Abstract
Many gram-negative pathogenic bacteria directly translocate effector proteins into eukaryotic host cells via type III delivery systems. Type III effector proteins are determinants of virulence on susceptible plant hosts; they are also the proteins that trigger specific disease resistance in resistant plant hosts. Evolution of type III effectors is dominated by competing forces: the likely requirement for conservation of virulence function, the avoidance of host defenses, and possible adaptation to new hosts. To understand the evolutionary history of type III effectors in Pseudomonas syringae, we searched for homologs to 44 known or candidate P. syringae type III effectors and two effector chaperones. We examined 24 gene families for distribution among bacterial species, amino acid sequence diversity, and features indicative of horizontal transfer. We assessed the role of diversifying and purifying selection in the evolution of these gene families. While some P. syringae type III effectors were acquired recently, others have evolved predominantly by descent. The majority of codons in most of these genes were subjected to purifying selection, suggesting selective pressure to maintain presumed virulence function. However, members of 7 families had domains subject to diversifying selection.
Full Text
The Full Text of this article is available as a PDF (488.5 KB).
Selected References
These references are in PubMed. This may not be the complete list of references from this article.
- Abramovitch Robert B., Kim Young-Jin, Chen Shaorong, Dickman Martin B., Martin Gregory B. Pseudomonas type III effector AvrPtoB induces plant disease susceptibility by inhibition of host programmed cell death. EMBO J. 2003 Jan 2;22(1):60–69. doi: 10.1093/emboj/cdg006. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Alfano J. R., Charkowski A. O., Deng W. L., Badel J. L., Petnicki-Ocwieja T., van Dijk K., Collmer A. The Pseudomonas syringae Hrp pathogenicity island has a tripartite mosaic structure composed of a cluster of type III secretion genes bounded by exchangeable effector and conserved effector loci that contribute to parasitic fitness and pathogenicity in plants. Proc Natl Acad Sci U S A. 2000 Apr 25;97(9):4856–4861. doi: 10.1073/pnas.97.9.4856. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Altschul S. F., Gish W., Miller W., Myers E. W., Lipman D. J. Basic local alignment search tool. J Mol Biol. 1990 Oct 5;215(3):403–410. doi: 10.1016/S0022-2836(05)80360-2. [DOI] [PubMed] [Google Scholar]
- Anderson D. M., Fouts D. E., Collmer A., Schneewind O. Reciprocal secretion of proteins by the bacterial type III machines of plant and animal pathogens suggests universal recognition of mRNA targeting signals. Proc Natl Acad Sci U S A. 1999 Oct 26;96(22):12839–12843. doi: 10.1073/pnas.96.22.12839. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Anisimova M., Bielawski J. P., Yang Z. Accuracy and power of the likelihood ratio test in detecting adaptive molecular evolution. Mol Biol Evol. 2001 Aug;18(8):1585–1592. doi: 10.1093/oxfordjournals.molbev.a003945. [DOI] [PubMed] [Google Scholar]
- Anisimova Maria, Bielawski Joseph P., Yang Ziheng. Accuracy and power of bayes prediction of amino acid sites under positive selection. Mol Biol Evol. 2002 Jun;19(6):950–958. doi: 10.1093/oxfordjournals.molbev.a004152. [DOI] [PubMed] [Google Scholar]
- Apanius V., Penn D., Slev P. R., Ruff L. R., Potts W. K. The nature of selection on the major histocompatibility complex. Crit Rev Immunol. 1997;17(2):179–224. doi: 10.1615/critrevimmunol.v17.i2.40. [DOI] [PubMed] [Google Scholar]
