Skip to main content
Log in

Genome-scale identification of resistance gene analogs and the development of their intron length polymorphism markers in maize

  • Published:
Molecular Breeding Aims and scope Submit manuscript

Abstract

As introns are vulnerable to changes such as insertions and deletions when exposed to various evolutionary forces, they constitute a repository for developing genetic markers based on intron length polymorphisms (ILP). This study developed a set of genetic markers that use the potential intron length polymorphism in resistance gene analogs (RGAs) in Zea mays. By searching the genome of Zea mays B73 for the homologs of 73 R genes which have already been identified in plants, we found 861 RGAs, 632 of which have at least one intron that can serve as putative markers targeting the intron length polymorphism in RGAs (RGA-ILP). We developed 1972 candidate markers via electronic PCR (e-PCR) with primer pairs designed in each pair of exonic regions that flank an intron. Furthermore, the performance of RGA-ILP among four maize inbred lines (Huangzao4, B73, Mo17, and Dan340) was evaluated with 69 pairs of randomly selected primers. Of them, 46.4% showed bands that had discriminating length polymorphism, and between any two of the inbred lines the proportion of polymorphism ranged from 23.2 to 31.9%. To make it convenient to use these markers for those interested in molecular breeding of disease-resistant maize, we provide all related information in a web-based database named MaizeRGA, which is available at http://www.sicau.edu.cn/web/yms/rga/maizeRGA.html.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2

Similar content being viewed by others

References

  • Altschul SF, Madden TL, Schaffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucl Acids Res 25:3389–3402

    Article  PubMed  CAS  Google Scholar 

  • Anderson JA, Churchill GA, Autrique JE, Tanksley SD, Sorrells ME (1993) Optimizing parental selection for genetic linkage maps. Genome 36:181–186

    Article  PubMed  CAS  Google Scholar 

  • Ayliffe MA, Lagudah ES (2004) Molecular genetics of disease resistance in cereals. Ann Bot 94:765–773

    Article  PubMed  CAS  Google Scholar 

  • Balint-Kurti PL, Johal GS (2009) Maize disease resistance. In: Bennetzen JL, Hake SC (eds) Handbook of maize: its biology. Springer, New York, pp 229–250

    Chapter  Google Scholar 

  • Bentolila S, Guitton C, Bouvet N, Sailland A, Nykaza S, Freyssinet G (1991) Identification of an RFLP marker tightly linked to the Ht1 gene in maize. Theor Appl Genet 82:393–398

    Article  CAS  Google Scholar 

  • Chung CL, Jamann T, Longfello J, Nelson R (2010) Characterization and fine-mapping of a resistance locus for northern leaf blight in maize bin 8.06. Theor Appl Genet 121:205–227

    Article  PubMed  CAS  Google Scholar 

  • Collins NC, Webb CA, Seah S, Ellis JG, Hulbert SH, Pryor A (1998) The isolation and mapping of disease resistance gene analogs in maize. MPMI 10:968–978

    Article  Google Scholar 

  • Collins N, Drake J, Ayliffe M, Sun Q, Ellis J, Hulbert S, Tony P (1999) Molecular characterization of the maize Rp1-D rust resistance haplotype and its mutants. Plant Cell 11:1365–1376

    Article  PubMed  CAS  Google Scholar 

  • Dangl JL, Jones JDG (2001) Plant pathogens and integrated defence responses to infection. Nature 411:826–833

    Article  PubMed  CAS  Google Scholar 

  • Dangl JL, Jones JDG (2006) The plant immune system. Nature 444:323–329

    Article  PubMed  Google Scholar 

  • Delorenzi M, Speed T (2002) An HMM model for coiled-coil domains and a comparison with PSSM-based predictions. Bioinformatics 18:617–625

    Article  PubMed  CAS  Google Scholar 

  • Duble CM, Melchinger AE, Kuntze L, Stork A, Lübberstedt T (2000) Molecular mapping and gene action of Scm1 and Scm2, two major QTL contributing to SCMV resistance in maize. Plant Breed 119:299–303

    Article  Google Scholar 

  • Eddy SR (1998) Profile hidden Markov models. Bioinformatics 14:755–763

    Article  PubMed  CAS  Google Scholar 

  • Edwards MD, Helentjaris T, Wright S, Stuber CW (1992) Molecular-marker-facilitated investigations of quantitative trait loci in maize. Theor Appl Genet 83:765–774

    Article  CAS  Google Scholar 

  • Fan XM, Tan J, Zhang SH, Li MS, Huang YX, Yang JY, Peng ZB, Li XH (2003) Heterotic grouping for 25 tropical maize inbreds and 4 temperate maize inbreds by SSR markers. Acta Agron Sin 29:835–840

    Google Scholar 

  • Feltus FA, Singh HP, Lohithaswa HC, Schulze SR, Silva TD, Paterson AH (2006) A comparative genomics strategy for targeted discovery of single-nucleotide polymorphisms and conserved-noncoding sequences in orphan crops. Plant Physiol 140:1183–1191

