|
|
|
Evolution of Xanthomonas Gene Content: Gene Gain/Loss History and Species Divergence |
JIN Gu-lei, ZHANG Guo-qing, ZHU Jun, ZHOU Xue-ping, SUN Guo-chang, LI Bin, ZHU Bo |
1.State Key Laboratory of Rice Biology and Key Laboratory of Molecular Biology of Crop Pathogens and Insects, Ministry of Agriculture/Institute of Biotechnology, Zhejiang University, Hangzhou 310029, P.R.China
2.Institute of Bioinformatics, Zhejiang University, Hangzhou 310029, P.R.China
3.Crop Management Station, Jiaxing 314051, P.R.China
4.State Key Laboratory Breeding Base for Zhejiang Sustainable Pest and Disease Control/Institute of Plant Protection and Microbiology,Zhejiang Academy of Agricultural Sciences, Hangzhou 310021, P.R.China |
|
|
摘要 Horizontal gene transfer (HGT) plays key roles in the evolution of pathogenetic bacteria, especially in pathogenetic associated genes. In this study, the evolutionary dynamics of Xanthomonas at species level were determined by the comparative analysis of the complete genomes of 15 Xanthomonas strains. A concatenated multiprotein phyletic pattern and a dataset with Xanthomonas clusters of orthologous genes were constructed. Mathematical extrapolation estimates that the core genome will reach a minimum of about 1 547 genes while the pan-genome will increase up to 22 624 genes when sequencing 1 000 genomes. The HGT extent in this genus was assessed by using a Markov-based probabilistic method. The reconstructed gene gain/loss history, which contained several features consistent with biological observations, showed that nearly 60% of the Xanthomonas genes were acquired by HGT. A large fraction of variability was in the clade ancestor nodes and “leaves of the tree”. Coexpression analysis suggested that the pathogenic and metabolic variation between Xanthomonas oryzae pv. oryzicola and Xanthomonas oryzae pv. oryzae might due to recently-transferred genes. Our results strongly supported that the gene gain/loss may play an important role in divergence and pathogenicity variation of Xanthomonas species.
Abstract Horizontal gene transfer (HGT) plays key roles in the evolution of pathogenetic bacteria, especially in pathogenetic associated genes. In this study, the evolutionary dynamics of Xanthomonas at species level were determined by the comparative analysis of the complete genomes of 15 Xanthomonas strains. A concatenated multiprotein phyletic pattern and a dataset with Xanthomonas clusters of orthologous genes were constructed. Mathematical extrapolation estimates that the core genome will reach a minimum of about 1 547 genes while the pan-genome will increase up to 22 624 genes when sequencing 1 000 genomes. The HGT extent in this genus was assessed by using a Markov-based probabilistic method. The reconstructed gene gain/loss history, which contained several features consistent with biological observations, showed that nearly 60% of the Xanthomonas genes were acquired by HGT. A large fraction of variability was in the clade ancestor nodes and “leaves of the tree”. Coexpression analysis suggested that the pathogenic and metabolic variation between Xanthomonas oryzae pv. oryzicola and Xanthomonas oryzae pv. oryzae might due to recently-transferred genes. Our results strongly supported that the gene gain/loss may play an important role in divergence and pathogenicity variation of Xanthomonas species.
|
Received: 16 May 2011
Accepted:
|
Fund: This project was supported by the Natural Science Foundation of Zhejiang Province of China (Y3090150), the Fundamental Research Funds for the Central Universities, China, the Zhejiang Provincial Project, China (2010R10091), the Research Project for Commonweal Industry of Agricultural Ministry, China (nyhyzx 201003029; 201003066), the Specialized Research Fund for the Doctoral Program of Higher Education, China (20090101120083), and the Key Subject Construction Program for Modern Agricultural Biotechnology and Crop Disease Control of Zhejiang, China. |
Corresponding Authors:
LI Bin, Tel: +86-571-88982412, E-mail: libin0571@zju.edu.cn; ZHU Bo, Tel: +86-571-88982412, E-mail:bzhu@zju.edu.cn
E-mail: libin0571@zju.edu.cn
|
About author: JIN Gu-lei, E-mail: guleijin@zju.edu.cn |
Cite this article:
JIN Gu-lei, ZHANG Guo-qing, ZHU Jun, ZHOU Xue-ping, SUN Guo-chang, LI Bin, ZHU Bo .
2012.
