Baltrus, David A., Nishimura, Marc T., Dougherty, Kevin M., Biswas, Surojit, Mukhtar, M. Shahid, Vicente, Joana G., Holub, E. B. and Dangl, J. L. (Jeffery L.). (2012) The molecular basis of host specialization in bean pathovars of Pseudomonas syringae. Molecular Plant-Microbe Interactions, Vol.25 (No.7). pp. 877-888. ISSN 0894-0282

Preview

Text WRAP_Vicente_MPMI-08-11-0218.pdf - Published Version Download (771Kb) | Preview

Abstract

Biotrophic phytopathogens are typically limited to their adapted host range. In recent decades, investigations have teased apart the general molecular basis of intraspecific variation for innate immunity of plants, typically involving receptor proteins that enable perception of pathogen-associated molecular patterns or avirulence elicitors from the pathogen as triggers for defense induction. However, general consensus concerning evolutionary and molecular factors that alter host range across closely related phytopathogen isolates has been more elusive. Here, through genome comparisons and genetic manipulations, we investigate the underlying mechanisms that structure host range across closely related strains of Pseudomonas syringae isolated from different legume hosts. Although type III secretionindependent virulence factors are conserved across these three strains, we find that the presence of two genes encoding type III effectors (hopC1 and hopM1) and the absence of another (avrB2) potentially contribute to host range differences between pathovars glycinea and phaseolicola. These findings reinforce the idea that a complex genetic basis underlies host range evolution in plant pathogens. This complexity is present even in host–microbe interactions featuring relatively little divergence among both hosts and their adapted pathogens.

Item Type:	Journal Article
Subjects:	Q Science > QR Microbiology
Divisions:	Faculty of Science > Life Sciences (2010- )
Library of Congress Subject Headings (LCSH):	Pseudomonas syringae -- Genetics, Pseudomonas syringae -- Host plants
Journal or Publication Title:	Molecular Plant-Microbe Interactions
Publisher:	The American Phytopathological Society
ISSN:	0894-0282
Date:	2012
Volume:	Vol.25
Number:	No.7
Page Range:	pp. 877-888
Identification Number:	10.1094/MPMI-08-11-0218
Status:	Peer Reviewed
Publication Status:	Published
Access rights to Published version:	Restricted or Subscription Access
Funder:	National Institutes of Health (U.S.) (NIH), United States. Dept. of Energy
Grant number:	GM066025 (NIH), 95ER20187 (DOE), GM082279-01 (NIH)
References:	Abramovitch, R. B., Anderson, J. C., and Martin, G. B. 2006. Bacterial elicitation and evasion of plant innate immunity. Nat. Rev. Mol. Cell Biol. 7:601-611. Almeida, N. F., Yan, S., Lindeberg, M., Studholme, D. J., Schneider, D. J., Condon, B., Liu, H., Viana, C. J., Warren, A., Evans, C., Kemen, E., Maclean, D., Angot, A., Martin, G. B., Jones, J. D., Collmer, A., Setubal, J. C., and Vinatzer, B. A. 2009. 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. 22:52-62. Arnold, D. L., Jackson, R. W., Fillingham, A. J., Goss, S. C., Taylor, J. D., Mansfield, J. W., and Vivian, A. 2001. Highly conserved sequences flank avirulence genes: Isolation of novel avirulence genes from Pseudomonas syringae pv. pisi. Microbiology 147:1171-1182. Arnold, D. L., Lovell, H. C., Jackson, R. W., and Mansfield, J. W. 2011. Pseudomonas syringae pv. phaseolicola: From ‘has bean’ to supermodel. Mol. Plant Pathol. 12:617-627. Baltrus, D. A., Nishimura, M. T., Romanchuk, A., Chang, J. H., Mukhtar, M. S., Cherkis, K., Roach, J., Grant, S. R., Jones, C. D., and Dangl, J. L. 2011. Dynamic evolution of pathogenicity revealed by sequencing and comparative genomics of 19 Pseudomonas syringae isolates. PLoS Pathog. 