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Annual Review of Phytopathology

Volume 60, 2022

Diversity, Evolution, and Function of Effectoromes

Abstract

is an evolutionarily diverse bacterial species complex and a preeminent model for the study of plant–pathogen interactions due in part to its remarkably broad host range. A critical feature of virulence is the employment of suites of type III secreted effector (T3SE) proteins, which vary widely in composition and function. These effectors act on a variety of plant intracellular targets to promote pathogenesis but can also be avirulence factors when detected by host immune complexes. In this review, we survey the phylogenetic diversity (PD) of the effectorome, comprising 70 distinct T3SE families identified to date, and highlight how avoidance of host immune detection has shaped effectorome diversity through functional redundancy, diversification, and horizontal transfer. We present emerging avenues for research and novel insights that can be gained via future investigations of plant–pathogen interactions through the fusion of large-scale interaction screens and phylogenomic approaches.

Keyword(s): avirulence, effector-triggered immunity, evolution, functional diversity, genetic diversity, plant immunity, Pseudomonas syringae, type III effectors, virulence
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/content/journals/10.1146/annurev-phyto-021621-121935
2022-08-26
2024-05-04
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Literature Cited

  1. 1.
    Adachi H, Sakai T, Kourelis J, Hernandez JLG, Maqbool A, Kamoun S. 2021. Jurassic NLR: conserved and dynamic evolutionary features of the atypically ancient immune receptor ZAR1. bioRxiv 333484. https://doi.org/10.1101/2020.10.12.333484
    [Crossref]
  2. 2.
    Alfano JR, Charkowski AO, Deng WL, Badel JL, Petnicki-Ocwieja T et al. 2000. 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. PNAS 97:4856–61
     [Google Scholar]
  3. 3.
    Almeida NF, Yan S, Lindeberg M, Studholme DJ, Schneider DJ 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
     [Google Scholar]
  4. 4.
    Altschul SF, Madden TL, Schaffer AA, Zhang J, Zhang Z et al. 1997. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25:3389–402
     [Google Scholar]
  5. 5.
    Araki H, Tian D, Goss EM, Jakob K, Halldorsdottir SS et al. 2006. Presence/absence polymorphism for alternative pathogenicity islands in Pseudomonas viridiflava, a pathogen of Arabidopsis. PNAS 103:5887–92
     [Google Scholar]
  6. 6.
    Ashfield T, Keen NT, Buzzell RI, Innes RW. 1995. Soybean resistance genes specific for different Pseudomonas syringae avirulence genes are allelic, or closely linked, at the RPG1 locus. Genetics 141:1597–604
     [Google Scholar]
  7. 7.
    Axtell MJ, Staskawicz BJ. 2003. Initiation of RPS2-specified disease resistance in Arabidopsis is coupled to the AvrRpt2-directed elimination of RIN4. Cell 112:369–77
     [Google Scholar]
  8. 8.
    Baltrus DA, McCann HC, Guttman DS. 2017. Evolution, genomics and epidemiology of Pseudomonas syringae: challenges in bacterial molecular plant pathology. Mol. Plant Pathol. 18:152–68
     [Google Scholar]
  9. 9.
    Baltrus DA, Nishimura MT, Romanchuk A, Chang JH, Mukhtar MS et al. 2011. Dynamic evolution of pathogenicity revealed by sequencing and comparative genomics of 19 Pseudomonas syringae isolates. PLOS Pathog 7:e1002132
     [Google Scholar]
  10. 10.
    Baltrus DA, Orth KN. 2018. Understanding genomic diversity in Pseudomonas syringae throughout the forest and on the trees. New Phytol 219:482–84
     [Google Scholar]
  11. 11.
    Bartoli C, Berge O, Monteil CL, Guilbaud C, Balestra GM et al. 2014. The Pseudomonas viridiflava phylogroups in the P. syringae species complex are characterized by genetic variability and phenotypic plasticity of pathogenicity-related traits. Environ. Microbiol. 16:2301–15
     [Google Scholar]
  12. 12.
    Bastedo DP, Khan M, Martel A, Seto D, Kireeva I et al. 2019. Perturbations of the ZED1 pseudokinase activate plant immunity. PLOS Pathog 15:e1007900
     [Google Scholar]
  13. 13
    Bastedo DP, Lo T, Laflamme B, Desveaux D, Guttman DS. 2020. Diversity and evolution of type III secreted effectors: a case study of three families. Curr. Top. Microbiol. Immunol. 427:201–30
     [Google Scholar]
  14. 14.
    Belkhadir Y, Nimchuk Z, Hubert DA, Mackey D, Dangl JL. 2004. Arabidopsis RIN4 negatively regulates disease resistance mediated by RPS2 and RPM1 downstream or independent of the NDR1 signal modulator and is not required for the virulence functions of bacterial type III effectors AvrRpt2 or AvrRpm1. Plant Cell 16:2822–35
     [Google Scholar]
  15. 15.
    Berge O, Monteil CL, Bartoli C, Chandeysson C, Guilbaud C et al. 2014. A user's guide to a data base of the diversity of Pseudomonas syringae and its application to classifying strains in this phylogenetic complex. PLOS ONE 9:e105547
     [Google Scholar]
  16. 16.
    Buell CR, Joardar V, Lindeberg M, Selengut J, Paulsen IT et al. 2003. The complete genome sequence of the Arabidopsis and tomato pathogen Pseudomonas syringae pv. tomato DC3000. PNAS 100:10181–86
     [Google Scholar]
  17. 17.
