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Genome-wide association study for resistance to the southern root-knot nematode (Meloidogyne incognita) in soybean

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Abstract

Soybean [Glycine max (L.) Merrill] is one of the most important traded commodities for the world’s economy. However, soybean cultivation is often affected by biotic and abiotic factors that prevent the crop from attaining its full yield potential. With the advent of new tools for next-generation sequencing, the genomic knowledge gained from the study of this major oilseed crop has increased considerably in recent years. In this study, we performed a genotypic characterization of 188 plant introductions (PIs) and five cultivars using a genotyping-by-sequencing (GBS) approach and a phenotypic characterization for resistance/tolerance to the southern root-knot nematode, Meloidogyne incognita. We then performed a genome-wide association study (GWAS) for this important trait. From 46,196 SNP markers identified and validated on this set of genotypes, three were significantly associated with nematode resistance. Remarkably, all of these were in a single, very small (3.4 kb) region of chromosome 10. Most lines (48 out of 57) with the highest level of resistance shared the haplotype composed of the alleles associated with resistance at these three SNP loci. Interestingly, nine of the lines exhibiting a high level of resistance did not exhibit the “resistant haplotype” on Gm10. This suggests either that recombination has broken the association between the SNPs and the resistance locus or that resistance is conferred by a different locus altogether. In the latter case, these lines represent a putative alternative source of resistance, an important information for breeding programs.

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References

  • Almeida AMR, Ferreira LP, Yorinori JT, Silva JFV, Henning AA, Godoy CV, Costamilan L M, Meyer MC (2005) Doenças da soja (Glycine max). In: Kimati H, Amorim L, Rezende JAM, Bergamim Filho A, Camargo LEA (Eds) Manual de Fitopatologia, vol. 2. Doenças das plantas cultivadas. 4th edn. Ceres. Piracicaba-SP, pp 569–588

  • Barcala M, García A, Cabrera J, Casson S, Lindsey K, Favery B, García-Casado G, Solano R, Fenoll C, Escobar C (2010) Early transcriptomic events in microdissected Arabidopsis nematode-induced giant cells. Plant J 61:698–712

    Article  CAS  PubMed  Google Scholar 

  • Bastien M, Sonah H, Belzile F (2014) Genome wide association mapping of Sclerotinia sclerotiorum resistance in soybean with a genotyping-by-sequencing approach. Plant Genome 7(1)

  • Bradbury PJ, Zhang Z, Kroon DE, Casstevens TM, Ramdoss Y, Buckler ES (2007) TASSEL: software for association mapping of complex traits in diverse samples. Bioinformatics 23(19):2633–2635

  • Bridge J, Starr JL (2007) Plant nematodes of agricultural importance. Academic Press, Boston, pp 19–32

    Book  Google Scholar 

  • Brzyski D, Peterson CB, Sobczyk P, Candès EJ, Bogdan M, Sabatti C (2017) Controlling the rate of GWAS false discoveries. Genetics 205(1):61–75

    Article  PubMed  Google Scholar 

  • Chung G, Singh RJ (2008) Broadening the genetic base of soybean: a multidisciplinary approach. Crit Rev Plant Sci 27:295–341

    Article  CAS  Google Scholar 

  • CONAB - Companhia Nacional de Abastecimento (2013) Monitoring the Brazilian harvest: grains. Data collection Fourth, 1:67, Avaiable: http://www.conab.gov.br/OlalaCMS/uploads/arquivos/14_01_10_15_07_19_boletim_graos_janeiro_2014.pdf. Accessed Jan 2014

  • Cosgrove DJ (1997) Assembly and enlargement of the primary cell wall in plants. Annu Rev Cell Dev Biol 13:171–201

    Article  CAS  PubMed  Google Scholar 

  • Crochet WD, Wad D (2004) The uniform soybean tests northern region uniform soybean tests. https://www.ars.usda.gov/ARSUserFiles/50200500/UST/2004.PDF

  • Di MA et al (2005) Structural basis for the interaction between pectin methylesterase and a specific inhibitor protein. Plant Cell 17(3):849–858. https://doi.org/10.1105/tpc.104.028886

  • Elshire RJ, Glaubitz JC, Sun Q, Poland JA, Kawamoto K, Buckler ES, Mitchell SE (2011) A robust, simple genotyping-by-sequencing (GBS) approach for high diversity species. PLoS One 6:e19379

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • EMBRAPA - Empresa Brasileira de Pesquisa Agropecuária (2011) Cultivares de soja de Minas Gerais e região central do Brasil. Safra 2010/2011. Londrina, PR. Accessed Jan 2013. http://www.cnpso.embrapa.br/download/cultivares/Soja_2010-11MG.pdf

  • Fourie H, Mc Donald AH, De Waele D (2013) Host and yield responses of soybean genotypes resistant or susceptible to. Int J Pest Manag 59(2):111–121

  • Fourie H, Mc Donald AH, Loots GC (1999) Host suitability of South African commercial soybean cultivars to two root- knot nematode species. Afr Plant Prot 5:119–124