- Axtell Michael J., Staskawicz Brian J. Initiation of RPS2-specified disease resistance in Arabidopsis is coupled to the AvrRpt2-directed elimination of RIN4. Cell. 2003 Feb 7;112(3):369–377. doi: 10.1016/s0092-8674(03)00036-9. [DOI] [PubMed] [Google Scholar]
- Bai J., Choi S. H., Ponciano G., Leung H., Leach J. E. Xanthomonas oryzae pv. oryzae avirulence genes contribute differently and specifically to pathogen aggressiveness. Mol Plant Microbe Interact. 2000 Dec;13(12):1322–1329. doi: 10.1094/MPMI.2000.13.12.1322. [DOI] [PubMed] [Google Scholar]
- Bellgard M. I., Gojobori T. Significant differences between the G+C content of synonymous codons in orthologous genes and the genomic G+C content. Gene. 1999 Sep 30;238(1):33–37. doi: 10.1016/s0378-1119(99)00318-2. [DOI] [PubMed] [Google Scholar]
- Boch Jens, Joardar Vinita, Gao Lisa, Robertson Tara L., Lim Melisa, Kunkel Barbara N. Identification of Pseudomonas syringae pv. tomato genes induced during infection of Arabidopsis thaliana. Mol Microbiol. 2002 Apr;44(1):73–88. doi: 10.1046/j.1365-2958.2002.02877.x. [DOI] [PubMed] [Google Scholar]
- Chang Jeff H., Goel Ajay K., Grant Sarah R., Dangl Jeffery L. Wake of the flood: ascribing functions to the wave of type III effector proteins of phytopathogenic bacteria. Curr Opin Microbiol. 2004 Feb;7(1):11–18. doi: 10.1016/j.mib.2003.12.006. [DOI] [PubMed] [Google Scholar]
- Charkowski A. O., Alfano J. R., Preston G., Yuan J., He S. Y., Collmer A. The Pseudomonas syringae pv. tomato HrpW protein has domains similar to harpins and pectate lyases and can elicit the plant hypersensitive response and bind to pectate. J Bacteriol. 1998 Oct;180(19):5211–5217. doi: 10.1128/jb.180.19.5211-5217.1998. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Collmer Alan, Lindeberg Magdalen, Petnicki-Ocwieja Tanja, Schneider David J., Alfano James R. Genomic mining type III secretion system effectors in Pseudomonas syringae yields new picks for all TTSS prospectors. Trends Microbiol. 2002 Oct;10(10):462–469. doi: 10.1016/s0966-842x(02)02451-4. [DOI] [PubMed] [Google Scholar]
- Cornelis G. R., Van Gijsegem F. Assembly and function of type III secretory systems. Annu Rev Microbiol. 2000;54:735–774. doi: 10.1146/annurev.micro.54.1.735. [DOI] [PubMed] [Google Scholar]
- Dale Colin, Plague Gordon R., Wang Ben, Ochman Howard, Moran Nancy A. Type III secretion systems and the evolution of mutualistic endosymbiosis. Proc Natl Acad Sci U S A. 2002 Sep 4;99(19):12397–12402. doi: 10.1073/pnas.182213299. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Dangl J. L., Jones J. D. Plant pathogens and integrated defence responses to infection. Nature. 2001 Jun 14;411(6839):826–833. doi: 10.1038/35081161. [DOI] [PubMed] [Google Scholar]
- Daubin Vincent, Moran Nancy A., Ochman Howard. Phylogenetics and the cohesion of bacterial genomes. Science. 2003 Aug 8;301(5634):829–832. doi: 10.1126/science.1086568. [DOI] [PubMed] [Google Scholar]
- Endo T., Ikeo K., Gojobori T. Large-scale search for genes on which positive selection may operate. Mol Biol Evol. 1996 May;13(5):685–690. doi: 10.1093/oxfordjournals.molbev.a025629. [DOI] [PubMed] [Google Scholar]
- Fouts Derrick E., Badel Jorge L., Ramos Adela R., Rapp Ryan A., Collmer Alan. A pseudomonas syringae pv. tomato DC3000 Hrp (Type III secretion) deletion mutant expressing the Hrp system of bean pathogen P. syringae pv. syringae 61 retains normal host specificity for tomato. Mol Plant Microbe Interact. 2003 Jan;16(1):43–52. doi: 10.1094/MPMI.2003.16.1.43. [DOI] [PubMed] [Google Scholar]
