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Isolation and Characterization of NBS-Encoding Disease Resistance Gene Analogs in Watermelon against Fusarium Wilt
Fusarium wilt (Fusarium oxysporum f. sp. niveum) in watermelon is one of the deadliest diseases around the globe, and availability of disease-resistant varieties is moderate. Disease management utilizing resistance genes (R-genes)/resistance gene analogs (RGAs) has proven to be a promising and successful approach. In the present study, six watermelon RGAs were isolated from wild, fusarium wilt resistant genotype IIHR-82 (Citrullus lanatus var. citroides) using degenerate primers that identify nucleotide binding site-leucine-rich repeat (NBS–LRR) regions. Multiple sequence alignment of these RGAs identified the characteristic NBS– LRR motif, and BLASTp search revealed similarity of these RGAs with other pathogenesis-related proteins. Phylogeny and motif analysis revealed genetic diversity of RGAs within those isolated from watermelon and with other plant R-genes. The watermelon RGAs isolated in this study contained both TIR–NBS–LRR (TNL) and non-TIR–NBS–LRR (CNL) classes of Rgenes. Protein secondary structure prediction of these watermelon RGAs revealed the composition of proteins, including α -helix, β -strand, disordered region and other template-related information. Watermelon RGAs identified in the present study will help in the development of RGA-based markers for resistance to fusarium wilt of watermelon.
Keywords
Disease Management, Fusarium Wilt, Resistance Genes, Watermelon.
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- FAO, Food and Agriculture Organization of the United Nations – Statistics Division, 2016; http://www.fao.org/faostat/en/#data/QC (accessed on 23 March 2018).
- Martyn, R. D. and Netzer, D., Resistance to races 0, 1 and 2 of Fusarium wilt of watermelon in Citrullus sp. PI-296341-FR. HortScience, 1991, 26(4), 429–432.
- Gusmini, G., Song, R. and Wehner, T. C., New sources of resistance to gummy stem blight in watermelon. Crop Sci., 2005, 45(2), 582–588.
- Thies, J. A. and Levi, A., Resistance of watermelon germplasm to the peanut ischolar_main-knot nematode. HortScience, 2003, 38(7), 1417– 1421.
- Thies, J. A. and Levi, A., Characterization of watermelon (Citrullus lanatus var. citroides) germplasm for resistance to ischolar_main-knot nematodes. HortScience, 2007, 42(7), 1530–1533.
- Thomas, C. E., Levi, A. and Caniglia, E., Evaluation of US plant introductions of watermelon for resistance to powdery mildew. HortScience, 2005, 40(1), 154–156.
- Davis, A. R., Levi, A., Wehner, T. and Pitrat, M., PI 525088PMR, a melon race 1 powdery mildew-resistant watermelon line. HortScience, 2006, 41(7), 1527–1528.
- Hopkins, D. L. and Thompson, C. M., Evaluation of Citrullus sp. germ plasm for resistance to Acidovorax avenae subsp. citrulli. Plant Dis., 2002, 86, 61–64.
- Sowell Jr, G., Rhodes, B. B. and Norton, J. D., New sources of resistance to watermelon anthracnose. J. Am. Soc. Hortic. Sci., 1980, 105, 197–199.
- Provvidenti, R., Inheritance of resistance to the Florida strain of zucchini yellow mosaic virus in watermelon. HortScience, 1991, 26(4), 407–408.
- Harris, K. R., Ling, K. S., Wechter, W. P. and Levi, A., Identification and utility of markers linked to the zucchini yellow mosaic virus resistance gene in watermelon. J. Am. Soc. Hortic. Sci., 2009, 134(5), 529–534.
- Swamy, K. M. et al., Development and evaluation of an interspecific population involving Citrullus lanatus var. citroides to develop pre-bred lines for resistance to WBNV in watermelon. In VIROCON, Indian Institute of Horticultural Research, Bengaluru, 2016.
- Guner, N. and Wehner, T. C., Overview of potyvirus resistance in watermelon. In Proceedings of the IX EUCARPIA Meeting Cucurbitaceae, l’institut National de la Recherche Agronom-ique, Avignon, France, 2008.
