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Functional Plant Biology Functional Plant Biology Society
Plant function and evolutionary biology
RESEARCH FRONT

Deciphering the mode of action and host recognition of bacterial type III effectors

Selena Gimenez-Ibanez A , Dagmar R. Hann B and John P. Rathjen C D
+ Author Affiliations
- Author Affiliations

A Departamento de Genética Molecular de Plantas, Centro Nacional de Biotecnología-CSIC, Campus Universidad Autónoma, 28049 Madrid, Spain.

B Botanical Institute, University of Basel, Section of Plant Physiology, Hebelstrasse 1, CH-4056 Basel, Switzerland.

C Research School of Biology, The Australian National University, RN Robertson Building, Biology Place, Acton, ACT 0200, Australia.

D Corresponding author. Email: john.rathjen@anu.edu.au

Functional Plant Biology 37(10) 926-932 https://doi.org/10.1071/FP10085
Submitted: 16 April 2010  Accepted: 8 July 2010   Published: 23 September 2010

Abstract

Plant pathogenic bacteria adhere to cell walls and remain external to the cell throughout the pathogenic lifecycle, where they elicit host immunity through host plasma membrane localised receptors. To be successful pathogens, bacteria must suppress these defence responses, which they do by secreting a suite of virulence effector molecules into the host cytoplasm. However, effectors themselves can act as elicitors after perception by intracellular host immune receptors, thus, re-activating plant immunity. Bacterial effectors generally target host molecules through specific molecular activities to defeat plant defence responses. Although effectors can be used as tools to elucidate components of plant immunity, only a handful of these molecular targets are known and much remains to be learnt about effector strategies for bacterial pathogenicity. This review highlights recent advances in our understanding of the mode of action of bacterial effectors, which in the future will lead to improvements in agriculture.

Additional keywords: bacteria, defense, effector, NB-LRR, plant immunity, PRR.


Acknowledgements

We apologise to those authors whose work could not be cited owing to space limitations. SGI is funded by the Federation of European Biochemical Societies (FEBS). DRH is funded by the Suisse National Science foundation and the Suisse Initiative in Systems Biology (SystemsX: Plant growth in a changing environment). JPR is an Australian Research Council Future Fellow (FT0992129).


References


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. Molecular Plant-Microbe Interactions 22(1), 52–62.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Asai T, Tena G, Plotnikova J, Willmann MR, Chiu WL, Gomez-Gomez L, Boller T, Ausubel FM, Sheen J (2002) MAP kinase signalling cascade in Arabidopsis innate immunity. Nature 415(6875), 977–983.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Axtell MJ, Staskawicz B (2003) Initiation of RPS2-specified disease resistance in Arabidopsis is coupled to the AvrRpt2-directed elimination of RIN4. Cell 112, 369–377.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Bartetzko V, Sonnewald S, Vogel F, Hartner K, Stadler R, Hammes UZ, Bornke F (2009) The Xanthomonas campestris pv. vesicatoria type III effector protein XopJ inhibits protein secretion: evidence for interference with cell wall-associated defense responses. Molecular Plant-Microbe Interactions 22(6), 655–664.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Birker D, Heidrich K, Takahara H, Narusaka M, Deslandes L, Narusaka Y, Reymond M, Parker JE, O’Connell R (2009) A locus conferring resistance to Colletotrichum higginsianum is shared by four geographically distinct Arabidopsis accessions. The Plant Journal 60(4), 602–613.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Boch J, Scholze H, Schornack S, Landgraf A, Hahn S, Kay S, Lahaye T, Nickstadt A, Bonas U (2009) Breaking the code of DNA binding specificity of TAL-type III effectors. Science 326(5959), 1509–1512.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Boller T, Felix G (2009) A renaissance of elicitors: perception of microbe-associated molecular patterns and danger signals by pattern-recognition receptors. Annual Review of Plant Biology 60, 379–406.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

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. Proceedings of the National Academy of Sciences of the United States of America 100(18), 10181–10186.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Chinchilla D, Zipfel C, Robatzek S, Kemmerling B, Nurnberger T, Jones JD, Felix G, Boller T (2007) A flagellin-induced complex of the receptor FLS2 and BAK1 initiates plant defence. Nature 448(7152), 497–500.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Cui H, Wang Y, Xue L, Chu J, Yan C, Fu J, Chen M, Innes RW, Zhou JM (2010) Pseudomonas syringae effector protein AvrB perturbs Arabidopsis hormone signaling by activating MAP kinase 4. Cell Host & Microbe 7(2), 164–175.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Dangl JL, Jones JDG (2001) Plant pathogens and integrated defence responses to infection. Nature 411, 826–833.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Deslandes L, Olivier J, Peeters N, Feng DX, Khounlotham M, Boucher C, Somssich IE, Genin S, Marco Y (2003) Physical interaction between RRS1-R, a protein conferring resistance to bacterial wilt, and PopP2, a type III effector targeted to the plant nucleus. Proceedings of the National Academy of Sciences of the United States of America 100(13), 8024–8029.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

