Abstract
Conserved domains or motifs shared by most known resistance (R) genes have been extensively exploited to identify unknown R-gene analogs (RGAs). In an attempt to isolate all potential RGAs from the maize genome, we adopted the following three methods: modified amplified fragment length polymorphism (AFLP), modified rapid amplification of cDNA ends (RACE), and data mining. The first two methods involved PCR-based isolations of RGAs with degenerate primers designed based on the conserved NBS domain; while the third method involved mining of RGAs from the maize EST database using full-length R-gene sequences. A total of 23 and 12 RGAs were obtained from the modified AFLP and RACE methods, respectively; while, as many as 109 unigenes and 77 singletons with high homology to known R-genes were recovered via data-mining. Moreover, R-gene-like ESTs (or RGAs) identified from the data-mining method could cover all RACE-derived RGAs and nearly half AFLP-derived RGAs. Totally, the three methods resulted in 199 non-redundant RGAs. Of them, at least 186 were derived from putative expressed R-genes. RGA-tagged markers were developed for 55 unique RGAs, including 16 STS and 39 CAPS markers.
Similar content being viewed by others
References
Bent AF, Kunkel BN, Dahlbeck D, Brown KL, Schmidt R, Giraudat J, Leung J, Staskawicz BJ (1994) RPS2 of Arabidopsis thaliana: a leucine-rich repeat class of plant disease resistance gene. Science 265:1856–1860
Botella MA, Coleman MJ, Hughes DE, Nishimura MT, Jones JDG, Somerville SC (1997) Map positions of 47 Arabidopsis sequences with sequence similarity to disease resistance genes. Plant J 12:1197–1211
Brueggeman R, Rostoks N, Kudrna D, Kilian A, Han F, Chen J, Druka A, Steffenson B, Kleinhofs A (2002) The barley stem rust-resistance gene Rpg1 is a novel disease-resistance gene with homology to receptor kinases. Proc Natl Acad Sci USA 99:9328–9333
Brutnell TP (2002) Transposon tagging in maize. Funct Integr Genomics 2:4–12
Buschges R, Hollricher K, Panstruga R, Simons G, Wolter M, Frijters A, van Daelen R, van der Lee T, Diergaarde P, Groenendijk J, Topsch S, Vos P, Salamini F, Schulze-Lefert P (1997) The barley Mlo gene: a novel control element of plant pathogen resistance. Cell 88:695–705
Chen BJ, Ling XY (1996) Extraction genome DNA from Z. mays. J Anhui Agro tech Normal School 10:27–28
Collins NC, Webb CA, Seah S, Ellis JG, Hulbert SH, Pryor A (1998) The isolation and mapping of disease resistance gene analogs in maize. Mol Plant Microbe Interact 11:968–978
Collins N, Drake J, Ayliffe M, Sun Q, Ellis J, Hulbert S, Pryor T (1999) Molecular characterization of the maize Rp1-D rust resistance haplotype and its mutants. Plant Cell 11:1365–1376
Collins N, Park R, Spielmeyer W, Ellis J, Pryor AJ (2001) Resistance gene analogs in barley and their relationship to rust resistance genes. Genome 44:375–381
Cooley MB, Pathirana S, Wu HJ, Kachroo P, Klessig DF (2000) Members of the Arabidosis HRT/RPP8 family of resistance gene confer resistance to both viral and oomycete pathogens. Plant cell 12:663–676
Dilbirligi M, Gill KS (2003) Identification and analysis of expressed resistance gene sequences in wheat. Plant Mol Biol 53:771–787
Dilbirligi M, Erayman M, Sandhu D, Sidhu D, Gill KS (2004) Identification of wheat chromosomal regions containing expressed resistance genes. Genetics 166:461–481
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 11:45–52
Frye CA, Innes RW (1998) An Arabidopsis mutant with enhanced resistance to powdery mildew. Plant Cell 10:947–956
Graham MA, Marek LF, Lohnes D, Cregan P, Shoemaker RC (2000) Expression and genome organization of resistance gene analogs in soybean. Genome 43:86–93
Hulbert SH, Webb CA, Smith SM, Sun Q (2001) Resistance gene complexes: evolution and utilization. Annu Rev Phytopathol 39:285–312