- Levi, A., Wechter, P., Massey, L., Carter, L. and Hopkins, D., An extended genetic linkage map for watermelon based on a testcross and a BC2F2 population. Am. J. Plant Sci., 2011, 2(2), 93.
- Levi, A. et al., High frequency oligonucleotides: targeting active gene (HFO-TAG) markers revealed wide genetic diversity among Citrullus spp. accessions useful for enhancing disease or pest resistance in watermelon cultivars. Genet. Resour. Crop Evol., 2013, 60(2), 427–440.
- Egel, D. S. and Martyn, R. D., Fusarium wilt of watermelon and other cucurbits. The Plant Health Instructor, 2007; doi:10.1094/ PHI-I-2007-0122-01 (updated 2013).
- Wan, H., Yuan, W., Bo, K., Shen, J., Pang, X. and Chen, J., Genome-wide analysis of NBS-encoding disease resistance genes in Cucumis sativus and phylogenetic study of NBS-encoding genes in Cucurbitaceae crops. BMC Genomics, 2013, 14(1), 109.
- Inohara, N., Chamaillard, M., McDonald, C. and Nunez, G., NOD–LRR proteins: role in host–microbial interactions and inflammatory disease. Ann. Rev. Biochem., 2005, 74, 355–383.
- DeYoung, B. J. and Innes, R. W., Plant NBS-LRR proteins in pathogen sensing and host defense. Nature Immunol., 2006, 7, 1243–1249.
- Martin, G. B., Bogdanove, A. J. and Sessa, G., Understanding the function of plant disease resistance proteins. Annu. Rev. Plant Biol., 2003, 54, 23–61.
- Kobe, B. and Kajava, A. V., The leucine-rich repeat as a protein recognition motif. Curr. Opin. Struct. Biol., 2001, 11(6), 725– 732.
- Ellis, J. G., Lawrence, G. J., Luck, J. E. and Dodds, P. N., Identification of regions in alleles of the flax rust resistance gene L that determine differences in gene-for-gene specificity. Plant Cell, 1999, 11, 495–506.
- Luck, J. E., Lawrence, G. J., Dodds, P. N., Shepherd, K. W. and Ellis, J. G., Regions outside of the leucine-rich repeats of flax rust resistance proteins play a role in specificity determination. Plant Cell, 2000, 12, 1367–1377.
- Meyers, B. C., Dickerman, A. W., Michelmore, R. W., Sivaramakrishnan, S., Sobral, B. W. and Young, N. D., Plant disease resistance genes encode members of an ancient and diverse protein family within the nucleotide‐binding superfamily. Plant J., 1999, 20(3), 317–332.
- Sekhwal, M. K., Li, P., Lam, I., Wang, X., Cloutier, S. and You, F. M., Disease resistance gene analogs (RGAs) in plants. Int. J. Mol. Sci., 2015, 16(8), 19248–19290.
- Harris, K. R., Wechter, W. P. and Levi, A., Isolation, sequence analysis, and linkage mapping of nucleotide binding site–leucinerich repeat disease resistance gene analogs in watermelon. J. Am. Soc. Hortic. Sci., 2009, 134(6), 649–657.
- Lin, X., Zhang, Y., Kuang, H. and Chen, J., Frequent loss of lineages and deficient duplications accounted for low copy number of disease resistance genes in Cucurbitaceae. BMC Genomics, 2013, 14, 335.
- Ori, N. et al., The I2C family from the wilt disease resistance locus I2 belongs to the nucleotide binding, leucine-rich repeat superfamily of plant resistance genes. Plant Cell, 1997, 9(4), 521– 532.
- Simons, G. et al., Dissection of the Fusarium I2 gene cluster in tomato reveals six homologs and one active gene copy. Plant Cell, 1998, 10(6), 1055–1068.
- McGrath, D. J., Gillespie, D. and Vawdrey, L., Inheritance of resistance to Fusarium oxysporum f. sp. lycopersici races 2 and 3 in Lycopersicon pennellii. Aust. J. Agric. Res., 1997, 38, 729–733.