7:e1002132. Published online Besemer, J., and Borodovsky, M. 2005. GeneMark: Web software for gene finding in prokaryotes, eukaryotes and viruses. Nucleic Acids Res. 33:W451-W454. Borhan, M. H., Gunn, N., Cooper, A., Gulden, S., Tör, M., Rimmer, S. R., and Holub, E. B. 2008. WRR4 encodes a TIR-NB-LRR protein that confers broad-spectrum white rust resistance in Arabidopsis thaliana to four physiological races of Albugo candida. Mol. Plant-Microbe Interact. 21:757-768. Cai, R., Lewis, J., Yan, S., Liu, H., Clarke, C. R., Campanile, F., Almeida, N. F., Studholme, D. J., Lindeberg, M., Schneider, D., Zaccardelli, M., Setubal, J. C., Morales-Lizcano, N. P., Bernal, A., Coaker, G., Baker, C., Bender, C. L., Leman, S., and Vinatzer, B. A. 2011. The plant pathogen Pseudomonas syringae pv. tomato is genetically monomorphic and under strong selection to evade tomato immunity. PLoS Pathog. 7:e1002130. Published online. Chang, J. H., Urbach, J. M., Law, T. F., Arnold, L. W., Hu, A., Gombar, S., Grant, S. R., Ausubel, F. M., and Dangl, J. L. 2005. A high-throughput, near-saturating screen for type III effector genes from Pseudomonas syringae. Proc. Natl. Acad. Sci. U.S.A. 102:2549-2554. Cunnac, S., Chakravarthy, S., Kvitko, B. H., Russell, A. B., Martin, G. B., and Collmer, A. 2011. Genetic disassembly and combinatorial reassembly identify a minimal functional repertoire of type III effectors in Pseudomonas syringae. Proc. Natl. Acad. Sci. U.S.A. 108:2975-2980. Delgado-Salinas, A., Bibler, R., and Lavin, M. 2006. Phylogeny of the genus Phaseolus (Leguminosae): A recent diversification in an ancient landscape. Syst. Bot. 31:779-791. Do, C. B. 2005. ProbCons: Probabilistic consistency-based multiple sequence alignment. Genome Res. 15:330-340. Fan, J., Crooks, C., and Lamb, C. 2007. High-throughput quantitative luminescence assay of the growth in planta of Pseudomonas syringae chromosomally tagged with Photorhabdus luminescens luxCDABE. Plant J. 53:393-399. Ferrante, P., Clarke, C. R., Cavanaugh, K. A., Michelmore, R. W., Buonaurio, R., and Vinatzer, B. A. 2009. Contributions of the effector gene hopQ1-1 to differences in host range between Pseudomonas syringae pv. phaseolicola and P. syringae pv. tabaci. Mol. Plant Pathol. 10:837-842. Gardan, L., Shafik, H., Belouin, S., Broch, R., Grimont, F., and Grimont, P. A. 1999. DNA relatedness among the pathovars of Pseudomonas syringae and description of Pseudomonas tremae sp. nov. and Pseudomonas cannabina sp. nov. (ex Sutic and Dowson 1959). Int. J. Syst. Bacteriol. 492:469-478. Gassmann, W., Hinsch, M. E., and Staskawicz, B. J. 1999. The Arabidopsis RPS4 bacterial-resistance gene is a member of the TIR-NBS-LRR family of disease-resistance genes. Plant J. 20:265-277. Glickmann, E., Gardan, L., Jacquet, S., Hussain, S., Elasri, M., Petit, A., and Dessaux, Y. 1998. Auxin production is a common feature of most pathovars of Pseudomonas syringae. Mol. Plant-Microbe Interact. 11:156-162. Ham, J. H., Kim, M. G., Lee, S. Y., and Mackey, D. 2007. Layered basal defenses underlie non-host resistance of Arabidopsis to Pseudomonas syringae pv. phaseolicola. Plant J. 51:604-616. Hirano, S. S., Charkowski, A. O., Collmer, A., Willis, D. K., and Upper, C. D. 1999. Role of the Hrp type III protein secretion system in growth of Pseudomonas syringae pv. syringae B728a on host plants in the field. Proc. Natl. Acad. Sci. U.S.A. 96:9851-9856. Holt, B. F., Belkhadir, Y., and Dangl, J. L. 2005. Antagonistic control of disease resistance protein stability in the plant immune system. Science 309:929-932. Hwang, M. S. H., Morgan, R. L., Sarkar, S. F., Wang, P. W., and Guttman, D. S. 2005. Phylogenetic characterization of virulence and resistance phenotypes of Pseudomonas syringae. Appl. Environ. Microbiol. 