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PMID: 23418910 Published · epublish English Journal Article Research Support, Non-U.S. Gov't

Genome-wide analysis of NBS-encoding disease resistance genes in Cucumis sativus and phylogenetic study of NBS-encoding genes in Cucurbitaceae crops.

BMC genomics ·Vol. 14 ·2013-02-19 ·Pages 109

Wan H, Yuan W, Bo K, Shen J, Pang X, Chen J

Abstract

Plant nucleotide-binding site (NBS)-leucine-rich repeat (LRR) proteins encoded by resistance genes play an important role in the responses of plants to various pathogens, including viruses, bacteria, fungi, and nematodes. In this study, a comprehensive analysis of NBS-encoding genes within the whole cucumber genome was performed, and the phylogenetic relationships of NBS-encoding resistance gene homologues (RGHs) belonging to six species in five genera of Cucurbitaceae crops were compared. Cucumber has relatively few NBS-encoding genes. Nevertheless, cucumber maintains genes belonging to both Toll/interleukine-1 receptor (TIR) and CC (coiled-coil) families. Eight commonly conserved motifs have been established in these two families which support the grouping into TIR and CC families. Moreover, three additional conserved motifs, namely, CNBS-1, CNBS-2 and TNBS-1, have been identified in sequences from CC and TIR families. Analyses of exon/intron configurations revealed that some intron loss or gain events occurred during the structural evolution between the two families. Phylogenetic analyses revealed that gene duplication, sequence divergence, and gene loss were proposed as the major modes of evolution of NBS-encoding genes in Cucurbitaceae species. Compared with NBS-encoding sequences from the Arabidopsis thaliana genome, the remaining seven TIR familes of NBS proteins and RGHs from Cucurbitaceae species have been shown to be phylogenetically distinct from the TIR family of NBS-encoding genes in Arabidopsis, except for two subfamilies (TIR4 and TIR9). On the other hand, in the CC-NBS family, they grouped closely with the CC family of NBS-encoding genes in Arabidopsis. Thus, the NBS-encoding genes in Cucurbitaceae crops are shown to be ancient, and NBS-encoding gene expansions (especially the TIR family) may have occurred before the divergence of Cucurbitaceae and Arabidopsis. The results of this paper will provide a genomic framework for the further isolation of candidate disease resistance NBS-encoding genes in cucumber, and contribute to the understanding of the evolutionary mode of NBS-encoding genes in Cucurbitaceae crops.