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. Proceedings of the National Academy of Sciences of the United States of America 102(31), 11064–11069.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Fu ZQ, Guo M, Jeong BR, Tian F, Elthon TE, Cerny RL, Staiger D, Alfano JR (2007) A type III effector ADP-ribosylates RNA-binding proteins and quells plant immunity. Nature 447(7142), 284–288.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Gassmann W, Hinsch ME, Staskawicz BJ (1999) The Arabidopsis RPS4 bacterial-resistance gene is a member of the TIR-NBS-LRR family of disease-resistance genes. The Plant Journal 20(3), 265–277.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Gimenez-Ibanez S, Hann DR, Ntoukakis V, Petutschnig E, Lipka V, Rathjen JP (2009) AvrPtoB targets the LysM receptor kinase CERK1 to promote bacterial virulence on plants. Current Biology 19(5), 423–429.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Göhre V, Robatzek S (2008) Breaking the barriers: microbial effector molecules subvert plant immunity. Annual Review of Phytopathology 46, 189–215.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Gohre V, Spallek T, Haweker H, Mersmann S, Mentzel T, Boller T, de Torres M, Mansfield JW, Robatzek S (2008) Plant pattern-recognition receptor FLS2 is directed for degradation by the bacterial ubiquitin ligase AvrPtoB. Current Biology 18(23), 1824–1832.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Gómez-Gómez L, Boller T (2000) FLS2: An LRR receptor-like kinase involved in the perception of the bacterial elicitor flagellin in Arabidopsis. Molecular Cell 5(6), 1003–1011.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Guo M, Tian F, Wamboldt Y, Alfano JR (2009) The majority of the type III effector inventory of Pseudomonas syringae pv. tomato DC3000 can suppress plant immunity. Molecular Plant-Microbe Interactions 22(9), 1069–1080.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Gurlebeck D, Thieme F, Bonas U (2006) Type III effector proteins from the plant pathogen Xanthomonas and their role in the interaction with the host plant. Journal of Plant Physiology 163(3), 233–255.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Gutierrez JR, Balmuth AL, Ntoukakis V, Mucyn TS, Gimenez-Ibanez S, Jones AM, Rathjen JP (2010) Prf immune complexes of tomato are oligomeric and contain multiple Pto-like kinases that diversify effector recognition. Plant Journal 61, 507–518.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

He P, Shan L, Lin NC, Martin GB, Kemmerling B, Nurnberger T, Sheen J (2006) Specific bacterial suppressors of MAMP signaling upstream of MAPKKK in Arabidopsis innate immunity. Cell 125(3), 563–575.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Heese A, Hann DR, Gimenez-Ibanez S, Jones AM, He K, Li J, Schroeder JI, Peck SC, Rathjen JP (2007) The receptor-like kinase SERK3/BAK1 is a central regulator of innate immunity in plants. Proceedings of the National Academy of Sciences of the United States of America 104(29), 12217–12222.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

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. Journal of Bacteriology 187(18), 6488–6498.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Jones JD, Dangl JL (2006) The plant immune system. Nature 444(7117), 323–329.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Kalde M, Nuhse TS, Findlay K, Peck SC (2007) The syntaxin SYP132 contributes to plant resistance against bacteria and secretion of pathogenesis-related protein 1. Proceedings of the National Academy of Sciences of the United States of America 104(28), 11850–11855.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Kay S, Bonas U (2009) How Xanthomonas type III effectors manipulate the host plant. Current Opinion in Microbiology 12(1), 37–43.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Kvitko BH, Park DH, Velasquez AC, Wei CF, Russell AB, Martin GB, Schneider DJ, Collmer A (2009) Deletions in the repertoire of Pseudomonas syringae pv. tomato DC3000 type III secretion effector genes reveal functional overlap among effectors. PLoS Pathogens 5(4), e1000388.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Liu J, Elmore JM, Fuglsang AT, Palmgren MG, Staskawicz BJ, Coaker G (2009) RIN4 functions with plasma membrane H+-ATPases to regulate stomatal apertures during pathogen attack. PLoS Biology 7(6), e1000139.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Mackey D, Holt BF, 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(6), 743–754.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Mackey D, Belkhadir Y, Alonso JM, Ecker JR, Dangl J (2003) Arabidopsis RIN4 is a target of the type III virulence effector AvrRpt2 and modulates RPS2-mediated resistance. Cell 112, 379–389.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Melotto M, Underwood W, Koczan J, Nomura K, He SY (2006) Plant stomata function in innate immunity against bacterial invasion. Cell 126(5), 969–980.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Melotto M, Underwood W, He SY (2008) Role of stomata in plant innate immunity and foliar bacterial diseases. Annual Review of Phytopathology 46, 101–122.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Moscou MJ, Bogdanove AJ (2009) A simple cipher governs DNA recognition by TAL effectors. Science 326(5959), 1501.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Mucyn TS, Clemente A, Andriotis VM, Balmuth AL, Oldroyd GE, Staskawicz BJ, Rathjen JP (2006) The tomato NBARC-LRR protein Prf interacts with Pto kinase in vivo to regulate specific plant immunity. The Plant Cell 18(10), 2792–2806.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Narusaka M, Shirasu K, Noutoshi Y, Kubo Y, Shiraishi T, Iwabuchi M, Narusaka Y (2009) RRS1 and RPS4 provide a dual Resistance-gene system against fungal and bacterial pathogens. The Plant Journal 60(2), 218–226.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

