Identification of a candidate gene in solanum habrochaites for resistance to a race 1 strain of Pseudomonas syringae pv. Tomato

Plant Genome

Volumn 8, Issue 3, 2015, Pages

  Bao, Zhilong ^a   Meng, Fanhong ^a   Strickler, Susan R ^a   Dunham, Diane M ^a   Munkvold, Kathy R ^a   Martin, Gregory B ^a,b  

^a United States Department of Agriculture Agricultural Research Service and Boyce Thompson Institute for Plant Research   (United States)

^b Department of Obstetrics Gynecology   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

EID: 84946762489     PISSN: None     EISSN: 19403372     Source Type: Journal    
DOI: 10.3835/plantgenome2015.02.0006     Document Type: Article

References (75)

1. Almeida, N.F., S. Yan, M. Lindeberg, D.J. Studholme, D.J. Schneider, B. Condon, et al. 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. doi:10.1094/MPMI-22-1-0052
2. Anderson, D.M., and D.W. Frank. 2012. Five mechanisms of manipulation by bacterial effectors: A ubiquitous theme. PLoS Pathog. 8:E1002823. doi:10.1371/journal.ppat.1002823
3. Arredondo, C.R., and R.M. Davis. 2000. First report of Pseudomonas syringae pv. tomato race 1 on tomato in California. Plant Dis. 84:371. doi:10.1094/PDIS.2000.84.3.371A
4. Boller, T., and G. Felix. 2009. A renaissance of elicitors: Perception of microbe-associated molecular patterns and danger signals by pattern-recognition receptors. Annu. Rev. Plant Biol. 60:379-406. doi:10.1146/ annurev.arplant.57.032905.105346
5. Broman, K.W., H. Wu, S. Sen, and G.A. Churchill. 2003. R/qtl: QTL mapping in experimental crosses. Bioinformatics 19:889-890. doi:10.1093/bioinformatics/btg112
6. Buell, C.R., V. Joardar, M. Lindeberg, J. Selengut, I.T. Paulsen, M.L. Gwinn, et al. 2003. The complete genome sequence of the Arabidopsis and tomato pathogen Pseudomonas syringae pv. tomato DC3000. Proc. Natl. Acad. Sci. USA 100:10181-10186. doi:10.1073/pnas.1731982100
7. Buonaurio, R., V.M. Stravato, and C. Capelli. 1996. Occurrence of Pseudomonas syringae pv. tomato race 1 in Italy on Pto gene-bearing tomato plants. Phytopathology 144:437-440. doi:10.1111/j.1439-0434.1996. tb00320.x
8. Cai, R.M., J. Lewis, S.C. Yan, H.J. Liu, C.R. Clarke, F. Campanile, et al. 2011a. The plant pathogen Pseudomonas syringae pv. Tomato is genetically monomorphic and under strong selection to evade tomato immunity. PLoS Pathog. 7:E1002130. doi:10.1371/journal.ppat.1002130
9. Cai, R., S. Yan, H. Liu, S. Leman, and B.A. Vinatzer. 2011b. Reconstructing host range evolution of bacterial plant pathogens using Pseudomonas syringae pv. tomato and its close relatives as a model. Infect. Genet. Evol. 11:1738-1751. doi:10.1016/j.meegid.2011.07.012
10. Chakravarthy, S., A.C. Velasquez, and G.B. Martin. 2009. Assay for pathogen-associated molecular pattern (PAMP)-triggered immunity (PTI) in plants. J. Vis. Exp. 31:e1442. doi:10.3791/1442
11. Chen, X., S. Zuo, B. Schwessinger, M. Chern, P.E. Canlas, D. Ruan, et al. 2014. An XA21-associated kinase (OsSERK2) regulates immunity mediated by the XA21 and XA3 immune receptors. Mol. Plant 7:874-892. doi:10.1093/mp/ssu003
12. Cheng, W., K.R. Munkvold, H. Gao, J. Mathieu, S. Schwizer, S. Wang, et al. 2011. Structural analysis of Pseudomonas syringae AvrPtoB bound to host BAK1 reveals two similar kinase-interacting domains in a type III effector. Cell Host Microbe 10:616-626. doi:10.1016/j. chom.2011.10.013