MeSH Terms
Arabidopsis/genetics Binding Sites Chromosomes, Plant/genetics Conserved Sequence Crops, Agricultural/genetics,immunology Cucumis sativus/genetics,immunology Databases, Genetic Disease Resistance/genetics Exons/genetics Genes, Plant/genetics Genetic Variation/genetics Genomics Introns/genetics Nucleotide Motifs/genetics Nucleotides/metabolism Phylogeny Plant Diseases/immunology Sequence Homology, Nucleic Acid
Chemicals
Nucleotides
Authors & Affiliations
6 authors, click to expand affiliations / ORCID
Wan Hongjian
State Key Laboratory of Crop Genetics and Germplasm Enhancement, College of Horticulture, Nanjing Agricultural University, Nanjing 210095, People's Republic of China.
Yuan Wei
Bo Kailiang
Shen Jia
Pang Xin
Chen Jinfeng
References (47)
47 references, click to expand
  1. Predicting coiled coils from protein sequences.
    Science. 1991 May 24;252(5009):1162-4 PMID: 2031185
  2. Mode of amplification and reorganization of resistance genes during recent Arabidopsis thaliana evolution.
    Mol Biol Evol. 2002 Jan;19(1):76-84 PMID: 11752192
  3. Diversity in nucleotide binding site-leucine-rich repeat genes in cereals.
    Genome Res. 2002 Dec;12(12):1871-84 PMID: 12466291
  4. Resistance gene candidates identified by PCR with degenerate oligonucleotide primers map to clusters of resistance genes in lettuce.
    Mol Plant Microbe Interact. 1998 Aug;11(8):815-23 PMID: 9675895
  5. From Guard to Decoy: a new model for perception of plant pathogen effectors.
    Plant Cell. 2008 Aug;20(8):2009-17 PMID: 18723576
  6. The genome of black cottonwood, Populus trichocarpa (Torr. & Gray).
    Science. 2006 Sep 15;313(5793):1596-604 PMID: 16973872
  7. Genome-wide investigation on the genetic variations of rice disease resistance genes.
    Plant Mol Biol. 2006 Sep;62(1-2):181-93 PMID: 16915523
  8. Structure and function of proteins controlling strain-specific pathogen resistance in plants.
    Curr Opin Plant Biol. 1998 Aug;1(4):288-93 PMID: 10066601
  9. Plant disease resistance genes: recent insights and potential applications.
    Trends Biotechnol. 2003 Apr;21(4):178-83 PMID: 12679066
  10. Genome-wide identification of NBS genes in japonica rice reveals significant expansion of divergent non-TIR NBS-LRR genes.
    Mol Genet Genomics. 2004 May;271(4):402-15 PMID: 15014983
  11. Comparative genetics of nucleotide binding site-leucine rich repeat resistance gene homologues in the genomes of two dicotyledons: tomato and arabidopsis.
    Genetics. 2000 May;155(1):309-22 PMID: 10790405
  12. Plant disease resistance genes encode members of an ancient and diverse protein family within the nucleotide-binding superfamily.
    Plant J. 1999 Nov;20(3):317-32 PMID: 10571892
  13. Resistance gene homologues in melon are linked to genetic loci conferring disease and pest resistance.
    Theor Appl Genet. 2002 May;104(6-7):1055-1063 PMID: 12582612
  14. Gourds afloat: a dated phylogeny reveals an Asian origin of the gourd family (Cucurbitaceae) and numerous oversea dispersal events.
    Proc Biol Sci. 2009 Mar 7;276(1658):843-51 PMID: 19033142
  15. Gene-for-gene complementarity in plant-pathogen interactions.
    Annu Rev Genet. 1990;24:447-63 PMID: 2088175
  16. Plant disease-resistance proteins and the gene-for-gene concept.
    Trends Biochem Sci. 1998 Dec;23(12):454-6 PMID: 9868361
  17. Identification and localisation of the NB-LRR gene family within the potato genome.
    BMC Genomics. 2012 Feb 15;13:75 PMID: 22336098
  18. Phylogenetic relationships among domesticated and wild species of Cucurbita (Cucurbitaceae) inferred from a mitochondrial gene: Implications for crop plant evolution and areas of origin.
    Proc Natl Acad Sci U S A. 2002 Jan 8;99(1):535-40 PMID: 11782554
  19. TIR-NBS-LRR genes are rare in monocots: evidence from diverse monocot orders.
    BMC Res Notes. 2009 Sep 28;2:197 PMID: 19785756
  20. Genome-wide analysis of NBS-LRR-encoding genes in Arabidopsis.
    Plant Cell. 2003 Apr;15(4):809-34 PMID: 12671079
  21. Genome-wide identification of NBS resistance genes in Populus trichocarpa.
    Plant Mol Biol. 2008 Apr;66(6):619-36 PMID: 18247136