Evolution of Xanthomonas Gene Content: Gene Gain/Loss History and Species Divergence. Journal of Integrative Agriculture, 12(6): 954-961.
|
[1]Aritua V, Parkinson N, Thwaites R, Heeney J V, Jones D R, Tushemereirwe W, Crozier J, Reeder R, Stead D E, Smith J. 2008. Characterization of the Xanthomonas sp causing wilt of enset and banana and its proposed reclassification as a strain of X. vasicola. Plant Pathology, 57, 170-177. [2]Blaby-Haas C E, de Crecy-Lagard V. 2011. Mining highthroughput experimental data to link gene and function. Trends in Biotechnology, 29, 174-182. [3]Büttner D, Bonas U. 2010. Regulation and secretion of Xanthomonas virulence factors. FEMS Microbiology Reviews, 34, 107-133. [4]de Buck E, Lammertyn E, Anné J. 2008. The importance of the twin-arginine translocation pathway for bacterial virulence. Trends in Microbiology, 16, 442-453. [5]Capella-Gutierrez S, Silla-Martinez J M, Gabaldon T. 2009. trimAl: a tool for automated alignment trimming in largescale phylogenetic analyses. Bioinformatics, 25, 1972-1973. [6]Champoiseau P, Daugrois J H, Pieretti I, Cociancich S, Royer M, Rott P. 2006. High variation in pathogenicity of genetically closely related strains of Xanthomonas albilineans, the sugarcane leaf scald pathogen, in guadeloupe. Phytopathology, 96, 1081-1091. [7]Cohen O, Pupko T. 2010. Inference and characterization of horizontally transferred gene families using stochastic mapping. Molecular Biology and Evolution, 27, 703-713. [8]Collado-Vides J, Salgado H, Morett E, Gama-Castro S, Jimenez-Jacinto V, Martinez-Flores I, Medina-Rivera A, Muniz-Rascado L, Peralta-Gil M, Santos-Zavaleta A. 2009. Bioinformatics resources for the study of gene regulation in bacteria. Journal of Bacteriology, 191, 23-31. [9]Comas I, Moya A, Azad R K, Lawrence J G, Gonzalez-Candelas F. 2006. The evolutionary origin of Xanthomonadales genomes and the nature of the horizontal gene transfer process. Molecular Biology and Evolution, 23, 2049-2057. [10]Csürös M, Holey J A, Rogozin I B. 2007. In search of lost introns. Bioinformatics, 23, i87-i96. Csürös M, Rogozin I B, Koonin E V. 2008. Extremely intronrich genes in the alveolate ancestors inferred with a flexible maximum-likelihood approach. Molecular Biology and Evolution, 25, 903-911. [11]Edgar R C. 2004. MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Research, 32, 1792-1797. [12]Felsenstein J. 1995. PHYLIP (Phylogeny Inference Package). ver. 3.57 c. Department of Genetics, University of Washington, Seattle. [13]Gentleman R C, Carey V J, Bates D M, Bolstad B, Dettling M, Dudoit S, Ellis B, Gautier L, Ge Y C, Gentry J, et al. 2004. Bioconductor: open software development for computational biology and bioinformatics. Genome Biology, 5, R80. [14]Guindon S, Gascuel O. 2003. A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Systematic Biology, 52, 696-704. [15]Johnson T L, Abendroth J, Hol W G J, Sandkvist M. 2006. Type II secretion: from structure to function. FEMS Microbiology Letters, 255, 175-186. [16]Jones D T, Taylor W R, Thornton J M. 1994. A mutation data matrix for transmembrane proteins. FEBS Letters, 339, 269-275. [17]Juhas M, van der Meer J R, Gaillard M, Harding R M, Hood D W, Crook D W. 2009. Genomic islands: tools of bacterial horizontal gene transfer and evolution. FEMS Microbiology Reviews, 33, 376-393. [18]Keshavarzi M, Soylu S, Brown I, Bonas U, Nicole M, Rossiter J, Mansfield J. 2004. Basal defenses induced in pepper by lipopolysaccharides are suppressed by Xanthomonas campestris pv. vesicatoria. Molecular Plant-Microbe Interactions, 17, 805-815. [19]Kettler G C, Martiny A C, Huang K, Zucker J, Coleman M L, Rodrigue S, Chen F, Lapidus A, Ferriera S, Johnson