- Scott, J. W. and Jones, J. P., Monogenic resistance in tomato to Fusarium oxysporum f. sp. lycopersici race 3. Euphytica, 1989, 40, 49–53.
- Catanzariti, A. M., Lim, G. T. and Jones, D. A., The tomato I‐3 gene: a novel gene for resistance to Fusarium wilt disease. New Phytol., 2015, 207(1), 106–118.
- Diener, A. C. and Ausubel, F. M., Resistance to Fusarium oxysporum 1, a dominant Arabidopsis disease-resistance gene, is not race specific. Genetics, 2005, 171(1), 305–321.
- Wechter, W. P., Kousik, C., McMillan, M. and Levi, A., Identification of resistance to Fusarium oxysporum f. sp. niveum race 2 in Citrullus lanatus var. citroides plant introductions. HortScience, 2012, 47(3), 334–338.
- Murray, M. G. and Thompson, W. R., Rapid isolation of high molecular weight plant DNA. Nucl. Acids Res., 1980, 8, 4321– 4325.
- Reddy, A. C., Venkat, S., Singh, T. H., Aswath, C., Reddy, K. M. and Reddy, D. L., Isolation, characterization and evolution of NBS–LRR encoding disease-resistance gene analogs in eggplant against bacterial wilt. Eur. J. Plant Pathol., 2015, 143(3), 417– 426.
- Bailey, T. L. et al., MEME SUITE: tools for motif discovery and searching. Nucleic Acids Res., 2009, 37, W202–W208.
- Kumar, S., Stecher, G. and Tamura, K., MEGA7: molecular evolutionary genetics analysis version 7.0 for bigger datasets. Mol. Biol. Evol., 2016, 33(7), 1870–1874.
- Kelley, L. A., Mezulis, S., Yates, C. M., Wass, M. N. and Sternberg, M. J., The Phyre2 web portal for protein modeling, prediction and analysis. Nature Proto., 2015, 10(6), 845–858.
- Koonin, E. V., Wolf, Y. I. and Karev, G. P., The structure of the protein universe and genome evolution. Nature, 2002, 420(6912), 218.
- Shao, M., Wang, S. and Wang, C., Incorporating ab initio energy into threading approaches for protein structure prediction. BMC Bioinfor. (Suppl 1), 2011, 12, S54.
- Zviling, M., Kochva, U. and Arkin, I. T., How important are transmembrane helices of bitopic membrane proteins? Biochim. Biophys. Acta (BBA)-Biomembr., 2007, 1768(3), 387–392.
- Bryan, G. T. et al., A single amino acid difference distinguishes resistant and susceptible alleles of the rice blast resistance gene Pi-ta. Plant Cell, 2000, 12(11), 2033–2045.
- Okuyama, Y. et al., A multifaceted genomics approach allows the isolation of the rice Pia‐blast resistance gene consisting of two adjacent NBS–LRR protein genes. Plant J., 2011, 66(3), 467– 479.
- Tan, X. et al., Global expression analysis of nucleotide binding site–leucine-rich repeat-encoding and related genes in Arabidopsis. BMC Plant Biol., 2007, 7(1), 56.
- Borhan, M. H., Gunn, N., Cooper, A., Gulden, S., Tör, M., Rimmer, S. R. and Holub, E. B., WRR4 encodes a TIR–NB–LRR protein that confers broad-spectrum white rust resistance in Arabidopsis thaliana to four physiological races of Albugo candida. Mol. Plant–Microb. Interact., 2008, 21(6), 757–768.
- Zhang, C. et al., The Ph-3 gene from Solanum pimpinellifolium encodes CC–NBS–LRR protein conferring resistance to Phytophthora infestans. Theoret. Appl. Genet., 2014, 127(6), 1353– 1364.
- Daryono, B. S., Wakui, K. and Natsuaki, K. T., Linkage analysis and mapping of SCAR markers linked to CMV-B2 resistance gene in melon. SABRAO J. Breed. Genet., 2010, 42(1), 35–45.
- Wan, H. et al., Analysis of TIR- and non-TIR–NBS–LRR disease resistance gene analogous in pepper: characterization, genetic variation, functional divergence and expression patterns. BMC Genomics, 2012, 13(1), 502.