71:5182-5191. Joardar, V., Lindeberg, M., Jackson, R. W., Selengut, J., Dodson, R., Brinkac, L. M., Daugherty, S. C., Deboy, R., Durkin, A. S., Giglio, M. G., Madupu, R., Nelson, W. C., Rosovitz, M. J., Sullivan, S., Crabtree, J., Creasy, T., Davidsen, T., Haft, D. H., Zafar, N., Zhou, L., Halpin, R., Holley, T., Khouri, H., Feldblyum, T., White, O., Fraser, C. M., Chatterjee, A. K., Cartinhour, S., Schneider, D. J., Mansfield, J., Collmer, A., and Buell, C. R. 2005. Whole-genome sequence analysis of Pseudomonas syringae pv. phaseolicola 1448A reveals divergence among pathovars in genes involved in virulence and transposition. J. Bacteriol. 187:6488-6498. Jones, J. D. G., and Dangl, J. L. 2006. The plant immune system. Nature 444:323-329. Kobayashi, D. Y., Tamaki, S. J., and Keen, N. T. 1989. Cloned avirulence genes from the tomato pathogen Pseudomonas syringae pv. tomato confer cultivar specificity on soybean. Proc. Natl. Acad. Sci. U.S.A. 86:157-161. Lacombe, S. E. V., Rougon-Cardoso, A., Sherwood, E., Peeters, N., Dahlbeck, D., van Esse, H. P., Smoker, M., Rallapalli, G., Thomma, B. P. H. J., Staskawicz, B., Jones, J. D. G., and Zipfel, C. 2010. Interfamily transfer of a plant pattern-recognition receptor confers broad-spectrum bacterial resistance. Nat. Biotechnol. 28:365-369. Li, R., Li, Y., Kristiansen, K., and Wang, J. 2008. SOAP: Short oligonucleotide alignment program. Bioinformatics 24:713-714. Li, R., Zhu, H., Ruan, J., Qian, W., Fang, X., Shi, Z., Li, Y., Li, S., Shan, G., Kristiansen, K., Li, S., Yang, H., Wang, J., and Wang, J. 2010. De novo assembly of human genomes with massively parallel short read sequencing. Genome Res. 20:265-272. Li, X., Lin, H., Zhang, W., Zou, Y., Zhang, J., Tang, X., and Zhou, J.-M. 2005. Flagellin induces innate immunity in nonhost interactions that is suppressed by Pseudomonas syringae effectors. Proc. Natl. Acad. Sci. U.S.A. 102:12990-12995. Lin, N.-C., and Martin, G. B. 2007. Pto- and Prf-mediated recognition of AvrPto and AvrPtoB restricts the ability of diverse Pseudomonas syringae pathovars to infect tomato. Mol. Plant-Microbe Interact. 20:806- 815. Lindeberg, M., Cunnac, S., and Collmer, A. 2009. The evolution of Pseudomonas syringae host specificity and type III effector repertoires. Mol. Plant Pathol. 10:767-775. Lorang, J., Shen, H., and Kobayashi, D. 1994. avrA and avrE in Pseudomonas syringae pv. tomato PT23 play a role in virulence on tomato plants. Mol. Plant-Microbe Interact. 7:508-515. Marco, M. L., Legac, J., and Lindow, S. E. 2005. Pseudomonas syringae genes induced during colonization of leaf surfaces. Environ. Microbiol. 7:1379-1391. Marques, A., Corbiere, R., Gardan, L., Tourte, C., Manceau, C., Taylor, J., and Samson, R. 2000. Multiphasic approach for the identification of the different classification levels of Pseudomonas savastanoi pv. phaseolicola. Eur. J. Plant Pathol. 106:715-734. Mazzola, M., and White, F. F. 1994. A mutation in the indole-3-acetic acid biosynthesis pathway of Pseudomonas syringae pv. syringae affects growth in Phaseolus vulgaris and syringomycin production. J. Bacteriol. 176:1374-1382. McClean, P., Lavin, M., Gepts, P., and Jackson, S. 2008. Phaseolus vulgaris: A diploid model for soybean. Pages 55-78 in: Soybean Genomics. Springer, Berlin. McDermott, J., Corrigan, A., and Peterson, E. 2011. Computational prediction of type III and IV secreted effectors in gram-negative bacteria. Infect. Immun. 79:23-32. Mellersh, D. G., and Heath, M. C. 2003. An investigation into the involvement of defense signaling pathways in components of the nonhost resistance of Arabidopsis thaliana to rust fungi also reveals a model system for studying rust fungal compatibility. Mol. Plant-Microbe Interact. 