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(5784), 220–223.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Ntoukakis V, Mucyn TS, Gimenez-Ibanez S, Chapman HC, Gutierrez JR, Balmuth AL, Jones AM, Rathjen JP (2009) Host inhibition of a bacterial virulence effector triggers immunity to infection. Science 324(5928), 784–787.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Romer P, Hahn S, Jordan T, Strauss T, Bonas U, Lahaye T (2007) Plant pathogen recognition mediated by promoter activation of the pepper Bs3 resistance gene. Science 318(5850), 645–648.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Romer P, Recht S, Lahaye T (2009) A single plant resistance gene promoter engineered to recognize multiple TAL effectors from disparate pathogens. Proceedings of the National Academy of Sciences of the United States of America 106(48), 20526–20531.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Rosebrock TR, Zeng L, Brady JJ, Abramovitch RB, Xiao F, Martin GB (2007) A bacterial E3 ubiquitin ligase targets a host protein kinase to disrupt plant immunity. Nature 448(7151), 370–374.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Sawada H, Suzuki F, Matsuda I, Saitou N (1999) Phylogenetic analysis of Pseudomonas syringae pathovars suggests the horizontal gene transfer of argK and the evolutionary stability of hrp gene cluster. Journal of Molecular Evolution 49(5), 627–644.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Shan L, He P, Li J, Heese A, Peck SC, Nurnberger T, Martin GB, 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(1), 17–27.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

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(5637), 1230–1233.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Shiu SH, Bleecker AB (2003) Expansion of the receptor-like kinase/Pelle gene family and receptor-like proteins in Arabidopsis. Plant Physiology 132(2), 530–543.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Steinmann T, Geldner N, Grebe M, Mangold S, Jackson CL, Paris S, Galweiler L, Palme K, Jurgens G (1999) Coordinated polar localization of auxin efflux carrier PIN1 by GNOM ARF GEF. Science 286(5438), 316–318.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Studholme DJ, Ibanez SG, MacLean D, Dangl JL, Chang JH, Rathjen JP (2009) A draft genome sequence and functional screen reveals the repertoire of type III secreted proteins of Pseudomonas syringae pathovar tabaci 11528. BMC Genomics 10, 395.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Suarez-Rodriguez MC, Adams-Phillips L, Liu Y, Wang H, Su SH, Jester PJ, Zhang S, Bent AF, Krysan PJ (2007) MEKK1 is required for flg22-induced MPK4 activation in Arabidopsis plants. Plant Physiology 143(2), 661–669.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

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. The Plant Journal 51(1), 32–46.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

White FF, Potnis N, Jones JB, Koebnik R (2009) The type III effectors of Xanthomonas. Molecular Plant Pathology 10(6), 749–766.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

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. Proceedings of the National Academy of Sciences of the United States of America 107(5), 2349–2354.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Wu A-J, Andriotis VME, Durrant MC, Rathjen JP (2004) A patch of surface-exposed residues mediates negative regulation of immune signaling by tomato Pto kinase. The Plant Cell 16(10), 2809–2821.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Xiang T, Zong N, Zou Y, Wu Y, Zhang J , et al . (2008) Pseudomonas syringae effector AvrPto blocks innate immunity by targeting receptor kinases. Current Biology 18(1), 74–80.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Yang B, Sugio A, White FF (2005) Avoidance of host recognition by alterations in the repetitive and C-terminal regions of AvrXa7, a type III effector of Xanthomonas oryzae pv. oryzae. Molecular Plant-Microbe Interactions 18(2), 142–149.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Zhang J, Shao F, Li Y, Cui H, Chen L , et al . (2007) A Pseudomonas syringae effector inactivates MAPKs to suppress PAMP-induced immunity in plants. Cell Host & Microbe 1(3), 175–185.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Zhang J, Li W, Xiang T, Liu Z, Laluk K , et al . (2010) Receptor-like cytoplasmic kinases integrate signaling from multiple plant immune receptors and are targeted by a Pseudomonas syringae effector. