Molecular Breeding

, 39:110 | Cite as

QTL mapping in Vigna radiata × Vigna umbellata population uncovers major genomic regions associated with bruchid resistance

  • Irulappan Mariyammal
  • Devina Seram
  • Santhi Madhavan Samyuktha
  • Adhimoolam Karthikeyan
  • Manickam Dhasarathan
  • Jayakodi Murukarthick
  • John Samuel Kennedy
  • Devarajan Malarvizhi
  • Tae-Jin Yang
  • Muthaiyan Pandiyan
  • Natesan SenthilEmail author


Mungbean (Vigna radiata), genus Vigna, is an economically important legume crop that is valued for its protein-rich dry seeds. However, bruchid infestation causes severe threat to seed storage in terms of deterioration in quantity along with nutritional quality. A new resistance source was found in Vigna umbellata, a species that is cross compatible with mungbean. Thus, the objective of this study is to identify the quantitative trait locus (QTL) controlling the bruchid resistance in RIL (recombinant inbred line) population developed from a hybridization between VRM (Gg) 1 (V. radiata) and TNAU RED (V. umbellata). The RIL population was screened for bruchid resistance using the following traits, viz. per cent of seed damage (SD), the total developmental period (TDP) and per cent of adult emergence (AE) in 2017 and 2018. The QTL analysis of these traits using a genetic map composed of 538 single nucleotide polymorphism (SNP) markers covering 11 chromosomes detected 12 QTLs in over the 2 years. Among them, the QTLs on chromosomes 05 and 08, designated qSD05 and qAE08, respectively, were stably detected in both years. qSD05 exhibited large effects in both years and mapped to 1.58-Mb genomic region of the mungbean reference genome. Genome mining of this QTL region identified the likely candidate genes involved in bruchid resistance. The outcomes and QTLs found in this study may provide useful information for fine mapping, marker-assisted selection (MAS), gene cloning and breeding for the resistance to bruchids.


Bruchids Candidate genes Quantitative trait locus Single nucleotide polymorphism 



Centre of Innovation (CI), Agricultural College and Research Institute, Tamil Nadu Agricultural University, Madurai, is acknowledged for providing instrumentation facilities.

Author contributions

NS, MP and AK conceived and designed the experiments. DS, IM, SMS and JSK performed the phenotype screening. TYJ and DM provided advice on the experimental design and data analysis. MD, DS, AK, IM, SMS and JM analysed the data. AK, SMS and NS wrote the manuscript. All authors have read and approved the final manuscript.


This work was financially supported through grants from the Science and Engineering Research Board (SERB), Department of Science and Technology (DST), Government of India (GOI) project entitled "Developement and validation of SNP markers platform for Vigna complex to map the MYMV and bruchid resistance (SERB/F/1506/2013-14 Dt 11.06.2013) and the Tamil Nadu state government under the National Agricultural Development Programme (NADP)/Rashtriya Krishi Vikas Yojana (RKVY).

Compliance with ethical standards


The funders had no role in work design, data collection and analysis or decision and preparation of the manuscript.

Conflict of interest

The authors declare that they have no conflict of interest.

Ethical approval

This article does not contain any studies with human participants or animals performed by the authors.