    Bull CT, De Boer SH, Denny TP, Firrao G, Fischer-Le Saux M et al. 2008. Demystifying the nomenclature of bacterial plant pathogens. J. Plant Pathol. 90:403–17
     [Google Scholar]
  18. 18.
    Bundalovic-Torma C, Desveaux D, Guttman DS. 2021. RecPD: a recombination-aware measure of phylogenetic diversity. PLOS Comput. Biol. 18:2e1009899
     [Google Scholar]
  19. 19.
    Buttner D. 2016. Behind the lines: actions of bacterial type III effector proteins in plant cells. FEMS Microbiol. Rev. 40:894–937
     [Google Scholar]
  20. 20.
    Cai R, Yan S, Liu H, Leman S, Vinatzer BA. 2011. Reconstructing host range evolution of bacterial plant pathogens using Pseudomonas syringae pv. tomato and its close relatives as a model. Infect. Genet. Evol. 11:1738–51
     [Google Scholar]
  21. 21.
    Cao FY, Khan M, Taniguchi M, Mirmiran A, Moeder W et al. 2019. A host-pathogen interactome uncovers phytopathogenic strategies to manipulate plant ABA responses. Plant J 100:187–98
     [Google Scholar]
  22. 22.
    Caverly LJ, LiPuma JJ. 2018. Good cop, bad cop: anaerobes in cystic fibrosis airways. Eur. Respir. J. 52:1801146
     [Google Scholar]
  23. 23.
    Chang JH, Urbach JM, Law TF, Arnold LW, Hu A et al. 2005. A high-throughput, near-saturating screen for type III effector genes from Pseudomonas syringae. PNAS 102:2549–54
     [Google Scholar]
  24. 24.
    Choi S, Prokchorchik M, Lee H, Gupta R, Lee Y et al. 2021. Direct acetylation of a conserved threonine of RIN4 by the bacterial effector HopZ5 or AvrBsT activates RPM1-dependent immunity in Arabidopsis. Mol. Plant 14:1951–60
     [Google Scholar]
  25. 25.
    Chung EH, El-Kasmi F, He Y, Loehr A, Dangl JL. 2014. A plant phosphoswitch platform repeatedly targeted by type III effector proteins regulates the output of both tiers of plant immune receptors. Cell Host Microbe 16:484–94
     [Google Scholar]
  26. 26.
    Clarke CR, Cai R, Studholme DJ, Guttman DS, Vinatzer BA. 2010. Pseudomonas syringae strains naturally lacking the classical P. syringae hrp/hrc locus are common leaf colonizers equipped with an atypical type III secretion system. Mol. Plant-Microbe Interact. 23:198–210
     [Google Scholar]
  27. 27.
    Cui F, Wu S, Sun W, Coaker G, Kunkel B et al. 2013. The Pseudomonas syringae type III effector AvrRpt2 promotes pathogen virulence via stimulating Arabidopsis auxin/indole acetic acid protein turnover. Plant Physiol 162:1018–29
     [Google Scholar]
  28. 28.
    Cui H, Tsuda K, Parker JE. 2015. Effector-triggered immunity: from pathogen perception to robust defense. Annu. Rev. Plant Biol. 66:487–511
     [Google Scholar]
  29. 29.
    Cunnac S, Chakravarthy S, Kvitko BH, Russell AB, Martin GB, Collmer A. 2011. Genetic disassembly and combinatorial reassembly identify a minimal functional repertoire of type III effectors in Pseudomonas syringae. PNAS 108:2975–80
     [Google Scholar]
  30. 30.
    Cunnac S, Lindeberg M, Collmer A. 2009. Pseudomonas syringae type III secretion system effectors: repertoires in search of functions. Curr. Opin. Microbiol. 12:53–60
     [Google Scholar]
  31. 31.
    Demba Diallo M, Monteil CL, Vinatzer BA, Clarke CR, Glaux C et al. 2012. Pseudomonas syringae naturally lacking the canonical type III secretion system are ubiquitous in nonagricultural habitats, are phylogenetically diverse and can be pathogenic. ISME J 6:1325–35
     [Google Scholar]
  32. 32.
    Dillon MM, Almeida RND, Laflamme B, Martel A, Weir BS et al. 2019. Molecular evolution of Pseudomonas syringae type III secreted effector proteins. Front. Plant Sci. 10:418
     [Google Scholar]
  33. 33.
    Dillon MM, Thakur S, Almeida RND, Wang PW, Weir BS, Guttman DS. 2019. Recombination of ecologically and evolutionarily significant loci maintains genetic cohesion in the Pseudomonas syringae species complex. Genome Biol 20:3
     [Google Scholar]
  34. 34.
    Dodds PN, Rathjen JP. 2010. Plant immunity: towards an integrated view of plant-pathogen interactions. Nat. Rev. Genet. 11:539–48
     [Google Scholar]
  35. 35.
    Eschen-Lippold L, Scheel D, Lee J. 2016. Teaching an old dog new tricks: suppressing activation of specific mitogen-activated kinases as a potential virulence function of the bacterial AvrRpt2 effector protein. Plant Signal Behav 11:e1257456
     [Google Scholar]
  36. 36.
    Faith DP. 1992. Conservation evaluation and phylogenetic diversity. Biol. Conserv. 61:1–10
     [Google Scholar]
  37. 37.