    Article  PubMed  CAS  Google Scholar 

  • Finn RD, Tate J, Mistry J, Coggill PC, Sammut JS, Hotz HR, Ceric G, Forslund K, Eddy SR, Sonnhammer EL, Bateman A (2008) The Pfam protein families database. Nucl Acids Res 36:D281–D288

    Article  PubMed  CAS  Google Scholar 

  • Florea L, Hartzell G, Zhang Z, Rubin GM, Miller W (1998) A computer program for aligning a cDNA sequence with a genomic DNA sequence. Genome Res 8:967–974

    PubMed  CAS  Google Scholar 

  • Gore MA, Chia JM, Elshire RJ, Sun Q, Ersoz ES, Hurwitz BL, Peiffer JA, McMullen MD, Grills GS, Ross-Ibarra J, Ware DH, Buckler ES (2009) A first-generation haplotype map of maize. Science 326:1115–1117

    Article  PubMed  CAS  Google Scholar 

  • Gou MY, Su N, Zheng J, Huai JL, Wu GH, Zhao JF, He JG, Tang DZ, Yang SH, Wang GY (2009) An F-box gene, CPR30, functions as a negative regulator of the defense response in Arabidopsis. Plant J 60:757–770

    Article  PubMed  CAS  Google Scholar 

  • Hammond-Kosack KE, Jones JDG (1997) Plant disease resistance genes. Annu Rev Plant Biol 48:575–607

    Article  CAS  Google Scholar 

  • Ingvardsen CR, Xing YZ, Frei UK, Lübberstedt T (2010) Genetic and physical fine mapping of Scmv2, a potyvirus resistance gene in maize. Theor Appl Genet 120:1621–1634

    Article  PubMed  Google Scholar 

  • Jiang L, Ingvardsen CR, Lübberstedt T, Xu ML (2008) The Pic19 NBS-LRR gene family members are closely linked to Scmv1, but not involved in maize resistance to sugarcane mosaic virus. Genome 51:673–684

    Article  PubMed  CAS  Google Scholar 

  • Jones JDG (2001) Putting knowledge of plant disease resistance genes to work. Curr Opin Plant Biol 4:281–287

    Article  PubMed  CAS  Google Scholar 

  • Marsan PA, Gorni C, Chitto A, Redaelli R, Vijk RV, Stam P, Motto M (2001) Identification of QTLs for grain yield and grain-related traits of maize (Zea mays L.) using an AFLP map, different testers, and cofactor analysis. Theor Appl Genet 102:230–243

    Article  CAS  Google Scholar 

  • 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

    Article  PubMed  CAS  Google Scholar 

  • Meyers BC, Kaushik S, Nandety RS (2005) Evolving disease resistance genes. Curr Opin Plant Biol 8:129–134

    Article  PubMed  CAS  Google Scholar 

  • Ming R, Brewbaker JL, Pratt RC, Musket TA, McMullen MD (1997) Molecular mapping of a major gene conferring resistance to maize mosaic virus. Theor Appl Genet 95:271–275

    Article  CAS  Google Scholar 

  • Moller S, Croning MDR, Apweiler R (2001) Evaluation of methods for the prediction of membrane spanning regions. Bioinformatics 17:646–653

    Article  PubMed  CAS  Google Scholar 

  • Monosi B, Wisser RJ, Pennill L, Hulbert SH (2004) Full-genome analysis of resistance gene homologues in rice. Theor Appl Genet 109:1434–1447

    Article  PubMed  CAS  Google Scholar 

  • Pflieger S, Lefebvre V, Causse M (2001) The candidate gene approach in plant genetics: a review. Mol Breed 7:275–291

    Article  CAS  Google Scholar 

  • Poland JA, Balint-Kurti PJ, Wisser RJ, Pratt RC, Nelson RJ (2009) Shades of gray: the world of quantitative disease resistance. Trends Plant Sci 14:21–29

    Article  PubMed  CAS  Google Scholar 

  • Quint M, Mihaljevic R, Dussle CM, Xu ML, Melchinger AE, Lübberstedt T (2002) Development of RGA-CAPS markers and genetic mapping of candidate genes for sugarcane mosaic virus resistance in maize. Theor Appl Genet 105:355–363

    Article  PubMed  CAS  Google Scholar 

  • Ramakrishna W, Emberton J, SanMiguel P, Ogden M, Llaca V, Messing J, Bennetzen JL (2002) Comparative sequence analysis of the sorghum Rph region and the maize Rp1 resistance gene complex. Plant Physiol 130:1728–1738

    Article  PubMed  CAS  Google Scholar 

  • Ribaut JM, Betran J (1999) Single large-scale marker-assisted selection (SLS-MAS). Mol Breed 5:531–541

    Article  Google Scholar 

  • Rozen S, Skaletsky H (2000) Primer3 on the WWW for general users and for biologist programmers. Methods Mol Biol 132:365–386

    PubMed  CAS  Google Scholar 

  • Sanseverino W, Roma G, Simone MD, Faino L, Melito S, Stupka E, Frusciante L, Ercolano MR (2009) PRGdb: a bioinformatics platform for plant resistance gene analysis. Nucl Acids Res 38:D814–D821

