Abstract
To identify the powdery mildew (PM) resistance gene in mungbean, inter-simple sequence repeat (ISSR) markers and newly developed ISSR-anchored resistance gene analog (ISSR-RGA) markers were evaluated. When F2:7 and F2:8 recombinant inbred line populations derived from a cross between CN72 (susceptible cultivar in Thailand) and V4718 (resistant line from Asian Vegetable Research and Development Center) were evaluated for PM resistance under field conditions, the PM resistance gene from V4718 was found to be inherited as a single major gene. Fifteen out of 75 ISSR primers produced 27 DNA bands putatively associated with PM resistance in bulk segregant analysis (BSA). Ten ISSR primers were combined with four RGA primers homologous to the nucleotide-binding site and kinase domains of resistance (R) genes to generate 40 ISSR-RGA primer combinations. When these 40 ISSR-RGA primer combinations and 10 corresponding ISSR primers were used in BSA, 873 ISSR and 756 ISSR-RGA loci were amplified. Fifty-two of 756 ISSR-RGA loci were new, and 11 of these 23 ISSR-RGA loci were putatively associated with the PM resistance. Simple linear regression confirmed that 5 of the 27 ISSR markers and 3 of the 11 ISSR-RGA markers were significantly associated with the PM resistance gene. When these eight ISSR and ISSR-RGA markers were used for quantitative trait loci (QTL) analysis, multiple interval mapping identified a major QTL, qPMC72V18-1, explaining up to 92.4% of the phenotypic variation, flanked by I42PL229 and I85420 markers at the distance of 4 and 9 cM, respectively. These results suggest that ISSR and ISSR-RGA markers are highly efficient tools for mapping PM resistance gene in mungbean. The markers closely linked to the PM resistance gene will be useful for future marker-assisted selection to develop mungbean varieties resistant to PM.
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References
Ajibade SR, Weeden NF, Chite SM (2000) Inter simple sequence repeat analysis of genetic relationships in the genus Vigna. Euphytica 111(1):47–55. https://doi.org/10.1023/A:1003763328768
Ali Z, Xu ZL, Zhang DY, He XL, Bahadur S, Yi JX (2011) Molecular diversity analysis of eggplant (Solanum melongena) genetic resources. Genet Mol Res 10(2):1141–1155. https://doi.org/10.4238/vol10-2gmr1279
Arunakumari K, Durgarani CV, Satturu V, Sarikonda KR, Chittoor PDR, Vutukuri B, Laha GS, Nelli APK, Gattu S, Jamal M, Prasadbabu A, Hajira S, Sundaram RM (2016) Marker-assisted pyramiding of genes conferring resistance against bacterial blight and blast diseases into Indian rice variety MTU1010. Rice Sci 23(6):306–316. https://doi.org/10.1016/j.rsci.2016.04.005
Bainade PS, Kale AA, Kumbhar SD, Deshmukh SG (2014) Inter simple sequence repeats (ISSR) based polymorphism for powdery mildew resistance in green gram (Vigna radiata (L.) Wilczek). J Cell Tissue Res 14(3):4547–4550
Bassi D, Briñez B, Rosa JS, Oblessuc PR, Almeida CP, Nucci SM, Silva LCD, Chiorato AF, Vianello RP, Camargo LEA, Blair MW, Benchimol-Reis LL (2017) Linkage and mapping of quantitative trait loci associated with angular leaf spot and powdery mildew resistance in common beans. Genet Mol Biol 40(1):109–122. https://doi.org/10.1590/1678-4685-GMB-2015-0314
Binyamin R, Khan MA, Khan NA, Khan AI (2015) Application of SCAR markers linked with mungbean yellow mosaic virus disease-resistance gene in Pakistan mungbean germplasm. Genet Mol Res 14(1):2825–2830. https://doi.org/10.4238/2015.March.31.13
Chankaew S, Somta P, Isemura T, Tomooka N, Kaga A, Vaughan DA, Srinives P (2013) Quantitative trait locus mapping reveals conservation of major and minor loci for powdery mildew resistance in four sources of resistance in mungbean [Vigna radiata (L.) Wilczek.] Mol Breeding 32(1):121–130. https://doi.org/10.1007/s11032-013-9856-6
Chen XM, Line RF, Leung H (1998) Genome scanning for resistance-gene analogs in rice, barley and wheat by high-resolution electrophoresis. Theor Appl Genet 97(3):345–355. https://doi.org/10.1007/s001220050905
Fayyaz E, Shahnejat-Bushehri AA, Tabatabaei BES, Adel J (2007) Constructing a preliminary wheat genetic map using RGA and AFLP markers. Int J Agri Biol 9(6):863–867