  1. Abuqamar S, Chai MF, Luo H, Song F, Mengiste T (2008) Tomato protein kinase 1b mediates signaling of plant responses to necrotrophic fungi and insect herbivory. Plant Cell 20:1964–1983. CrossRefPubMedPubMedCentralGoogle Scholar
  2. Atamian HS, Eulgem T, Kaloshian I (2012) SlWRKY70 is required for Mi-1-mediated resistance to aphids and nematodes in tomato. Planta 235:299–309. CrossRefPubMedGoogle Scholar
  3. Beekwilder J, Van Leeuwen W, Van Dam NM, Bertossi M, Grandi V, Mizzi L, Soloviev M, Szabados L, Molthoff JW, Schipper B, Verbocht H (2008) The impact of the absence of aliphatic glucosinolates on insect herbivory in Arabidopsis. PLoS One 3(4):e2068. CrossRefPubMedPubMedCentralGoogle Scholar
  4. Bodenhausen N, Reymond P (2007) Signaling pathways controlling induced resistance to insect herbivores in Arabidopsis. Mol Plant-Microbe Interact 20:1406–1420. CrossRefPubMedGoogle Scholar
  5. Chen M-S (2008) Inducible direct plant defense against insect herbivores: a review. Insect Sci 15:101–114. CrossRefGoogle Scholar
  6. Cheval C, Aldon D, Galaud JP, Ranty B (2013) Calcium/calmodulin-mediated regulation of plant immunity. Biochim Biophys Acta 1833(7):1766–1771. CrossRefPubMedGoogle Scholar
  7. Chi YH, Ahn JE, Yun DJ, Lee SY, Liu TX, ZhuSalzman K (2011) Changes in oxygen and carbon dioxide environment alter gene expression of cowpea bruchids. J Insect Physiol 57:220–230. CrossRefPubMedGoogle Scholar
  8. Chotechung S, Somta P, Chen J, Yimran T, Chen X, Srinives P (2016) A gene encoding a polygalacturonase-inhibiting protein (PGIP) is a candidate gene for bruchid (Coleoptera: Bruchidae) resistance in mungbean (Vigna radiata). Theor Appl Genet 129:1673–1683. CrossRefPubMedGoogle Scholar
  9. Clissold FJ, Sanson GD, Read J (2004) Indigestibility of plant cell wall by the Australian plague locust, Chortoicetes terminifera. Entomol Exp Appl 112:159–168. CrossRefGoogle Scholar
  10. Daglish GJ, Erbacher JM, Eelkema M (1993) Efficacy of protectants against Callosobruchus phaseoli (Gyll.) and C. maculatus (F.) (Coleoptera: Bruchidae) in mungbean. J Stored Prod Res 29:345–349. CrossRefGoogle Scholar
  11. Divol F, Vilaine F, Thibivilliers S, Kusiak C, Sauge MH, Dinant S (2007) Involvement of the xyloglucan endotransglycosylase/hydrolases encoded by celery XTH1 and Arabidopsis XTH33 in the phloem response to aphids. Plant Cell Environ 30:187–201. CrossRefPubMedGoogle Scholar
  12. Dongre TK, Pawar SE, Thakare RG, Harwalker MR (1996) Identification of resistance sources to cowpea weevil in Vigna sp. and inheritance of their resistance in black gram. J Stored Prod Res 32:201–204. CrossRefGoogle Scholar
  13. Fujii K, Ishimoto M, Kitamura K (1989) Patterns of resistance to bean weevils (Bruchidae) in Vigna radiata-mungo sublobata complex inform the breeding of new resistant variety. Appl Entomol Zool 24:126–132. CrossRefGoogle Scholar
  14. Gao LL, Kamphuis LG, Kakar K, Edwards OR, Udvardi MK, Singh KB (2010) Identification of potential early regulators of aphid resistance in Medicago truncatula via transcription factor expression profiling. New Phytol 186:980–994. CrossRefPubMedGoogle Scholar
  15. Gbaye OA, Millard JC, Holloway GJ (2011) Legume type and temperature effects on the toxicity of insecticide to the genus Callosobruchus (Coleoptera: Bruchidae). J Stored Prod Res 47:8–12. CrossRefGoogle Scholar
  16. Goussain MM, Prado E, Moraes JC (2005) Effect of silicon applied to wheat plants on the biology and probing behaviour of the green bug Schizaphis graminum (Rond.) (Hemiptera: Aphididae). Neotrop Entomol 34:807–813. CrossRefGoogle Scholar
  17. Gutterson N, Reuber TL (2004) Regulation of disease resistance pathways by AP2 / ERF transcription factors. Curr Opin Plant Biol 7:465–471. CrossRefPubMedGoogle Scholar
  18. Hogenboom NG (1972) Breaking breeding barriers in Lycopersicon. 1. The genus Lycopersicon, its breeding barriers and the importance of breaking these barriers. Euphytica 21:221–227. CrossRefGoogle Scholar
  19. Howe GA, Jander G (2008) Plant immunity to insect herbivores. Annu Rev Plant Biol 59:41–66. CrossRefPubMedGoogle Scholar
  20. Kaewwongwal A, Chen J, Somta P, Kongjaimun A, Yimram T, Chen X, Srinives P (2017) Novel alleles of two tightly linked genes encoding polygalacturonase-inhibiting proteins (VrPGIP1 and VrPGIP2) associated with the Br locus that confer bruchid (Callosobruchus spp.) resistance to mungbean (Vigna radiata) accession V2709. Front Plant Sci 8:1692. CrossRefPubMedPubMedCentralGoogle Scholar
  21. Karthikeyan A, Shobhana VG, Sudha M, Raveendran M, Senthil N (2014) Mungbean yellow mosaic virus (MYMV): a threat to green gram (Vigna radiata) production in Asia. Int J Pest Manage 60:314–324. CrossRefGoogle Scholar