    Article  PubMed  Google Scholar 

  • Sanz-Alferez S, Richter TE, Hulbert SH, Bennetzen JL (1995) The Rp3 disease resistance gene of maize: mapping and characterization of introgressed alleles. Theor Appl Genet 91:25–32

    Article  CAS  Google Scholar 

  • Schnable PS, Ware D, Fulton RS et al (2009) The B73 Maize genome: complexity, diversity, and dynamics. Science 326:1112–1115

    Article  PubMed  CAS  Google Scholar 

  • Schuler GD (1997) Sequence mapping by electronic PCR. Genome Res 7:541–550

    PubMed  CAS  Google Scholar 

  • Shang W, Zhou RH, Jia JZ, Gao LF (2010) RGA-ILP, a new type of functional molecular markers in bread wheat. Euphytica 172:263–273

    Article  CAS  Google Scholar 

  • Wang XS, Wu WR, Jin GL, Zhu J (2005a) Genome-wide identification of R genes and exploitation of candidate RGA markers in rice. Chin Sci Bull 50:1120–1125

    Article  Google Scholar 

  • Wang XS, Zhao XQ, Zhu J, Wu WR (2005b) Genome-wide investigation of intron length polymorphisms and their potential as molecular markers in rice (Oryza sativa L.). DNA Res 12:417–427

    Article  PubMed  CAS  Google Scholar 

  • Wei H, Fu Y, Arora R (2005) Intron-flanking EST-PCR markers: from genetic marker development to gene structure analysis in Rhododendron. Theor Appl Genet 111:1347–1356

    Article  PubMed  CAS  Google Scholar 

  • Welz HG, Schechert A, Pernet A, Pixley KV, Geiger HH (1998) A gene for resistance to the maize streak virus in the African CIMMYT maize inbred line CML202. Mol Breed 4:147–154

    Article  CAS  Google Scholar 

  • Wisser RJ, Balint-Kurti PJ, Nelson RJ (2006) The genetic architecture of disease resistance in maize: a synthesis of published studies. Phytopathology 96:120–129

    Article  PubMed  CAS  Google Scholar 

  • Xiao WK, Xu ML, Zhao JR, Wang FG, Li JS, Dai JR (2006) Genome-wide isolation of resistance gene analogs in maize (Zea mays L.). Theor Appl Genet 113:63–72

    Article  CAS  Google Scholar 

  • Xiao WK, Zhao J, Fan SC, Li L, Dai JR, Xu ML (2007) Mapping of genome-wide resistance gene analogs (RGAs) in maize (Zea mays L.). Theor Appl Genet 115:501–508

    Article  PubMed  CAS  Google Scholar 

  • Xu ML, Melchinger AE, Xia XC, Lübberstedt T (1999) High-resolution mapping of loci conferring resistance to sugarcane mosaic virus in maize using RFLP, SSR, and AFLP markrs. Mol Gen Genet 261:574–581

    Article  PubMed  CAS  Google Scholar 

  • Xu ML, Melchinger AE, Lübberstedt T (2000) Origin of Scm1 and Scm2-two loci conferring resistance to sugarcane mosaic virus (SCMV) in maize. Theor Appl Genet 100:934–941

    Article  CAS  Google Scholar 

  • Yang L, Jin GL, Zhao XQ, Zheng Y, Xu ZH, Wu WR (2007) PIP: a database of potential intron polymorphism markers. Bioinformatics 23:2174–2177

    Article  PubMed  CAS  Google Scholar 

  • Zhang LQ, Peek AS, Dunams D, Gaut BS (2002) Population genetics of duplicated disease-defense genes, hm1 and hm2, in maize (Zea mays ssp. mays L.) and its wild ancestor (Zea mays ssp. parviglumis). Genetics 162:851–860

    PubMed  CAS  Google Scholar 

  • Zhou T, Wang Y, Chen JQ, Araki H, Jing Z, Jiang K, Shen J, Tian D (2004) Genome-wide identification of NBS genes in japonica rice reveals significant expansion of divergent non-TIR NBS-LRR genes. Mol Gen Genet 271:402–415

    CAS  Google Scholar 

Download references

Acknowledgments

We thank Dr. Chen Guoyue from the Triticeae Research Institute of Sichuan Agricultural University for helpful discussions during this study. The authors thank two anonymous reviewers and Dr Yann Klimentidis for critical reading. This work is supported by the grants from National Natural Science Foundation of China (No.30800687 and 31071434), Applied Basic Research Program of Sichuan Provincial Science and Technology Department (No.2008JY0096), and the ‘863’ High Technology Development Program (No.2009AA10AA03_2).

Author information

Authors and Affiliations

Authors

Corresponding authors

Correspondence to Hailan Liu or Suzhi Zhang.

Additional information

H. Liu and Y. Lin have contributed equally to this work.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Liu, H., Lin, Y., Chen, G. et al. Genome-scale identification of resistance gene analogs and the development of their intron length polymorphism markers in maize. Mol Breeding 29, 437–447 (2012). https://doi.org/10.1007/s11032-011-9560-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11032-011-9560-3

Keywords

Navigation