Analysis of TIR- and non-TIR-NBS-LRR disease resistance gene analogous in pepper: characterization, genetic variation, functional divergence and expression patterns
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  • 作者:Hongjian Wan (1)
    Wei Yuan (1)
    Qingjing Ye (1)
    Rongqing Wang (1)
    Meiying Ruan (1)
    Zhimiao Li (1)
    Guozhi Zhou (1)
    Zhuping Yao (1)
    Jing Zhao (1)
    Shujun Liu (1)
    Yuejian Yang (1)
  • 刊名:BMC Genomics
  • 出版年:2012
  • 出版时间:December 2012
  • 年:2012
  • 卷:13
  • 期:1
  • 全文大小:1564KB
  • 参考文献:1. Flor HH: The current status of gene for gene concept. / Ann Rev Phytopathol 1971, 9:275鈥?96. CrossRef
    2. Dangl JL, Jones JDG: Plant pathogens and integrated responses to infection. / Nature 2001, 411:826鈥?33. CrossRef
    3. Meyers BC, Kozik A, Griego A, Kuang H, Michelmore RW: Genome wide analysis of NBS-LRR-encoding genes in Arabidopsis . / Plant Cell 2003, 15:809鈥?34. CrossRef
    4. DeYoung BJ, Innes RW: Plant NBS-LRR proteins in pathogen sensing and host. / Nat Immunol 2006, 7:1243鈥?249. CrossRef
    5. McHale L, Tan X, Koehl P, Michelmore RW: Plant NBS-LRR proteins: adaptable guards. / Genome Biol 2006, 7:212. CrossRef
    6. Liu JL, Liu XL, Dai LY, Wang GL: Recent progress in elucidating the structure, function and evolution of disease resistance genes in plants. / J Genet Genomics 2007, 34:765鈥?76. CrossRef
    7. Holub EB: The arms race is ancient history in Arabidopsis , the wildflower. / Nat Rev Genet 2001, 2:516鈥?27. CrossRef
    8. Yue JX, Meyers BC, Chen JQ, Tian DC, Yang SH: Tracing the origin and evolutionary history of plant nucleotide-binding site-leucine-rich repeat (NBS-LRR) genes. / New Phytol 2012, 193:1049鈥?063. CrossRef
    9. Meyers BC, Dickerman AW, Michelmore RW, Sivaramakrishnan S, Sobral BW, Young ND: Plant disease resistance genes encode members of an ancient and diverse protein family within the nucleotide-binding super family. / Plant J 1999, 20:317鈥?32. CrossRef
    10. Tameling WI, Elzinga SD, Darmin PS, Vossen JH, Takken FL, Haring MA, Cornelissen BJ: The tomato R gene products I-2 and Mi-1 are functional ATP binding proteins with ATPase activity. / Plant Cell 2002, 14:2929鈥?939. CrossRef
    11. Kobe B, Deisenhofer J: A structural basis of the interactions between leucine-rich repeats and protein ligands. / Nature 1995, 374:183鈥?86. CrossRef
    12. Leister RT, Katagiri F: A resistance gene product of the nucleotide binding site-leucine rich repeats class can form a complex with bacterial avirulence proteins in vivo. / Plant J 2000, 22:345鈥?54. CrossRef
    13. Yu YG, Buss GR, Saghai Maroof MA: Isolation of a superfamily of candidate disease-resistance genes in soybean based on a conserved nucleotide-binding site. / Proc Natl Acad Sci USA 1996, 93:11751鈥?1756. CrossRef
    14. Gentzbittel L, Mouzeyar S, Badaoui S, Mestries E, Vear F, Tourvieille de Labrouhe D, Nicolas P: Cloning of molecular markers for disease resistance in sunflower, Helianthus annuus L. / Theor Appl Genet 1998, 96:519鈥?25. CrossRef
    15. Pan QL, Wendel J, Fluhr R: Divergent evolution of plant NBS LRR resistance gene homologues in dicot and cereal genomes. / J Mol Evol 2000, 50:203鈥?13.