13. Chinchilla, D., C. Zipfel, S. Robatzek, B. Kemmerling, T. Nurnberger, J.D. Jones, et al. 2007. A flagellin-induced complex of the receptor FLS2 and BAK1 initiates plant defense. Nature 448:497-500. doi:10.1038/ nature05999
14. Clarke, C.R., D. Chinchilla, S.R. Hind, F. Taguchi, R. Miki, Y. Ichinose, et al. 2013. Allelic variation in two distinct Pseudomonas syringae flagellin epitopes modulates the strength of plant immune responses but not bacterial motility. New Phytol. 200:847-860. doi:10.1111/nph.12408
15. Danecek, P., A. Auton, G. Abecasis, C.A. Albers, E. Banks, M.A. DePristo, et al. 2011. The variant call format and VCFtools. Bioinformatics 27:2156-2158. doi:10.1093/bioinformatics/btr330
16. De la Torre, F., E. Gutierrez-Beltran, Y. Pareja-Jaime, S. Chakravarthy, G.B. Martin, and O. del Pozo. 2013. The tomato calcium sensor Cbl10 and its interacting protein kinase Cipk6 define a signaling pathway in plant immunity. Plant Cell 25:2748-2764. doi:10.1105/tpc.113.113530
17. DePristo, M.A., E. Banks, R. Poplin, K.V. Garimella, J.R. Maguire, C. Hartl, et al. 2011. A framework for variation discovery and genotyping using next-generation DNA sequencing data. Nat. Genet. 43:491-498. doi:10.1038/ng.806
18. Dodds, P.N., and J.P. Rathjen. 2010. Plant immunity: Towards an integrated view of plant-pathogen interactions. Nat. Rev. Genet. 11:539-548. doi:10.1038/nrg2812
19. Dou, D., and J. M Zhou. 2012. Phytopathogen effectors subverting host immunity: Different foes, similar battleground. Cell Host Microbe 12:484-495. doi:10.1016/j.chom.2012.09.003
20. Felix, G., and T. Boller. 2003. Molecular sensing of bacteria in plants. The highly conserved RNA-binding motif RNP-1 of bacterial cold shock proteins is recognized as an elicitor signal in tobacco. J. Biol. Chem. 278:6201-6208. doi:10.1074/jbc.M209880200
21. Fernandez-Pozo, N., N. Menda, J.D. Edwards, S. Saha, I.Y. Tecle, S.R. Strickler, et al. 2015. The Sol Genomics Network (SGN)-from genotype to phenotype to breeding. Nucleic Acids Res. 43:D1036-D1041. doi:10.1093/nar/gku1195
22. Goldman, A. 2008. The heirloom tomato: From garden to table: Recipes, portraits, and history of the world’s most beautiful fruit. 1st ed. Bloomsbury, New York.
23. Gouy, M., S. Guindon, and O. Gascuel. 2010. SeaView version 4: A multiplatform graphical user interface for sequence alignment and phylogenetic tree building. Mol. Biol. Evol. 27:221-224. doi:10.1093/molbev/msp259
24. Grandillo, S., R.T. Chetelat, S. Knapp, D. Spooner, I. Peralta, M. Cammareri, et al. 2011. Solanum sect. Lycopersicon. In: C. Kole, editor, Wild crop relatives: Genomics and breeding resources, vegetables. Springer-Verlag. Heidleberg, Berlin. p. 129-215.
25. Guo, M., F. Tian, Y. Wamboldt, and J.R. Alfano. 2009. The majority of the type III effector inventory of Pseudomonas syringae pv. Tomato DC3000 can suppress plant immunity. Mol. Plant Microbe Interact. 22:1069-1080. doi:10.1094/MPMI-22-9-1069
26. Heese, A., D.R. Hann, S. Gimenez-Ibanez, A.M. Jones, K. He, J. Li, et al. 2007. The receptor-like kinase SERK3/BAK1 is a central regulator of innate immunity in plants. Proc. Natl. Acad. Sci. USA 104:12217-12222. doi:10.1073/pnas.0705306104
27. Jones, J.B. 1991. Bacterial speck. In: J.B. Jones, J.P. Jones, R.E. Stall, and T.A. Zitter, editors, Compendium of tomato diseases. APS Press, St. Paul, MN. p. 26-27.