    Feehan JM, Castel B, Bentham AR, Jones JD. 2020. Plant NLRs get by with a little help from their friends. Curr. Opin. Plant Biol. 56:99–108
     [Google Scholar]
  38. 38.
    Feil H, Feil WS, Chain P, Larimer F, DiBartolo G et al. 2005. Comparison of the complete genome sequences of Pseudomonas syringae pv. syringae B728a and pv. tomato DC3000. PNAS 102:11064–69
     [Google Scholar]
  39. 39.
    Fellay R, Rahme L, Mindrinos M, Frederick R, Pisi A, Panopoulos N 1991. Genes and signals controlling the Pseudomonas syringae pv. phaseolicola-plant interaction. Advances in Molecular Genetics of Plant-Microbe Interactions, Vol. 1 H Hennecke, DPS Verma 45–52 Cham, Switz: Springer
     [Google Scholar]
  40. 40.
    Fenselau S, Balbo I, Bonas U. 1992. Determinants of pathogenicity in Xanthomonas campestris pv. vesicatoria are related to proteins involved in secretion in bacterial pathogens of animals. Mol. Plant-Microbe Interact. 5:390–96
     [Google Scholar]
  41. 41.
    Ferreira AO, Myers CR, Gordon JS, Martin GB, Vencato M et al. 2006. Whole-genome expression profiling defines the HrpL regulon of Pseudomonas syringae pv. tomato DC3000, allows de novo reconstruction of the Hrp cis clement, and identifies novel coregulated genes. Mol. Plant-Microbe Interact. 19:1167–79
     [Google Scholar]
  42. 42.
    Flor HH. 1971. Current status of the gene-for-gene concept. Annu. Rev. Phytopathol. 9:275–96
     [Google Scholar]
  43. 43.
    Fouts DE, Abramovitch RB, Alfano JR, Baldo AM, Buell CR et al. 2002. Genomewide identification of Pseudomonas syringae pv. tomato DC3000 promoters controlled by the HrpL alternative sigma factor. PNAS 99:2275–80
     [Google Scholar]
  44. 44.
    Gazi AD, Sarris PF, Fadouloglou VE, Charova SN, Mathioudakis N et al. 2012. Phylogenetic analysis of a gene cluster encoding an additional, rhizobial-like type III secretion system that is narrowly distributed among Pseudomonas syringae strains. BMC Microbiol 12:188
     [Google Scholar]
  45. 45.
    Giska F, Lichocka M, Piechocki M, Dadlez M, Schmelzer E et al. 2013. Phosphorylation of HopQ1, a type III effector from Pseudomonas syringae, creates a binding site for host 14–3–3 proteins. Plant Physiol 161:2049–61
     [Google Scholar]
  46. 46.
    Gohre V, Spallek T, Haweker H, Mersmann S, Mentzel T et al. 2008. Plant pattern-recognition receptor FLS2 is directed for degradation by the bacterial ubiquitin ligase AvrPtoB. Curr. Biol. 18:1824–32
     [Google Scholar]
  47. 47.
    Gough CL, Genin S, Zischek C, Boucher CA. 1992. hrp genes of Pseudomonas solanacearum are homologous to pathogenicity determinants of animal pathogenic bacteria and are conserved among plant pathogenic bacteria. Mol. Plant-Microbe Interact. 5:384–89
     [Google Scholar]
  48. 48.
    Gregory TR. 2009. Understanding natural selection: essential concepts and common misconceptions. Evol. Educ. Outreach 2:156–75
     [Google Scholar]
  49. 49.
    Guttman DS, Greenberg JT. 2001. Functional analysis of the type III effectors AvrRpt2 and AvrRpm1 of Pseudomonas syringae with the use of a single-copy genomic integration system. Mol. Plant-Microbe Interact. 14:145–55
     [Google Scholar]
  50. 50.
    Guttman DS, Vinatzer BA, Sarkar SF, Ranall MV, Kettler G, Greenberg JT. 2002. A functional screen for the type III (Hrp) secretome of the plant pathogen Pseudomonas syringae. Science 295:1722–26
     [Google Scholar]
  51. 51.
    Ham JH, Majerczak DR, Nomura K, Mecey C, Uribe F et al. 2009. Multiple activities of the plant pathogen type III effector proteins WtsE and AvrE require WxxxE motifs. Mol. Plant-Microbe Interact. 22:703–12
     [Google Scholar]
  52. 52.
    Hann DR, Domínguez-Ferreras A, Motyka V, Dobrev PI, Schornack S et al. 2014. The Pseudomonas type III effector HopQ1 activates cytokinin signaling and interferes with plant innate immunity. New Phytol 201:585–98
     [Google Scholar]
  53. 53.
    Hu Y, Huang H, Cheng X, Shu X, White AP et al. 2017. A global survey of bacterial type III secretion systems and their effectors. Environ. Microbiol. 19:3879–95
     [Google Scholar]
  54. 54.
    Hulin MT, Armitage AD, Vicente JG, Holub EB, Baxter L et al. 2018. Comparative genomics of Pseudomonas syringae reveals convergent gene gain and loss associated with specialization onto cherry (Prunus avium). New Phytol 219:672–96
     [Google Scholar]
  55. 55.
