期刊论文详细信息
BMC Microbiology
Extensive remodeling of the Pseudomonas syringae pv. avellanae type III secretome associated with two independent host shifts onto hazelnut
David S Guttman1  Marco Scortichini3  Choseung Yong2  Pauline W Wang1  Lijie Yuan1  Jianfeng Zhang1  Pauline Fung1  Yunchen Gong1  Shalabh Thakur2  Heath E O’Brien2 
[1] Center for the Analysis of Genome Evolution & Function, University of Toronto, 25 Willcocks St., Toronto, ON, M5S 3B2, Canada;Department of Cell and Systems Biology, University of Toronto, 25 Willcocks St., Toronto, ON, M5S 3B2, Canada;C.R.A.- Fruit Crops Research Centre, Via di Fioranello, 52; I-00134, Rome, Italy
关键词: Molecular dating;    Host specificity;    Effector;   
Others  :  1221823
DOI  :  10.1186/1471-2180-12-141
 received in 2012-01-06, accepted in 2012-07-16,  发布年份 2012
PDF
【 摘 要 】

Background

Hazelnut (Corylus avellana) decline disease in Greece and Italy is caused by the convergent evolution of two distantly related lineages of Pseudomonas syringae pv. avellanae (Pav). We sequenced the genomes of three Pav isolates to determine if their convergent virulence phenotype had a common genetic basis due to either genetic exchange between lineages or parallel evolution.

Results

We found little evidence for horizontal transfer (recombination) of genes between Pav lineages, but two large genomic islands (GIs) have been recently acquired by one of the lineages. Evolutionary analyses of the genes encoding type III secreted effectors (T3SEs) that are translocated into host cells and are important for both suppressing and eliciting defense responses show that the two Pav lineages have dramatically different T3SE profiles, with only two shared putatively functional T3SEs. One Pav lineage has undergone unprecedented secretome remodeling, including the acquisition of eleven new T3SEs and the loss or pseudogenization of 15, including five of the six core T3SE families that are present in the other Pav lineage. Molecular dating indicates that divergence within both of the Pav lineages predates their observation in the field. This suggest that both Pav lineages have been cryptically infecting hazelnut trees or wild relatives for many years, and that the emergence of hazelnut decline in the 1970s may have been due to changes in agricultural practice.

Conclusions

These data show that divergent lineages of P. syringae can converge on identical disease etiology on the same host plant using different virulence mechanisms and that dramatic shifts in the arsenal of T3SEs can accompany disease emergence.

【 授权许可】

   
2012 O'Brien et al.; licensee BioMed Central Ltd.

【 预 览 】
附件列表
Files Size Format View
20150804004717243.pdf 994KB PDF download
Figure 4. 120KB Image download
Figure 3. 38KB Image download
Figure 2. 138KB Image download
Figure 1. 29KB Image download
【 图 表 】

Figure 1.

Figure 2.

Figure 3.

Figure 4.

