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Genome-wide analysis of nucleotide-binding site disease resistance genes in Medicago truncatula

  • Article
  • Bioinformatics
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Chinese Science Bulletin

Abstract

The class of nucleotide-binding site (NBS)-Leucine-rich repeat (LRR) disease resistance genes play an important role in defending plants from a variety of pathogens and insect pests. Consequently, many NBS-LRR genes have been identified in various plant species. In this study, we identified 617 NBS-encoding genes in the Medicago truncatula genome (Mt3.5v5) and divided them into two groups, regular (490) and non-regular (127) NBS-LRR genes. The regular NBS-LRR genes were characterized on the bases of structural diversity, chromosomal location, gene duplication, conserved protein motifs, and EST expression profiling. According to N-terminal motifs and LRR motifs, the 490 regular NBS-LRR genes were then classified into 10 types: CC-NBS (4), CC-NBS-LRR (212), TIR-NBS (20), TIR-NBS-LRR (160), TIR-NBS-TIR (1), TIR-NBS-TIR-LRR (2), NBS-TIR (7), NBS-TIR-LRR (1), NBS (10), and NBS-LRR (73). Analysis of the physical location and duplications of the regular NBS-LRR genes revealed that the M. truncatula genome is similar to rice. Interestingly, we found that TIR-type genes are more frequently expressed than non-TIR-type genes in M. truncatula, whereas the number of non-TIR-type regular NBS-LRR genes was greater than TIR-type genes, suggesting the gene expression was not associated with the total number of NBS-LRR genes. Moreover, we found that the phylogenetic tree supported our division of the regular NBS-LRR genes into two distinct clades (TIR-type and non-TIR-type), but some of the non-TIR-type lineages contain TIR-type genes. These analyses provide a robust database of NBS-LRR genes in M. truncatula that will facilitate the isolation of new resistance genes and breeding strategies to engineer disease resistance in leguminous crop.

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References

  1. Flor HH (1971) Current status of the gene-for-gene concept. Annu Rev Phytopathol 9:275–296

    Article  Google Scholar 

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

    Article  Google Scholar 

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

    Article  Google Scholar 

  4. Martin GB, Bogdanove AJ, Sessa G (2003) Understanding the functions of plant disease resistance proteins. Annu Rev Plant Biol 54:23–61

    Article  Google Scholar 

  5. Staskawicz BJ, Mudgett MB, Dangl JL et al (2001) Common and contrasting themes of plant and animal diseases. Science 292:2285–2289

    Article  Google Scholar 

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

    Article  Google Scholar 

  7. McHale L, Tan X, Koehl P et al (2006) Plant NBS–LRR proteins: adaptable guards. Genome Biol 7:212

    Article  Google Scholar 

  8. Dodds PN, Rathjen JP (2010) Plant immunity: towards an integrated view of plant–pathogen interactions. Nat Rev Genet 11:539–548

    Article  Google Scholar 

  9. Gay NJ, Gangloff M (2007) Structure and function of Toll receptors and their ligands. Annu Rev Biochem 76:141–165

    Article  Google Scholar 

  10. Meyers BC, Kozik A, Griego A et al (2003) Genome-wide analysis of NBS-LRR-encoding genes in Arabidopsis. Plant Cell 15:809–834

    Article  Google Scholar 

  11. Mun JH, Yu HJ, Park S et al (2009) Genome-wide identification of NBS-encoding resistance genes in Brassica rapa. Mol Genet Genomics 282:617–631

    Article  Google Scholar 

  12. Tameling WI, Elzinga SD, Darmin PS et al (2002) The tomato R gene products I-2 and MI-1 are functional ATP binding proteins with ATPase activity. Plant Cell 14:2929–2939

    Article  Google Scholar 

  13. Tameling WI, Vossen JH, Albrecht M et al (2006) Mutations in the NB-ARC domain of I-2 that impair ATP hydrolysis cause autoactivation. Plant Physiol 140:1233–1245

    Article  Google Scholar 

  14. Swiderski MR, Birker D, Jones JD (2009) The TIR domain of TIR-NB-LRR resistance proteins is a signaling domain involved in cell death induction. Mol Plant Microbe Interact 22:157–165

    Article  Google Scholar 

  15. Krasileva KV, Dahlbeck D, Staskawicz BJ (2010) Activation of an Arabidopsis resistance protein is specified by the in planta association of its leucine-rich repeat domain with the cognate oomycete effector. Plant Cell 22:2444–2458

    Article  Google Scholar 

  16. Maekawa T, Cheng W, Spiridon LN et al (2011) Coiled-coil domain-dependent homodimerization of intracellular barley immune receptors defines a minimal functional module for triggering cell death. Cell Host Microbe 9:187–199