- Genevaux Pierre, Schwager Françoise, Georgopoulos Costa, Kelley William L. Scanning mutagenesis identifies amino acid residues essential for the in vivo activity of the Escherichia coli DnaJ (Hsp40) J-domain. Genetics. 2002 Nov;162(3):1045–1053. doi: 10.1093/genetics/162.3.1045. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Gopaul D. N., Meyer S. L., Degano M., Sacchettini J. C., Schramm V. L. Inosine-uridine nucleoside hydrolase from Crithidia fasciculata. Genetic characterization, crystallization, and identification of histidine 241 as a catalytic site residue. Biochemistry. 1996 May 14;35(19):5963–5970. doi: 10.1021/bi952998u. [DOI] [PubMed] [Google Scholar]
- Greenberg Jean T., Vinatzer Boris A. Identifying type III effectors of plant pathogens and analyzing their interaction with plant cells. Curr Opin Microbiol. 2003 Feb;6(1):20–28. doi: 10.1016/s1369-5274(02)00004-8. [DOI] [PubMed] [Google Scholar]
- Guttman David S., Vinatzer Boris A., Sarkar Sara F., Ranall Max V., Kettler Gregory, Greenberg Jean T. A functional screen for the type III (Hrp) secretome of the plant pathogen Pseudomonas syringae. Science. 2002 Mar 1;295(5560):1722–1726. doi: 10.1126/science.295.5560.1722. [DOI] [PubMed] [Google Scholar]
- Ham J. H., Bauer D. W., Fouts D. E., Collmer A. A cloned Erwinia chrysanthemi Hrp (type III protein secretion) system functions in Escherichia coli to deliver Pseudomonas syringae Avr signals to plant cells and to secrete Avr proteins in culture. Proc Natl Acad Sci U S A. 1998 Aug 18;95(17):10206–10211. doi: 10.1073/pnas.95.17.10206. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Hauck Paula, Thilmony Roger, He Sheng Yang. A Pseudomonas syringae type III effector suppresses cell wall-based extracellular defense in susceptible Arabidopsis plants. Proc Natl Acad Sci U S A. 2003 Jun 19;100(14):8577–8582. doi: 10.1073/pnas.1431173100. [DOI] [PMC free article] [PubMed] [Google Scholar]
- He S. Y., Huang H. C., Collmer A. Pseudomonas syringae pv. syringae harpinPss: a protein that is secreted via the Hrp pathway and elicits the hypersensitive response in plants. Cell. 1993 Jul 2;73(7):1255–1266. doi: 10.1016/0092-8674(93)90354-s. [DOI] [PubMed] [Google Scholar]
- Jackson R. W., Athanassopoulos E., Tsiamis G., Mansfield J. W., Sesma A., Arnold D. L., Gibbon M. J., Murillo J., Taylor J. D., Vivian A. Identification of a pathogenicity island, which contains genes for virulence and avirulence, on a large native plasmid in the bean pathogen Pseudomonas syringae pathovar phaseolicola. Proc Natl Acad Sci U S A. 1999 Sep 14;96(19):10875–10880. doi: 10.1073/pnas.96.19.10875. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Jakobek J. L., Smith J. A., Lindgren P. B. Suppression of Bean Defense Responses by Pseudomonas syringae. Plant Cell. 1993 Jan;5(1):57–63. doi: 10.1105/tpc.5.1.57. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Jin Q., He S. Y. Role of the Hrp pilus in type III protein secretion in Pseudomonas syringae. Science. 2001 Dec 21;294(5551):2556–2558. doi: 10.1126/science.1066397. [DOI] [PubMed] [Google Scholar]
- Jin Qiaoling, Thilmony Roger, Zwiesler-Vollick Julie, He Sheng-Yang. Type III protein secretion in Pseudomonas syringae. Microbes Infect. 2003 Apr;5(4):301–310. doi: 10.1016/s1286-4579(03)00032-7. [DOI] [PubMed] [Google Scholar]