【 参考文献 】
  • [1]Hwang MSH, Morgan RL, Sarkar SF, Wang PW, Guttman DS: Phylogenetic characterization of virulence and resistance phenotypes of Pseudomonas syringae. Appl Environ Microbiol 2005, 71:5182-5191.
  • [2]Sarkar SF, Guttman DS: Evolution of the core genome of Pseudomonas syringae, a highly clonal, endemic plant pathogen. Appl Environ Microbiol 2004, 70:1999-2012.
  • [3]Scortichini M: Bacterial canker and decline of European hazelnut. Plant Dis 2002, 86:704-709.
  • [4]Baltrus DA, Nishimura MT, Romanchuk A, Chang JH, Mukhtar MS, Cherkis K, Roach J, Grant SR, Jones CD, Dangl JL: Dynamic evolution of pathogenicity revealed by sequencing and comparative genomics of 19 Pseudomonas syringae isolates. PLoS Pathog 2011, 7:e1002132.
  • [5]Marcelletti S, Ferrante P, Petriccione M, Firrao G, Scortichini M: Pseudomonas syringae pv. actinidiae draft genomes comparison reveal strain-specific features involved in adaptation and virulence to Actinidia species. PLoS One 2011, 6:e27297.
  • [6]Wang PW, Morgan RL, Scortichini M, Guttman DS: Convergent evolution of phytopathogenic pseudomonads onto hazelnut. Microbiology 2007, 153:2067-2073.
  • [7]Cai R, Lewis J, Yan S, Liu H, Clarke CR, Campanile F, Almeida NF, Studholme DJ, Lindeberg M, Schneider D, et al.: The plant pathogen Pseudomonas syringae pv. tomato is genetically monomorphic and under strong selection to evade tomato immunity. PLoS Pathog 2011, 7:e1002130.
  • [8]Joardar V, Lindeberg M, Jackson RW, Selengut J, Dodson R, Brinkac LM, Daugherty SC, DeBoy R, Durkin AS, Giglio MG, et al.: Whole-genome sequence analysis of Pseudomonas syringae pv. phaseolicola 1448A reveals divergence among pathovars in genes involved in virulence and transposition. J Bacteriol 2005, 187:6488-6498.
  • [9]Studholme DJ, Gimenez Ibanez S, MacLean D, Dangl JL, Chang JH, Rathjen JP: A draft genome sequence and functional screen reveals the repertoire of type III secreted proteins of Pseudonomas syringae pathovar tabaci 11528. BMC Genomics 2009, 10:395. BioMed Central Full Text
  • [10]Almeida NF, Yan S, Lindeberg M, Studholme DJ, Schneider DJ, Condon B, Liu H, Viana CJ, Warren A, Evans C, et al.: A draft genome sequence of Pseudomonas syringae pv. tomato T1 reveals a type III effector repertoire significantly divergent from that of Pseudomonas syringae pv. tomato DC3000. Mol Plant Microbe Interact 2009, 22:52-62.
  • [11]Farrer RA, Kemen E, Jones JDG, Studholme DJ: De novo assembly of the Pseudomonas syringae pv. syringae B728a genome using Illumina/Solexa short sequence reads. FEMS Microbiol Lett 2009, 291:103-111.
  • [12]Green S, Studholme DJ, Laue BE, Dorati F, Lovell H, Arnold D, Cottrell JE, Bridgett S, Blaxter M, Huitema E, et al.: Comparative genome analysis provides insights into the evolution and adaptation of Pseudomonas syringae pv. aesculi on Aesculus hippocastanum. PLoS One 2010, 5:e10224.
  • [13]Qi M, Wang D, Bradley CA, Zhao Y: Genome sequence analyses of Pseudomonas savastanoi pv. glycinea and subtractive hybridization-based comparative genomics with nine pseudomonads. PLoS One 2011, 6:e16451.
  • [14]Reinhardt JA, Baltrus DA, Nishimura MT, Jeck WR, Jones CD, Dangl JL: De novo assembly using low-coverage short read sequence data from the rice pathogen Pseudomonas syringae pv. oryzae. Genome Res 2009, 19:294-305.