    Article  Google Scholar 

  17. Sayar-Turet M, Dreisigacker S, Braun HJ et al (2011) Genetic variation within and between winter wheat genotypes from Turkey, Kazakhstan, and Europe as determined by nucleotide-binding-site profiling. Genome 54:419–430

    Article  Google Scholar 

  18. Belkhadir Y, Nimchuk Z, Hubert DA et al (2004) Arabidopsis RIN4 negatively regulates disease resistance mediated by RPS2 and RPM1 downstream or independent of the NDR1 signal modulator and is not required for the virulence functions of bacterial type III effectors AvrRpt2 or AvrRpm1. Plant Cell 16:2822–2835

    Article  Google Scholar 

  19. Young ND, Debellé F, Oldroyd GE et al (2011) The Medicago genome provides insight into the evolution of rhizobial symbioses. Nature 480:520–524

    Article  Google Scholar 

  20. Akita M, Valkonen JP (2002) A novel gene family in moss (Physcomitrella patens) shows sequence homology and a phylogenetic relationship with the TIR-NBS class of plant disease resistance genes. J Mol Evol 55:595–605

    Article  Google Scholar 

  21. Meyers BC, Dickrman AW, Michelmore RW et al (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  Google Scholar 

  22. Ameline-Torregrosa C, Wang BB, O’Bleness MS et al (2008) Identification and characterization of nucleotide-binding site-leucine-rich repeat genes in the model plant Medicago truncatula. Plant Physiol 146:5–21

    Article  Google Scholar 

  23. Branca A, Paape TD, Zhou P et al (2011) Whole-genome nucleotide diversity, recombination, and linkage disequilibrium in the model legume Medicago truncatula. Proc Natl Acad Sci USA 108:E864–E870

    Article  Google Scholar 

  24. Finn RD, Mistry J, Schuster-Böckler B et al (2006) Pfam:clan, web tools and services. Nucleic Acids Res 34:247–251

    Article  Google Scholar 

  25. Zhou T, Wang Y, Chen JQ et al (2004) Genome-wide identification of NBS genes in japonica rice reveals significant expansion of divergent non-TIR NBS-LRR genes. Mol Genet Genomics 271:402–415

    Article  Google Scholar 

  26. Berger B, Wilson DB, Wolf E et al (1995) Predicting coiled coils by use of pairwise residue correlations. Proc Natl Acad Sci USA 92:8259–8263

    Article  Google Scholar 

  27. Thompson JD, Higgings DG, Gibson TJ (1994) CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res 22:4673–4680

    Article  Google Scholar 

  28. Bailey TL, Elkan C (1995) The value of prior knowledge in discovering motifs with MEME. Proc Int Conf Intell Syst Mol Biol 3:21–29

    Google Scholar 

  29. Zhao Y, Li X, Chen W et al (2011) Whole-genome survey and characterization of MADS-box gene family in maize and sorghum. Plant Cell Tiss Organ Cult 105:159–173

    Article  Google Scholar 

  30. Letunic I, Doerks T, Bork P (2012) SMART 7: recent updates to the protein domain annotation resource. Nucleic Acids Res 40:302–305

    Article  Google Scholar 

  31. Thompson JD, Gibson TJ, Plewniak F et al (1997) The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 25:4876–4882

    Article  Google Scholar 

  32. Tamura K, Dudley J, Nei M et al (2007) MEGA4: molecular evolutionary genetics analysis (MEGA) software version 4.0. Mol Biol Evol 24:1596–1599

    Article  Google Scholar 

  33. Li X, Cheng Y, Ma W et al (2010) Identification and characterization of NBS-encoding disease resistance genes in Lotus japonicus. Plant Syst Evol 289:101–110

    Article  Google Scholar 

  34. Cheng Y, Li X, Jiang H et al (2012) Systematic analysis and comparison of nucleotide-binding site disease resistance genes in maize. FEBS J 279:2431–2443

    Article  Google Scholar 

  35. Pan Q, Wendel J, Fluhr R (2000) Divergent evolution of plant NBS-LRR resistance gene homologues in dicot and cereal genomes. J Mol Evol 50:203–213

    Google Scholar 

  36. Meyers BC, Morgante M, Michelmore RW (2002) TIR-X and TIR-NBS proteins: two new families related to disease resistance TIR-NBS-LRR proteins encoded in Arabidopsis and other plant genomes. Plant J 32:77–92

