Abstract
Two bruchid species, azuki bean weevil (Callosobruchus chinensis L.) and cowpea weevil (Callosobruchus maculatus F.), are the most important insect pests of mungbean [Vigna radiata (L.) Wilczek] after harvest. Improving bruchid resistance is a major goal for mungbean breeders. Bruchid resistance in mungbean is controlled by a single major locus, Br. The tightly linked VrPGIP1 and VrPGIP2, which encode polygalacturonase-inhibiting proteins (PGIPs), are the candidate genes at the Br locus associated with bruchid resistance. One VrPGIP1 resistance allele and two VrPGIP2 resistance alleles have been identified. In this study, we fine-mapped the bruchid-resistance genes in wild mungbean (V. radiata var. sublobata) accession ACC41 using the F2 population (574 individuals) derived from the ‘Kamphaeng Saen 2’ (susceptible) × ACC41 (resistant) cross. A QTL analysis indicated that the resistance to the azuki bean weevil and cowpea weevil in ACC41 is controlled by a major QTL (qBr5.1) and a minor QTL (qBr5.2), which are only 0.3 cM apart. qBr5.1 and qBr5.2 accounted for about 82% and 2% of the resistance variation in the F2 population, respectively. qBr5.1 was mapped to a 237.35-kb region on mungbean chromosome 5 containing eight annotated genes, including VrPGIP1 and VrPGIP2. An examination of the ACC41 VrPGIP1 and VrPGIP2 sequences revealed a new allele for VrPGIP1 (i.e., VrPGIP1-2). Compared with the wild-type sequence, VrPGIP1-2 has five SNPs, of which four cause amino acid changes (residues 125, 129, 188, and 336). A protein sequence analysis indicated that residues 125 and 129 in VrPGIP1-2 are in a β-sheet B1 region, whereas residues 188 and 336 are in a C10-helix region and at the end of the C-terminal region, respectively. Because the β-sheet B1 region is important for interactions with polygalacturonase (PG), residues 125 and 129 in VrPGIP1-2 likely contribute to bruchid resistance by inhibiting PG. Our results imply that VrPGIP1-2 is associated with the bruchid resistance of wild mungbean accession ACC41. This new resistance allele may be useful for breeding mungbean varieties exhibiting durable bruchid resistance.
Similar content being viewed by others
References
Alamzeb A, Khan U, Khan GZ, Khan I, Zahid M, Haq MM (2016) Screening for bruchids (Callosobruchus maculatus) resistance in mungbean genotypes under lab condition. In: Shakoori AR (ed) Proceedings of 36th Pakistan Congress of Zoology. The Zoological Society of Pakistan, pp 167–168
Casasoli M, Federici L, Spinelli F, Di Matteo A, Vella N, Scaloni F, Fernandez-Recio J, Cervone F, De Lorenzo G (2009) Integration of evolutionary and desolvation energy analysis identifies functional sites in a plant immunity protein. Proc Natl Acad Sci USA 106:7666–7671
Chotechung S, Somta P, Chen J, Yimram 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
Chrispeels MJ, Grossi-de-Sá MF, Higgins TJV (1998) Genetic engineering with α-amylase inhibitors seeds resistant to bruchids. Seed Sci Res 8:257–263
Di Matteo A, Federici L, Mattei B, Salvi G, Johnson KA, Savino C, De Lorenzo G, Tsernoglou D, Cervone F (2003) The crystal structure of polygalacturonase-inhibiting protein (PGIP), a leucine-rich repeat protein involved in plant defense. Proc Natl Acad Sci USA 100:10124–10128
Doostdar H, McCollum TG, Mayer RT (1997) Purification and characterization of an endo-polygalacturonase from the gut of West Indies sugarcane rootstalk borer weevil (Diaprepes abbreviatus L.) larvae. Comp Biochem Phys B 118:861–867
D’Ovidio R, Raiola A, Capodicasa C, Devoto A, Pontiggia D, Roberti S, Galletti R, Conti E, O’Sullivan D, De Lorenzo G (2004) Characterization of the complex locus of bean encoding polygalacturonase-inhibiting proteins reveals subfunctionalization for defense against fungi and insects. Plant Physiol 135:2424–2435
Falk CT (1989) A simple scheme for preliminary ordering of multiple loci: application to 45 Cf families. Prog Clin Biol Res 329:17–22
Frati F, Galletti R, De Lorenzo G, Salerno G, Conti E (2006) Activity of endo-polygalacturonases in mirid bugs (Heteroptera: Miridae) and their inhibition by plant cell wall proteins (PGIPs). Eur J Entomol 103:515–522
Fujii K, Miyazaki S (1987) Infestation resistance of wild legumes (Vigna sublobata) to azuki bean weevil., Callosobruchus chinensis (L.) (Coleoptera: Bruchidae) and its relationship with cytogenetic classification. Appl Ent Zool 22:229–230