Hunger S, Gaspero GD, Mohring S, Bellin D, Schafer-Pregl R, Borchardt DC, Durel CE, Werber M, Weisshaar B, Salamini F, Schneider K (2003) Isolation and linkage analysis of expressed disease-resistance gene analogues of sugar beet (Beta vulgaris L.). Genome 46:70–82
Johal GS, Briggs SP (1992) Reductase activity encoded by the Hm1 disease resistance gene in maize. Science 258:985–987
Jones DA, Thomas CM, Hammond-Kosack KE, Balint-Kurti PJ, Jones JD (1994) Isolation of the tomato Cf-9 gene for resistance to Cladosporium fulvum by transposon tagging. Science 266:789–793
Kaloshian I, Yaghoobi J, Liharska T, Hontelez J, Hanson D, Hogan P, Jesse T, Wijbrandi J, Simons G, Vos P, Zabel P, Williamson VM (1998) Genetic and physical localization of the root-knot nematode locus Mi in tomato. Mol Gen Genet 257:376–385
Kanazin V, Marek LF, Shoemaker RC (1996) Resistance gene analogs are conserved and clustered in soybean. Proc Natl Acad Sci USA 93:11746–11750
Kim MC, Panstruga R, Elliott C, Muller J, Devoto A, Yoon HW, Park HC, Cho MJ, Schulze-Lefert P (2002) Calmodulin interacts with MLO protein to regulate defense against mildew in barley. Nature 416:447–451
Lawrence GJ, Finnegan EJ, Ayliffe MA, Ellis JG (1995) The L6 gene for flax rust resistance is related to the Arabidopsis bacterial resistance gene RPS2 and tobacco viral resistance gene N. Plant Cell 7:1195–1206
Leister D, Kurth J, Laurie DA, Yano M, Sasaki T, Graner A, Schulze-Lefert P (1999) RFLP and physical mapping of resistance gene homologues in rice (O. sativa) and barley (H. vulgare). Theor Appl Genet 98:509–520
Liu JJ, Ekramoddoullah AKM (2004) Isolation, genetic variation and expression of TIR-NBS-LRR resistance gene analogs from western white pine (Pinus monticola Dougl. ex. D. Don.). Mol Genet Genomics 270:432–441
Liu GZ, Pi LY, Walker JC, Ronald PC, Song WY (2002) Biochemical characterization of the kinase domain of the rice disease resistance receptor-like kinase Xa21. J Biol Chem 277:20264–20269
Madsen LH, Collins NC, Rakwalska M, Backes G, Sandal N, Krusell L, Jensen J, Waterman EH, Jahoor A, Ayliffe M, Pryor AJ, Langridge P, Schulze-Lefert P, Stougaard J (2003) Barley disease resistance gene analogs of the NBS-LRR class: identification and mapping. Mol Genet Genomics 269:150–161
Martin GB, Brommonschenkel SH, Chunwongse J, Frary A, Ganal MW, Spivey R, Wu T, Earle ED, Tanksley SD (1993) Map-based cloning of a protein kinase gene conferring disease resistance in tomato. Science 262:1432–1436
Meyers BC, Dickerman AW, Michelmore RW, Sivaramakrishnan S, Sobral BW, Young ND (1999) Plant disease resistance genes encode members of an ancient and diverse protein family within the nucleotide-binding superfamily. Plant J 20:317–332
Meyers BC, Kozik A, Griego A, Kuang H, Michelmore RW (2003) Genome-wide analysis of NBS-LRR-encoding genes in Arabidopsis. Plant cell 15:809–834
Mindrinos M, Katagiri F, Yu GL, Ausubel FM (1994) The A. thaliana disease resistance rene RPS2 encodes a protein containing a nucleotide-binding site and leucine-rich repeats. Cell 78:1089–1099
Monosi B, Wisser RJ, Pennill L, Hulbert SH (2004) Full-genome analysis of resistance gene homologues in rice. Theor Appl Genet 109:1434–1447
Pan QL, Wendel J, Fluhr R (2000) Divergent evolution of plant NBS-LRR resistance gene homologues in dicot and cereal genomes. J Mol Evol 50:203–213
Quint M, Dußle CM, Melchinger AE, Lübberstedt T (2003) Identification of genetically linked RGAs by BAC screening in maize and implications for gene cloning, mapping and MAS. Theor Appl Genet 106:1171–1177
Rafalski A (2002) Applications of single nucleotide polymorphisms in crop genetics. Curr Opin Plant Biol 5:94–100
Rossi M, Araujo PG, Paulet F, Garsmeur O, Dias VM, Chen H, Van Sluys MA, D’Hont A (2003) Genomic distribution and characterization of EST-derived resistance gene analogs (RGAs) in sugarcane. Mol Gen Genomics 269:406–419