    Hutcheson SW, Heu S, Huang H-C, MC Lidell Xiao Y. 1994. Organization, regulation and function of Pseudomonas syringae pv. syringae hrp genes. Molecular Mechanisms of Bacterial Virulence CI Kado, JH Crosa 593–603 Boston: Kluwer
     [Google Scholar]
  56. 56.
    Huynh TV, Dahlbeck D, Staskawicz BJ. 1989. Bacterial blight of soybean: regulation of a pathogen gene determining host cultivar specificity. Science 245:1374–77
     [Google Scholar]
  57. 57.
    Innes RW, Bent AF, Kunkel BN, Bisgrove SR, Staskawicz BJ. 1993. Molecular analysis of avirulence gene avrRpt2 and identification of a putative regulatory sequence common to all known Pseudomonas syringae avirulence genes. J. Bacteriol. 175:4859–69
     [Google Scholar]
  58. 58.
    Jamir Y, Guo M, Oh HS, Petnicki-Ocwieja T, Chen S et al. 2004. Identification of Pseudomonas syringae type III effectors that can suppress programmed cell death in plants and yeast. Plant J 37:554–65
     [Google Scholar]
  59. 59.
    Jeleńska J, Lee J, Manning AJ, Wolfgeher DJ, Ahn Y et al. 2021. Pseudomonas syringae effector HopZ3 suppresses the bacterial AvrPto1-tomato PTO immune complex via acetylation. PLOS Pathog 17:e1010017
     [Google Scholar]
  60. 60.
    Jiang S, Yao J, Ma KW, Zhou H, Song J et al. 2013. Bacterial effector activates jasmonate signaling by directly targeting JAZ transcriptional repressors. PLOS Pathog. 9:e1003715
     [Google Scholar]
  61. 61.
    Joardar V, Lindeberg M, Jackson RW, Selengut J, Dodson R et al. 2005. Whole-genome sequence analysis of Pseudomonas syringae pv. phaseolicola 1448A reveals divergence among pathovars in genes involved in virulence and transposition. J. Bacteriol. 187:6488–98
     [Google Scholar]
  62. 62.
    Jones JD, Dangl JL. 2006. The plant immune system. Nature 444:323–29
     [Google Scholar]
  63. 63.
    Jubic LM, Saile S, Furzer OJ, El Kasmi F, Dangl JL. 2019. Help wanted: helper NLRs and plant immune responses. Curr. Opin. Plant Biol. 50:82–94
     [Google Scholar]
  64. 64.
    Karasov TL, Almario J, Friedemann C, Ding W, Giolai M et al. 2018. Arabidopsis thaliana and Pseudomonas pathogens exhibit stable associations over evolutionary timescales. Cell Host Microbe 24:168–79.e4
     [Google Scholar]
  65. 65.
    Keen NT. 1990. Gene-for-gene complementarity in plant-pathogen interactions. Annu. Rev. Genet. 24:447–63
     [Google Scholar]
  66. 66.
    Khan M, Seto D, Subramaniam R, Desveaux D. 2018. Oh, the places they'll go! A survey of phytopathogen effectors and their host targets. Plant J 93:651–63
     [Google Scholar]
  67. 67.
    Kim HS, Desveaux D, Singer AU, Patel P, Sondek J, Dangl JL. 2005. The Pseudomonas syringae effector AvrRpt2 cleaves its C-terminally acylated target, RIN4, from Arabidopsis membranes to block RPM1 activation. PNAS 102:6496–501
     [Google Scholar]
  68. 68.
    Kourelis J, van der Hoorn RAL. 2018. Defended to the nines: 25 years of resistance gene cloning identifies nine mechanisms for R protein function. Plant Cell 30:285–99
     [Google Scholar]
  69. 69.
    Kvitko BH, Park DH, Velasquez AC, Wei CF, Russell AB et al. 2009. Deletions in the repertoire of Pseudomonas syringae pv. tomato DC3000 type III secretion effector genes reveal functional overlap among effectors. PLOS Pathog. 5:e1000388
     [Google Scholar]
  70. 70.
    Laflamme B, Dillon MM, Martel A, Almeida RND, Desveaux D, Guttman DS. 2020. The pan-genome effector-triggered immunity landscape of a host-pathogen interaction. Science 367:763–68
     [Google Scholar]
  71. 71.
    Lamichhane JR, Messéan A, Morris CE. 2015. Insights into epidemiology and control of diseases of annual plants caused by the Pseudomonas syringae species complex. J. Gen. Plant Pathol. 81:331–50
     [Google Scholar]
  72. 72.
    Lee AH, Hurley B, Felsensteiner C, Yea C, Ckurshumova W et al. 2012. A bacterial acetyltransferase destroys plant microtubule networks and blocks secretion. PLOS Pathog. 8:e1002523
     [Google Scholar]
  73. 73.
    Lee J, Manning AJ, Wolfgeher D, Jelenska J, Cavanaugh KA et al. 2015. Acetylation of an NB-LRR plant immune-effector complex suppresses immunity. Cell Rep 13:1670–82
     [Google Scholar]
  74. 74.
    Lewis JD, Abada W, Ma W, Guttman DS, Desveaux D. 2008. The HopZ family of Pseudomonas syringae type III effectors require myristoylation for virulence and avirulence functions in Arabidopsis thaliana. J. Bacteriol. 190:2880–91
     [Google Scholar]
  75. 75.
