Molecular Genetics and Genomics

, Volume 269, Issue 3, pp 406–419 | Cite as

Genomic distribution and characterization of EST-derived resistance gene analogs (RGAs) in sugarcane

  • M. Rossi
  • P. G. Araujo
  • F. Paulet
  • O. Garsmeur
  • V. M. Dias
  • H. Chen
  • M.-A. Van Sluys
  • A. D'Hont
Original Paper


A large sugarcane EST (expressed sequence tag) project recently gave us access to 261,609 EST sequences from sugarcane, assembled into 81,223 clusters. Among these, we identified 88 resistance gene analogs (RGAs) based on their homology to typical pathogen resistance genes, using a stringent BLAST search with a threshold e-value of e−50. They included representatives of the three major groups of resistance genes with NBS/LRR, LRR or S/T KINASE domains. Fifty RGAs showed a total of 148 single-dose polymorphic RFLP markers, which could be located on the sugarcane reference genetic map (constructed in cultivar R570, 2n=~115). Fifty-five SSR loci corresponding to 134 markers in R570 were also mapped to enable the classification of the various haplotypes into homology groups. Several RGA clusters were found. One cluster of two LRR-like loci mapped close to the only disease resistance gene known so far in sugarcane, which confers resistance to common rust. Detailed sequence comparison between two NBS/LRR RGA clusters in relation to their orthologs in rice and maize suggests their polyphyletic origins, and indicates that the degree of divergence between paralogous RGAs in sugarcane can be larger than that from an ortholog in a distant species.


Sugarcane Polyploid Genetic mapping Resistance gene analogs (RGAs) Nucleotide binding site/leucine rich repeat (NBS/LRR) 



M. Rossi, P. G. Araujo and V. M. Dias were recipients of FAPESP fellowships. This work was partially supported by grants from FAPESP and CNPq (Brazil). We thank J. C. Glaszmann, L. Grivet, G. Piperidis, J. B. Morel and Cristina Juarez for helpful contributions


