Abstract
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.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
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. https://doi.org/10.1105/tpc.108.059477
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. https://doi.org/10.1007/s00425-011-1509-6
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. https://doi.org/10.1371/journal.pone.0002068
Bodenhausen N, Reymond P (2007) Signaling pathways controlling induced resistance to insect herbivores in Arabidopsis. Mol Plant-Microbe Interact 20:1406–1420. https://doi.org/10.1094/MPMI-20-11-1406
Chen M-S (2008) Inducible direct plant defense against insect herbivores: a review. Insect Sci 15:101–114. https://doi.org/10.1111/j.1744-7917.2008.00190.x
Cheval C, Aldon D, Galaud JP, Ranty B (2013) Calcium/calmodulin-mediated regulation of plant immunity. Biochim Biophys Acta 1833(7):1766–1771. https://doi.org/10.1016/j.bbamcr.2013.01.031
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. https://doi.org/10.1016/j.jinsphys.2010.11.011
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. https://doi.org/10.1007/s00122-016-2731-1
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. https://doi.org/10.1111/j.0013-8703.2004.00192.x
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. https://doi.org/10.1016/0022-474X(93)90050-E
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. https://doi.org/10.1111/j.1365-3040.2006.01618.x
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. https://doi.org/10.1016/S0022-474X(96)00028-8
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. https://doi.org/10.1303/aez.24.126
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. https://doi.org/10.1111/j.1469-8137.2010.03229.x
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. https://doi.org/10.1016/j.jspr.2010.08.001
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. https://doi.org/10.1590/S1519-566X2005000500013
Gutterson N, Reuber TL (2004) Regulation of disease resistance pathways by AP2 / ERF transcription factors. Curr Opin Plant Biol 7:465–471. https://doi.org/10.1016/j.pbi.2004.04.007
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. https://doi.org/10.1007/BF00036762
Howe GA, Jander G (2008) Plant immunity to insect herbivores. Annu Rev Plant Biol 59:41–66. https://doi.org/10.1146/annurev.arplant.59.032607.092825
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. https://doi.org/10.3389/fpls.2017.01692
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. https://doi.org/10.1080/09670874.2014.982230
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. https://doi.org/10.1093/jee/96.1.207
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. https://doi.org/10.1007/s10681-013-1021-0
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. https://doi.org/10.1270/jsbbs1951.38.459
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. https://doi.org/10.3389/fpls.2016.01292
Kosambi DD (1943) The estimation of map distances from recombination values. Ann Eugenics 12:172–175. https://doi.org/10.1007/978-81-322-3676-4_16
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. https://doi.org/10.1016/j.plaphy.2014.04.010
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. https://doi.org/10.3389/fpls.2016.01000
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. https://doi.org/10.1094/MPMI-20-8-0900
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. https://doi.org/10.1038/nbt.3069
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. https://doi.org/10.1186/s12870-016-0736-1
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. https://doi.org/10.1104/pp.105.068544
Mittapalli O, Neal JJ, Shukle RH (2007) Antioxidant defense response in a galling insect. Proc Natl Acad Sci U S A 104:1889–1894. https://doi.org/10.1073/pnas.0604722104
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. https://doi.org/10.1002/jsfa.6110
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. https://doi.org/10.1371/journal.pone.0189440
Pandey SP, Somssich IE (2009) The role of WRKY transcription factors in plant immunity. Plant Physiol 150(4):1648–1655. https://doi.org/10.1104/pp.109.138990
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. https://doi.org/10.1007/s11103-012-9896-z
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. https://doi.org/10.1007/s11248-013-9725-4
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. https://doi.org/10.1186/s12870-016-0847-8
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. https://doi.org/10.1073/pnas.0602328103
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. https://doi.org/10.1104/pp.107.097154
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):1–12
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. https://doi.org/10.1016/j.jspr.2016.08.008
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. https://doi.org/10.1534/genetics.107.083899
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. https://doi.org/10.1105/tpc.108.058594
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. https://doi.org/10.1002/ps.1714
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. https://doi.org/10.1111/j.1439-0523.2006.01123.x
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. https://doi.org/10.1007/s10681-006-9299-9
Sudha M (2009) DNA isolation protocol for Vigna radiata with free of phenolics. Nat protocl 167
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. https://doi.org/10.1023/A:1003906715119
Tripathy SK (2016) Bruchid resistance in food legumes-an overview. Res J Biotechnol 7:98–105
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. https://doi.org/10.4161/psb.21664
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. https://doi.org/10.1007/s11103-012-9952-8
Van Ooijen J (2006) JoinMap 4. Software for the calculation of genetic linkage maps in experimental populations. Kyazma BV. Wageningen
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 341–352
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. https://doi.org/10.1007/s11104-014-2267-6
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. https://doi.org/10.1016/j.cj.2016.06.010
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. https://doi.org/10.3389/fpls.2013.00087
Wu J, Baldwin IT (2010) New insights into plant responses to the attack from insect herbivores. Annu Rev Genet 44:1–24. https://doi.org/10.1146/annurev-genet-102209-163500
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. https://doi.org/10.1093/jxb/eru472
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:e36214
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. https://doi.org/10.1007/BF00227394
Acknowledgements
Centre of Innovation (CI), Agricultural College and Research Institute, Tamil Nadu Agricultural University, Madurai, is acknowledged for providing instrumentation facilities.
Funding
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).
Author information
Authors and Affiliations
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.
Corresponding author
Ethics declarations
Disclaimer
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.
Additional information
Publisher’s note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Mariyammal, I., Seram, D., Samyuktha, S.M. et al. QTL mapping in Vigna radiata × Vigna umbellata population uncovers major genomic regions associated with bruchid resistance. Mol Breeding 39, 110 (2019). https://doi.org/10.1007/s11032-019-1006-3
Received:
Accepted:
Published:
DOI: https://doi.org/10.1007/s11032-019-1006-3