Systematic analysis and comparison of nucleotide-binding site disease resistance genes in maize

FEBS Journal

Volumn 279, Issue 13, 2012, Pages 2431-2443

  Cheng, Ying ^a,b   Li, Xiaoyu ^a,b   Jiang, Haiyang ^a   Ma, Wei ^a   Miao, Weiyun ^a   Yamada, Toshihiko ^b   Zhang, Ming ^a  

^a ANHUI AGRICULTURAL UNIVERSITY   (China)

^b HOKKAIDO UNIVERSITY   (Japan)

Author keywords

Disease resistance genes; Genome; Leucinerich repeat; Maize; Nucleotide binding site

Indexed keywords

SALICYLIC ACID;

ARTICLE; EXPRESSED SEQUENCE TAG; GENE DUPLICATION; GENE IDENTIFICATION; GENE SEQUENCE; LATE BLIGHT; MAIZE; MULTIGENE FAMILY; NONHUMAN; NUCLEOTIDE BINDING SITE DISEASE RESISTANCE GENE; PEST RESISTANCE; PHYLOGENY; PLANT BREEDING; PLANT CHROMOSOME; PLANT DEFENSE; PLANT DISEASE; PLANT GENE; PLANT GENOME; PLANT STRUCTURES; PRIORITY JOURNAL; PROTEIN MOTIF;

ASCOMYCOTA; BINDING SITES; CHROMOSOMES, PLANT; DISEASE RESISTANCE; DNA, PLANT; EVOLUTION, MOLECULAR; EXPRESSED SEQUENCE TAGS; GENE DUPLICATION; GENE EXPRESSION REGULATION, PLANT; GENES, PLANT; GENOME, PLANT; MYCOSES; NUCLEOTIDES; PHYLOGENY; PLANT DISEASES; REAL-TIME POLYMERASE CHAIN REACTION; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; ZEA MAYS;

HEXAPODA; ZEA MAYS;

EID: 84862546210     PISSN: 1742464X     EISSN: 17424658     Source Type: Journal    
DOI: 10.1111/j.1742-4658.2012.08621.x     Document Type: Article

References (59)