    Lewis JD, Lee A, Ma W, Zhou H, Guttman DS, Desveaux D. 2011. The YopJ superfamily in plant-associated bacteria. Mol. Plant Pathol. 12:928–37
     [Google Scholar]
  76. 76.
    Lewis JD, Lee AH, Hassan JA, Wan J, Hurley B et al. 2013. The Arabidopsis ZED1 pseudokinase is required for ZAR1-mediated immunity induced by the Pseudomonas syringae type III effector HopZ1a. PNAS 110:18722–27
     [Google Scholar]
  77. 77.
    Lewis JD, Wan J, Ford R, Gong Y, Fung P et al. 2012. Quantitative interactor screening with next-generation sequencing (QIS-Seq) identifies Arabidopsis thaliana MLO2 as a target of the Pseudomonas syringae type III effector HopZ2. BMC Genom 13:8
     [Google Scholar]
  78. 78.
    Lewis JD, Wu R, Guttman DS, Desveaux D. 2010. Allele-specific virulence attenuation of the Pseudomonas syringae HopZ1a type III effector via the Arabidopsis ZAR1 resistance protein. PLOS Genet 6:e1000894
     [Google Scholar]
  79. 79.
    Li W, Yadeta KA, Elmore JM, Coaker G. 2013. The Pseudomonas syringae effector HopQ1 promotes bacterial virulence and interacts with tomato 14–3–3 proteins in a phosphorylation-dependent manner. Plant Physiol 161:2062–74
     [Google Scholar]
  80. 80.
    Lindeberg M, Cartinhour S, Myers CR, Schechter LM, Schneider DJ, Collmer A. 2006. Closing the circle on the discovery of genes encoding Hrp regulon members and type III secretion system effectors in the genomes of three model Pseudomonas syringae strains. Mol. Plant-Microbe Interact. 19:1151–58
     [Google Scholar]
  81. 81.
    Lindgren PB, Peet RC, Panopoulos NJ. 1986. Gene cluster of Pseudomonas syringae pv. phaseolicola controls pathogenicity of bean plants and hypersensitivity of nonhost plants. J. Bacteriol. 168:512–22
     [Google Scholar]
  82. 82.
    Liu J, Elmore JM, Lin ZJ, Coaker G. 2011. A receptor-like cytoplasmic kinase phosphorylates the host target RIN4, leading to the activation of a plant innate immune receptor. Cell Host Microbe 9:137–46
     [Google Scholar]
  83. 83.
    Lozano-Durán R, Bourdais G, He SY, Robatzek S. 2014. The bacterial effector HopM1 suppresses PAMP-triggered oxidative burst and stomatal immunity. New Phytol 202:259–69
     [Google Scholar]
  84. 84.
    Lozano-Durán R, Zipfel C 2015. Trade-off between growth and immunity: role of brassinosteroids. Trends Plant Sci 20:12–19
     [Google Scholar]
  85. 85.
    Ma KW, Ma W. 2016. YopJ family effectors promote bacterial infection through a unique acetyltransferase activity. Microbiol. Mol. Biol. Rev. 80:1011–27
     [Google Scholar]
  86. 86.
    Ma W, Dong FF, Stavrinides J, Guttman DS. 2006. Type III effector diversification via both pathoadaptation and horizontal transfer in response to a coevolutionary arms race. PLOS Genet 2:e209
     [Google Scholar]
  87. 87.
    Macho AP, Guevara CM, Tornero P, Ruiz-Albert J, Beuzon CR. 2010. The Pseudomonas syringae effector protein HopZ1a suppresses effector-triggered immunity. New Phytol 187:1018–33
     [Google Scholar]
  88. 88.
    Macho AP, Schwessinger B, Ntoukakis V, Brutus A, Segonzac C et al. 2014. A bacterial tyrosine phosphatase inhibits plant pattern recognition receptor activation. Science 343:1509–12
     [Google Scholar]
  89. 89.
    Macho AP, Zipfel C. 2015. Targeting of plant pattern recognition receptor-triggered immunity by bacterial type-III secretion system effectors. Curr. Opin. Microbiol. 23:14–22
     [Google Scholar]
  90. 90.
    Mackey D, Belkhadir Y, Alonso JM, Ecker JR, Dangl JL. 2003. Arabidopsis RIN4 is a target of the type III virulence effector AvrRpt2 and modulates RPS2-mediated resistance. Cell 112:379–89
     [Google Scholar]
  91. 91.
    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 108:743–54
     [Google Scholar]
  92. 92.
    Madden LV, Hughes G, van den Bosch F. 2017. The Study of Plant Disease Epidemics St. Paul, MN: APS Press
  93. 93.
    Mansfield J, Genin S, Magori S, Citovsky V, Sriariyanum M et al. 2012. Top 10 plant pathogenic bacteria in molecular plant pathology. Mol. Plant Pathol. 13:614–29
     [Google Scholar]
  94. 94.
    Martel A, Laflamme B, Seto D, Bastedo DP, Dillon MM et al. 2020. Immunodiversity of the Arabidopsis ZAR1 NLR is conveyed by receptor-like cytoplasmic kinase sensors. Front. Plant Sci. 11:1290
     [Google Scholar]
  95. 95.
    Martel A, Ruiz-Bedoya T, Breit-McNally C, Laflamme B, Desveaux D, Guttman DS. 2021. The ETS-ETI cycle: evolutionary processes and metapopulation dynamics driving the diversification of pathogen effectors and host immune factors. Curr. Opin. Plant Biol. 62:102011
     [Google Scholar]
  96. 96.