16:398-404. Morris, C. E., Sands, D. C., Vanneste, J. L., Montarry, J., Oakley, B., Guilbaud, C., and Glaux, C. 2010. Inferring the evolutionary history of the plant pathogen Pseudomonas syringae from its biogeography in headwaters of rivers in North America, Europe, and New Zealand. mBio 1:e00107-00110-e00107-00120. Published online. Mysore, K. S., and Ryu, C.-M. 2004. Nonhost resistance: How much do we know? Trends Plant Sci. 9:97-104. Ortiz-Martín, I., Macho, A. P., Lambersten, L., Ramos, C., and Beuzón, C.R. 2006. Suicide vectors for antibiotic marker exchange and rapid generation of multiple knockout mutants by allelic exchange in gramnegative bacteria. J. Microbiol. Methods 67:395-407. Ortiz-Martín, I., Thwaites, R., Macho, A. P., Mansfield, J. W., and Beuzón, C. R. 2010. Positive regulation of the Hrp type III secretion system in Pseudomonas syringae pv. phaseolicola. Mol. Plant-Microbe Interact. 23:665-681. Patil, S. S., Hayward, A., and Emmons, R. 1974. An ultraviolet-induced nontoxigenic mutant of Pseudomonas phaseolicola of altered pathogenicity. Phytopathology 64:590-595. Perchepied, L., Kroj, T., Tronchet, M., Loudet, O., and Roby, D. 2006. Natural variation in partial resistance to Pseudomonas syringae is controlled by two major QTLs in Arabidopsis thaliana. PLoS ONE 1:e123. Published online. Qi, M., Wang, D., Bradley, C. A., and Zhao, Y. 2011. Genome sequence analyses of Pseudomonas savastanoi pv. glycinea and subtractive hybridization- based comparative genomics with nine pseudomonads. PLoS ONE 6:e16451. Published online. Rico, A., and Preston, G. M. 2008. Pseudomonas syringae pv. tomato DC3000 uses constitutive and apoplast-induced nutrient assimilation pathways to catabolize nutrients that are abundant in the tomato apoplast. Mol. Plant-Microbe Interact. 21:269-282. Roine, E., Wei, W., Yuan, J., Nurmiaho-Lassila, E. L., Kalkkinen, N., Romantschuk, M., and He, S. Y. 1997. Hrp pilus: An hrp-dependent bacterial surface appendage produced by Pseudomonas syringae pv. tomato DC3000. Proc. Natl. Acad. Sci. U.S.A. 94:3459-3464. Schulze-Lefert, P., and Panstruga, R. 2011. A molecular evolutionary concept connecting nonhost resistance, pathogen host range, and pathogen speciation. Trends Plant Sci. 16:117-125. Shan, L., He, P., Li, J., Heese, A., Peck, S. C., Nürnberger, T., Martin, G. B., and Sheen, J. 2008. Bacterial effectors target the common signaling partner BAK1 to disrupt multiple MAMP receptor-signaling complexes and impede plant immunity. Cell Host Microbe 4:17-27. Sohn, K. H., Saucet, S. B., Clarke, C. R., Vinatzer, B. A., O’Brien, H. E., Guttman, D. S., and Jones, J. D. G. 2011. HopAS1 recognition significantly contributes to Arabidopsis nonhost resistance to Pseudomonas syringae pathogens. New Phytol. 193:58-66. Song, J., Bradeen, J. M., Naess, S. K., Raasch, J. A., Wielgus, S. M., Haberlach, G. T., Liu, J., Kuang, H., Austin-Phillips, S., Buell, C. R., Helgeson, J. P., and Jiang, J. 2003. Gene RB cloned from Solanum bulbocastanum confers broad spectrum resistance to potato late blight. Proc. Natl. Acad. Sci. U.S.A. 100:9128-9133. Stamatakis, A. 2004. RAxML-III: A fast program for maximum likelihood- based inference of large phylogenetic trees. Bioinformatics 21:456-463. Stamatakis, A. 2006. RAxML-VI-HPC: Maximum likelihood-based phylogenetic analyses with thousands of taxa and mixed models. Bioinformatics 22:2688-2690. Staskawicz, B. J., Dahlbeck, D., and Keen, N. T. 1984. Cloned avirulence gene of Pseudomonas syringae pv. glycinea determines race-specific incompatibility on Glycine max (L.) Merr. Proc. Natl. Acad. Sci. U.S.A. 81:6024-6028. Stevens, C., Bennett, M. A., Athanassopoulos, E., Tsiamis, G., Taylor, J. D., and Mansfield, J. W. 1998. Sequence variations in alleles of the avirulence gene avrPphE.R2 from Pseudomonas syringae pv. phaseolicola lead to loss of recognition of the AvrPphE protein within bean cells and a gain in cultivar-specific virulence. Mol. Microbiol. 