Feuillet C, Schachermayr G, Keller B (1997) Molecular cloning of a new receptor-like kinase gene encoded at the Lr10 disease resistance locus of wheat. Plant J 11(1):45–52. https://doi.org/10.1046/j.1365-313X.1997.11010045.x
Flor HH (1955) Host–parasite interactions in flax rust—its genetics and other implications. Phytopathol 45:2128–2136
Hanai LR, Santini L, Camargo LEA, Fungaro MHP, Gepts P, Tsai SM, Vieira MLC (2010) Extension of the core map of common bean with EST-SSR, RGA, AFLP, and putative functional markers. Mol Breeding 25(1):25–45. https://doi.org/10.1007/s11032-009-9306-7
Joshi RK, Nayak S (2010) Gene pyramiding—a broad spectrum technique for developing durable stress resistance in crops. Biotechnol Mol Biol Rev 5(3):51–60
Kao CH, Zeng ZB, Teasdale RD (1999) Multiple interval mapping for quantitative trait loci. Genetics 152(3):1203–1216
Kasettranan W, Somta P, Srinives P (2010) Mapping of quantitative trait loci controlling powdery mildew resistance in mungbean (Vigna radiata (L.) Wilczek). J Crop Sci Biotech 13(3):155–161
Kassa MT, You FM, Hiebert CW, Pozniak CJ, Fobert PR, Sharpe AG, Menzies JG, Humphreys DG, Harrison NR, Fellers JP, McCallum BD, McCartney CA (2017) Highly predictive SNP markers for efficient selection of the wheat leaf rust resistance gene Lr16. BMC Plant Biol 17(1):45. https://doi.org/10.1186/s12870-017-0993-7
Khajudparn P (2009) Characters associated with yield potential and development of molecular markers for powdery mildew resistance in mungbean. Dissertation, Suranaree University of Technology
Khajudparn P, Prajongjai T, Poolsawat O, Tantasawat PA (2012) Application of ISSR markers for verification of F1 hybrids in mungbean (Vigna radiata). Genet Mol Res 11(2):3329–3338. https://doi.org/10.4238/2012.September.17.3
Khajudparn P, Wongkaew S, Thipyapong P (2007) Mungbean powdery mildew resistance. Identification of genes for powdery mildew resistance in mungbean. Afr Crop Sci Conf Proc 8:743–745
Kosambi DD (1994) The estimation of map distances from recombination values. Ann Eugenics 12:172–175
Lakhanpaul S, Chadha S, Bhat KV (2000) Random amplified polymorphic DNA (RAPD) analysis in Indian mungbean (Vigna radiata (L.) Wilczek) cultivars. Genetica 109(3):227–234. https://doi.org/10.1023/A:1017511918528
Levesque R, SPSS Inc (2006) SPSS programming and data management, 3rd edn. SPSS Institute, Somers, New York
Lincoln SE, Daly MJ, Lander ES (1993) Constructing genetic linkage maps with MAPMAKER/EXP version 3.0: a tutorial and reference manual. A Whitehead Institute for Biomedical Research Technical Report, 3rd edn. Cambridge, MA, USA
Liu Z, Feng S, Pandey MK, Chen X, Culbreath AK, Varshney RK, Guo B (2013) Identification of expressed resistance gene analogs from peanut (Arachis hypogaea L.) expressed sequence tags. J Int Plant Biol 55(5):453–461. https://doi.org/10.1111/jipb.12037
Mahanil S (2007) Inheritance and cloning of candidate resistance gene analogs (RGAs) for downy mildew in grapevine (Vitis spp.). Dissertation, Suranaree University of Technology
Meziadi C, Richard MMS, Derquennes A, Thareau V, Blanchet S, Gratias A, Pflieger S, Geffroy V (2016) Development of molecular markers linked to disease resistance genes in common bean based on whole genome sequence. Plant Sci 242:351–357. https://doi.org/10.1016/j.plantsci.2015.09.006
Mutlu N, Boyac FH, Göçmen M, Abak K (2008) Development of SRAP, SRAP-RGA, RAPD, and SCAR markers linked with a fusarium wilt resistance gene in eggplant. Theor Appl Genet 117(8):1303–1312. https://doi.org/10.1007/s00122-008-0864-6
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 Agr 93(8):1805–1813. https://doi.org/10.1002/jsfa.6110
Oumer A, Yohannes P, Kassahun T, Abel T, Endashaw B (2015) Inter simple sequence repeat (ISSR) analysis of Ethiopian white lupine (Lupinus albus L.) Afr J Biotechnol 14(18):1552–1563
Owens CL (2003) SNP detection and genotyping in Vitis. Acta Hort 603:139–140
Patil PG, Datta S, Agbagwa IO, Singh IP, Soren KR, Das A, Choudhary AK, Chaturvedi SK (2014) Using AFLP-RGA markers to assess genetic diversity among pigeon pea (Cajanus cajan) genotypes in relation to major diseases. Acta Bot Bras 28(2):198–205. https://doi.org/10.1590/S0102-33062014000200007