28. Jones, L.A., S. Saha, A. Collmer, C.D. Smart, and M. Lindeberg. 2015. Genome-assisted development of a diagnostic protocol for distinguishing high virulence Pseudomonas syringae pv. tomato strains. Plant Dis. 99:527-534. doi:10.1094/PDIS-08-14-0833-RE
29. Kunkeaw, S., S. Tan, and G. Coaker. 2010. Molecular and evolutionary analyses of Pseudomonas syringae pv. tomato race 1. Mol. Plant Microbe Interact. 23:415-424. doi:10.1094/MPMI-23-4-0415
30. Lacombe, S., A. Rougon-Cardoso, E. Sherwood, N. Peeters, D. Dahlbeck, H.P. van Esse, et al. 2010. Interfamily transfer of a plant pattern-recognition receptor confers broad-spectrum bacterial resistance. Nat. Biotechnol. 28:365-369. doi:10.1038/nbt.1613
31. Langmead, B., and S.L. Salzberg. 2012. Fast gapped-read alignment with Bowtie 2. Nat. Methods 9:357-359. doi:10.1038/nmeth.1923
32. Leinonen, R., H. Sugawara, and M. Shumway. 2011. The sequence read archive. On behalf of International Nucleotide Sequence Database Collaboration. Nucleic Acids Res. 39:D19-D21. doi:10.1093/nar/gkq1019
33. Li, H. 2011. A statistical framework for SNP calling, mutation discovery, association mapping and population genetical parameter estimation from sequencing data. Bioinformatics 27:2987-2993. doi:10.1093/bioinformatics/btr509
34. Li, H., B. Handsaker, A. Wysoker, T. Fennell, J. Ruan, N. Homer, et al. 2009. The sequence alignment/map format and SAMtools. Bioinformatics 25:2078-2079. doi:10.1093/bioinformatics/btp352
35. Li, W., and R.T. Chetelat. 2010. A pollen factor linking inter and intraspecific pollen rejection in tomato. Science 330:1827-1830. doi:10.1126/science.1197908
36. Li, W., and R.T. Chetelat. 2015. Unilateral incompatibility gene ui1.1 encodes an S-locus F-box protein expressed in pollen of Solanum species. Proc. Natl. Acad. Sci. USA 112:4417-4422. doi:10.1073/ pnas.1423301112
37. Lin, N.C., R.B. Abramovitch, Y.J. Kim, and G.B. Martin. 2006. Diverse AvrPtoB homologs from several Pseudomonas syringae pathovars elicit Pto-dependent resistance and have similar virulence activities. Appl. Environ. Microbiol. 72:702-712. doi:10.1128/AEM.72.1.702-712.2006
38. Lin, N.C., and G.B. Martin. 2005. An avrPto/avrPtoB mutant of Pseudo- monas syringae pv. tomato DC3000 does not elicit Pto-mediated resistance and is less virulent on tomato. Mol. Plant Microbe Interact. 18:43-51. doi:10.1094/MPMI-18-0043
39. Lin, N.C., and G.B. Martin. 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. doi:10.1094/MPMI-20-7-0806
40. Maekawa, T., T.A. Kufer, and P. Schulze-Lefert. 2011. NLR functions in plant and animal immune systems: So far and yet so close. Nat. Immunol. 12:817-826. doi:10.1038/ni.2083
41. Male, C.J. 1999. 100 heirloom tomatoes for the American garden. Workman Publishing, New York.
42. Martin, G.B. 2012. Suppression and activation of the plant immune system by Pseudomonas syringae effectors AvrPto and AvrPtoB. In: F. Marin and S. Kamoun, editors, Effectors in plant-microbe interactions. Wiley-Blackwell, Hoboken, NJ. p. 123-154.
43. Mendes, B.M.J., S.C. Cardoso, R.L. Boscariol-Camargo, R.B. Cruza, F.A.A. Mourao Filho, and A. Bergamin Filho. 2010. Reduction in susceptibility to Xanthomonas axonopodis pv. citri in transgenic Citrus sinensis expressing the rice Xa21 gene. Plant Pathol. 59:68-75. doi:10.1111/ j.1365-3059.2009.02148.x
44. Nguyen, H.P., S. Chakravarthy, A.C. Velásquez, H.S. McLane, L. Zeng, D.-W. Park, et al. 2010. Methods to study PAMP-triggered immunity using tomato and Nicotiana benthamiana. Mol. Plant Microbe Interact. 23:991-999. doi:10.1094/MPMI-23-8-0991
45. Oh, C.S., and G.B. Martin. 2011. Effector-triggered immunity mediated by the Pto kinase. Trends Plant Sci. 16:132-140. doi:10.1016/j.tplants.2010.11.001
46. Pedley, K.F., and G.B. Martin. 2003. Molecular basis of Pto-mediated resistance to bacterial speck disease in tomato. Annu. Rev. Phytopathol. 41:215-243. doi:10.1146/annurev.phyto.41.121602.143032