Imrie BC and Lambrides CJ (1998) Marker-assisted selection for resistance to bruchids. In: Libas EM, Lopez KS (eds) International consultation workshop on mungbean: proceedings of the mungbean workshop, AVRDC, Tainan, Taiwan, pp 135–140
Ishimoto M, Kitamura K (1989) Growth inhibitory effects of an α-amylase inhibitor from kidney bean, Phaseolus vulgaris (L.) on three species of bruchids (Coleoptera: Bruchidae). Appl Entomol Zool 24:281–286
Jones DA, Jones JDG (1997) The role of leucine-rich repeat proteins in plant defences. Adv Bot Res 24:89–167
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
Kaga A, Ishimoto M (1998) Genetic localization of a bruchid resistance gene and its relationship to insecticidal cyclopeptide alkaloids., the vignatic acids in mungbean (V. radiata L. Wilczek). Mol Gen Genet 258:378–384
Kang YJ, Kim S, Kim MY, Lestari P, Kim KH, Ha BK, Jun TH, Hwang WJ, Lee T, Lee J, Shim S, Yoon MY, Jang YE, Han KS, Taeprayoon P, Yoon N, Somta P, Tanya P, Kim KS, Gwag JG, Moon JK, Lee YH, Park BS, Bombarely A, Doyle JJ, Jackson SA, Schafleitner R, Srinives P, Varshney RK, Lee SH (2014) Genome sequence of mungbean and insights into evolution within Vigna species. Nat Commun 5:5443. https://doi.org/10.1038/ncomms6443
Kirsch R, Heckel DG, Pauchet Y (2016) How the rice weevil breaks down the pectin network: enzymatic synergism and sub-functionalization. Insect Biochem Mol 71:72–82
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. Jap J Breed 38:459–464
Konarev AV (1996) Interaction of insect digestive enzymes with plant protein inhibitors and host-parasite co-evolution. Euphytica 92:89–94
Kosambi D (1944) The estimation of map distances from recombination values. Ann Eugen 12:172–175
Lambrides CJ, Godwin ID (2007) Mungbean. In: Kole C (ed) Genome mapping and molecular breeding in plants, vol 3. Pulses, sugar and tuber crops. Springer, Berlin, pp 69–90
Lambrides CJ, Imrie BC (2000) Susceptibility of mungbean varieties to the bruchid species Callosobruchus maculatus (F.), C. analis (Gyll.), C. chinenis (L.) and Scanthoscelides obtectus (Say.) (Coleoptera: Chrysomelidae). Aust J Agric Res 51:85–89
Lawrence PK, Koundal KR (2002) Plant protease inhibitors in control of phytophagous insects. Electron J Biotechnol 5(1):3. https://doi.org/10.2225/vol5-issue1-fulltext-3
Leckie F, Mattei B, Capodicasa C, Hemmings A, Nuss L, Aracri B, De Lorenzo G, Cervone F (1999) The specificity of polygalacturonase-inhibiting protein (PGIP): a single amino acid substitution in the solvent-exposed beta-strand/beta-turn region of the leucine-rich repeats (LRRs) confers a new recognition capability. EMBO J 418:2352–2363
Li H, Ye G, Wang J (2007) A modified algorithm for the improvement of composite interval mapping. Genetics 175:361–374
Lin C, Chen CS, Horng SB (2005) Characterization of resistance to Callosobruchus maculatus (F.) (Coleoptera: Bruchidae) in a mungbean variety VC6089A and its resistance associated protein VrD1. J Econ Entomolo 98:1369–1373
Liu MS, Kuo TCY, Ko CY, Wu DC, Li KY, Lin WJ, Lin CP, Wang YW, Schafleitner R, Lo HF, Chen CY, Chen LF (2016) Genomic and transcriptomic comparison of nucleotide variations for insights into bruchid resistance of mungbean (Vigna radiata [L.] R. Wilczek). BMC Plant Biol 16:46. https://doi.org/10.1186/s12870-016-0736-1
Lodhi MA, Ye GN, Weeden NF, Reisch BI (1994) A simple and efficient method for DNA extraction from grapevine cultivars and Vitis species. Plant Mol Biol Rep 12:6–13
Mei L, Cheng XZ, Wang SH, Wang LX, Liu CY, Sun L, Xu N, Humphry ME, Lambrides CJ, Li HB, Liu CJ (2009) Relationship between bruchid resistance and seed mass in mungbean based on QTL analysis. Genome 52:589–596
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
Nogueira FCS, Silva CP, Alexandre D, Samuels RI, Soares EL, Aragão FJL, Palmisano G, Domont GB, Roepstorff P, Campos FA (2012) Global proteome changes in larvae of Callosobruchus maculatus (Coleoptera: Chrysomelidae: Bruchinae) following ingestion of a cysteine proteinase inhibitor. Proteomics 12:2704–2715
Pauchet Y, Wilkinson P, Chauhan R, Ffrench-Constant RH (2010) Diversity of beetle genes encoding novel plant cell wall degrading enzymes. PLoS One 5:e15635. https://doi.org/10.1371/journal.pone.0015635