- Kim J. F., Beer S. V. HrpW of Erwinia amylovora, a new harpin that contains a domain homologous to pectate lyases of a distinct class. J Bacteriol. 1998 Oct;180(19):5203–5210. doi: 10.1128/jb.180.19.5203-5210.1998. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Kimura M. A simple method for estimating evolutionary rates of base substitutions through comparative studies of nucleotide sequences. J Mol Evol. 1980 Dec;16(2):111–120. doi: 10.1007/BF01731581. [DOI] [PubMed] [Google Scholar]
- Kumar S., Tamura K., Jakobsen I. B., Nei M. MEGA2: molecular evolutionary genetics analysis software. Bioinformatics. 2001 Dec;17(12):1244–1245. doi: 10.1093/bioinformatics/17.12.1244. [DOI] [PubMed] [Google Scholar]
- Kurtz Jean-Emmanuel, Exinger Françoise, Erbs Philippe, Jund Richard. The URH1 uridine ribohydrolase of Saccharomyces cerevisiae. Curr Genet. 2002 Jun 12;41(3):132–141. doi: 10.1007/s00294-002-0296-9. [DOI] [PubMed] [Google Scholar]
- Lindgren P. B., Peet R. C., Panopoulos N. J. Gene cluster of Pseudomonas syringae pv. "phaseolicola" controls pathogenicity of bean plants and hypersensitivity of nonhost plants. J Bacteriol. 1986 Nov;168(2):512–522. doi: 10.1128/jb.168.2.512-522.1986. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Lloyd S. A., Norman M., Rosqvist R., Wolf-Watz H. Yersinia YopE is targeted for type III secretion by N-terminal, not mRNA, signals. Mol Microbiol. 2001 Jan;39(2):520–531. doi: 10.1046/j.1365-2958.2001.02271.x. [DOI] [PubMed] [Google Scholar]
- Mackey David, Holt Ben F., 3rd, Wiig Aaron, Dangl Jeffery L. RIN4 interacts with Pseudomonas syringae type III effector molecules and is required for RPM1-mediated resistance in Arabidopsis. Cell. 2002 Mar 22;108(6):743–754. doi: 10.1016/s0092-8674(02)00661-x. [DOI] [PubMed] [Google Scholar]
- Marchler-Bauer Aron, Anderson John B., DeWeese-Scott Carol, Fedorova Natalie D., Geer Lewis Y., He Siqian, Hurwitz David I., Jackson John D., Jacobs Aviva R., Lanczycki Christopher J. CDD: a curated Entrez database of conserved domain alignments. Nucleic Acids Res. 2003 Jan 1;31(1):383–387. doi: 10.1093/nar/gkg087. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Marchler-Bauer Aron, Panchenko Anna R., Shoemaker Benjamin A., Thiessen Paul A., Geer Lewis Y., Bryant Stephen H. CDD: a database of conserved domain alignments with links to domain three-dimensional structure. Nucleic Acids Res. 2002 Jan 1;30(1):281–283. doi: 10.1093/nar/30.1.281. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Marois Eric, Van den Ackerveken Guido, Bonas Ulla. The xanthomonas type III effector protein AvrBs3 modulates plant gene expression and induces cell hypertrophy in the susceptible host. Mol Plant Microbe Interact. 2002 Jul;15(7):637–646. doi: 10.1094/MPMI.2002.15.7.637. [DOI] [PubMed] [Google Scholar]
- Michelmore R. W., Meyers B. C. Clusters of resistance genes in plants evolve by divergent selection and a birth-and-death process. Genome Res. 1998 Nov;8(11):1113–1130. doi: 10.1101/gr.8.11.1113. [DOI] [PubMed] [Google Scholar]
- Morgenstern B. DIALIGN 2: improvement of the segment-to-segment approach to multiple sequence alignment. Bioinformatics. 1999 Mar;15(3):211–218. doi: 10.1093/bioinformatics/15.3.211. [DOI] [PubMed] [Google Scholar]
- Moury Benoît, Morel Caroline, Johansen Elisabeth, Jacquemond Mireille. Evidence for diversifying selection in Potato virus Y and in the coat protein of other potyviruses. J Gen Virol. 2002 Oct;83(Pt 10):2563–2573. doi: 10.1099/0022-1317-83-10-2563. [DOI] [PubMed] [Google Scholar]