1. Dangl JL & Jones JD (2001) Plant pathogens and integrated defence responses to infection. Nature 411, 826-833.
2. Flor H (1971) Current status of the gene-for-gene concept. Annu Rev Phytopathol 19, 275-296.
3. 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.
4. Hulbert SH, Webb CA, Smith SM & Sun Q (2001) Resistance gene complexes: evolution and utilization. Annu Rev Phytopathol 39, 285-312.
5. Bourne HR, Sanders DA & McCormick F (1991) The GTPase superfamily: conserved structure and molecular mechanism. Nature 349, 117-127.
6. Saraste M, Sibbald PR & Wittinghofer A (1990) The P-loop: a common motif in ATP- and GTP-binding proteins. Trends Biochem Sci 15, 430-434.
7. 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.
8. Tameling WI, Elzinga SD, Darmin PS, Vossen JH, Takken FL, Haring MA & Cornelissen BJ (2002) The tomato R gene products I-2 and MI-1 are functional ATP binding proteins with ATPase activity. Plant Cell 14, 2929-2939.
9. Ellis JG, Lawrence GJ, Luck JE & Dodds PN (1999) Identification of regions in alleles of the flax rust resistance gene L that determine differences in gene-for-gene specificity. Plant Cell 11, 495-506.
10. Jia Y, McAdams SA, Bryan GT, Hershey HP & Valent B (2000) Direct interaction of resistance gene and avirulence gene products confers rice BLAST resistance. EMBO J 19, 4004-4014.
11. DeYoung BJ & Innes RW (2006) Plant NBS-LRR proteins in pathogen sensing and host defense. Nat Immunol 7, 1243-1249.
12. Martin GB, Bogdanove AJ & Sessa G (2003) Understanding the functions of plant disease resistance proteins. Annu Rev Plant Biol 54, 23-61.
13. Meyers BC, Dickerman AW & Michelmore RW (1999) Plant disease resistance genes encode members of an ancient and diverse protein family within the nucleotide-binding superfamily. Plant J 20, 317-332.
14. Luck JE, Lawrence GJ, Dodds PN, Shepherd KW & Ellis JG (2000) Regions outside of the leucine-rich repeats of Flax rust resistance proteins play a role in specificity determination. Plant Cell 12, 1367-1377.
15. van Ooijen G, van den Burg HA, Cornelissen BJ & Takken FL (2007) Structure and function of resistance proteins in solanaceous plants. Annu Rev Phytopathol 45, 43-72.
16. Bennetzen JL & Hake SC (2009) The Maize Handbook - Volume II: Genetics and Genomics, pp. 1-798. Springer, New York.
17. Schnable PS, Ware D, Fulton RS, Stein JC, Wei F, Pasternak S, Liang C, Zhang J, Fulton L, Graves TA et al. (2009) The B73 maize genome: complexity, diversity and dynamics. Science 326, 1112-1115.
18. Zwonitzer JC, Bubeck DM, Bhattramakki D, Goodman MM, Arellano C & Balint-Kurti PJ (2009) Use of selection with recurrent backcrossing and QTL mapping to identify loci contributing to southern leaf blight resistance in a highly resistant maize line. Theor Appl Genet 118, 911-925.
19. Mysore KS & Ryu CM (2004) Nonhost resistance: how much do we know? Trends Plant Sci 9, 97-104.
20. Ryals JA, Neuenschwander UH, Willits MG, Molina A, Steiner HY & Hunt MD (1996) Systemic acquired resistance. Plant Cell 8, 1809-1819.
21. Dong X (1998) SA, JA, ethylene, and disease resistance in plants. Curr Opin Plant Biol 1, 316-323.
22. Doares SH, Syrovets T, Weiler EW & Ryan CA (1995) Oligogalacturonidas and chitosan activate plant defensive genes through the octadecanoid pathway. Proc Nat Acad Sci USA 93, 4095-4098.
23. ODonnell PJ, Calvert C, Atzorn R, Wasternack C, Leyser HMO & Bowles DJ (1996) Ethylene as a signal mediating the wound response of tomato plants. Science 274, 1914-1917.
24. Dong J, Chen C & Chen Z (2003) Expression profiles of the Arabidopsis WRKY gene superfamily during plant defense response. Plant Mol Biol 51, 21-37.
25. Oh S, Baek K, Park J, Yi S, Yu S, Kamoun S & Choi D (2008) Capsicum annuum WRKY protein CaWRKY1 is a negative regulator of pathogen defense. New Phytol 177, 977-989.
26. MaizeSequence. Maize database. http://www.maizesequence. org/index.html.
27. 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 Genet Genomics 271, 402-415.
28. 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.
29. Holub EB (2001) The arms race is ancient history in Arabidopsis, the wildflower. Nat Rev Genet 2, 516-527.
30. Ameline-Torregrosa C, Wang BB & O'Bleness MS (2008) Identification and characterization of nucleotide-binding site-leucine-rich repeat genes in the model plant Medicago truncatula. Plant Physiol 146, 5-21.
31. Li X, Cheng Y, Ma W, Zhao Y, Jiang H & Zhang M (2010) Identification and characterization of NBS-encoding disease resistance genes in Lotus japonicus. Plant Syst Evol 289, 101-110.