  22. Kashiwaba K, Tomooka N, Kaga A, Han OK, Vaughan DA (2003) Characterization of resistance to three bruchid species (Callosobruchus spp., Coleoptera, Bruchidae) in cultivated rice bean (Vigna umbellata). J Econ Entomol 96:207–213. CrossRefPubMedGoogle Scholar
  23. Kim HJ, Xing GN, Wang YF, Zhao TJ, Yu DY, Yang SP, Li Y, Chen SY, Palmer RG, Gai JY (2014) Constitution of resistance to common cutworm in terms of antibiosis and antixenosis in soybean RIL populations. Euphytica 196:137–154. CrossRefGoogle Scholar
  24. Kitamura K, Ishimoto M, Sawa M (1988) Inheritance of resistance to infestation with azuki bean weevil in Vigna sublobata and successful incorporation to V. radiata. Jpn J Breed 38:459–464. CrossRefGoogle Scholar
  25. Kong W, Li J, Yu Q, Cang W, Xu R, Wang Y, Ji W (2016) Two novel flavin-containing monooxygenases involved in biosynthesis of aliphatic glucosinolates. Front Plant Sci 7:1292. CrossRefPubMedPubMedCentralGoogle Scholar
  26. Kosambi DD (1943) The estimation of map distances from recombination values. Ann Eugenics 12:172–175. CrossRefGoogle Scholar
  27. Lawrence SD, Novak NG, Jones RW, Farrar RR, Blackburn MB (2014) Herbivory responsive C2H2 zinc finger transcription factor protein StZFP2 from potato. Plant Physiol Biochem 80:226–233. CrossRefPubMedGoogle Scholar
  28. Liang D, Chen M, Qi X, Xu Q, Zhou F, Chen X (2016) QTL mapping by SLAF-seq and expression analysis of candidate genes for aphid resistance in cucumber. Front Plant Sci 7:1000. CrossRefPubMedPubMedCentralGoogle Scholar
  29. Libault M, Wan J, Czechowski T, Udvardi M, Stacey G (2007) Identification of Arabidopsis transcription factor and 30 ubiquitin ligase genes responding to chitin, a plant-defense elicitor. Mol Plant-Microbe Interact 20:900–911. CrossRefPubMedGoogle Scholar
  30. Liu Y, Wu H, Chen H, Liu Y, He J, Kang H, Sun Z, Pan G, Wang Q, Hu J, Zhou F, Zhou K, Zheng X, Ren Y, Chen L, Wang Y, Zhao Z, Lin Q, Wu F, Zhang X, Guo X, Cheng X, Jiang L, Wu C, Wang H, Wan J (2014) A gene cluster encoding lectin receptor kinases confers broad-spectrum and durable insect resistance in rice. Nat Biotechnol 33:301–305. CrossRefPubMedGoogle Scholar
  31. Liu MS, Kuo TCY, Ko CY, Wu DC, Li KY, Lin WJ, Lin CP, Wang YW, Schafleitner R, Lo HF, Chen CY (2016) Genomic and transcriptomic comparison of nucleotide variations for insights into bruchid resistance of mungbean (Vigna radiata [L.] R. Wilczek). BMC Plant Biol 16:1. CrossRefGoogle Scholar
  32. McGrath KC, Dombrecht B, Manners JM, Schenk PM, Edgar CI, Maclean DJ, Scheible WR, Udvardi MK, Kazan K (2005) Repressor and activator-type ethylene response factors functioning in jasmonate signaling and disease resistance identified via a genome-wide screen of Arabidopsis transcription factor gene expression. Plant Physiol 139:949–959. CrossRefPubMedPubMedCentralGoogle Scholar
  33. Mittapalli O, Neal JJ, Shukle RH (2007) Antioxidant defense response in a galling insect. Proc Natl Acad Sci U S A 104:1889–1894. CrossRefPubMedPubMedCentralGoogle Scholar
  34. Nair RM, Yang RY, Easdown WJ, Thavarajah D, Thavarajah P, Hughes J, Keatinge JDH (2013) Biofortification of mungbean (Vigna radiata) as a whole food to enhance human health. J Sci Food Agric 93:1805–1813. CrossRefPubMedGoogle Scholar
  35. Oki N, Kaga A, Shimizu T, Takahashi M, Kono Y, Takahashi M (2017) QTL mapping of antixenosis resistance to common cutworm (Spodoptera litura Fabricius) in wild soybean (Glycine soja). PLoS One 12(12):e0189440. CrossRefPubMedPubMedCentralGoogle Scholar
  36. Pandey SP, Somssich IE (2009) The role of WRKY transcription factors in plant immunity. Plant Physiol 150(4):1648–1655. CrossRefPubMedPubMedCentralGoogle Scholar
  37. Qiu YJ, Xi J, Du LQ, Suttle JC, Poovaiah BW (2012) Coupling calcium/calmodulin-mediated signaling and herbivore-induced plant response through calmodulin-binding transcription factor AtSR1/CAMTA3. Plant Mol Biol 79:89–99. CrossRefPubMedGoogle Scholar
  38. Santamaria ME, Martinez M, Cambra I, Grbic V, Diaz I (2013) Understanding plant defence responses against herbivore attacks: an essential first step towards the development of sustainable resistance against pests. Transgenic Res 22:697–708. CrossRefPubMedGoogle Scholar
  39. Schafleitner R, Huang SM, Chu SH, Yen JY, Lin CY, Yan MR, Krishnan B, Liu MS, Lo HF, Chen CY, Chen LFO, Wu DC, Bui TGT, Ramasamy S, Tung CW, Nair R (2016) Identification of single nucleotide polymorphism markers associated with resistance to bruchids (Callosobruchus spp.) in wild mungbean (Vigna radiata var. sublobata) and cultivated V. radiata through genotyping by sequencing and quantitative trait locus analysis. BMC Plant Biol 16:159. CrossRefPubMedPubMedCentralGoogle Scholar
  40. Schmelz EA, Carroll MJ, LeClere S, Phipps SM, Meredith J, Chourey PS, Alborn HT, Teal PEA (2006) Fragments of ATP synthase mediate plant perception of insect attack. Proc Natl Acad Sci U S A 103:8894–8899. CrossRefPubMedPubMedCentralGoogle Scholar
