Afzal J, Hashmi R, Jasim M, Bond J, Arelli P, Lightfoot DA (2009) Iso-lines and inbred-lines confirmed loci that underlie resistance from cultivar ‘Hartwig’ to three soybean cyst nematode populations Theor Appl Genet 117 (in press)

  • Killen TC, Lambert L (1986) Evidence for different genes controlling insect resistance in three soybean genotypes. Crop Sci 26:869–871

    Article  Google Scholar 

  • Komatsu K, Okuda S, Takahashi M, Matsunaga R, Nakazawa Y (2005) QTL mapping of antibiosis resistance to common cutworm (Spodoptera litura Fabricius) in soybean. Crop Sci 45:2044–2048

    Article  CAS  Google Scholar 

  • Ladd TL Jr (1987) Japanese beetle (Coleoptera:Scarabaeidae): influence of favored food plants on feeding response. J Econ Entomol 80:1014–1017

    Google Scholar 

  • Ladd TL Jr (1989) Japanese beetle (Coleoptera: Scarabaeidae): feeding by adults on minor host and non-host plants. J Econ Entomol 82:1616–1619

    Google Scholar 

  • Lander ES, Green P, Abrahamson J, Barlow A, Daly MJ, Lincoln SE, Newburg L (1987) MAPMAKER: an interactive computer package for constructing primary genetic linkage map of experimental and natural populations. Genomics 1:174–181

    Article  PubMed  CAS  Google Scholar 

  • Lightfoot DA (2008) Soybean genomics: developments through the use of cultivar Forrest. Int J Plant Genome 2008:1–22. doi:10.1155/2008/793158

    Article  Google Scholar 

  • Lightfoot DA, Meksem K (2001) Novel polynucleotides and polypeptides relating to loci underlying Resistance to Soybean Cyst Nematode and methods of use thereof. Patent pending. # 2002 0144310). Filing Date 01-29-2001

  • Lightfoot DA, Njiti VN, Gibson PT, Kassem MA, Iqbal JM, Meksem K (2005) Registration of Essex × Forrest recombinant inbred line (RIL) mapping population. Crop Sci 45:1678–1681

    Google Scholar 

  • Loughrin JH, Potter DA, Hamilton-Kemp TR, Byers ME (1996) Volatile compounds from crabapple cultivars (Malus spp.) differing in susceptibility to the Japanese beetle (Popillia japonica Newman). J Chem Ecol 22:1295–1305

    Article  CAS  Google Scholar 

  • Mahalingham R, Skorupska HT (1996) Cytological expression of early response to infection by Heterodera glycines Ichinohe in resistant PI 437654 soybean. Genome 39:986–998

    Article  Google Scholar 

  • Martinez de Ilarduya O, Xie Q, Kaloshian I (2003) Aphid-induced defense responses in Mi-1-mediated compatible and incompatible tomato interactions. Mol Plant Microb Interact 16:699–708

    Article  CAS  Google Scholar 

  • Meksem K, Pantazopoulos P, Njiti VN, Hyten DL, Arelli PR, Lightfoot DA (2001) ‘Forrest’ resistance to the soybean cyst nematode is bigenic: saturation mapping of the rhg1 and Rhg4 loci. Theor Appl Genet 103:710–717

    Article  CAS  Google Scholar 

  • Mewis I, Appel HM, Hom A, Raina R, Schultz JC (2005) Major signaling pathways modulate Arabidopsis glucosinolate accumulation and response to both phloem feeding and chewing insects. Plant Physiol 138:1149–1162

    Article  PubMed  CAS  Google Scholar 

  • Nakazawa Y (2005) QTL mapping of antibiosis resistance to common cutworm (Spodoptera litura Fabricius) in soybean. Crop Sci 45:2044–2048

    Article  Google Scholar 

  • Narvel JM, Walker DR, Rector BG, All JN, Parrott WA, Boerma HR (2001) A retrospective DNA marker assessment of the development of insect resistant soybean. Crop Sci 41:1931–1939

    Article  CAS  Google Scholar 

  • Nombela G, Williamson VM, Muniz M (2003) The root-knot nematode resistance gene Mi-1.2 of tomato is responsible for resistance against the whitefly Bemisia tabaci. Mol Plant Microbe Interact 16:645–649

    Article  PubMed  CAS  Google Scholar 

  • Patton CA, Ranney TG, Burton JD, Walgenbach JF (1997a) Natural pest resistance of Prunus taxa to feeding by adult Japanese beetles: role of endogenous allelochemicals in host plant resistance. J Am Soc Hortic Sci 122:668–672

    Google Scholar 

  • Patton CA, Ranney TG, Burton JD, Walgenbach JF (1997b) Feeding responses of Japanese Beetle to naturally occurring metabolites found in rosaceous plants. J Environ Hort 15:222–227