32. Yang S, Zhang X, Yue J, Tian D & Chen J (2008) Recent duplications dominate NBS encoding gene expansion in two woody species. Mol Genet Genomics 280, 187-198.
33. Li J, Ding J, Zhang W, Zhang Y, Tang P, Chen J, Tian D & Yang S (2010) Unique evolutionary pattern of numbers of gramineous NBS-LRR genes. Mol Genet Genomics 283, 427-438.
34. Leister D (2004) Tandem and segmental gene duplication and recombination in the evolution of plant disease resistance genes. Trends Genet 20, 116-222.
35. Ding J, Araki H, Wang Q, Zhang P, Yang S, Chen J & Tian D (2007) Highly asymmetric rice genomes. BMC Genomics 8, 154.
36. Tian D, Traw MB, Chen JQ, Kreitman M & Bergelson J (2003) Fitness costs of R-gene-mediated resistance in Arabidopsis thaliana. Nature 423, 74-77.
37. Michelmore RW & Meyers BC (1998) Clusters of resistance genes in plants evolve by divergent selection and a birth-and-death process. Genome Res 8, 1113-1130.
38. Bennetzen JL, Qin MM, Ingels S & Ellingboe AH (1988) Allele-specific and Mutator-associated instability at the Rpl disease-resistance locus of maize. Nature 332, 369-370.
39. Richter TE, Pryor TJ, Bennetzen JL & Hulbert SH (1995) New rust resistance specificities associated with recombination in the Rp1 complex in maize. Genetics 141, 373-381.
40. Nagy ED & Bennetzen JL (2008) Pathogen corruption and site-directed recombination at a plant disease resistance gene cluster. Genome Res 18, 1918-1923.
41. 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.
42. Sun Q, Collins NC, Ayliffe M, Smith SM, Drake J, Pryor T & Hulbert SH (2001) Recombination between paralogues at the Rp1 rust resistance locus in maize. Genetics 158, 423-438.
43. Smith SM & Hulbert SH (2005) Recombination events generating a novel Rp1 race specificity. Mol Plant Microbe Interact 18, 220-228.
44. Smith SM, Pryor AJ & Hulbert SH (2004) Allelic and haplotypic diversity at the Rp1 rust resistance locus of maize. Genetics 167, 1939-1947.
45. Blanc G & Wolfe KH (2004) Functional divergence of duplicated genes formed by polyploidy during Arabidopsis evolution. Plant Cell 16, 1679-1691.
46. Tan X, Meyers B, Kozik A, West MAL, Morgante M, Clair DAS, Bent AF & Michelmore RW (2007) Global expression analysis of nucleotide binding site-leucine rich repeat-encoding and related genes in Arabidopsis. BMC Plant Biol 7, 56.
47. Kohler A, Rinaldi C, Duplessis S, Baucher M, Geelen D, Duchaussoy F, Meyers BC, Boerjan W & Martin F (2008) Genome-wide identification of NBS resistance genes in Populus trichocarpa. Plant Mol Biol 66, 619-636.
48. Finn RD, Mistry J, Tate J, Coggill P, Heger A, Pollington JE, Gavin OL, Gunasekaran P, Ceric G, Forslund K et al. (2010) The Pfam protein families database. Nucleic Acids Res 38(Database issue), D211-D222.
49. Schultz J, Milpetz F, Bork P & Ponting CP (1998) SMART, a simple modular architecture research tool: identification of signaling domains. Proc Natl Acad Sci USA 95, 5857-5864.
50. Lupas A, Van Dyke M & Stock J (1991) Predicting coiled coils from protein sequences. Science 252, 1162-1164.
51. Paterson AH, Bowers JE, Bruggmann R, Dubchak I, Grimwood J, Gundlach H, Haberer G, Hellsten U, Mitros T, Poliakov A et al. (2009) The Sorghum bicolor genome and the diversification of grasses. Nature 457, 551-556.
52. MapInspect software. http://www.plantbreeding.wur.nl/ uk/software-mapinspect.html.
53. Plocik A, Layden J & Kesseli R (2004) Comparative analysis of NBS domain sequences of NBS-LRR disease resistance genes from sunflower, lettuce, and chicory. Mol Phylogenet Evol 31, 153-163.
54. Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F & Higgins DG (1997) The CLUSTAL-X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 24, 4876-4882.
55. Tamura K, Dudley J, Nei M & Kumar S (2007) MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0. Mol Biol Evol 24, 1596-1599.
56. 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.
57. Gu Z, Cavalcanti A & Chen F (2002) Extent of gene duplication in the genomes of Drosophila, nematode, and yeast. Mol Biol Evol 19, 256-262.
58. Lin Y, Jiang H, Chu Z, Tang X, Zhu S & Cheng B (2011) Genome-wide identification, classification and analysis of heat shock transcription factor family in maize. BMC Genomics 12, 76.
59. Zhang D, Liu B, Zhao C, Lu X, Wan D, Ma F, Chen L & Liu J (2010) Ecological functions and differentially expressed transcripts of translucent bracts in an alpine 'glasshouse' plant Rheum nobile (Polygonaceae). Planta 231, 1505-1511.