- Naresh, P., Reddy, M. K., Reddy, A. C., Lavanya, B., Reddy, D. L. and Reddy, K. M., Isolation, characterization and genetic diversity of NBS–LRR class disease-resistant gene analogs in multiple virus resistant line of chilli (Capsicum annuum L.). 3 Biotech, 2017, 7(2), 114.
- Guo, S. et al., The draft genome of watermelon (Citrullus lanatus) and resequencing of 20 diverse accessions. Nature Genet., 2013, 45(1), 51.
- Lambel, S. et al., A major QTL associated with Fusarium oxysporum race 1 resistance identified in genetic populations derived from closely related watermelon lines using selective genotyping and genotyping-by-sequencing for SNP discovery. Theoret. Appl. Genet., 2014, 127(10), 2105–2115.
- Joobeur, T., King, J. J., Nolin, S. J., Thomas, C. E. and Dean, R. A., The fusarium wilt resistance locus Fom-2 of melon contains a single resistance gene with complex features. Plant J., 2004, 39(3), 283–297.
- Tezuka, T., Waki, K., Yashiro, K., Kuzuya, M., Ishikawa, T., Takatsu, Y. and Miyagi, M., Construction of a linkage map and identification of DNA markers linked to Fom-1, a gene conferring resistance to Fusarium oxysporum f. sp. melonis race 2 in melon. Euphytica, 2009, 168(2), 177.
- Okubara, P. A., Keller, K. E., McClendon, M. T., Inglis, D. A., McPhee, K. E. and Coyne, C. J., Y15_999Fw, a dominant SCAR marker linked to the Fusarium wilt race 1 (Fw) resistance gene in pea. Pisum Genet., 2005, 37, 30–33.
- Donald, T. M., Pellerone, F., Adam-Blondon, A. F., Bouquet, A., Thomas, M. R. and Dry, I. B., Identification of resistance gene analogs linked to a powdery mildew resistance locus in grapevine. Theoret. Appl. Genet., 2002, 104, 610–618.
- Wan, H., Zhao, Z., Malik, A. A., Qian, C. and Chen, J., Identification and characterization of potential NBS-encoding resistance genes and induction kinetics of a putative candidate gene associated with downy mildew resistance in Cucumis. BMC Plant Biol., 2010, 10, 186.
- Joshi, R. K., Mohanty, S., Subudhi, E. and Nayak, S., Isolation and characterization of NBS–LRR-resistance gene candidates in turmeric (Curcuma longa cv. surama). Genet. Mol. Res., 2010, 9, 1796–1806.
- Aarts, N., Metz, M., Holub, E., Staskawicz, B. J., Daniels, M. J. and Parker, J. E., Different requirements for EDS1 and NDR1 by disease resistance genes define at least two R genemediated signaling pathways in Arabidopsis. Proc. Natl. Acad. Sci. USA, 1998, 95, 10306–10311.
- Speulman, E., Bouchez, D., Holub, E. B. and Beynon, J. L., Disease resistance gene homologs correlate with disease resistance loci of Arabidopsis thaliana. Plant J., 1998, 14(4), 467–474.
- Noir, S., Combes, M.-C., Anthony, F. and Lashermes, P., Origin, diversity, and evolution of NBS-type disease-resistance gene homologues in coffee trees (Coffea L.). Mol. Genet. Genom., 2001, 265, 654–662.
- Deng, Z. et al., Cloning and characterization of NBS–LRR class resistance gene candidate sequences in citrus. Theoret. Appl. Genet., 2000, 101, 814–822.
- Zhang, L., Chen, R., Zhang, J., Ouyang, B., Xiao, J., Li, H. and Ye, Z., Cloning and analysis of resistance gene analogs from pepper (Capsicum annuum L.). Sci. Agric. Sin., 2008, 41(1), 169– 175.
- Chen, X. M., Line, R. F. and Leung, H., Genome scanning for resistancegene analogs in rice, barley, and wheat by high-resolution electrophoresis. Theoret. Appl. Genet., 1998, 97(3), 345–355.
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