29:165- 177. Studholme, D. J. 2011. Application of high-throughput genome sequencing to intrapathovar variation in Pseudomonas syringae. Mol. Plant Pathol. 12:829-838. Tai, T. H., Dahlbeck, D., Clark, E. T., Gajiwala, P., Pasion, R., Whalen, M. C., Stall, R. E., and Staskawicz, B. J. 1999. Expression of the Bs2 pepper gene confers resistance to bacterial spot disease in tomato. Proc. Natl. Acad. Sci. U.S.A. 96:14153-14158. Takeuchi, K., Taguchi, F., Inagaki, Y., Toyoda, K., Shiraishi, T., and Ichinose, Y. 2003. Flagellin glycosylation island in Pseudomonas syringae pv. glycinea and its role in host specificity. J. Bacteriol. 185:6658- 6665. Taylor, J., Teverson, D., and Allen, D. 1996. Identification and origin of races of Pseudomonas syringae pv. phaseolicola from Africa and other bean growing areas. Plant Pathol. 45:469-478. Tsiamis, G., Mansfield, J. W., Hockenhull, R., Jackson, R. W., Sesma, A., Athanassopoulos, E., Bennett, M. A., Stevens, C., Vivian, A., Taylor, J. D., and Murillo, J. 2000. Cultivar-specific avirulence and virulence functions assigned to avrPphF in Pseudomonas syringae pv. phaseolicola, the cause of bean halo-blight disease. EMBO (Eur. Mol. Biol. Organ.) J. 19:3204-3214. Vera Cruz, C. M., Bai, J., Ona, I., Leung, H., Nelson, R. J., Mew, T. W., and Leach, J. E. 2000. Predicting durability of a disease resistance gene based on an assessment of the fitness loss and epidemiological consequences of avirulence gene mutation. Proc. Natl. Acad. Sci. U.S.A. 97:13500-13505. Vinatzer, B. A., Teitzel, G. M., Lee, M.-W., Jelenska, J., Hotton, S., Fairfax, K., Jenrette, J., and Greenberg, J. T. 2006. The type III effector repertoire of Pseudomonas syringae pv. syringae B728a and its role in survival and disease on host and non-host plants. Mol. Microbiol. 62:26- 44. Warren, R. F., Merritt, P. M., Holub, E., and Innes, R. W. 1999. Identification of three putative signal transduction genes involved in R genespecified disease resistance in Arabidopsis. Genetics 152:401-412. Wei, C.-F., Kvitko, B. H., Shimizu, R., Crabill, E., Alfano, J. R., Lin, N.- C., Martin, G. B., Huang, H.-C., and Collmer, A. 2007. A Pseudomonas syringae pv. tomato DC3000 mutant lacking the type III effector HopQ1-1 is able to cause disease in the model plant Nicotiana benthamiana. Plant J. 51:32-46. Weingart, H., Ullrich, H., Geider, K., and Völksch, B. 2001. The role of ethylene production in virulence of Pseudomonas syringae pvs. glycinea and phaseolicola. Phytopathology 91:511-518. Wen, C., Tang, X., Su, Z., and Zhou, J. 2010. Effector-triggered and pathogen- associated molecular pattern-triggered immunity differentially contribute to basal resistance to Pseudomonas syringae. Mol. Plant-Microbe Interact. 23:940-948. Wroblewski, T., Caldwell, K. S., Piskurewicz, U., Cavanaugh, K. A., Xu, H., Kozik, A., Ochoa, O., McHale, L. K., Lahre, K., Jelenska, J., Castillo, J. A., Blumenthal, D., Vinatzer, B. A., Greenberg, J. T., and Michelmore, R. W. 2009. Comparative large-scale analysis of interactions between several crop species and the effector repertoires from multiple pathovars of Pseudomonas and Ralstonia. Plant Physiol. 150:1733-1749. Xiang, T., Zong, N., Zou, Y., Wu, Y., Zhang, J., Xing, W., Li, Y., Tang, X., Zhu, L., Chai, J., and Zhou, J.-M. 2008. Pseudomonas syringae effector AvrPto blocks innate immunity by targeting receptor kinases. Curr. Biol. 18:74-80. Zumaquero, A., Macho, A. P., Rufián, J. S., and Beuzón, C. R. 2010. Analysis of the role of the type III effector inventory of Pseudomonas syringae pv. phaseolicola 1448a in interaction with the plant. J. Bacteriol. 192:4474-4488.
URI:	http://wrap.warwick.ac.uk/id/eprint/50231

Request changes to a record

Actions (login required)

View Item