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HopH1 effectors of Pseudomonas syringae pv. tomato DC3000 and pv. syringae B728a induce HR cell death in nonhost eggplant Solanum torvum

Abstract

HopH1 is an effector protein of Pseudomonas syringae pv. tomato DC3000 and P. syringae pv. syringae B728a and is a homolog of the putative Zn-dependent protease effector Rip36 of Ralstonia solanacearum, which induces hypersensitive response (HR) cell death in a nonhost plant, Solanum torvum Sw. cv. Torubamubiga. Although P. syringae pv. phaseolicola (Pph) 1448A neither produces HopH1 nor induces HR cell death, hopH1-introduced Pph 1448A acquired the ability to induce HR. These results indicate that the putative Zn-protease HopH1 effector induces HR cell death in nonhost S. torvum.

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References

  1. Agrios G (1997) Plant pathology, 4th edn. Academic Press, San Diego

    Google Scholar 

  2. Alexeyev MF, Shokolenko IN, Croughan TP (1995) New mini-Tn5 derivatives for insertion mutagenesis and genetic engineering in gram-negative bacteria. Can J Microbiol 41:1053–1055

    CAS  Article  Google Scholar 

  3. Alfano JR, Collmer A (1997) The type III (Hrp) secretion pathway of plant pathogenic bacteria: trafficking harpins, Avr proteins, and death. J Bacteriol 179:5655–5662

    CAS  Article  Google Scholar 

  4. Alfano JR, Collmer A (2004) Type III secretion system effector proteins: double agents in bacterial disease and plant defense. Annu Rev Phytopathol 42:385–414

    CAS  Article  Google Scholar 

  5. Axtell MJ, Staskawicz BJ (2003) Initiation of RPS2-specified disease resistance in Arabidopsis is coupled to the AvrRpt2-directed elimination of RIN4. Cell 112:369–377

    CAS  Article  Google Scholar 

  6. Baltrus DA, Nishimura MT, Romanchuk A, Chang JH, Mukhtar MS, Cherkis K, Roach J, Grant SR, Jones CD, Dangl JL (2011) Dynamic evolution of pathogenicity revealed by sequencing and comparative genomics of 19 Pseudomonas syringae isolates. PLoS Pathog 7:e1002132

    CAS  Article  Google Scholar 

  7. Baruch K, Gur-Arie L, Nadler C, Koby S, Yerushalmi G, Ben-Neriah Y, Yogev O, Shaulian E, Guttman C, Zarivach R, Rosenshine I (2011) Metalloprotease type III effectors that specifically cleave JNK and NF-κB. EMBO J 30:221–231

    CAS  Article  Google Scholar 

  8. Block A, Li G, Fu ZQ, Alfano JR (2008) Phytopathogen type III effector weaponry and their plant targets. Curr Opin Plant Biol 11:396–403

    CAS  Article  Google Scholar 

  9. Chien CF, Mathieu J, Hsu CH, Boyle P, Martin GB, Lin NC (2013) Nonhost resistance of tomato to the bean pathogen Pseudomonas syringae pv. syringae B728a is due to a defective E3 ubiquitin ligase domain in AvrPtoBB728a. Mol Plant Microbe Interact 26:387–397

    CAS  Article  Google Scholar 

  10. Deslandes L, Rivas S (2012) Catch me if you can: bacterial effectors and plant targets. Trends Plant Sci 17:644–655

    CAS  Article  Google Scholar 

  11. Desveaux D, Singer AU, Dangl JL (2006) Type III effector proteins: doppelgangers of bacterial virulence. Curr Opin Plant Biol 9:376–382

    CAS  Article  Google Scholar 

  12. Ferrante P, Clarke CR, Cavanaugh KA, Michelmore RW, Buonaurio R, Vinatzer BA (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

    CAS  Article  Google Scholar 

  13. Greenberg JT, Vinatzer BA (2003) Identifying type III effectors of plant pathogens and analyzing their interaction with plant cells. Curr Opin Microbiol 6:20–28

    CAS  Article  Google Scholar 

  14. Ichinose Y, Tasaka Y, Yamamoto S, Inoue Y, Takata M, Nakatsu Y, Taguchi F, Yamamoto M, Toyoda K, Noutoshi Y, Matsui H (2020) PsyR, a transcriptional regulator in quorum sensing system, binds lux box-like sequence in psyI promoter without AHL quorum sensing molecule and activates psyI transcription with AHL in Pseudomonas syringae pv. tabaci 6605. J Gen Plant Pathol 86:124–133

    CAS  Article  Google Scholar 

  15. Jia Y, McAdams SA, Bryan GT, Hershey HP, Valent B (2000) Direct interaction of resistance gene and avirulence gene products confers rice blast resistance. EMBO J 19:4004–4014

    CAS  Article  Google Scholar 

  16. Lindeberg (2014) Pseudomonas syringae genome resources home page. https://www.pseudomonas-syringae.org

  17. Lindeberg M, Stavrinides J, Chang JH, Alfano JR, Collmer A, Dangl JL, Greenberg JT, Mansfield JW, Guttman DS (2005) Proposed guidelines for a unified nomenclature and phylogenetic analysis of type III Hop effector proteins in the plant pathogen Pseudomonas syringae. Mol Plant Microbe Interact 18:275–282

    CAS  Article  Google Scholar 

  18. Lindeberg M, Cunnac S, Collmer A (2012) Pseudomonas syringae type III effector repertoires: last words in endless arguments. Trends Microbiol 20:199–208

    CAS  Article  Google Scholar 

  19. Loper JE, Lindow SE (1987) Lack of evidence for in situ fluorescent pigment production by Pseudomonas syringae pv. syringae on bean leaf surfaces. Phytopathol 77:1449–1454