47. Peralta, I.E., S. Knapp, and D.M. Spooner. 2006. Nomenclature for wild and cultivated tomatoes. TGR Report 56:6-12.
48. Pombo, M.A., Y. Zheng, N. Fernandez-Pozo, D.M. Dunham, Z. Fei, and G.B. Martin. 2014. Transcriptomic analysis reveals tomato genes whose expression is induced specifically during effector-triggered immunity and identifies the Epk1 protein kinase which is required for the host response to three bacterial effector proteins. Genome Biol. 15:492. doi:10.1186/s13059-014-0492-1
49. Riely, B.K., and G.B. Martin. 2001. Ancient origin of pathogen recognition specificity conferred by the tomato disease resistance gene Pto. Proc. Natl. Acad. Sci. USA 98:2059-2064. doi:10.1073/pnas.98.4.2059
50. Robatzek, S., and L. Wirthmueller. 2013. Mapping FLS2 function to structure: LRRs, kinase and its working bits. Protoplasma 250:671-681. doi:10.1007/s00709-012-0459-6
51. Rose, L.E., C.H. Langley, A.J. Bernal, and R.W. Michelmore. 2005. Natural variation in the Pto pathogen resistance gene within species of wild tomato (Lycopersicon). I. Functional analysis of Pto alleles. Genetics 171:345-357. doi:10.1534/genetics.104.039339
52. Rosebrock, T.R., L. Zeng, J.J. Brady, R.B. Abramovitch, F. Xiao, and G.B. Mar- tin. 2007. A bacterial E3 ubiquitin ligase targets a host protein kinase to disrupt plant immunity. Nature 448:370-374. doi:10.1038/nature05966
53. Rosli, H.G., Y. Zheng, M.A. Pombo, S. Zhong, A. Bombarely, Z. Fei, et al. 2013. Transcriptomics-based screen for genes induced by flagellin and repressed by pathogen effectors identifies a cell wall-associated kinase involved in plant immunity. Genome Biol. 14:R139. doi:10.1186/gb- 2013-14-12-r139
54. Roux, M., B. Schwessinger, C. Albrecht, D. Chinchilla, A. Jones, N. Holton, et al. 2011. The Arabidopsis leucine-rich repeat receptor-like kinases BAK1/SERK3 and BKK1/SERK4 are required for innate immunity to hemibiotrophic and biotrophic pathogens. Plant Cell 23:2440-2455. doi:10.1105/tpc.111.084301
55. Sakamoto, T., M. Deguchi, O.J. Brustolini, A.A. Santos, F.F. Silva, and E.P. Fontes. 2012. The tomato RLK superfamily: Phylogeny and functional predictions about the role of the LRRII-RLK subfamily in antiviral defense. BMC Plant Biol. 12:229. doi:10.1186/1471-2229-12-229
56. Salmeron, J.M., G.E.D. Oldroyd, C.M.T. Rommens, S.R. Scofield, H.-S. Kim, D.T. Lavelle, et al. 1996. Tomato Prf is a member of the leucine-rich repeat class of plant disease resistance genes and lies embedded within the Pto kinase gene cluster. Cell 86:123-133. doi:10.1016/S0092-8674(00)80083-5
57. Scott, J.W. 1997. Tomato improvement for bacterial disease resistance for the tropics: A contemporary basis and future prospects. In: Proceedings, 1st International Symposium on Tropical Tomato Diseases, Recife, Brazil. 21-22 Nov. 1996. Amer. Soc. Hort. Sci., Alexandria, VA. p. 117-125.
58. Shan, L., P. He, J. Li, A. Heese, S.C. Peck, T. Nurnberger, et al. 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. doi:10.1016/j.chom.2008.05.017
59. Shan, L., P. He, J.M. Zhou, and X. Tang. 2000. A cluster of mutations disrupt the avirulence but not the virulence function of AvrPto. Mol. Plant Microbe Interact. 13:592-598. doi:10.1094/MPMI.2000.13.6.592
60. Stamova, L., N. Bogatsevska, and M. Yordanov. 1990. Resistance to race 1 of Pseudomonas syringae pv. tomato. Tomato Genet. Coop. Rep. 40:33.
