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Genotyping-by-sequencing based genetic mapping reveals large number of epistatic interactions for stem rot resistance in groundnut

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Genetic mapping identified large number of epistatic interactions indicating the complex genetic architecture for stem rot disease resistance.

Abstract

Groundnut (Arachis hypogaea) is an important global crop commodity and serves as a major source of cooking oil, diverse confectionery preparations and livestock feed. Stem rot disease caused by Sclerotium rolfsii is the most devastating disease of groundnut and can cause up to 100% yield loss. Genomic-assisted breeding (GAB) has potential for accelerated development of stem rot resistance varieties in short period with more precision. In this context, linkage analysis and quantitative trait locus (QTL) mapping for resistance to stem rot disease was performed in a bi-parental recombinant inbred line population developed from TG37A (susceptible) × NRCG-CS85 (resistant) comprising of 270 individuals. Genotyping-by-sequencing approach was deployed to generate single nucleotide polymorphism (SNP) genotyping data leading to development of a genetic map with 585 SNP loci spanning map distance of 2430 cM. QTL analysis using multi-season phenotyping and genotyping data could not detect any major main-effect QTL but identified 44 major epistatic QTLs with phenotypic variation explained ranging from 14.32 to 67.95%. Large number interactions indicate the complexity of genetic architecture of resistance to stem rot disease. A QTL of physical map length 5.2 Mb identified on B04 comprising 170 different genes especially leucine reach repeats, zinc finger motifs and ethyleneresponsive factors, etc., was identified. The identified genomic regions and candidate genes will further validate and facilitate marker development to deploy GAB for developing stem rot disease resistance groundnut varieties.

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References

  • Akgul DS, Ozgonen H, Erkilic A (2011) The effects of seed treatments with fungicides on stem rot caused by Sclerotium rolfsii sacc., in peanut. Pak J Bot 43(6):2991–2996

    CAS  Google Scholar 

  • Bera SK, Kumar V, Sunkad G, Rathnakumar AL, Radhakrisihnan T (2011) NRCGCS 85 (IC0582473; INGR10030), Groundnut (Arachis hypogaea) Germplasm, a source of Resistance to PBND (Peanut bud necrosis diseases), Stem Rot, Late Leaf Spot, Early Leaf Spot, Rust and Alternaria Leaf Blight. Indian J Plant Genet Resour 24(1):96–153

    Google Scholar 

  • Bera SK, Kasundra SV, Kamdar JH, Ajay BC, Lal C, Thirumalasmy PP, Dash P, Maurya AK (2014) Variable response of interspecific breeding lines of groundnut to Sclerotium rolfsii infection under field and laboratory conditions. Electron J Plant Breed 5:22–29

    Google Scholar 

  • Bera SK, Kamdar JH, Kasundra SV, Ajay BC (2017) A novel QTL governing resistance to stem rot disease caused by Sclerotium rolfsii in peanut. Australas Plant Pathol 45(6):637–644

    Article  Google Scholar 

  • Bertioli DJ, Cannon SB, Froenicke L, Huang G, Farmer AD, Cannon EK, Liu X, Gao D, Clevenger J, Dash S, Ren L, Moretzsohn MC, Shirasawa K, Huang W, Vidigal B, Abernathy B, Chu Y, Niederhuth CE, Umale P, Araújo AC, Kozik A, Kim KD, Burow MD, Varshney RK, Wang X, Zhang X, Barkley N, Guimarães PM, Isobe S, Guo B, Liao B, Stalker HT, Schmitz RJ, Scheffler BE, Leal-Bertioli SC, Xun X, Jackson SA, Michelmore R, Ozias-Akins P (2016) The genome sequences of Arachis duranensis and Arachis ipaensis, the diploid ancestors of cultivated peanut. Nat Genet 48:438–446

    Article  CAS  PubMed  Google Scholar 

  • 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 23:2633–2635

    Article  CAS  PubMed  Google Scholar 

  • Chen X, Li H, Pandey MK, Yang Q, Wang X, Garg V, Li H, Chi X, Doddamani D, Hong Y, Upadhyaya H, Guo H, Khan AW, Zhu F, Zhang X, Pan L, Pierce GJ, Zhou G, Krishnamohan KA, Chen M, Zhong N, Agarwal G, Li S, Chitikineni A, Zhang GQ, Sharma S, Chen N, Liu H, Janila P, Li S, Wang M, Wang T, Sun J, Li X, Li C, Wang M, Yu L, Wen S, Singh S, Yang Z, Zhao J, Zhang C, Yu Y, Bi J, Zhang X, Liu ZJ, Paterson AH, Wang S, Liang X, Varshney RK, Yu S (2016) Draft genome of the peanut A-genome progenitor (Arachis duranensis) provides insights into geocarpy, oil biosynthesis and allergens. Proc Natl Acad Sci USA 113:6785–6790