    Martin-Sanz A, de la Vega MP, Murillo J, Caminero C. 2013. Strains of Pseudomonas syringae pv. syringae from pea are phylogenetically and pathogenically diverse. Phytopathology 103:673–81
     [Google Scholar]
  97. 97.
    Mazo-Molina C, Mainiero S, Hind SR, Kraus CM, Vachev M et al. 2019. The Ptr1 locus of Solanum lycopersicoides confers resistance to race 1 strains of Pseudomonas syringae pv. tomato and to Ralstonia pseudosolanacearum by recognizing the type III effectors AvrRpt2 and RipBN. Mol. Plant-Microbe Interact. 32:949–60
     [Google Scholar]
  98. 98.
    McCann HC, Guttman DS. 2008. Evolution of the type III secretion system and its effectors in plant-microbe interactions. New Phytol 177:33–47
     [Google Scholar]
  99. 99.
    Monteil CL, Cai R, Liu H, Llontop ME, Leman S et al. 2013. Nonagricultural reservoirs contribute to emergence and evolution of Pseudomonas syringae crop pathogens. New Phytol 199:800–11
     [Google Scholar]
  100. 100.
    Morris CE, Kinkel LL, Xiao K, Prior P, Sands DC. 2007. Surprising niche for the plant pathogen Pseudomonas syringae. Infect. Genet. Evol. 7:84–92
     [Google Scholar]
  101. 101.
    Morris CE, Lamichhane JR, Nikolić I, Stanković S, Moury B. 2019. The overlapping continuum of host range among strains in the Pseudomonas syringae complex. Phytopathol. Res. 1:4
     [Google Scholar]
  102. 102.
    Morris CE, Monteil CL, Berge O. 2013. The life history of Pseudomonas syringae: linking agriculture to earth system processes. Annu. Rev. Phytopathol. 51:85–104
     [Google Scholar]
  103. 103.
    Morris CE, Moury B. 2019. Revisiting the concept of host range of plant pathogens. Annu. Rev. Phytopathol. 57:63–90
     [Google Scholar]
  104. 104.
    Morris CE, Sands DC, Vinatzer BA, Glaux C, Guilbaud C et al. 2008. The life history of the plant pathogen Pseudomonas syringae is linked to the water cycle. ISME J 2:321–34
     [Google Scholar]
  105. 105.
    Mudgett MB, Staskawicz BJ. 1999. Characterization of the Pseudomonas syringae pv. tomato AvrRpt2 protein: demonstration of secretion and processing during bacterial pathogenesis. Mol. Microbiol. 32:927–41
     [Google Scholar]
  106. 106.
    Mukhtar MS, Carvunis AR, Dreze M, Epple P, Steinbrenner J et al. 2011. Independently evolved virulence effectors converge onto hubs in a plant immune system network. Science 333:596–601
     [Google Scholar]
  107. 107.
    Napoli C, Staskawicz B. 1987. Molecular characterization and nucleic acid sequence of an avirulence gene from race 6 of Pseudomonas syringae pv. glycinea. J. Bacteriol. 169:572–78
     [Google Scholar]
  108. 108.
    Nicaise V, Joe A, Jeong BR, Korneli C, Boutrot F et al. 2013. Pseudomonas HopU1 modulates plant immune receptor levels by blocking the interaction of their mRNAs with GRP7. EMBO J. 32:5701–12
     [Google Scholar]
  109. 109.
    Niepold F, Anderson D, Mills D 1985. Cloning determinants of pathogenesis from Pseudomonas syringae pathovar syringae. PNAS 82:406–10
     [Google Scholar]
  110. 110.
    Nomura K, Debroy S, Lee YH, Pumplin N, Jones J, He SY. 2006. A bacterial virulence protein suppresses host innate immunity to cause plant disease. Science 313:220–23
     [Google Scholar]
  111. 111.
    Nomura K, Mecey C, Lee YN, Imboden LA, Chang JH, He SY. 2011. Effector-triggered immunity blocks pathogen degradation of an immunity-associated vesicle traffic regulator in Arabidopsis. PNAS 108:10774–79
     [Google Scholar]
  112. 112.
    O'Brien HE, Thakur S, Gong Y, Fung P, Zhang J et al. 2012. Extensive remodeling of the Pseudomonas syringae pv. avellanae type III secretome associated with two independent host shifts onto hazelnut. BMC Microbiol 12:141
     [Google Scholar]
  113. 113.
    Petnicki-Ocwieja T, Schneider DJ, Tam VC, Chancey ST, Shan L et al. 2002. Genomewide identification of proteins secreted by the Hrp type III protein secretion system of Pseudomonassyringae pv. tomato DC3000. PNAS 99:7652–57
     [Google Scholar]
  114. 114.
    Ploetz RC. 2015. Fusarium wilt of banana. Phytopathology 105:1512–21
     [Google Scholar]
  115. 115.
    Prokchorchik M, Choi S, Chung EH, Won K, Dangl JL, Sohn KH. 2020. A host target of a bacterial cysteine protease virulence effector plays a key role in convergent evolution of plant innate immune system receptors. New Phytol 225:1327–42
     [Google Scholar]
  116. 116.
    Ristaino JB, Anderson PK, Bebber DP, Brauman KA, Cunniffe NJ et al. 2021. The persistent threat of emerging plant disease pandemics to global food security. PNAS 118:23e2022239118
     [Google Scholar]
  117. 117.