- Mudgett M. B., Staskawicz B. J. Characterization of the Pseudomonas syringae pv. tomato AvrRpt2 protein: demonstration of secretion and processing during bacterial pathogenesis. Mol Microbiol. 1999 Jun;32(5):927–941. doi: 10.1046/j.1365-2958.1999.01403.x. [DOI] [PubMed] [Google Scholar]
- Needleman S. B., Wunsch C. D. A general method applicable to the search for similarities in the amino acid sequence of two proteins. J Mol Biol. 1970 Mar;48(3):443–453. doi: 10.1016/0022-2836(70)90057-4. [DOI] [PubMed] [Google Scholar]
- Nielsen R., Yang Z. Likelihood models for detecting positively selected amino acid sites and applications to the HIV-1 envelope gene. Genetics. 1998 Mar;148(3):929–936. doi: 10.1093/genetics/148.3.929. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Nimchuk Z., Rohmer L., Chang J. H., Dangl J. L. Knowing the dancer from the dance: R-gene products and their interactions with other proteins from host and pathogen. Curr Opin Plant Biol. 2001 Aug;4(4):288–294. doi: 10.1016/s1369-5266(00)00175-8. [DOI] [PubMed] [Google Scholar]
- Orth Kim. Function of the Yersinia effector YopJ. Curr Opin Microbiol. 2002 Feb;5(1):38–43. doi: 10.1016/s1369-5274(02)00283-7. [DOI] [PubMed] [Google Scholar]
- Pellé R., Schramm V. L., Parkin D. W. Molecular cloning and expression of a purine-specific N-ribohydrolase from Trypanosoma brucei brucei. Sequence, expression, and molecular analysis. J Biol Chem. 1998 Jan 23;273(4):2118–2126. doi: 10.1074/jbc.273.4.2118. [DOI] [PubMed] [Google Scholar]
- Petnicki-Ocwieja Tanja, Schneider David J., Tam Vincent C., Chancey Scott T., Shan Libo, Jamir Yashitola, Schechter Lisa M., Janes Misty D., Buell C. Robin, Tang Xiaoyan. Genomewide identification of proteins secreted by the Hrp type III protein secretion system of Pseudomonas syringae pv. tomato DC3000. Proc Natl Acad Sci U S A. 2002 May 28;99(11):7652–7657. doi: 10.1073/pnas.112183899. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Reid S. D., Herbelin C. J., Bumbaugh A. C., Selander R. K., Whittam T. S. Parallel evolution of virulence in pathogenic Escherichia coli. Nature. 2000 Jul 6;406(6791):64–67. doi: 10.1038/35017546. [DOI] [PubMed] [Google Scholar]
- Rice Full-Length cDNA Consortium. National Institute of Agrobiological Sciences Rice Full-Length cDNA Project Team. Kikuchi Shoshi, Satoh Kouji, Nagata Toshifumi, Kawagashira Nobuyuki, Doi Koji, Kishimoto Naoki, Yazaki Junshi, Ishikawa Masahiro. Collection, mapping, and annotation of over 28,000 cDNA clones from japonica rice. Science. 2003 Jul 18;301(5631):376–379. doi: 10.1126/science.1081288. [DOI] [PubMed] [Google Scholar]
- Sawada H., Suzuki F., Matsuda I., Saitou N. Phylogenetic analysis of Pseudomonas syringae pathovars suggests the horizontal gene transfer of argK and the evolutionary stability of hrp gene cluster. J Mol Evol. 1999 Nov;49(5):627–644. doi: 10.1007/pl00006584. [DOI] [PubMed] [Google Scholar]
- Schneider David S. Plant immunity and film Noir: what gumshoe detectives can teach us about plant-pathogen interactions. Cell. 2002 May 31;109(5):537–540. doi: 10.1016/s0092-8674(02)00764-x. [DOI] [PubMed] [Google Scholar]
- Shan L., He P., Zhou J. M., Tang X. A cluster of mutations disrupt the avirulence but not the virulence function of AvrPto. Mol Plant Microbe Interact. 2000 Jun;13(6):592–598. doi: 10.1094/MPMI.2000.13.6.592. [DOI] [PubMed] [Google Scholar]
- Shao Feng, Golstein Catherine, Ade Jules, Stoutemyer Mark, Dixon Jack E., Innes Roger W. Cleavage of Arabidopsis PBS1 by a bacterial type III effector. Science. 2003 Aug 29;301(5637):1230–1233. doi: 10.1126/science.1085671. [DOI] [PubMed] [Google Scholar]