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cilliers AJ, Herselman L, Pretorius ZA (2000) Genetic variability within and among mycelial compatibility groups of Sclerotium rolfsii in South Africa. Phytopathology 90:1026–1031

    Article  CAS  PubMed  Google Scholar 

  • Deepthi KC, Reddy NPE (2013) Stem rot disease of groundnut (Arachis hypogaea L) induced by Sclerotium rolfsii and its management. Int J Life Sci Biotechnol Pharma Res 2(3):26–38

    Google Scholar 

  • Durrant WE, Dong X (2004) Systemic acquired resistance. Annu Rev Plant Pathol 42:185–209

    CAS  Google Scholar 

  • Elshire RJ, Glaubitz JC, Sun Q, Poland SA, Kawamoto K, Buckler ES, Mitchel 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 

  • Eulgem T, Somssich IE (2007) Networks of WRKY transcription factors in defense signaling. Curr Opin Plant Biol 10:366–371

    Article  CAS  PubMed  Google Scholar 

  • Fischer U, Dröge-Laser W (2004) Overexpression of NtERF5, a new member of the tobacco ethylene response transcription factor family enhances resistance to tobacco mosaic virus. Mol Plant Microbe Interact 17:1162–1171

    Article  CAS  PubMed  Google Scholar 

  • Ganesan S, Kuppusamy GR, Sekar R (2007) Integrated management of stem rot disease (Sclerotium rolfsii) of groundnut (Arachis hypogaea L.) using rhizobium and Trichoderma harzianum (ITCC-4572). Turk J Agric For 31(2):103–108

    Google Scholar 

  • Gautami B, Pandey MK, Vadez V, Nigam SN, Ratnakumar P, Krishnamurthy L, Radhakrishnan T, Gowda MVC, Narasu ML, Hoisington DA, Knapp SJ, Varshney RK (2012) Quantitative trait locus analysis and construction of consensus genetic map for drought tolerance traits based on three recombinant inbred line populations in cultivated groundnut (Arachis hypogaea L.). Mol Breeding 30:773–788

    Article  Google Scholar 

  • Gupta SK, Rai AK, Kanwar SS, Sharma TR (2012) Comparative analysis of zinc finger proteins involved in plant disease resistance. PLoS ONE 7(8):42578

    Article  CAS  Google Scholar 

  • Gutterson N, Reuber TL (2004) Regulation of disease resistance pathways by AP2/ERF transcription factors. Curr Opin Plant Biol 7:465–471

    Article  CAS  PubMed  Google Scholar 

  • Kale DM, Murty GSS, Badigannavar AM (2004) TG 37A—a new Trombay groundnut variety with wide adaptation. Int Arachis Newsl 24:19–20

    Google Scholar 

  • Li H, Durbin R (2009) Fast and accurate short read alignment with Burrows–Wheeler transform. Bioinformatics 25:1754–1760

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • McHale L, Tan X, Koehl P, Michelmore RW (2006) Plant NBS-LRR proteins: adaptable guards. Genome Biol 7(4):212

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Meng L, Li H, Zhang L, Wang J (2015) QTL IciMapping: integrated software for genetic linkage map construction and quantitative trait locus mapping in biparental populations. Crop J 3:269–283

    Article  Google Scholar 

  • Nigam SN, Rao MJ, Gibbons RW (1990) Artificial hybridization in groundnut. Information Bulletin No. 29. Patancheru, A.P. 502 324, India: International Crops Research Institute for the Semi-Arid Tropics

  • Pandey SP, Somssich IE (2009) The role of WRKY transcription factors in plant immunity. Plant Physiol 150:1648–1655

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pandey MK, Monyo E, Ozias-Akins P, Liang X, Guimarães P, Nigam SN, Upadhyaya HD, Janila P, Zhang X, Guo B, Cook DR, Bertioli DJ, Michelmore R, Varshney RK (2012) Advances in Arachis genomics for peanut improvement. Biotechnol Adv 30:639–651

    Article  CAS  PubMed  Google Scholar 

  • Pandey MK, Roorkiwal M, Singh V, Lingam A, Kudapa H, Thudi M, Chitikineni A, Rathore A, Varshney RK (2016) Emerging genomic tools for legume breeding: current status and future perspectives. Front Plant Sci 7:45510

    Google Scholar 

  • Pandey MK, Agarwal G, Kale SM, Clevenger J, Nayak SN, Sriswathi M, Chitikineni A, Chavarro C, Chen X, Upadhyaya HD, Vishwakarma MK, Bertoli SL, Liang X, Bertioli DJ, Guo B, Jackson SA, Ozias-Akins P, Varshney RK (2017) Development and evaluation of a high density genotyping ‘Axiom_Arachis’ array with 58 K SNPs for accelerating genetics and breeding in groundnut. Sci Rep 7:40577