    Ritter C, Dangl JL. 1996. Interference between two specific pathogen recognition events mediated by distinct plant disease resistance genes. Plant Cell 8:251–57
     [Google Scholar]
  118. 118.
    Rufián JS, Lucía A, Rueda-Blanco J, Zumaquero A, Guevara CM et al. 2018. Suppression of HopZ effector-triggered plant immunity in a natural pathosystem. Front. Plant Sci. 9:977
     [Google Scholar]
  119. 119.
    Rufián JS, Rueda-Blanco J, López-Márquez D, Macho AP, Beuzón CR, Ruiz-Albert J. 2021. The bacterial effector HopZ1a acetylates MKK7 to suppress plant immunity. New Phytol 231:1138–56
     [Google Scholar]
  120. 120.
    Salmeron JM, Staskawicz BJ. 1993. Molecular characterization and hrp dependence of the avirulence gene avrPto from Pseudomonas syringae pv. tomato. Mol. Gen. Genet. 239:6–16
     [Google Scholar]
  121. 121.
    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. 186:543–55
     [Google Scholar]
  122. 122.
    Schechter LM, Vencato M, Jordan KL, Schneider SE, Schneider DJ, Collmer A. 2006. Multiple approaches to a complete inventory of Pseudomonas syringae pv. tomato DC3000 type III secretion system effector proteins. Mol. Plant-Microbe Interact. 19:1180–92
     [Google Scholar]
  123. 123.
    Scholthof KB. 2007. The disease triangle: pathogens, the environment and society. Nat. Rev. Microbiol. 5:152–56
     [Google Scholar]
  124. 124.
    Schreiber KJ, Chau-Ly IJ, Lewis JD 2021. What the wild things do: mechanisms of plant host manipulation by bacterial type III-secreted effector proteins. Microorganisms 9:51029
     [Google Scholar]
  125. 125.
    Schreiber KJ, Hassan JA, Lewis JD. 2021. Arabidopsis Abscisic Acid Repressor 1 is a susceptibility hub that interacts with multiple Pseudomonas syringae effectors. Plant J 105:1274–92
     [Google Scholar]
  126. 126.
    Schreiber KJ, Lewis JD. 2021. Identification of a putative DNA-binding protein in Arabidopsis that acts as a susceptibility hub and interacts with multiple Pseudomonas syringae effectors. Mol. Plant-Microbe Interact. 34:410–25
     [Google Scholar]
  127. 127.
    Selote D, Kachroo A. 2010. RPG1-B-derived resistance to AvrB-expressing Pseudomonas syringae requires RIN4-like proteins in soybean. Plant Physiol 153:1199–211
     [Google Scholar]
  128. 128.
    Seto D, Koulena N, Lo T, Menna A, Guttman DS, Desveaux D. 2017. Expanded type III effector recognition by the ZAR1 NLR protein using ZED1-related kinases. Nat. Plants 3:17027
     [Google Scholar]
  129. 129.
    Shan L, He P, Li J, Heese A, Peck SC 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
     [Google Scholar]
  130. 130.
    Staskawicz BJ, Dahlbeck D, Keen NT. 1984. Cloned avirulence gene of Pseudomonas syringae pv. glycinea determines race-specific incompatibility on Glycine max (L.) Merr. PNAS 81:6024–28
     [Google Scholar]
  131. 131.
    Stavrinides J, Ma W, Guttman DS. 2006. Terminal reassortment drives the quantum evolution of type III effectors in bacterial pathogens. PLOS Pathog. 2:e104
     [Google Scholar]
  132. 132.
    Sun X, Greenwood DR, Templeton MD, Libich DS, McGhie TK et al. 2014. The intrinsically disordered structural platform of the plant defence hub protein RPM1-interacting protein 4 provides insights into its mode of action in the host-pathogen interface and evolution of the nitrate-induced domain protein family. FEBS J 281:3955–79
     [Google Scholar]
  133. 133.
    Tegli S, Gori A, Cerboneschi M, Cipriani MG, Sisto A. 2011. Type three secretion system in Pseudomonas savastanoi pathovars: Does timing matter?. Genes 2:957–79
     [Google Scholar]
  134. 134.
    Tsiamis G, Mansfield JW, Hockenhull R, Jackson RW, Sesma A et al. 2000. Cultivar-specific avirulence and virulence functions assigned to avrPphF in Pseudomonas syringae pv. phaseolicola, the cause of bean halo-blight disease. EMBO J 19:3204–14
     [Google Scholar]
  135. 135.
    Ustun S, Konig P, Guttman DS, Bornke F. 2014. HopZ4 from Pseudomonas syringae, a member of the HopZ type III effector family from the YopJ superfamily, inhibits the proteasome in plants. Mol. Plant-Microbe Interact. 27:611–23
     [Google Scholar]
  136. 136.
    Vencato M, Tian F, Alfano JR, Buell CR, Cartinhour S et al. 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. 19:1193–206
     [Google Scholar]
  137. 137.
    Vinatzer BA, Teitzel GM, Lee MW, Jelenska J, Hotton S et al. 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
     [Google Scholar]
  138. 138.
    Wang G, Roux B, Feng F, Guy E, Li L et al. 2015. The decoy substrate of a pathogen effector and a pseudokinase specify pathogen-induced modified-self recognition and immunity in plants. Cell Host Microbe 18:285–95
     [Google Scholar]
  139. 139.