  • Fourie H, Mienie CMS, McDonald AH, De Waele D (2008) Identification and validation of genetic markers associated with Meloidogyne incognita race 2 resistance in soybean, Glycine max (L.) Merr. Nematology 10:651–661

  • Goodstein DM, Shu S, Howson R, Neupane R, Hayes RD, Fazo J, Mitros T, Dirks W, Hellsten U, Putnam N, Rokhsar DS (2012) Phytozome: a comparative platform for green plant genomics. Nucleic Acids Res 40(D1):D1178–D1186

  • Ha B, Bennett JB, Hussey RS, Finnerty SL, Boerma HR (2004) Pedigree analysis of a major QTL conditioning soybean resistance to southern root-knot nematode. Crop Sci Soc 40:758–763

    Article  Google Scholar 

  • Hoagland DR, Arnon DI (1950) The water-culture method for growing plants without soil. California Agric Exp Station Circular 347:1–32

    Google Scholar 

  • Hyten DL, Song Q, Zhu Y, Choi I-Y, Nelson RL, Costa JM, Specht JE, Shoemaker RC, Cregan PB (2006) Impacts of genetic bottlenecks on soybean genome diversity. Proc Natl Acad Sci 103:16666–16671

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ibrahim H, Hosseini P, Alkharouf N, Hussein E, Gamal El-Din AEK, Aly M, Matthews B (2011) Analysis of gene expression in soybean (Glycine max) roots in response to the root knot nematode Meloidogyne incognita using microarrays and KEGG pathways. BMC Genomics 12:220

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Iquira E, Sonah H, Belzile F (2015) Association mapping of QTLs for sclerotinia stem rot resistance in a collection of soybean plant introductions using a genotyping by sequencing (GBS) approach. BMC Plant Biology 15(1):1

    Article  Google Scholar 

  • Jammes F, Lecomte P, de Almeida-Engler J, Bitton F, Martin- Magniette M-L, Renou JP, Abad P, Favery B (2005) Genome-wide expression profiling of the host response to root-knot nematode infection in Arabidopsis. Plant J 44:447–458

    Article  CAS  PubMed  Google Scholar 

  • Jannink J-L, Lorenz AJ, Iwata H (2010) Genomic selection in plant breeding: from theory to practice. Brief Funct Genomics 9:166–177

    Article  CAS  PubMed  Google Scholar 

  • Korte A, Farlow A (2013) The advantages and limitations of trait analysis with GWAS: a review. Plant Methods 9(1):29

  • Lam H-M, Xu X, Liu X, Chen W, Yang G, Wong F-L, Li M-W, He W, Qin N, Wang B, Li J, Jian M, Wang J, Shao G, Wang J, Sun SS-M, Zhang G (2011) Addendum: Resequencing of 31 wild and cultivated soybean genomes identifies patterns of genetic diversity and selection. Nat Genet 43(4):387–387

  • Li Z, Jakkula L, Hussey R (2001) SSR mapping and confirmation of the QTL from PI96354 conditioning soybean resistance to southern root-knot nematode. Theor Appl 1167–1173

  • Li Y-H, Zhao S-C, Ma J-X, Li D, Yan L, Li J, Qi X-T, Guo X-S, Zhang L, He W-M (2013) Molecular footprints of domestication and improvement in soybean revealed by whole genome re-sequencing. BMC Genomics 14:579

    Article  PubMed  PubMed Central  Google Scholar 

  • Lipka AE, Tian F, Wang Q, Peiffer J, Li M, Bradbury PJ, Gore MA, Buckler ES, Zhang Z (2012) GAPIT: genome association and prediction integrated tool. Bioinformatics 28(18):2397–2399

  • Pham A-T, McNally K, Abdel-Haleem H, Roger Boerma H, Li Z (2013) Fine mapping and identification of candidate genes controlling the resistance to southern root-knot nematode in PI 96354. Theor Appl Genet 126:1825–1838

    Article  CAS  PubMed  Google Scholar 

  • Poland J, Endelman J, Dawson J, Rutkoski J, Wu S, et al (2012) Genomic selection in wheat breeding using genotyping-by-sequencing. Plant Genome J 5:103. Available: https://www.crops.org/publications/tpg/abstracts/5/3/103. Accessed 31 Oct 2013

  • Purcell S, Neale B, Todd-Brown K, Thomas L, Ferreira MAR, Bender D, Maller J, Sklar P, de Bakker PIW, Daly MJ, Sham PC (2007) PLINK: A Tool Set for Whole-Genome Association and Population-Based Linkage Analyses. Am J Hum Genet 81(3):559–575

  • Raj A, Stephens M, Pritchard JK (2014) fastSTRUCTURE: variational inference of population structure in large SNP data sets. 197(June):573–589

  • Riekert HF, Henshaw GE (1998) Effect of soybean, cowpea and groundnut rotations on root-knot nematode build-up and infestation of dryland maize. Afr Crop Sci J 6:377–383

    Article  Google Scholar 

  • Rincker K, Lipka AE, & Diers BW (2016) Genome-wide association study of brown stem rot resistance in soybean across multiple populations. 1–11