61. Thapa, S.P., E.M. Miyao, R. Michael Davis, and G. Coaker. 2015. Identification of QTLs controlling resistance to Pseudomonas syringae pv. tomato race 1 strains from the wild tomato, Solanum habrochaites LA1777. Theor. Appl. Genet. 128:681-692. doi:10.1007/s00122-015-2463-7
62. Tomato Genome Consortium. 2012. The tomato genome sequence provides insights into fleshy fruit evolution. Nature 485:635-641. doi:10.1038/ nature11119
63. Tripathi, J.N., J. Lorenzen, O. Bahar, P. Ronald, and L. Tripathi. 2014. Transgenic expression of the rice Xa21 pattern-recognition receptor in banana (Musa sp.) confers resistance to Xanthomonas campestris pv. musacearum. Plant Biotechnol. J. 12:663-673. doi:10.1111/pbi.12170
64. Tsuda, K., and I.E. Somssich. 2015. Transcriptional networks in plant immunity. New Phytol. 206:932-947. doi:10.1111/nph.13286
65. Velasquez, A.C., and G.B. Martin. 2013. Molecular mechanisms involved in the interaction between tomato and Pseudomonas syrinage pv. tomato. In: G. Sessa, editor, Molecular plant immunity. John Wiley & Sons, Oxford, England.
66. Veluchamy, S., S.R. Hind, D.M. Dunham, G.B. Martin, and D.R. Panthee. 2014. Natural variation for responsiveness to flg22, flgII-28, and csp22 and Pseudomonas syringae pv. tomato in heirloom tomatoes. PLoS ONE 9:E106119. doi:10.1371/journal.pone.0106119
67. Wei, H.L., S. Chakravarthy, J. Mathieu, T.C. Helmann, P. Stodghill, B. Swingle, et al. 2015. Pseudomonas syringae pv. tomato DC3000 type III secretion effector polymutants reveal an interplay between HopAD1 and AvrPtoB. Cell Host Microbe 17:752-762. doi:10.1016/j. chom.2015.05.007
68. Xiang, T., N. Zong, Y. Zou, Y. Wu, J. Zhang, W. Xing, et al. 2008. Pseudomonas syringae effector AvrPto blocks innate immunity by targeting receptor kinases. Curr. Biol. 18:74-80. doi:10.1016/j.cub.2007.12.020
69. Xiao, S., S. Ellwood, O. Calis, E. Patrick, T. Li, M. Coleman, et al. 2001. Broad-spectrum mildew resistance in Arabidopsis thaliana mediated by RPW8. Science 291:118-120. doi:10.1126/science.291.5501.118
70. Xing, W., Y. Zou, Q. Liu, J. Liu, X. Luo, Q. Huang, et al. 2007. The structural basis for activation of plant immunity by bacterial effector protein AvrPto. Nature 449:243-247. doi:10.1038/nature06109
71. Young, J.M., D.W. Dye, and J.P. Wilkie. 1986. Bacterial speck. In: A.F. Sherf, editor, Vegetable diseases and their control. J. Wiley & Sons, New York. p. 610-614.
72. Zhang, L.P., A. Khan, D. Nino-Liu, and M.R. Foolad. 2002. A molecular linkage map of tomato displaying chromosomal locations of resistance gene analogs based on a Lycopersicon esculentum Lycopersicon hirsutum cross. Genome 45:133-146.
73. Zhong, S., J.G. Joung, Y. Zheng, Y.R. Chen, B. Liu, Y. Shao, et al. 2011. High-throughput Illumina strand-specific RNA sequencing library preparation. Cold Spring Harb. Protoc. 2011:940-949. doi:10.1101/ pdb.prot5652
74. Zipfel, C. 2014. Plant pattern-recognition receptors. Trends Immunol. 35:345-351. doi:10.1016/j.it.2014.05.004
75. Zipfel, C., G. Kunze, D. Chinchilla, A. Caniard, J.D. Jones, T. Boller, et al. 2006. Perception of the bacterial PAMP EF-Tu by the receptor EFR restricts Agrobacterium-mediated transformation. Cell 125:749-760. doi:10.1016/j.cell.2006.03.037