  41. Schmelz EA, LeClere S, Carroll MJ, Alborn HT, Teal PEA (2007) Cowpea chloroplastic ATP synthase is the source of multiple plant defense elicitors during insect herbivory. Plant Physiol 144:793–805. CrossRefPubMedPubMedCentralGoogle Scholar
  42. Scholz S, Heyer M, Vadassery J, Mithofer A (2016) A role for calmodulin-like proteins in herbivore defense pathways in plants. Endocytobiosis Cell Res 27(1):1–12Google Scholar
  43. Seram D, Senthil N, Pandiyan M, Kennedy J (2016) Resistance determination of a South Indian bruchid strain against rice bean landraces of Manipur (India). J Stored Prod Res 69:199–206. CrossRefGoogle Scholar
  44. Simon M, Loudet O, Durand S, Berard A, Brunel D, Sennesal FX, Durand-Tardif M, Pelletier G, Camilleri C (2008) Quantitative trait loci mapping in five new large recombinant inbred line populations of Arabidopsis thaliana genotyped with consensus single-nucleotide polymorphism markers. Genetics 178:2253–2264. CrossRefPubMedPubMedCentralGoogle Scholar
  45. Skibbe M, Qu N, Galis I, Baldwin IT (2008) Induced plant defenses in the natural environment: Nicotiana attenuata WRKY3 and WRKY6 coordinate responses to herbivory. Plant Cell 20:1984–2000. CrossRefPubMedPubMedCentralGoogle Scholar
  46. Smith JL, De Moraes CM, Mescher MC (2009) Jasmonate and salicylate-mediated plant defense responses to insect herbivores, pathogens and parasitic plants. Pest Manag Sci 65:497–503. CrossRefPubMedGoogle Scholar
  47. Somta P, Kaga A, Tomooka N, Isemura T, Chaitieng B, Srinives P, Vaughan DA (2006) Development of an interspecific Vigna linkage map between Vigna umbellata (Thunb.) Ohwi & Ohashi and V. nakashimae (Ohwi) Ohwi & Ohashi and its use in analysis of bruchid resistance and comparative genomics. Plant Breed 125:77–84. CrossRefGoogle Scholar
  48. Somta P, Ammaranan C, Ooi PAC, Srinives P (2007) Inheritance of seed resistance to bruchids in cultivated mungbean (Vigna radiata, L. Wilczek). Euphytica 155:47–55. CrossRefGoogle Scholar
  49. Sudha M (2009) DNA isolation protocol for Vigna radiata with free of phenolics. Nat protocl 167Google Scholar
  50. Tomooka N, Kashiwaba K, Vaugham DA, Ishimoto M, Egawa Y (2000) The effectiveness of evaluating wild species: searching for sources of resistance to bruchid beetles in the genus Vigna subgenus Ceratotropis. Euphytica 115:27–41. CrossRefGoogle Scholar
  51. Tripathy SK (2016) Bruchid resistance in food legumes-an overview. Res J Biotechnol 7:98–105Google Scholar
  52. Vadassery J, Scholz SS, Mithofer A (2012) Multiple calmodulin-like proteins in Arabidopsis are induced by insect-derived (Spodoptera littoralis) oral secretion. Plant Signal Behav 7:1277–1280. CrossRefPubMedPubMedCentralGoogle Scholar
  53. Vaid N, Pandey PK, Tuteja N (2012) Genome-wide analysis of lectin receptor-like kinase family from Arabidopsis and rice. Plant Mol Biol 80:365–388. CrossRefPubMedGoogle Scholar
  54. Van Ooijen J (2006) JoinMap 4. Software for the calculation of genetic linkage maps in experimental populations. Kyazma BV. WageningenGoogle Scholar
  55. Vaughan DA, Tommoka N, Kaga A (2004) Azuki bean. In: Singh RJ, Jauhar PP (eds) Genetic resources, chromosome engineering, crop improvement: grain legumes. CRC, Boca Raton, pp 341–352Google Scholar
  56. Wang G, Zeng H, Hu X, Zhu Y, Chen Y, Shen C, Wang H, Poovaiah B, Du L (2015) Identification and expression analyses of calmodulin-binding transcription activator genes in soybean. Plant Soil 386:205–221. CrossRefGoogle Scholar
  57. Wang L, Wu C, Zhong M, Zhao D, Mei L, Chen H, Wang S, Liu C, Cheng X (2016) Construction of an integrated map and location of a bruchid resistance gene in mungbean. Crop J 4:360–366. CrossRefGoogle Scholar
  58. Wondafrash M, Van Dam NM, Tytgat TOG (2013) Plant systemic induced responses mediate interactions between root parasitic nematodes and aboveground herbivorous insects. Front Plant Sci 4:87. CrossRefPubMedPubMedCentralGoogle Scholar
  59. Wu J, Baldwin IT (2010) New insights into plant responses to the attack from insect herbivores. Annu Rev Genet 44:1–24. CrossRefPubMedGoogle Scholar
  60. Wu C, Ávila CA, Goggin FL (2015) The ethylene response factor Pti5 contributes to potato aphid resistance in tomato independent of ethylene signalling. J Exp Bot 66:559–570. CrossRefPubMedGoogle Scholar
  61. Ye M, Luo SM, Xie JF, Li YF, Xu T, Liu Y, Song YY, Zhu-Salzman K, Zeng RS (2012) Silencing COI1 in rice increases susceptibility to chewing insects and impairs inducible defense. PLoS One 7:e36214CrossRefGoogle Scholar
  62. Young ND, Kumar L, Menancio-Hautea D, Danesh D, Talekar NS, Shanmugasundaram S, Kim DH (1992) RFLP mapping of a major bruchid resistance gene in mungbean (Vigna radiata L. Wilczek). Theor Appl Genet 84:839–844. CrossRefPubMedGoogle Scholar