- Sharp P. M., Li W. H. The codon Adaptation Index--a measure of directional synonymous codon usage bias, and its potential applications. Nucleic Acids Res. 1987 Feb 11;15(3):1281–1295. doi: 10.1093/nar/15.3.1281. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Staskawicz B. J., Mudgett M. B., Dangl J. L., Galan J. E. Common and contrasting themes of plant and animal diseases. Science. 2001 Jun 22;292(5525):2285–2289. doi: 10.1126/science.1062013. [DOI] [PubMed] [Google Scholar]
- Sullivan Christopher S., Pipas James M. T antigens of simian virus 40: molecular chaperones for viral replication and tumorigenesis. Microbiol Mol Biol Rev. 2002 Jun;66(2):179–202. doi: 10.1128/MMBR.66.2.179-202.2002. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Szurek B., Marois E., Bonas U., Van den Ackerveken G. Eukaryotic features of the Xanthomonas type III effector AvrBs3: protein domains involved in transcriptional activation and the interaction with nuclear import receptors from pepper. Plant J. 2001 Jun;26(5):523–534. doi: 10.1046/j.0960-7412.2001.01046.x. [DOI] [PubMed] [Google Scholar]
- Tarr Cheryl L., Whittam Thomas S. Molecular evolution of the intimin gene in O111 clones of pathogenic Escherichia coli. J Bacteriol. 2002 Jan;184(2):479–487. doi: 10.1128/JB.184.2.479-487.2002. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Thompson J. D., Higgins D. G., Gibson T. J. CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res. 1994 Nov 11;22(22):4673–4680. doi: 10.1093/nar/22.22.4673. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Tsiamis G., Mansfield J. W., Hockenhull R., Jackson R. W., Sesma A., Athanassopoulos E., Bennett M. A., Stevens C., Vivian A., Taylor J. D. Cultivar-specific avirulence and virulence functions assigned to avrPphF in Pseudomonas syringae pv. phaseolicola, the cause of bean halo-blight disease. EMBO J. 2000 Jul 3;19(13):3204–3214. doi: 10.1093/emboj/19.13.3204. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Venisse Jean-Stéphane, Barny Marie-Anne, Paulin Jean-Pierre, Brisset Marie-Noëlle. Involvement of three pathogenicity factors of Erwinia amylovora in the oxidative stress associated with compatible interaction in pear. FEBS Lett. 2003 Feb 27;537(1-3):198–202. doi: 10.1016/s0014-5793(03)00123-6. [DOI] [PubMed] [Google Scholar]
- Yang B., Zhu W., Johnson L. B., White F. F. The virulence factor AvrXa7 of Xanthomonas oryzae pv. oryzae is a type III secretion pathway-dependent nuclear-localized double-stranded DNA-binding protein. Proc Natl Acad Sci U S A. 2000 Aug 15;97(17):9807–9812. doi: 10.1073/pnas.170286897. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Yang Z. PAML: a program package for phylogenetic analysis by maximum likelihood. Comput Appl Biosci. 1997 Oct;13(5):555–556. doi: 10.1093/bioinformatics/13.5.555. [DOI] [PubMed] [Google Scholar]
- Yeager M., Hughes A. L. Evolution of the mammalian MHC: natural selection, recombination, and convergent evolution. Immunol Rev. 1999 Feb;167:45–58. doi: 10.1111/j.1600-065x.1999.tb01381.x. [DOI] [PubMed] [Google Scholar]
- Zwiesler-Vollick Julie, Plovanich-Jones Anne E., Nomura Kinya, Bandyopadhyay Sruti, Joardar Vinita, Kunkel Barbara N., He Sheng Yang. Identification of novel hrp-regulated genes through functional genomic analysis of the Pseudomonas syringae pv. tomato DC3000 genome. Mol Microbiol. 2002 Sep;45(5):1207–1218. doi: 10.1046/j.1365-2958.2002.02964.x. [DOI] [PubMed] [Google Scholar]