  • [15]Rodríguez-Palenzuela P, Matas IM, Murillo J, López-Solanilla E, Bardaji L, Pérez-Martínez I, Rodríguez-Moskera ME, Penyalver R, López MM, Quesada JM, et al.: Annotation and overview of the Pseudomonas savastanoi pv. savastanoi NCPPB 3335 draft genome reveals the virulence gene complement of a tumour-inducing pathogen of woody hosts. Environ Microbiol 2010, 12:1604-1620.
  • [16]Buell CR, Joardar V, Lindeberg M, Selengut J, Paulsen IT, Gwinn ML, Dodson RJ, Deboy RT, Durkin AS, Kolonay JF, et al.: The complete genome sequence of the Arabidopsis and tomato pathogen Pseudomonas syringae pv. tomato DC3000. Proc Natl Acad Sci U S A 2003, 100:10181-10186.
  • [17]Feil H, Feil WS, Chain P, Larimer F, DiBartolo G, Copeland A, Lykidis A, Trong S, Nolan M, Goltsman E, et al.: Comparison of the complete genome sequences of Pseudomonas syringae pv. syringae B728a and pv. tomato DC3000. Proc Natl Acad Sci U S A 2005, 102:11064-11069.
  • [18]Fox J, Weisberg S: An R Companion to Applied Regression. 2nd edition. Sage Publications, Thousand Oaks CA; 2011.
  • [19]R Deveolpment Core Team: R: A Language and Environment for Statistical Computing. R Foundation for Statistical Computing, Vienna, Austria; 2011.
  • [20]Darling AE, Mau B, Perna NT: progressiveMauve: multiple genome alignment with gene gain, loss and rearrangement. PLoS One 2010, 5:e11147.
  • [21]Nübel U, Dordel J, Kurt K, Strommenger B, Westh H, Shukla SK, Žemličková H, Leblois R, Wirth T, Jombart T, et al.: A timescale for evolution, population expansion, and spatial spread of an emerging clone of methicillin-resistant Staphylococcus aureus. PLoS Pathog 2010, 6:e1000855.
  • [22]Ochman H, Wilson AC: Evolution in bacteria: evidence for a universal substitution rate in cellular genomes. J Mol Evol 1987, 26:74-86.
  • [23]Kim SW, Jung WH, Ryu JM, Kim JB, Jang HW, Jo YB, Jung JK, Kim JH: Identification of an alternative translation initiation site for the Pantoea ananatis lycopene cyclase (crtY) gene in E. coli and its evolutionary conservation. Protein Expr Purif 2008, 58:23-31.
  • [24]Morelli G, Didelot X, Kusecek B, Schwarz S, Bahlawane C, Falush D, Suerbaum S, Achtman M: Microevolution of Helicobacter pylori during prolonged infection of single hosts and within families. PLoS Genet 2010, 6:e1001036.
  • [25]Bos KI, Schuenemann VJ, Golding GB, Burbano HA, Waglechner N, Coombes BK, Mcphee JB, Dewitte SN, Meyer M, Schmedes S, et al.: A draft genome of Yersinia pestis from victims of the Black Death. Nature 2011, 478:506-510.
  • [26]Scortichini M: The problem caused by Pseudomonas avellanae on hazelnut in Italy. Proceedings of the Fifth International Congress on Hazelnut. Acta Horticulturae 2001, 556:503-508.
  • [27]Scortichini M, Marchesi U, Angelucci L: Occurrence of Pseudomonas avellanae (Psallidas) Janse et al. and related pseudomonads on wild Corylus avellana trees and genetic relationships with strains isolated from cultivated hazelnuts. J Phytopathol 2000, 148:523-532.
  • [28]Lorang JM, Keen NT: Characterization of avrE from Pseudomonas syringae pv. tomato: a hrp-linked avirulence locus consisting of at least two transcriptional units. MPMI 1995, 8:49-57.
  • [29]DebRoy S, Thilmony R, Kwack Y-B, Nomura K, He SY: A family of conserved bacterial effectors inhibits salicylic acid-mediated basal immunity and promotes disease necrosis in plants. Proc Natl Acad Sci USA 2004, 101:9927-9932.