    Article  Google Scholar 

  37. Tan S, Wu S (2012) Genome wide analysis of nucleotide-binding site disease resistance genes in Brachypodium distachyon. Comp Funct Genomics 2012:418208

    Article  Google Scholar 

  38. Kohler A, Rinaldi C, Duplessis S et al (2008) Genome-wide identification of NBS resistance genes in Populus trichocarpa. Plant Mol Biol 66:619–636

    Article  Google Scholar 

  39. Li L, Stoeckert CJ Jr, Roos DS (2003) OrthoMCL: identification of ortholog groups for eukaryotic genomes. Genome Res 13:2178–2189

    Article  Google Scholar 

  40. Holub EB (2001) The arms race is ancient history in Arabidopsis, the wildflower. Nat Rev Genet 2:516–527

    Article  Google Scholar 

  41. Ohlrogge J, Benning C (2000) Unraveling plant metabolism by EST analysis. Curr Opin Plant Biol 3:224–228

    Article  Google Scholar 

  42. Bai J, Pennill LA, Ning J et al (2002) Diversity in nucleotide binding site-leucine-rich repeat genes in cereals. Genome Res 12:1871–1884

    Article  Google Scholar 

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

    Article  Google Scholar 

  44. Yang S, Zhang X, Yue JX et al (2008) Recent duplications dominate NBS-encoding gene expansion in two woody species. Mol Genet Genomics 280:187–198

    Article  Google Scholar 

  45. Zhang X, Feng Y, Cheng H et al (2011) Relative evolutionary rates of NBS-encoding genes revealed by soybean segmental duplication. Mol Genet Genomics 285:79–90

    Article  Google Scholar 

  46. Luo S, Zhang Y, Hu Q et al (2012) Dynamic nucleotide-binding site and leucine-rich repeat-encoding genes in the grass family. Plant Physiol 159:197–210

    Article  Google Scholar 

  47. Lozano R, Ponce O, Ramirez M et al (2012) Genome-wide identification and mapping of NBS-encoding resistance genes in Solanum tuberosum group phureja. PLoS ONE 7:e34775

    Article  Google Scholar 

  48. Porter BW, Paidi M, Ming R et al (2009) Genome-wide analysis of Carica papaya reveals a small NBS resistance gene family. Mol Genet Genomics 281:609–626

    Article  Google Scholar 

  49. Richly E, Kurth J, Leister D (2002) Mode of amplification and reorganization of resistance genes during recent Arabidopsis thaliana evolution. Mol Biol Evol 19:76–84

    Article  Google Scholar 

  50. Yue JX, Meyers BC, Chen JQ et al (2012) Tracing the origin and evolutionary history of plant nucleotide-binding site-leucine-rich repeat (NBS-LRR) genes. New Phytol 193:1049–1063

    Article  Google Scholar 

  51. Shen QH, Zhou F, Birei S et al (2003) Recognition specificity and RAR1/SGT1 dependence in barley Mla disease resistance genes to the powdery mildew fungus. Plant Cell 15:732–744

    Article  Google Scholar 

  52. Rairdan GJ, Moffett P (2006) Distinct domains in the ARC region of the potato resistance protein Rx mediate LRR binding and inhibition of activation. Plant Cell 18:2082–2093

    Article  Google Scholar 

  53. Nobuta K, Ashfield T, Kim S et al (2005) Diversification of non-TIR class NB-LRR genes in relation to whole-genome duplication events in Arabidopsis. Mol Plant Microbe Interact 18:103–109

    Article  Google Scholar 

  54. Yu J, Wang J, Lin W et al (2005) The genomes of Oryza sativa: a history of duplications. PLoS Biol 3:e38

    Article  Google Scholar 

  55. Tan X, Meyers BC, Kozik A et al (2007) Global expression analysis of nucleotide binding site-leucine rich repeat-encoding and related genes in Arabidopsis. BMC Plant Biol 7:56

    Article  Google Scholar 

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Acknowledgments

This work was supported by the National Basic Research Program of China (2014CB138702). We thank members of the State Key Laboratory of Grassland Agro-ecosystems for their assistance in this study.

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  1. Key Laboratory of Grassland Agro-Ecosystems of Ministry of Agriculture, College of Pastoral Agriculture Science and Technology, Lanzhou University, Lanzhou, 730000, China

    Hui Song & Zhibiao Nan

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  1. Hui Song
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  2. Zhibiao Nan
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Correspondence to Zhibiao Nan.

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Song, H., Nan, Z. Genome-wide analysis of nucleotide-binding site disease resistance genes in Medicago truncatula . Chin. Sci. Bull. 59, 1129–1138 (2014). https://doi.org/10.1007/s11434-014-0155-3

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