    CAS  Google Scholar 

  • Potter DA, Held DW (2002) Biology and management of the Japanese Beetle. Ann Rev Entomol 47:175–205

    Article  CAS  Google Scholar 

  • Rector BG, All JN, Parrott WA, Boerma HR (2000) Quantitative trait loci for antibiosis resistance to corn earworm in soybean. Crop Sci 40:233–238

    Google Scholar 

  • SAS Inc., Cary, NC (2006)

  • Schuster I, Abdelnoor RV, Marin SRR, Carvalho VP, Kiihl AS, Silva JFV, Sedyama CS, Barros EG, Moreira MA (2001) Identification of a new major QTL associated with resistance to the soybean cyst nematode (Heterodera glycines). Theor Appl Genet 102:91–96

    Article  CAS  Google Scholar 

  • Shultz JL, Kazi S, Afzal JA, Bashir R, Lightfoot DA (2007) The development of BAC‐end sequence‐based microsatellite markers and placement in the physical and genetic maps of soybean. Theor Appl Genet 114:1081–1090

    Google Scholar 

  • Smith AW, Hammond RB, Stinner BR (1988) Influence of rye-cover crop management on soybean foliage arthropods. Environ Entomol 17:109–114

    Google Scholar 

  • Snedecor GW, Cochran WG (1980) “Statistical Methods”©. The Iowa State University Press, Ames. ISBN 0-8138-1560-6

  • Szalma SJ, Buckler ES IV, Snook ME, McMullen MD (2005) Association analysis of candidate genes for maysin and chlorogenic acid accumulation in maize silks. Theor Appl Genet 110(7):1324–1333

    Article  PubMed  CAS  Google Scholar 

  • Tigreros N, Switzer PV (2009) Observations of multiple mating under field conditions for Japanese Beetles (Popillia japonica Newman) (Coleoptera: Scarabaeidae). J Kansas Entomol Soc 82:151–159

    Article  Google Scholar 

  • Triwitayakorn K, Njiti VN, Iqbal MJ, Yaegashi S, Town C, Lightfoot DA (2005) Genomic analysis of a region encompassing QRfs1 and QRfs2: genes that underlie soybean resistance to sudden death syndrome. Genome/Génome 48:125–138

    Google Scholar 

  • Underwood N, Rausher M (2002) Comparing the consequences of induced and constitutive plant resistance for herbivore population dynamics. Am Nature 160:20–30

    Article  Google Scholar 

  • Walker DR, All JN, McPherson RM, Boerma HR, Parrott WA (2000) Field evaluation of soybean engineered with a synthetic cry1Ac transgene for resistance to corn earworm, soybean looper, velvetbean caterpillar (Lepidoptera: Noctuidae), and lesser cornstalk borer (Lepidoptera: Pyralidae). J Econ Entomol 93:613–622

    Article  PubMed  CAS  Google Scholar 

  • Walker DR, Narvel JM, Boerma HR, All JN, Parrott WA (2004) A QTL that enhances and broadens Bt insect resistance in soybean. Theor Appl Genet 109:1051–1057

    Article  PubMed  Google Scholar 

  • Webb DM, Baltazar BM, Arelli PR, Schupp J, Keim P, Clayton K, Ferreira AR, Owens T, Beavis WD (1995) QTL affecting soybean cyst-nematode resistance. Theor Appl Genet 91:574–581

    Article  CAS  Google Scholar 

  • Yesudas CR (2007) Seed and leaf trait correlations and identification of underlying loci in soybean. MS thesis, PLB, SIUC, Carbondale IL, 161pp

  • Zavala JA, Casteel CL, Nabity PD, Berenbaum MR, DeLucia EH (2009) Role of cysteine proteinase inhibitors in preference of Japanese beetles (Popillia japonica) for soybean (Glycine max) leaves of different ages and grown under elevated CO2. Oecologia 161:35–41

    Article  PubMed  Google Scholar 

Download references

Acknowledgments

This research was funded by grants from the College of Agriculture and Office of the Vice Chancellor for Research. The authors thank Drs. P. Gibson, O. Myers Jr. and M. Schmidt for assistance with germplasm development and maintenance from 1991 to 2000. We thank the “Soybean Genome Project”, at DoE Joint Genome Institute, for the timely release of the WGS reads, scaffolds and genome sequence.

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Correspondence to D. A. Lightfoot.

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Communicated by C. Gebhardt.

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Yesudas, C.R., Sharma, H. & Lightfoot, D.A. Identification of QTL in soybean underlying resistance to herbivory by Japanese beetles (Popillia japonica, Newman). Theor Appl Genet 121, 353–362 (2010). https://doi.org/10.1007/s00122-010-1314-9

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