  • [30]Bogdanove AJ, Kim JF, Wei Z, Kolchinsky P, Charkowski AO, Conlin AK, Collmer A, Beer SV: Homology and functional similarity of an hrp-linked pathogenicity locus, dspEF, of Erwinia amylovora and the avirulence locus avrE of Pseudomonas syringae pathovar tomato. Proc Natl Acad Sci USA 1998, 95:1325-1330.
  • [31]Frederick RD, Ahmad M, Majerczak DR, Arroyo-Rodríguez AS, Manulis S, Coplin DL: Genetic organization of the Pantoea stewartii subsp. stewartii hrp gene cluster and sequence analysis of the hrpA, hrpC, hrpN, and wtsE operons. MPMI 2001, 14:1213-1222.
  • [32]Gaudriault S, Malandrin L, Paulin JP, Barny MA: DspA, an essential pathogenicity factor of Erwinia amylovora showing homology with AvrE of Pseudomonas syringae, is secreted via the Hrp secretion pathway in a DspB-dependent way. Mol Microbiol 1997, 26:1057-1069.
  • [33]Badel JL, Shimizu R, Oh H-S, Collmer A: A Pseudomonas syringae pv. tomato avrE1/hopM1 mutant is severely reduced in growth and lesion formation in tomato. Mol Plant Microbe Interact 2006, 19:99-111.
  • [34]Kvitko BH, Park DH, Velasquez AC, Wei CF, Russell AB, Martin GB, Schneider DJ, Collmer A: Deletions in the repertoire of Pseudomonas syringae pv. tomato DC3000 type III secretion effector genes reveal functional overlap among effectors. PLoS Pathog 2009, 5:e1000388.
  • [35]Li X, Lin H, Zhang W, Zou Y, Zhang J, Tang X, Zhou J-M: Flagellin induces innate immunity in nonhost interactions that is suppressed by Pseudomonas syringae effectors. Proc Natl Acad Sci USA 2005, 102:12990-12995.
  • [36]O'Brien HE, Gong Y, Fung P, Wang PW, Guttman DS: Use of low-coverage, large-insert, short-read data for rapid and accurate generation of enhanced-quality draft Pseudomonas genome sequences. PLoS One 2011, 6:e27199.
  • [37]Boetzer M, Henkel CV, Jansen HJ, Butler D, Pirovano W: Scaffolding pre-assembled contigs using SSPACE. Bioinformatics (Oxford, England) 2011, 27:578-579.
  • [38]Aziz RK, Bartels D, Best AA, DeJongh M, Disz T, Edwards RA, Formsma K, Gerdes S, Glass EM, Kubal M, et al.: The RAST server: rapid annotations using subsystems technology. BMC Bioinforma 2008, 9:75. BioMed Central Full Text
  • [39]Altschul SF, Madden TL, Schäffer AA, Zhang J, Zhang Z, Miller W, Lipman DJ: Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 1997, 25:3389-3402.
  • [40]Li L, Stoeckert CJ, Roos DS: OrthoMCL: identification of ortholog groups for eukaryotic genomes. Genome Res 2003, 13:2178-2189.
  • [41]Carver TJ, Rutherford KM, Berriman M, Rajandream M-A, Barrell BG, Parkhill J: ACT: the Artemis Comparison Tool. Bioinformatics (Oxford, England) 2005, 21:3422-3423.
  • [42]Edgar RC: MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 2004, 32:1792-1797.
  • [43]Abascal F, Zardoya R, Telford MJ: TranslatorX: multiple alignment of nucleotide sequences guided by amino acid translations. Nucleic Acids Res 2010, 38:W7-W13.
  • [44]Guindon S, Gascuel O: A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst Biol 2003, 52:696-704.
  • [45]Anisimova M, Gascuel O: Approximate likelihood-ratio test for branches: A fast, accurate, and powerful alternative. Syst Biol 2006, 55:539-552.
  • [46]Katoh K, Misawa K, Kuma K-, Miyata T: MAFFT: a novel method for rapid multiple sequence alignment based on fast Fourier transform. Nucleic Acids Res 2002, 30:3059-3066.
  • [47]Drummond AJ, Rambaut A: BEAST: Bayesian evolutionary analysis by sampling trees. BMC Evol Biol 2007, 7:214. BioMed Central Full Text
  文献评价指标  
  下载次数:14次 浏览次数:23次