Copyright information

© Springer Nature B.V. 2019

Authors and Affiliations

  • Irulappan Mariyammal
    • 1
  • Devina Seram
    • 2
  • Santhi Madhavan Samyuktha
    • 1
  • Adhimoolam Karthikeyan
    • 3
  • Manickam Dhasarathan
    • 3
  • Jayakodi Murukarthick
    • 4
  • John Samuel Kennedy
    • 5
  • Devarajan Malarvizhi
    • 6
  • Tae-Jin Yang
    • 7
  • Muthaiyan Pandiyan
    • 8
  • Natesan Senthil
    • 3
    • 9
    Email author
  1. 1.Department of Plant Breeding and Genetics, Agricultural College and Research InstituteTamil Nadu Agricultural UniversityMaduraiIndia
  2. 2.Department of Entomology, Center for Plant Protection StudiesTamil Nadu Agricultural UniversityCoimbatoreIndia
  3. 3.Department of Biotechnology, Agricultural College and Research InstituteTamil Nadu Agricultural UniversityMaduraiIndia
  4. 4.Leibniz Institute of Plant Genetics and Crop Plant Research (IPK Gatersleben)SeelandGermany
  5. 5.Department of Entomology, Horticultural Research StationTamil Nadu Agricultural UniversityYercaudIndia
  6. 6.Agricultural Research StationTamil Nadu Agricultural UniversityBhavanisagarIndia
  7. 7.Department of Plant Science, Plant Genomics and Breeding Institute, Research Institute for Agriculture and Life Sciences, College of Agriculture and Life SciencesSeoul National UniversitySeoulRepublic of Korea
  8. 8.Agricultural College and Research InstituteTamil Nadu Agricultural UniversityEchangkottaiIndia
  9. 9.Department of Plant Molecular Biology and Bioinformatics, Center for Plant Molecular Biology and BiotechnologyTamil Nadu Agricultural UniversityCoimbatoreIndia

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