  22. The genome of melon (Cucumis melo L.).
    Proc Natl Acad Sci U S A. 2012 Jul 17;109(29):11872-7 PMID: 22753475
  23. Fine genetic mapping localizes cucumber scab resistance gene Ccu into an R gene cluster.
    Theor Appl Genet. 2011 Mar;122(4):795-803 PMID: 21104067
  24. Diversity, distribution, and ancient taxonomic relationships within the TIR and non-TIR NBS-LRR resistance gene subfamilies.
    J Mol Evol. 2002 Apr;54(4):548-62 PMID: 11956693
  25. Understanding the functions of plant disease resistance proteins.
    Annu Rev Plant Biol. 2003;54:23-61 PMID: 14502984
  26. The neighbor-joining method: a new method for reconstructing phylogenetic trees.
    Mol Biol Evol. 1987 Jul;4(4):406-25 PMID: 3447015
  27. Systematic analysis and comparison of nucleotide-binding site disease resistance genes in maize.
    FEBS J. 2012 Jul;279(13):2431-43 PMID: 22564701
  28. Identification and 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 Aug 23;10:186 PMID: 20731821
  29. [GSDS: a gene structure display server].
    Yi Chuan. 2007 Aug;29(8):1023-6 PMID: 17681935
  30. Genome-wide analysis of Carica papaya reveals a small NBS resistance gene family.
    Mol Genet Genomics. 2009 Jun;281(6):609-26 PMID: 19263082
  31. Isolation and diversity analysis of resistance gene analogues (RGAs) from cultivated and wild strawberries.
    Mol Genet Genomics. 2004 Nov;272(4):480-7 PMID: 15565466
  32. Divergent evolution of plant NBS-LRR resistance gene homologues in dicot and cereal genomes.
    J Mol Evol. 2000 Mar;50(3):203-13 PMID: 10754062
  33. Resistance gene analogs are conserved and clustered in soybean.
    Proc Natl Acad Sci U S A. 1996 Oct 15;93(21):11746-50 PMID: 8876208
  34. Isolation of TIR and non-TIR 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 Sep;111(5):819-30 PMID: 16075209
  35. MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods.
    Mol Biol Evol. 2011 Oct;28(10):2731-9 PMID: 21546353
  36. PRGdb: a bioinformatics platform for plant resistance gene analysis.
    Nucleic Acids Res. 2010 Jan;38(Database issue):D814-21 PMID: 19906694
  37. A PCR-based approach for isolating pathogen resistance genes from potato with potential for wide application in plants.
    Nat Genet. 1996 Dec;14(4):421-9 PMID: 8944022
  38. Identification and characterization of nucleotide-binding site-leucine-rich repeat genes in the model plant Medicago truncatula.
    Plant Physiol. 2008 Jan;146(1):5-21 PMID: 17981990
  39. Origin, diversity and evolution of NBS-type disease-resistance gene homologues in coffee trees (Coffea L.).
    Mol Genet Genomics. 2001 Jun;265(4):654-62 PMID: 11459185
  40. The Fusarium wilt resistance locus Fom-2 of melon contains a single resistance gene with complex features.
    Plant J. 2004 Aug;39(3):283-97 PMID: 15255859
  41. Comparative analysis of NBS domain sequences of NBS-LRR disease resistance genes from sunflower, lettuce, and chicory.
    Mol Phylogenet Evol. 2004 Apr;31(1):153-63 PMID: 15019616
  42. The genome of the cucumber, Cucumis sativus L.
    Nat Genet. 2009 Dec;41(12):1275-81 PMID: 19881527
  43. Recent duplications dominate NBS-encoding gene expansion in two woody species.
    Mol Genet Genomics. 2008 Sep;280(3):187-98 PMID: 18563445
  44. Isolation, characterization and expression studies of resistance gene candidates (RGCs) from Zingiber spp.
    Theor Appl Genet. 2007 Dec;116(1):123-34 PMID: 17928987
  45. Broad-spectrum mildew resistance in Arabidopsis thaliana mediated by RPW8.
    Science. 2001 Jan 5;291(5501):118-20 PMID: 11141561
  46. The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools.
    Nucleic Acids Res. 1997 Dec 15;25(24):4876-82 PMID: 9396791
  47. Plant pathogens and integrated defence responses to infection.
    Nature. 2001 Jun 14;411(6839):826-33 PMID: 11459065
Article Info
Journal
BMC genomics
Abbr.
BMC Genomics
ISSN
1471-2164
DOI
10.1186/1471-2164-14-109
Published
2013-02-19
Epub
2013-00-19
Pages
109
Language
English
Region
England
NLM ID
100965258
PMCID
PMC3599390
Subset
IM
External Links
PubMed source DOI: 10.1186/1471-2164-14-109 PMC Full Text View journal details
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