  1. Asnaghi C, Paulet F, Kaye C, Grivet L, Deu M, Glaszmann JC, D'Hont A (2000) Application of synteny across Poaceae to determine the map location of a sugarcane rust resistance gene. Theor Appl Genet 101:962–969Google Scholar
  2. Brueggeman R, Rostoks N, Kudrna D, Kilian A, Han F, Chen J, Druka A, Steffenson B (2002) The barley stem rust-resistance gene Rpg1is a novel disease-resistance gene with homology to receptor kinases. Proc Natl Acad Sci USA 99:9328–9333CrossRefPubMedGoogle Scholar
  3. Butterfield MK, D'Hont A, Berding N (2001) The sugarcane genome: a synthesis of current understanding, and lessons for breeding and biotechnology. Proc Soc Afr Sugarcane Technol Assoc 75:1–5Google Scholar
  4. 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 11:1365–1376PubMedGoogle Scholar
  5. Daugrois JH, Grivet L, Roques D, Hoarau JY, Lombard H., Glaszmann JC, D´Hont A (1996) A putative major gene for rust resistance linked with a RFLP marker in sugarcane cultivar "R570". Theor Appl Genet 92:1059–1064CrossRefGoogle Scholar
  6. Dixon MS, Hatzixanthis K, Jones DA, Harrison K, Jones JDG (1998) The tomato Cf-5disease resistance gene and six homologs show pronounced allelic variation in leucine-rich repeat copy number. Plant Cell 10:1915–1925PubMedGoogle Scholar
  7. D'Hont A, Glaszmann JC (2001) Sugarcane genome analysis with molecular markers, a first decade of research. Proc Int Soc Sugarcane Technol 24:556–559Google Scholar
  8. Dufour P, Deu M, Grivet L, D´Hont A, Paulet F, Bouet A, Lanaud C, Glaszmann JC, Hamon P (1997) Construction of a composite sorghum genome map and comparison with sugarcane, a related complex polyploid. Theor Appl Genet 94:409–418CrossRefGoogle Scholar
  9. Feuillet C, Penger A, Gellner K, Mast A, Keller B (2001) Molecular evolution of receptor-like kinase genes in hexaploid wheat. Independent evolution of orthologs after polyploidization and mechanisms of local rearrangements at paralogous loci. Plant Physiol 125:1304–1313PubMedGoogle Scholar
  10. Flor HH (1971) Current status of the gene-for-gene concept. Annu Rev Phytopathol 9:275–96Google Scholar
  11. Glaszmann JC, Dufour P, Grivet L, D'Hont A, Deu M, Paulet F, Hamon P (1997) Comparative genome analysis between several tropical grasses. Euphytica 96:13–21CrossRefGoogle Scholar
  12. Goff AS, et al (2002) A draft sequence of the rice genome ( Oryza sativa L. ssp japonica). Science 296:92–100PubMedGoogle Scholar
  13. Graham MA, Marek LF, Lohnes D, Cregan P, Schoemaker RC (2000) Expression and genome organization of resistance gene analogs in soybean. Genome 43:86–93PubMedGoogle Scholar
  14. Grivet L, Arruda P (2001) Sugarcane genomics: depicting the complex genome of an important tropical crop. Curr Opin Plant Biol 5:122–127CrossRefGoogle Scholar
  15. Grivet L, D'Hont A, Roques D, Feldman P, Lanaud C, Glaszmann JC (1996) RFLP mapping in cultivated sugarcane ( Saccharum spp.): genome organization in a highly polyploid and aneuploid interspecific hybrid. Genetics 142:987–1000PubMedGoogle Scholar
  16. Hammond-Kosack K, Jones J (1997) Plant disease resistance genes. Annu Rev Plant Physiol Plant Mol Biol 48:575–607Google Scholar
  17. Hoarau JY, Offman B, D´Hont A, Risterucci AM, Roques D, Glaszman JC, Grivet L (2001) Genetic dissection of a modern sugarcane cultivar ( Saccharum spp.). I. Genome mapping with AFLP markers. Theor Appl Genet 103:84–97Google Scholar
  18. Keen NT (1990) Gene-for-gene complementarity in plant-pathogen interactions. Annu Rev Genet 24:447–463PubMedGoogle Scholar
  19. Lander ES, Green P, Abrahamson J, Barlow A, Daly MJ, Lincoln SE, Newburg L (1987) MAPMAKER: an interactive computer package for constructing primary genetic linkage maps of experimental and natural populations. Genomics 1:174–181PubMedGoogle Scholar
  20. Martin GB, Brommonschenkel SH, Chunwongse J, Frary A, Ganal MW, Spivey R, Wu T, Earie E, Tanksley SD (1993) Map-based cloning of a protein kinase gene conferring disease resistance in tomato. Science 262:1432–1436PubMedGoogle Scholar
  21. Michelmore RW, Meyers BC (1998) Clusters of resistance genes in plants evolve by divergent selection and a birth-and-death process. Genome Res 8:1113–1130PubMedGoogle Scholar
  22. Pan Q, Wendel J, Fluhr R (2000) Divergent evolution of plant NBS-LRR resistance gene homologues in dicot and cereal genomes. J Mol Evol 50:203–213PubMedGoogle Scholar
  23. Raboin LM, Offmann B, Hoarau JY, Notise J, Costet L, Telismart H, Roques D, Rott P, D'Hont A (2001) Undertaking genetic mapping of sugarcane smut resistance. Proc Soc Afr Sugarcane Technol Assoc 75:94–98Google Scholar
  24. Rozas J, Rozas R (1997) DnaSP version 2.0: a novel software package for extensive molecular population genetic analysis. Comput Appl Biosci 13:307–311PubMedGoogle Scholar
  25. Sakamoto K, Tada Y, Yokozeki Y, Akagi H, Hayashi N, Fujimura T, Ichikawa N (1999) Chemical induction of disease resistance in rice is correlated with the expression of a gene encoding a nucleotide binding site and leucine-rich repeats. Plant Mol Biol 40:847–855PubMedGoogle Scholar
  26. Salmeron JM, Oldroyd GED, Rommens CMT, Scofield SR, Kim HS, Lavelle DT, Dahlbeck D, Staskawicz BJ (1996) Tomato Prf is a member of the leucine-rich repeat class of plant disease resistance genes and lies embedded within the Pto kinase gene cluster. Cell 86:123–133PubMedGoogle Scholar
  27. Song W, 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 270:1804–1806PubMedGoogle Scholar
  28. Telles GP, Braga MDV, Dias Z, Lin TL, Quitzau JAA, da Silva FR, Meidanis J (2001) Bioinformatics of the sugarcane EST project. Genet Mol Biol 24:9–15Google Scholar
  29. The Arabidopsis Genome Initiative (2000) Analysis of the genome sequence of the flowering plant Arabidopsis thaliana. Nature 408:796–815PubMedGoogle Scholar
  30. Vettore AL, da Silva FR, Kemper EL, Arruda P (2001) The libraries that made SUCEST. Genet Mol Biol 24:1–7Google Scholar
  31. Vicente JG, King GJ (2001) Characterization of disease resistance gene-like sequences in Brassica oleracea L. Theor Appl Genet 102:555–563Google Scholar
  32. Wang Z, Taramino D, Yang D, Liu G, Tingey SV, Miao G, Wang G (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 265:302–310PubMedGoogle Scholar
  33. Wendel JF (2000) Genome evolution in polyploids. Plant Mol Biol 42:225–249PubMedGoogle Scholar
  34. Wu KK, Burnquist W, Sorrells ME, Tew TL, Moore PH, Tanksley SD (1992) The detection and estimation of linkage in polyploids using single-dose restriction fragments. Theor Appl Genet 83:294–300Google Scholar
  35. Xiao S, Ellwood S, Calis O, Patrick E, Li T, Coleman M, Turner JG (2001) Broad-spectrum mildew resistance in Arabidopsis thaliana mediated by RPW8. Science 291:118–120PubMedGoogle Scholar
  36. Zhou J, Loh YT, Bressan RA, Martin GB (1995) The tomato gene Pti1encodes a serine/threonine kinase that is phosphorylated by Pto and is involved in the hypersensitive response.Google Scholar

Copyright information

© Springer-Verlag 2003

Authors and Affiliations

  • M. Rossi
    • 1
  • P. G. Araujo
    • 1
  • F. Paulet
    • 2
  • O. Garsmeur
    • 2
  • V. M. Dias
    • 1
  • H. Chen
    • 3
  • M.-A. Van Sluys
    • 1
  • A. D'Hont
    • 2
  1. 1.Departamento de Botanica, Instituto de BiocienciasUniversidade de São PauloSão PauloBrazil
  2. 2.UMR1096CIRADMontpellierFrance
  3. 3.Yunnan Sugarcane Research InstituteYunnan Academy of Agricultural SciencesKaiyuanP.R. China

Personalised recommendations