Shen KA, Chin DB, Arroyo-Garcia R, Ochoa OE, Lavelle DO, Wroblewski T, Meyers BC, Michelmore RW (2002) Dm3 is one member of a large constitutively expressed family of nucleotide binding site-leucine-rich repeat encoding genes. Mol Plant Microbe Interact 15:251–261
Song WY, Wang GL, Chen LL, Kim HS, Pi LY, Holsten T, Gardner J, Wang B, Zhai WX, Zhu LH, Fauquet C, Ronald P (1995) A receptor kinase-like protein encoded by the rice disease resistance gene, Xa21. Science 270:1804–1806
The Arabidopsis Genome Initiative (2000) Analysis of the genome sequence of the flowering plant Arabidopsis thaliana. Nature 408:796–815
Thomas CM, Jones DA, Parniske M, Harrison K, Balint-Kurti PJ, Hatzixanthis K, Jones JDG (1997) Characterization of the tomato Cf-4 gene for resistance to Cladosporium fulvum identifies sequences that determine recognitional specificity in Cf-4 and Cf-9. Plant Cell 9:2209–2224
Traut TW (1994) The functions and consensus motifs of nine types of peptide segments that form different types of nucleotide-binding sites. Eur J Biochem 222:9–19
Wang ZX, Yano M, Yamanouchi U, Iwamoto M, Monna L, Hayasaka H, Katayose Y, Sasaki T (1999) The Pib gene for rice blast resistance belongs to the nucleotide binding and leucine-rich repeat class of plant disease resistance genes. Plant J 19:55–64
Wang Z, Taramino G, Yang D, Liu G, Tingey SV, Miao GH, Wang GL (2001) Rice ESTs with disease-resistance gene or defense response gene-like sequences mapped to regions containing major resistance genes or QTLs. Mol Genet Genomics 265:302–310
Webb CA, Richter TE, Collins NC, Nicolas M, Trick HN, Pryor T, Hulbert SH (2002) Genetic and molecular characterization of the Maize rp3 rust resistance locus. Genetics 162:381–394
Whitham S, Dinesh-Kumar SP, Choi D, Hehl R, Corr C, Baker B (1994) The product of the tobacco mosaic virus resistance gene N: similarity to toll and the interleukin-1 receptor. Cell 78:1101–1115
Xu ML, Melchinger AE, Xia XC, Luebberstedt T (1999) High-resolution mapping of loci conferring resistance to sugarcane mosaic virus in maize using RFLP, SSR, and AFLP markers. Mol Gen Genet 261:574–581
Yoshimura S, Yamanouchi U, Katayose Y, Toki S, Wang ZX, Kono I, Kurata N, Yano M, Iwata N, Sasaki T (1998) Expression of Xa1, a bacterial blight resistance gene in rice, is induced by bacterial inoculation. Proc Natl Acad Sci USA 95:1663–1668
Yu J, Hu SN, Wang J, Wong GKS, Li SG, Liu B, Deng YJ, Dai L, Zhou Y, Zhang XQ, Cao ML, Liu J, Sun JD, Tang JB, Chen YJ, Huang XB, Lin WY, Tong W, Cong LJ, Geng JN, Han YJ, Li L, Li W, Hu GQ, Huang XG, Li WJ, Li J, Liu ZW, Liu JP, Qi QH, Liu JS, Li T, Wang XG, Lu H, Wu TT, Zhu M, Ni PX, Han H, Dong W, Ren XY, Feng XL, Cui P, Li XR, Wang H, Xu X, Zhai WX, Xu Z, Zhang JS, He SJ, Zhang JG, Xu JC, Zhang KL, Zheng XW, Dong JH, Zeng WY, Tao LY, Tan J, Ren XD, Chen XW, He J, Liu DF, Tian W, Tian CG, Xia HG, Bao QY, Li G, Gao H, Cao T, Zhao WM, Li P, Chen W, Wang XD, Zhang Y, Hu JF, Liu S, Yang J, Zhang GY, Xiong YQ, Li ZJ, Mao L, Zhou CS, Zhu Z, Chen RS, Hao BL, Zheng WM, Chen SY, Guo W, Li GJ, Liu SQ, Tao M, Zhu LH, Yuan LP, Yang HM (2002) A draft sequence of the rice genome (Oryza sativa L. ssp indica). Science 296:79–92
Acknowledgments
This study was financially supported by the national outstanding youth foundation of China, the talent people’s foundation of China Agricultural University, and the Beijing Agricultural Innovative Platform—Beijing Natural Science Fund Program, ‘Construction of the standard DNA fingerprint database for Chinese maize germplasm and study on innovative fingerprinting techniques’.
Author information
Authors and Affiliations
Corresponding author
Additional information
Communicated by T. Lübberstedt
Rights and permissions
About this article
Cite this article
Wenkai, X., Mingliang, X., Jiuren, Z. et al. Genome-wide isolation of resistance gene analogs in maize (Zea mays L.). Theor Appl Genet 113, 63–72 (2006). https://doi.org/10.1007/s00122-006-0272-8
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00122-006-0272-8