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Park JM, Park CJ, Lee SB, Ham BK, Shin R, Paek KH (2001) Overexpression of the tobacco Tsi1 gene encoding an EREBP/AP2-type transcription factor enhances resistance against pathogen attack and osmotic stress in tobacco. Plant Cell 13:1035–1046

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ravi K, Vadez V, Isobe S, Mir RR, Guo Y, Nigam SN, Gowda MV, Radhakrishnan T, Bertioli DJ, Knapp SJ, Varshney RK (2011) Identification of several small main-effect QTLs and a large number of epistatic QTLs for drought tolerance related traits in groundnut (Arachis hypogaea L.). Theor Appl Genet 122:1119–1132

    Article  CAS  PubMed  Google Scholar 

  • Shasidhar Y, Vishwakarma MK, Pandey MK, Janila P, Variath MT, Manohar SS, Nigam SN, Guo B, Varshney RK (2017) Molecular mapping of oil content and fatty acids using dense genetic maps in groundnut (Arachis hypogaea L.). Front Plant Sci 8:794

    Article  PubMed  PubMed Central  Google Scholar 

  • Shin R, Park JM, Paek KH (2002) Ectopic expression of Tsi1 in transgenic hot pepper plants enhances host resistance to viral, bacterial, and oomycete pathogens. Mol Plant Microbe Interact 15:983–989

    Article  CAS  PubMed  Google Scholar 

  • Shokes FM, Weber Z, Gorbet DW, Pudelko HA, Taczanowski M (1998) Evaluation of peanut genotypes for resistance to southern stem rot using an agar disk technique. Peanut Sci 25:12–17

    Article  Google Scholar 

  • Sujay V, Gowda MVC, Pandey MK, Bhat RS, Khedikar YP, Nadaf HL, Gautami B, Sarvamangala C, Lingaraju S, Radhakrishan T, Knapp SJ, Varshney RK (2012) Quantitative trait locus analysis and construction of consensus genetic map for foliar disease resistance based on two recombinant inbred line populations in cultivated groundnut (Arachis hypogaea L.). Mol Breed 30:773–788

    Article  CAS  PubMed  Google Scholar 

  • Ulker B, Somssich IE (2004) WRKY transcription factors: from DNA binding towards biological function. Curr Opin Plant Biol 7:491–498

    Article  CAS  PubMed  Google Scholar 

  • Van Ooijen JW (2006) JoinMap4, software for the calculation of genetic linkage maps in experimental populations. Kyazma BV, Wageningen, Netherland

    Google Scholar 

  • Varshney RK, Bertioli DJ, Moretzsohn MC, Vadez V, Krishnamurty L, Aruna R, Nigam SN, Moss BJ, Seetha K, Ravi K, He G, Knapp SJ, Hoisington DA (2009) The first SSR based genetic linkage map for cultivated groundnut (Arachis hypogaea L.). Theor Appl Genet 118:729–739

    Article  CAS  PubMed  Google Scholar 

  • Varshney RK, Mohan SM, Gaur PM, Gangarao NV, Pandey MK, Bohra A, Varshney RK, Mohan SM, Gaur PM, Gangarao NV, Pandey MK, Bohra A, Sawargaonkar SL, Chitikineni A, Kimurto PK, Janila P, Saxena KB, Fikre A, Sharma M, Rathore A, Pratap A, Tripathi S, Datta S, Chaturvedi SK, Mallikarjuna N, Anuradha G, Babbar A, Choudhary AK, Mhase MB, Bharadwaj Ch, Mannur DM, Harer PN, Guo B, Liang X, Nadarajan N, Gowda CL (2013) Achievements and prospects of genomics-assisted breeding in three legume crops of the semi-arid tropics. Biotechnol Adv 31:1120–1134

    Article  PubMed  Google Scholar 

  • Varshney RK, Pandey MK, Janila P, Nigam SN, Sudini H, Gowda MVC, Sriswathi M, Radhakrishnan T, Manohar SS, Nagesh P (2014) Marker-assisted introgression of a QTL region to improve rust resistance in three elite and popular varieties of peanut (Arachis hypogaea L.). Theor Appl Genet 127(8):1771–1781

    Article  PubMed  PubMed Central  Google Scholar 

  • Vishwakarma MK, Pandey MK, Shasidhar Y, Manohara SS, Nagesh P, Janila P (2016) Identification of two major quantitative trait locus for fresh seed dormancy using the diversity arrays technology and diversity arrays technology-seq based genetic map in Spanish-type peanuts. Plant Breed 135:367–375