Pedra JHF, Brandt A, Westerman R, Lobo N, Li HM, Romero-Severson J, Murdock LL, Pittendrigh BR (2003) Transcriptome analysis of the cowpea weevil bruchid: identification of putative proteinases and alpha-amylases associated with food breakdown. Insect Mol Biol 12:405–412
R Development Core Team (2012) R: a language and environment for statistical somputing. R Foundation for Statistical Computing, Vienna. Available online at: https://www.r-project.org
Raina AK (1970) Callosobruchus spp. infesting stored pulses (grain legumes) in India and a comparative study of their biology. Indian J Entomol 32:302–310
Rees D (2004) Insects of stored products. CSIRO publishing, Collingwood Victoria
Santana MC (2013) Identificação de poligalacturonases expressas no sistema digestório de Callosobruchus maculatus (Coleoptera: Chrysomelidae: Bruchinae). Dissertation, Universidade Federal de Santa Catarina, Brazil
Sarkar S, Ghosh S, Chatterjee M, Das P, Lahari T, Maji A, Mondal N, Pradhan KK, Bhattacharyya S (2011) Molecular markers linked with bruchid resistance in Vigna radiata var. sublobata and their validation. J Plant Biochem Biotechnol 20:155–160
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
Shade RE, Schroeder HE, Pueyo JJ, Tabe LL, Murdock TJV, Higgins MJ, Chrispeels MJ (1994) Transgenic pea seeds expressing the α-amylase inhibitor of the common bean are resistant to bruchid beetles. Bio/Technol 12:793–796
Somta P, Srinives P (2007) Genome research in mungbean [Vigna radiata (L.) Wilczek] and blackgram [V. mungo (L.) Hepper]. ScienceAsia 33(S1):69–74
Somta P, Ammaranan C, Ooi PAC, Srinives P (2007) Inheritance of seed resistance to bruchids in cultivated mungbean (Vigna radiata (L) Wilzcek). Euphytica 155:49–55
Somta C, Somta P, Tomooka N, Ooi PAC, Vaughan DA, Srinives P (2008) Characterization of new sources of mungbean (Vigna radiata (L) Wilczek) resistance to bruchids., Callosobruchus spp (Coleoptera: Bruchidae). J Stored Prod Res 44:316–321
Somta P, Seehalak W, Srinives P (2009) Development, characterization and cross-species amplifcation of mungbean (Vigna radiata) genic microsatellite markers. Conserv Genet 10:1939–1943
Southgate BJ (1979) Biology of the Bruchidae. Annu Rev Entomol 24:449–473
Srinives P, Somta P, Somta C (2007) Genetics and breeding of resistance to bruchids (Callosobruchus spp) in Vigna crops: a review. NU Sci J 4:1–17
Talekar NS (1988) Biology, damage and control of bruchid pests of mungbean. In: Shanmugasundaram S, McLean BT (eds) Mungbean: proceedings of the second international symposium. AVRDC, Tainan, Taiwan, pp 329–342
Talekar NS, Lin CL (1992) Characterization of Callosobruchus chinensis (Coleoptera: Bruchidae) resistance in mungbean. J Econ Entomol 85:1150–1153
Van Os H, Stam P, Visser RGF, Van Eck HJ (2005) RECORD: a novel method for ordering loci on a genetic linkage map. Theor Appl Genet 112:30–40
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 mung bean. Crop J 4:360–366
Young ND, Kumar L, Menancio-Hautea D, Danesh D, Talekar NS, Shanmugasundarum S et al (1992) RFLP mapping of a major bruchid resistance gene in mungbean (Vigna radiata, L. Wilczek). Theor Appl Genet 84:839–844
Acknowledgements
We are thankful to the Joint Legume Research Center between Kasetsart University and Jiangsu Academy of Agricultural Sciences for lab facilities. We thank Liwen Bianji, Edanz Editing China (https://www.liwenbianji.cn/ac) for editing the English text of a draft of this manuscript.
Funding
This work was supported by the Center for Advanced Studies for Agriculture and Food, Institute for Advanced Studies, Kasetsart University under the Higher Education Research Promotion and National Research University Project of Thailand, Office of the Higher Education Commission, Ministry of Education, Thailand.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Ethics approval
This article does not contain any studies with human participants or animals performed by any of the authors.
Additional information
Communicated by Stefan Hohmann.
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Kaewwongwal, A., Liu, C., Somta, P. et al. A second VrPGIP1 allele is associated with bruchid resistance (Callosobruchus spp.) in wild mungbean (Vigna radiata var. sublobata) accession ACC41. Mol Genet Genomics 295, 275–286 (2020). https://doi.org/10.1007/s00438-019-01619-y
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00438-019-01619-y