Poehlman JM (1991) The mungbean. Oxford and IBH Publishing Co., New Delhi
Sambrook J, Russell DW (2001) Molecular cloning: a laboratory manual. 3rd edn. Cold Spring Harbor Laboratory Press, Cold Spring Harbor, New York. A9.5–A9.7
Smolik M (2012) R-ISSR-tool for generation of a new type of products, applied for the identification of putative molecular marker linked to QTL determined tolerance to nutrient deprivation stress in rye (Secale cereal L.) Not Bot Horti Agrobo 40(2):238–246
Somta P, Srinives P (2007) Genome research in mungbean [Vigna radiata (L.) Wilczek] and blackgram [V. mungo (L.) Hepper]. ScienceAsia 33(Suppl 1):69–74
Soria JA, Quebral FC (1973) Occurrence and development of powdery mildew on mungbean. Philippine Agric 57:158–177
Soylu EM, Soylu S, Kurt S (2004) First report of powdery mildew caused by Podosphaera phaseoli (syn. Sphaerotheca phaseoli) on cowpea (Vigna sinensis) in Turkey. Plant Pathol 53(4):528. https://doi.org/10.1111/j.1365-3059.2004.01020.x
Sun S, Wang Z, Fu H, Duan C, Wang X, Zhu Z (2015) Resistance to powdery mildew in the pea cultivar Xucai 1 is conferred by the gene er1. The Crop J 3(6):489–499. https://doi.org/10.1016/j.cj.2015.07.006
Suneetha TB, Gopinath SM, Naik SL (2014) Identification of resistance gene analogs (RGAs) linked to powdery mildew resistance in peas. Int J Innov Res Adv Eng 1(6):33–36
Tantasawat PA, Poolsawat O, Prajongjai T, Chaowiset W, Tharapreuksapong A (2012) Association of RGA-SSCP markers with resistance to downy mildew and anthracnose in grapevines. Genet Mol Res 11(3):1799–1809. https://doi.org/10.4238/2012.July.2.1
Tantasawat P, Trongchuen J, Prajongjai T, Thongpae J, Petkhum C, Seehalak W, Machikowa T (2010) Variety identification and genetic relationships of mungbean and blackgram in Thailand based on morphological characters and ISSR analysis. Afr J Biotechnol 9(27):4452–4464
Tomooka N, Lairungreang C, Nakeeraks P, Egawa Y, Thavarasook C (1992) Center of genetic diversity and dissemination pathways in mungbean deduced from seed protein electrophoresis. Theor Appl Genet 83(3):289–293. https://doi.org/10.1007/BF00224273
Wang S, Basten CJ, Zeng ZB (2007) Windows QTL cartographer 2.5. Department of statistics, North Carolina State University, Raleigh
Yi Y, Li R, Xu H, Wu X, Li S, Zhang J, Yin Y (2013) Identification of SRAP and RGA markers linked to powdery mildew (Blumeria graminis) resistance gene PmZB90 in common wheat. Aust J Crop Sci 7(3):454–459
Young ND, Danesh D, Menancio-Hautea D, Kumar L (1993) Mapping oligogenic resistance to powdery mildew in mungbean with RFLP’s. Theor Appl Genet 87(1-2):243–249. https://doi.org/10.1007/BF00223772
Yu SC, Lin PC, Lin J (2011) Effects of extrusion processing condition on the physic-chemical properties of mungbean extrudates. Proc Asian food confer 2011, Bangkok, pp 524–526
Zhang J, Yuan Y, Niu C, Hinchliffe DJ, Lu Y, Yu S, Percy RG, Ulloa M, Cantrell RG (2007) AFLP-RGA markers in comparison with RGA and AFLP in cultivated tetraploid cotton. Crop Sci 47(1):180–187. https://doi.org/10.2135/cropsci2006.04.0249
Zhang N, BH X, Bi YF, Chen JF, Qian CT, Zhang YB, Yi HP (2017) Development of a muskmelon cultivar with improved resistance to gummy stem blight and desired agronomic traits using gene pyramiding. Czech J Genet Plant Breed 53(1):23–29. 10.17221/84/2016-CJGPB
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This work was supported by the Office of the Higher Education Commission under NRU project of Thailand and grants from Suranaree University of Technology, Thailand. We are thankful to AVRDC, Thailand, for providing the seeds of V4718 resistant line.
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Poolsawat, O., Kativat, C., Arsakit, K. et al. Identification of quantitative trait loci associated with powdery mildew resistance in mungbean using ISSR and ISSR-RGA markers. Mol Breeding 37, 150 (2017). https://doi.org/10.1007/s11032-017-0753-2
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DOI: https://doi.org/10.1007/s11032-017-0753-2