    16. Tian YY, Fan LJ, Thurau T, Jung C, Cai DG: The absence of TIR-type resistance gene analogues in the sugar beet ( Beta vulgaris L.) genome. / J Mol Evol 2004, 58:40鈥?3. CrossRef
    17. Wan HJ, Zhao ZG, Malik AA, Qian CT, Chen JF: Identification vand 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. CrossRef
    18. Zhang HL, Wang YJ, Zhang CH, Wang XP, Li HE, Xu WR: Isolation, characterization and expression analysis of resistance gene candidates in pear ( Pyrus spp.). / Sci Horticul 2011, 127:282鈥?89. CrossRef
    19. Mutlu N, Miklas PN, Coyne DP: Resistance gene analog polymorphism (RGAP) markers co-localize with disease resistance genes and QTL in common bean. / Mol breeding 2006, 17:127鈥?35. CrossRef
    20. Cannon SB, Zhu H, Baumgarten AM, Spangler R, May G, Cook DR, Young ND: Diversity, distribution and ancient taxonomic relationships within the TIR and non-TIR NBS-LRR resistance gene subfamilies. / J Mol Evol 2002, 54:548鈥?62. CrossRef
    21. Speulman E, Bouchez D, Holub EB, Beynon JL: Disease resistance gene homologs correlate with disease resistance loci of Arabidopsis thaliana . / Plant J 1998, 14:467鈥?74. CrossRef
    22. Ashfield T, Bocian A, Held D, Henk AD, Marek LF, Danesh D, Pen奴ela S, Meksem K, Lightfoot DA, Young ND, Shoemaker RC, Innes RW: Genetic and physical localization of the soybean Rpg1-b disease resistance gene reveals a complex locus containing several tightly linked families of NBS-LRR genes. / Mol Plant Microbe Interact 2003, 16:817鈥?26. CrossRef
    23. Radwan O, Bouzidi MF, Nicolas P, Mouzeyar S: Development of PCR markers of the PI5/PI8 locus for resistance to Plasmopara halstedii in sunflower, Helianthus annuus L. from complete CC-NBS鈥揕RR sequences. / Theor Appl Genet 2004, 109:176鈥?85. CrossRef
    24. Hulbert SH, Webb CA, Smith SM, Sun Q: Resistance gene complexes: Evolution and utilization. / Annu Rev Phytopathol 2001, 39:285鈥?12. CrossRef
    25. Richly E, Kurth J, Leister D: Mode of amplification and reorganization of resistance genes during recent Arabidopsis thaliana evolution. / Mol Biol Evol 2002, 19:76鈥?4. CrossRef
    26. Zhou T, Wang Y, Chen JQ, Araki H, Jing Z, Jiang K, Shen J, Tian D: Genome-wide identification of NBS genes in rice reveals significant expansion of divergent non-TIR NBS Genes. / Mol Genet Genomics 2004, 271:402鈥?15. CrossRef
    27. Mondrag贸n-Palomino M, Meyers BC, Michelmore RW, Gaut BS: Patterns of positive selection in the complete NBS-LRR gene family of Arabidopsis thaliana . / Genome Res 2002, 12:1305鈥?315. CrossRef
    28. Yang SH, Zhang XH, Yue JX, Tian DC, Chen JQ: Recent duplications domainate NBS-encoding gene expansion in two woody species. / Mol Genet Genomics 2008, 280:187鈥?98. CrossRef
    29. Xu Q, Wen XP, Deng XX: Isolation and TIR and nonTIR NBS-LRR resistance gene analogues and identification of molecular markers linked to a powdery mildew resistance locus in chestnut rose ( Rosa roxburghii Tratt). / Theor Appl Genet 2005, 111:819鈥?30. CrossRef
    30. Xu Q, Wen XP, Deng XX: Phylogenetic and evolutionary analysis of NBS-encoding genes in Rosaceae fruit crops. / Mol Phylogenet Evol 2007, 44:315鈥?24. CrossRef
    31. R枚mer P, Hahn S, Jordan T, Strau脽 T, Bonas U, Lahaye T: Plant pathogen recognition mediated by promoter activation of the pepper Bs3 resistance gene. / Science 2007, 318:645鈥?48. CrossRef
    32. Tai TH, Dahlbeck D, Clark ET, Gajiwala P, Pasion R, Whalen MC, Stall RE, Staskawicz BJ: Expression of the Bs2 pepper gene confers resistance to bacterial spot disease in tomato. / Proc Natl Acad Sci 1999, 96:14153鈥?4158. CrossRef
    33. Chen R, Li H, Zhang L, Zhang J, Xiao J, Ye Z: CaMi, a root-knot nematode resistance gene from hot pepper ( Capsium annuum L.) confers nematode resistance in tomato. / Plant Cell Rep 2007, 26:895鈥?05. CrossRef
    34. Egea-gilabert C, Dickinson MJ, Bilotti G, Candela ME: Isolation of resistance gene analogs in pepper using modified AFLPs. / Biol Plantarum 2003, 47:27鈥?2. CrossRef
    35. Pflieger S, Lefebvre V, Caranta C, Blattes A, Goffinet B, Palloix A: Disease resistance gene analogs as candidates for QTLs involved in pepper-pathogen interactions. / Genome 1999, 42:1100鈥?110. CrossRef
    36. Kochieva EZ, Ryzhova NN: Analysis of resistance gene family diversity in pepper ( Capsicum annuum ). / Biochem Biophy Mol Biol 2009, 425:256鈥?58.