  • Scheet P, Stephens M (2006) A Fast and Flexible Statistical Model for Large-Scale Population Genotype Data: Applications to Inferring Missing Genotypes and Haplotypic Phase. Am J Hum Genet 78(4):629–644

  • Severin AJ, Woody JL, Bolon Y, Joseph B, Diers BW, Farmer AD, Muehlbauer GJ, Nelson RT, Grant D, Specht JE, Graham MA, Cannon SB, May GD, Vance CP, Shoemaker RC (2010) RNA-Seq Atlas of glycine max: a guide to the soybean transcriptome. BMC Plant Biol 10:160

    Article  PubMed  PubMed Central  Google Scholar 

  • Shearin ZP, Finnerty SL, Wood ED, Hussey RS, Boerma HR (2009) A southern root-knot nematode resistance QTL linked to the locus in soybean. Crop Sci 49:467

    Article  CAS  Google Scholar 

  • Sikora RA, Fernández E (2005) Nematode parasites of vegetables. In: Luc M, Sikora RA, Bridge J (eds) Plant parasitic nematodes in subtropical and tropical agriculture, 2nd edn. CABI Publishing, Wallingford, pp 319–392

    Chapter  Google Scholar 

  • Sonah H, Bastien M, Iquira E, Tardivel A, Légaré G, Boyle B, Normandeau É, Laroche J, Larose S, Jean M, Belzile F (2013) An improved genotyping by sequencing (GBS) approach offering increased versatility and efficiency of SNP discovery and genotyping. PLoS One 8(1):e54603

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sonah H, O’Donoughue L, Cober R, Rajcan I, Belzile F (2015) Identification of loci governing eight agronomic traits using a GBS-GWAS approach and validation by QTL mapping in soya bean. Plant Biotechnol J 13(2):211–221. https://doi.org/10.1111/pbi.12249

    Article  CAS  PubMed  Google Scholar 

  • Song Q, Hyten DL, Jia G, Quigley CV, Fickus EW, Nelson RL, Cregan PB, Zhang T (2013) Development and evaluation of SoySNP50K, a high-density genotyping array for soybean. PLoS ONE 8 (1):e54985. https://doi.org/10.1371/journal.pone.0054985

  • Song Q, Hyten DL, Jia G, Quigley CV, Fickus EW, Nelson RL, Cregan PB (2015) Fingerprinting soybean germplasm and its utility in genomic research. G3: Genes|Genomes|Genetics 5(10):1999–2006

    Article  PubMed  PubMed Central  Google Scholar 

  • Tardivel A et al (2014) Rapid identification of alleles at the soybean maturity gene E3 using genotyping by sequencing and a haplotype-based approach. The Plant Genome 7(2):1–9

    Article  Google Scholar 

  • Varshney RK, Spurthi N, Nayak S, May GD, Jackson SA (2009) Next-generation sequencing technologies and their implications for crop genetics and breeding. Trends Biotechnol 27:522–530

    Article  CAS  PubMed  Google Scholar 

  • Vuong TD, Sonah H, Meinhardt CG, Deshmukh R, Kadam S, Nelson RL, Shannon JG, Nguyen HT (2015) Genetic architecture of cyst nematode resistance revealed by genome-wide association study in soybean. BMC genomics 16(1):1

    Article  Google Scholar 

  • Xu X, Zeng L, Tao Y, Vuong T, Wan J et al (2013) Pinpointing genes underlying the quantitative trait loci for root-knot nematode resistance in palaeopolyploid soybean by whole genome resequencing. Proc Natl Acad Sci U S A 110:13469–13474

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yamanaka N, Sato H, Yang Z, DH X, Catelli LL, Binneck E, Arias CAA, Abdelnoor RV, Nepomuceno AL (2007) Genetic relationships between Chinese, Japanese, and Brazilian soybean gene pools revealed by simple sequence repeat (SSR) markers. Genet Mol Biol 30:85–88

    Article  Google Scholar 

  • Zhang ZW, Ersoz E, Lai CQ, Todhunter RJ, Tiwari HK et al (2010) Mixed linear model approach adapted for genome-wide association studies. Nat Genet 42:355–U118

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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Acknowledgments

We greatly appreciate the financial support of the Coordination for the Improvement of Higher Level for Education program (CAPES), National Counsel of Technological and Scientific Development (CNPq), and Emerging Leaders in the Americas Program (ELAP). We thank the members of the plant biotechnology laboratory at Embrapa Soja, Brazil. Furthermore, we thank the Department of Plant Sciences and Institute of Integrative Biology and Systems (IBIS) at Université Laval, Canada, for supporting the doctoral student exchange program and this research. This paper was approved for publication by the Editorial Board of Embrapa Soja as manuscript number 119/2016.

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Correspondence to Francismar C. Marcelino-Guimarães.

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Passianotto, A.L.d.L., Sonah, H., Dias, W.P. et al. Genome-wide association study for resistance to the southern root-knot nematode (Meloidogyne incognita) in soybean. Mol Breeding 37, 148 (2017). https://doi.org/10.1007/s11032-017-0744-3

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