    Article  Google Scholar 

  20. Luo Y, Caldwell KS, Wroblewski T, Wright ME, Michelmore RW (2009) Proteolysis of a negative regulator of innate immunity is dependent on resistance genes in tomato and Nicotiana benthamiana and induced by multiple bacterial effectors. Plant Cell 21:2458–2472

    CAS  Article  Google Scholar 

  21. Mackey D, Holt BF 3rd, Wiig A, Dangl JL (2002) RIN4 interacts with Pseudomonas syringae type III effector molecules and is required for RPM1-mediated resistance in Arabidopsis. Cell 108:743–754

    CAS  Article  Google Scholar 

  22. Mansfield J, Jenner C, Hockenhull R, Bennett MA, Stewart R (1994) Characterization of avrPphE, a gene for cultivar-specific avirulence from Pseudomonas syringae pv. phaseolicola which is physically linked to hrpY, a new hrp gene identified in the halo-blight bacterium. Mol Plant Microbe Interact 7:726–739

    CAS  Article  Google Scholar 

  23. Morel A, Guinard J, Lonjon F, Sujeeun L, Barberis P, Genin S, Vailleau F, Daunay MC, Dintinger J, Poussier S, Peeters N, Wicker E (2018) The eggplant AG91-25 recognizes the type III-secreted effector RipAX2 to trigger resistance to bacterial wilt (Ralstonia solanacearum species complex). Mol Plant Pathol 19:2459–2472

    CAS  Article  Google Scholar 

  24. Mysore KS, Ryu C-M (2004) Nonhost resistance: how much do we know? Trends Plant Sci 9:97–104

    CAS  Article  Google Scholar 

  25. Nahar K, Matsumoto I, Taguchi F, Inagaki Y, Yamamoto M, Toyoda K, Shiraishi T, Ichinose Y, Mukaihara T (2014) Ralstonia solanacearum type III secretion system effector Rip36 induces a hypersensitive response in the nonhost wild eggplant Solanum torvum. Mol Plant Pathol 15:297–303

    CAS  Article  Google Scholar 

  26. Orbach MJ, Farrall L, Sweigard JA, Chumley FG, Valent B (2000) A telomeric avirulence gene determines efficacy for the rice blast resistance gene Pi-ta. Plant Cell 12:2019–2032

    CAS  PubMed  PubMed Central  Google Scholar 

  27. Schäfer A, Tauch A, Jager W, Kalinowski J, Thierbach G, Puhler A (1994) Small mobilizable multi-purpose cloning vectors derived from the Escherichia coli plasmids pK18 and pK19: selection of defined deletions in the chromosome of Corynebacterium glutamicum. Gene 145:69–73

    Article  Google Scholar 

  28. Schechter LM, Roberts KA, Jamir Y, Alfano JR, Collmer A (2004) Pseudomonas syringae type III secretion system targeting signals and novel effectors studied with a Cya translocation reporter. J Bacteriol 186:543–555

    CAS  Article  Google Scholar 

  29. Shao F, Golstein C, Ade J, Stoutemyer M, Dixon JE, Innes RW (2003) Cleavage of Arabidopsis PBS1 by a bacterial type III effector. Science 301:1230–1233

    CAS  Article  Google Scholar 

  30. Simon R, Priefer U, Pühler A (1983) A broad host range mobilization system for in vivo genetic engineering: transposon mutagenesis in Gram-negative bacteria. Nat Biotechnol 1:784–791

    CAS  Article  Google Scholar 

  31. Sohn KH, Saucet SB, Clarke CR, Vinatzer BA, O’Brien HE, Guttman DS, Jones JD (2012) HopAS1 recognition significantly contributes to Arabidopsis nonhost resistance to Pseudomonas syringae pathogens. New Phytol 193:58–66

    CAS  Article  Google Scholar 

  32. Vencato M, Tian F, Alfano JR, Buell CR, Cartinhour S, DeClerck GA, Guttman DS, Stavrinides J, Joardar V, Lindeberg M, Bronstein PA, Mansfield JW, Myers CR, Collmer A, Schneider DJ (2006) Bioinformatics-enabled identification of the HrpL regulon and type III secretion system effector proteins of Pseudomonas syringae pv. phaseolicola 1448A. Mol Plant Microbe Interact 19:1193–1206

    CAS  Article  Google Scholar 

  33. Vinatzer BA, Teitzel GM, Lee MW, Jelenska J, Hotton S, Fairfax K, Jenrette J, Greenberg JT (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

    CAS  Article  Google Scholar 

  34. Wei CF, Kvitko BH, Shimizu R, Crabill E, Alfano JR, Lin NC, Martin GB, Huang HC, 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

    CAS  Article  Google Scholar 

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Acknowledgements

We are grateful to Dr. A. Collmer (Cornell University) for providing P. syringae pvs. tomato DC3000, syringae B728a, and phaseolicola 1448A. This work was supported in part by Grants-in-Aid for Scientific Research (Nos. 24658042 and 19H02956) from the Ministry of Education, Culture, Sports, Science and Technology of Japan and Joint Research Project by Okayama Prefecture.

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Correspondence to Yuki Ichinose.

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Nahar, K., Mukaihara, T., Taguchi, F. et al. HopH1 effectors of Pseudomonas syringae pv. tomato DC3000 and pv. syringae B728a induce HR cell death in nonhost eggplant Solanum torvum. J Gen Plant Pathol 87, 24–29 (2021). https://doi.org/10.1007/s10327-020-00961-z

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Keywords

  • Effector
  • HopH1
  • HR
  • Rip36
  • Zn-protease