    37. Zhang LY, Chen RG, Zhang JH: Cloning and analysis of resistance gene analogs from pepper ( Capsicum annuum L.). / Agr Sci China (in Chinese) 2008, 41:169鈥?75.
    38. Noir S, Combes M-C, Anthony F, Lashermes P: Origin, diversity and evolution of NBS-type disease-resistance gene homologues in coffee trees ( Coffea L.). / Mol Gen Genomics 2001, 265:654鈥?62. CrossRef
    39. Deng Z, Huang S, Ling P, Chen C, Yu C, Weber CA, Moore GA, Gmitter FG: Cloning and characterization of NBS鈥揕RR class resistance-gene candidate sequences in citrus. / Theor Appl Genet 2000, 101:814鈥?22. CrossRef
    40. van der Biezen EA, Jones JDG: The NB-ARC domain: a novel signalling motif shared by plant resistance gene products and regulators of cell death in animals. / Curr Biol 1998, 8:R226-R227. CrossRef
    41. Aravind L, Iyer LM, Leipe DD, Koonin EV: A novel family of P-loop NTPases with an unusual phyletic distribution and transmembrane segments inserted within the NTPase domain. / Genome Biol 2004, 5:R30. CrossRef
    42. Leipe DD, Koonin EV, Aravind L: STAND, a class of P-loop NTPases including animal and plant regulators of programmed cell death: multiple, complex domain architectures, unusual phyletic patterns, and evolution by horizontal gene transfer. / J Mol Biol 2004, 343:1鈥?8. CrossRef
    43. Tamura K, Peterson D, Peterson N, Stecher G, Nei M, Kumar S: MEGA5: Molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. / Mol Biol Evol 2011, 28:2731鈥?739. CrossRef
    44. Gu X: Statistical methods for testing functional divergence after gene duplication. / Mol Biol Evol 1999, 16:1664鈥?674. CrossRef
    45. Gu X: A simple statistical method for estimating type-II (cluster-specific) functional divergence of protein sequences. / Mol Biol Evol 2006, 23:1937鈥?945. CrossRef
    46. Michelmore R, Meyers B: Clusters of resistance genes in plants evolve by divergent selection and birth-and-death process. / Genome Res 1998, 8:1113鈥?130.
    47. Martin GB, Brommonschenkel S, Chunwongse J, Frary A, Ganal MW, Spivey R, Wu T, Earle ED, Tanksley SD: Map-based cloning of a protein kinase gene conferring disease resistance in tomato. / Science 1993, 262:1432鈥?436. CrossRef
    48. Creevey CJ, McInerney JO: CRANN: Detecting adaptive evolution in protein-coding DNA sequences. / Bioinformatics 2003, 19:1726. CrossRef
    49. Mazin PV, Gelfand MS, Mironov AA, Rakhmaninova AB, Rubinov AR, Russell RB, Kalinina OV: An automated stochastic approach to the identification of the protein specificity determinants and functional subfamilies. / Algorithm Mol Biol 2010, 5:29. CrossRef
    50. Thomma BP, Penninckx IA, Broekaer WF, Cammue BP: The complexity of disese signaling in Arabidopsis . / Curr Opin Immunol 2011, 13:63鈥?8. CrossRef
    51. Shirano Y, Kachroo P, Shah J, Klessig DF: A gain-of-function mutation in an arabidopsis Toll interleukin1 receptor-nucleotide binding site-leucine-rich repeat type R gene triggers defense responses and results in enhanced disease resistance. / Plant Cell 2002, 14:3149鈥?162. CrossRef
    52. Xiao SX, Brown EP, Brearley C, Turner JG: Enhanced transcription of the Arabidopsis disease resistance genes RPW8.1and RPW8.2 via a salicylic acid-dependent amplification circuit is required for hypersensitive cell death. / Plant Cell 2003, 15:33鈥?5. CrossRef
    53. Xiong QY, Wei LJ, Sen ZJ, Hong RM, Ping XL, Qing ZM: Molecular cloning and characterisation of a non-TIR-NBS-LRR type disease resistance gene analogue from sugarcane. / Sugar Tech 2008, 10:71鈥?3. CrossRef
    54. Wang BJ, Zhang ZG, Li XG, Wang YJ, He CY, Zhang JS, Chen SY: Cloning and analysis of a disease resistance gene homolog from soybean. / Acta Botan Sin 2003, 45:864鈥?70.