    Article  CAS  Google Scholar 

  • Vishwakarma MK, Kale SM, Sriswathi M, Naresh T, Shasidhar Y, Garg V, Pandey MK, Varshney RK (2017) Genome-wide discovery and deployment of insertions and deletions markers provided greater insights on species, genomes, and sections relationships in the genus Arachis. Front Plant Sci 8:2064

    Article  PubMed  PubMed Central  Google Scholar 

  • Voorrips RE (2002) Mapchart: software for the graphical presentation of linkage maps and QTLs. J Hered 93:77–78

    Article  CAS  PubMed  Google Scholar 

  • Wang SC, Bastern J, Zeng ZB (2011) Windows QTL Cartographer 2.5. Department of Statistics, North Carolina State University, Raleigh

    Google Scholar 

  • Wang J, Li H, Zhang L, Meng L (2012) Users’ manual of QTL IciMapping version 3.3. Chinese Academy of Agricultural Sciences (CAAS), Beijing

    Google Scholar 

  • Zhang G, Chen M, Li L, Xu Z, Chen X, Gou J, Ma Y (2009) Over expression of soya bean GmERF3 gene, an AP2/ERF type transcription factor for increased tolerance to salt drought and disease in transgenic tobacco. J Exp Bot 60(13):3781–3796

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhou X, Xia Y, Ren X, Chen Y, Huang L, Huang S, Liao B, Lei Y, Yan L, Jiang H (2014) Construction of an SNP-based genetic linkage map in cultivated peanut based on large-scale marker development using next-generation double-digest restriction-site-associated DNA sequencing (ddRADseq). BMC Genom 15:351

    Article  CAS  Google Scholar 

  • Zuo KJ, Qin J, Zhao JY, Ling H, Zhang LD, Cao YF, Tang KX (2007) Over-expression GbERF2 transcription factor in tobacco enhances brown spots disease resistance by activating expression of downstream genes. Gene 391:80–90

    Article  CAS  PubMed  Google Scholar 

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Acknowledgments

This project was supported by the National Agricultural Science Fund (NASF) of Indian Council of Agricultural Research (ICAR), New Delhi, India. The help rendered by Ms. Vanika Garg in sequence analysis is thankfully acknowledged. The sequencing work reported in this article was undertaken as a part of the CGIAR Research Program on Grain Legumes and Dryland Cereals (GLDC). ICRISAT is a member of the CGIAR.

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Authors and Affiliations

  1. ICAR-Directorate of Groundnut Research (ICAR-DGR), Junagadh, 362001, India

    Sneha M. Dodia, Binal Joshi, Polavakkalipalayam P. Thirumalaisamy, Gyan P. Mishra, Dayama Narandrakumar, Arulthambi L. Rathnakumar, Jentilal R. Dobaria, Chandramohan Sangh & Radhakrishnan Thankappan

  2. International Crops Research Institute for the Semi-Arid Tropics (ICRISAT), Hyderabad, 502324, India

    Sunil S. Gangurde, Pooja Soni, Annapurna Chitikineni, Manish K. Pandey & Rajeev K. Varshney

  3. Saurashtra University, Rajkot, 360 005, India

    Sumitra V. Chanda

  4. Indian Agricultural Research Institute (IARI), New Delhi, 110012, India

    Gyan P. Mishra

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  1. Sneha M. Dodia
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  2. Binal Joshi
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  3. Sunil S. Gangurde
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  4. Polavakkalipalayam P. Thirumalaisamy
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  12. Sumitra V. Chanda
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  13. Manish K. Pandey
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Corresponding authors

Correspondence to Rajeev K. Varshney or Radhakrishnan Thankappan.

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The authors declare that there are no conflicts of interest.

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This study does not include human or animal subjects.

Additional information

Communicated by Henry T. Nguyen.

Electronic supplementary material

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Supplementary File 1:

Descriptive statistics of the phenotypic data recorded for stem rot and plant architecture (XLSX 11 kb)

Supplementary File 2:

Epistatic interactions (QTL × QTL) identified for stem rot resistance at various stages of infection (XLSX 63 kb)

Supplementary File 3:

Summary of candidate genes identified in the 5.2-Mb QTL region (XLSX 23 kb)

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Dodia, S.M., Joshi, B., Gangurde, S.S. et al. Genotyping-by-sequencing based genetic mapping reveals large number of epistatic interactions for stem rot resistance in groundnut. Theor Appl Genet 132, 1001–1016 (2019). https://doi.org/10.1007/s00122-018-3255-7

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  • DOI: https://doi.org/10.1007/s00122-018-3255-7

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