J, et al. 2007. Patterns and implications of gene gain and loss in the evolution of Prochlorococcus. PLoS Genetics, 3, 2515-2528. [20]Lapierrel P, Gogarten J P. 2009. Estimating the size of the bacterial pan-genome. Trends in Genetics, 25, 107-110. [21]Lee B M, Park Y J, Park D S, Kang H W, Kim J G, Song E S, Park I C, Yoon U H, Hahn J H, Koo B S, et al. 2005. The genome sequence of Xanthomonas oryzae pathovar oryzae KACC10331, the bacterial blight pathogen of rice. Nucleic Acids Research, 33, 577-586. [22]Li L, Stoeckert C J, Roos D S. 2003. OrthoMCL: Identification of ortholog groups for eukaryotic genomes. Genome Research, 13, 2178-2189. [23]Lima W, Paquola A C M, Varani A, Vansluys M A, Menck C M. 2008. Laterally transferred genomic islands in Xanthomonadales related to pathogenicity and primary metabolism. FEMS Microbiology Letters, 281, 87-97. [24]Moscou M J, Bogdanove A J. 2009. A simple cipher governs DNA recognition by TAL effectors. Science, 326, 1501-1501. [25]Ni Liu D O, Ronald P C, Bogdanove A J. 2006. Xanthomonas oryzae pathovars: model pathogens of a model crop. Molecular Plant Pathology, 7, 303-324. [26]Pieretti I, Royer M, Barbe V, Carrere S, Koebnik R, Cociancich S, Couloux A, Darrasse A, Gouzy J, Jacques M A, et al. 2009. The complete genome sequence of Xanthomonas albilineans provides new insights into the reductive genome evolution of the xylem-limited Xanthomonadaceae. BMC Genomics, 10, 616. [27]Sarkar S F, Guttman D S. 2004. Evolution of the core genome of Pseudomonas syringae, a highly clonal, endemic plant pathogen. Applied and Environmental Microbiology, 70, 1999-2012. [28]Seo Y S, Sriariyanun M, Wang L, Pfeiff J, Phetsom J, Lin Y, Jung K H, Chou H H, Bogdanove A, Ronald P. 2008. A two-genome microarray for the rice pathogens Xanthomonas oryzae pv. oryzae and X. oryzae pv. oryzicola and its use in the discovery of a difference in their regulation of hrp genes. BMC Microbiology, 8, 99. [29]Steel M. 1994. Recovering a tree from the leaf colourations it generates under a markov model. Applied Mathematics Letters, 7, 19-23. [30]Studholme D J, Kemen E, MacLean D, Schornack S, Aritua V, Thwaites R, Grant M, Smith J, Jones J D G. 2010. Genome-wide sequencing data reveals virulence factors implicated in banana Xanthomonas wilt. FEMS Microbiology Letters, 310, 182-192. [31]Tettelin H, Masignani V, Cieslewicz M J, Donati C, Medini D, Ward N L, Angiuoli S V, Crabtree J, Jones A L, Durkin A S, et al. 2005. Genome analysis of multiple pathogenic isolates of Streptococcus agalactiae: implications for the microbial an-genome? Proceedings of the National Academy of Sciences of the United States of America, 102, 13950-13955. [32]Verniere C, Pruvost O, Civerolo E L, Gambin O, Jacquemoudcollet J P, Luisetti J. 1993. Evaluation of the biolog substrate utilization system to identify and assess metabolic variation among strains of Xanthomonas campestris pv. citri. Applied and Environmental Microbiology, 59, 243-249. [33]Wattam A R, Williams K P, Snyder E E, Almeida N F, Shukla M, Dickerman A W, Crasta O R, Kenyon R, Lu J, Shallom J M, et al. 2009. Analysis of ten brucella genomes reveals evidence for horizontal gene transfer despite a preferred intracellular lifestyle. Journal of Bacteriology, 191, 3569-3579. [34]White F F, Potnis N, Jones J B, Koebnik R. 2009. The type III effectors of Xanthomonas. Molecular Plant Pathology, 10, 749-766. [35]White F F, Yang B. 2009. Host and Pathogen Factors Controlling the Rice-Xanthomonas oryzae Interaction. Plant Physiology, 150, 1677-1686. |
No Suggested Reading articles found! |
|
|
Viewed |
|
|
|
Full text
|
|
|
|
|
Abstract
|
|
|
|
|
Cited |
|
|
|
|
|
Shared |
|
|
|
|
|
Discussed |
|
|
|
|