    55. Wang BJ, Wang YJ, Wang Q, Luo GZ, Zhang ZG, He CY, He SJ, Zhang JS, Gai JY, Chen SY: Characterization of an NBS-LRR resistance gene homologue from soybean. / J Plant Physiol 2004, 161:815鈥?22. CrossRef
    56. Tian AG, Luo GZ, Wang YJ, Zhang JS, Gai JY, Chen SY: Isolation and characterization of a Pti1 homologue from soybean. / J Exp Bot 2004, 396:535鈥?37. CrossRef
    57. Bendahmane A, Querci M, Kanyuka K, Baulcombe DC: Agrobacterium transient expression system as a tool for isolation of disease resistance genes: application to the Rx2 locus in potato. / Plant J 2000, 21:73鈥?1. CrossRef
    58. Baulcombe DC: Fast forward genetics based on virus-induced gene silencing. / Curr Opin Plant Biol 1999, 2:109鈥?13. CrossRef
    59. Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG: The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. / Nucleic Acids Res 1997, 25:4876鈥?882. CrossRef
    60. van der Biezen EA, Jones JD: The NB-ARC domain: a novel signaling motif shared by plant resistance gene products and regulators of cell death in animals. / Curr Biol 1998, 8:R226-R227. CrossRef
    61. Gu X, Vander Velden K: DIVERGE: phylogeny-based analysis for functional-structural divergence of a protein family. / Bioinformatics 2002, 18:500鈥?01. CrossRef
    62. Nei M, Gojobori T: Simple methods for estimating the numbers of synonymous and nonsynonymous nucleotide substitutions. / Mol Biol Evol 1986, 3:418鈥?26.
    63. Comeron JM: A method for estimating the numbers of synonymous and non-synonymous substitutions per site. / J Mol Evol 1995, 41:1152鈥?159. CrossRef
    64. Comeron JM: K-Estimator: Calculation of the number of nucleotide substitutions per site and the confidence intervals. / Bioinformatics 1999, 15:763鈥?64. CrossRef
    65. Librado P, Rozas J: DnaSP v5: a software for comprehensive analysis of DNA polymorphism data. / Bioinformatics 2009, 25:1451鈥?452. CrossRef
    66. Wan HJ, Yuan W, Ruan MY, Ye QJ, Wang RQ, Li ZM, Zhou GZ, Yao ZP, Zhao J, Liu SJ, Yang YJ: Identification of reference genes for reverse transcription quantitative real-time PCR normalization in pepper ( Capsicum annuum L.). / Biochem Biophys Res Commun 2011, 416:24鈥?0. CrossRef
  • 作者单位:Hongjian Wan (1)
    Wei Yuan (1)
    Qingjing Ye (1)
    Rongqing Wang (1)
    Meiying Ruan (1)
    Zhimiao Li (1)
    Guozhi Zhou (1)
    Zhuping Yao (1)
    Jing Zhao (1)
    Shujun Liu (1)
    Yuejian Yang (1)

    1. Institute of Vegetables, Zhejiang Academy of Agricultural Sciences, Hangzhou, 310021, People鈥檚 Republic of China
文摘
Background Pepper (Capsicum annuum L.) is one of the most important vegetable crops worldwide. However, its yield and fruit quality can be severely threatened by several pathogens. The plant nucleotide-binding site (NBS)-leucine-rich repeat (LRR) gene family is the largest class of known disease resistance genes (R genes) effective against such pathogens. Therefore, the isolation and identification of such R gene homologues from pepper will provide a critical foundation for improving disease resistance breeding programs. Results A total of 78 R gene analogues (CaRGAs) were identified in pepper by degenerate PCR amplification and database mining. Phylogenetic tree analysis of the deduced amino acid sequences for 51 of these CaRGAs with typically conserved motifs ( P-loop, kinase-2 and GLPL) along with some known R genes from Arabidopsis and tomato grouped these CaRGAs into the non-Toll interleukin-1 receptor (TIR)-NBS-LRR (CaRGAs I to IV) and TIR-NBS-LRR (CaRGAs V to VII) subfamilies. The presence of consensus motifs (i.e. P-loop, kinase-2 and hydrophobic domain) is typical of the non-TIR- and TIR-NBS-LRR gene subfamilies. This finding further supports the view that both subfamilies are widely distributed in dicot species. Functional divergence analysis provided strong statistical evidence of altered selective constraints during protein evolution between the two subfamilies. Thirteen critical amino acid sites involved in this divergence were also identified using DIVERGE version 2 software. Analyses of non-synonymous and synonymous substitutions per site showed that purifying selection can play a critical role in the evolutionary processes of non-TIR- and TIR-NBS-LRR RGAs in pepper. In addition, four specificity-determining positions were predicted to be responsible for functional specificity. qRT-PCR analysis showed that both salicylic and abscisic acids induce the expression of CaRGA genes, suggesting that they may primarily be involved in defence responses by activating signaling pathways. Conclusion The identified CaRGAs are a valuable resource for discovering R genes and developing RGA molecular markers for genetic map construction. They will also be useful for improving disease resistance in pepper. The findings of this study provide a better understanding of the evolutionary mechanisms that drive the functional diversification of non-TIR- and TIR-NBS-LRR R genes in pepper.

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