    Wang Y, Li J, Hou S, Wang X, Li Y et al. 2010. A Pseudomonas syringae ADP-ribosyltransferase inhibits Arabidopsis mitogen-activated protein kinase kinases. Plant Cell 22:2033–44
     [Google Scholar]
  140. 140.
    Wei HL, Zhang W, Collmer A. 2018. Modular study of the type III effector repertoire in Pseudomonas syringae pv. tomato DC3000 reveals a matrix of effector interplay in pathogenesis. Cell Rep 23:1630–38
     [Google Scholar]
  141. 141.
    Weßling R, Epple P, Altmann S, He Y, Yang L et al. 2014. Convergent targeting of a common host protein-network by pathogen effectors from three kingdoms of life. Cell Host Microbe 16:364–75
     [Google Scholar]
  142. 142.
    Wilton M, Subramaniam R, Elmore J, Felsensteiner C, Coaker G, Desveaux D. 2010. The type III effector HopF2Pto targets Arabidopsis RIN4 protein to promote Pseudomonas syringae virulence. PNAS 107:2349–54
     [Google Scholar]
  143. 143.
    Xiang T, Zong N, Zhang J, Chen J, Chen M, Zhou JM 2011. BAK1 is not a target of the Pseudomonas syringae effector AvrPto. Mol. Plant-Microbe Interact. 24:100–7
     [Google Scholar]
  144. 144.
    Xiang T, Zong N, Zou Y, Wu Y, Zhang J et al. 2008. Pseudomonas syringae effector AvrPto blocks innate immunity by targeting receptor kinases. Curr. Biol. 18:74–80
     [Google Scholar]
  145. 145.
    Xiao Y, Heu S, Yi J, Lu Y, Hutcheson SW. 1994. Identification of a putative alternate sigma factor and characterization of a multicomponent regulatory cascade controlling the expression of Pseudomonas syringae pv. syringae Pss61 hrp and hrmA genes. J. Bacteriol. 176:1025–36
     [Google Scholar]
  146. 146.
    Xin XF, Kvitko B, He SY. 2018. Pseudomonas syringae: what it takes to be a pathogen. Nat. Rev. Microbiol. 16:316–28
     [Google Scholar]
  147. 147.
    Xin XF, Nomura K, Aung K, Velásquez AC, Yao J et al. 2016. Bacteria establish an aqueous living space in plants crucial for virulence. Nature 539:524–29
     [Google Scholar]
  148. 148.
    Xin XF, Nomura K, Ding X, Chen X, Wang K et al. 2015. Pseudomonas syringae effector avirulence protein E localizes to the host plasma membrane and down-regulates the expression of the NONRACE-SPECIFIC DISEASE RESISTANCE1/HARPIN-INDUCED1-LIKE13 gene required for antibacterial immunity in Arabidopsis. Plant Physiol 169:793–802
     [Google Scholar]
  149. 149.
    Young JM. 2008. An overview of bacterial nomenclature with special reference to plant pathogens. Syst. Appl. Microbiol. 31:405–24
     [Google Scholar]
  150. 150.
    Young JM. 2010. Taxonomy of Pseudomonas syringae. J. Plant Pathol. 92:S5–S14
     [Google Scholar]
  151. 151.
    Young JM, Bull CT, De Boer SH, Firrao G, Gardan L et al. 2001. Classification, nomenclature, and plant pathogenic bacteria – a clarification. Phytopathology 91:617–20
     [Google Scholar]
  152. 152.
    Young JM, Dye DW, Bradbury JF, Panagopoulos CG, Robbs CF. 1978. Proposed nomenclature and classification for plant pathogenic bacteria. N. Z. J. Agric. Res. 21:153–77
     [Google Scholar]
  153. 153.
    Zhou H, Lin J, Johnson A, Morgan RL, Zhong W, Ma W. 2011. Pseudomonas syringae type III effector HopZ1 targets a host enzyme to suppress isoflavone biosynthesis and promote infection in soybean. Cell Host Microbe 9:177–86
     [Google Scholar]
  154. 154.
    Zhou H, Morgan RL, Guttman DS, Ma W. 2009. Allelic variants of the Pseudomonas syringae type III effector HopZ1 are differentially recognized by plant resistance systems. Mol. Plant-Microbe Interact. 22:176–89
     [Google Scholar]
  155. 155.
    Zhou J, Wu S, Chen X, Liu C, Sheen J et al. 2014. The Pseudomonas syringae effector HopF2 suppresses Arabidopsis immunity by targeting BAK1. Plant J 77:235–45
     [Google Scholar]
  156. 156.
    Zwiesler-Vollick J, Plovanich-Jones AE, Nomura K, Bandyopadhyay S, Joardar V et al. 2002. Identification of novel hrp-regulated genes through functional genomic analysis of the Pseudomonas syringae pv. tomato DC3000 genome. Mol. Microbiol. 45:1207–18
     [Google Scholar]
/content/journals/10.1146/annurev-phyto-021621-121935
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Diversity, Evolution, and Function of Pseudomonas syringae Effectoromes
Annual Review of Phytopathology 60, 211 (2022); https://doi.org/10.1146/annurev-phyto-021621-121935
/content/journals/10.1146/annurev-phyto-021621-121935
/content/journals/10.1146/annurev-phyto-021621-121935
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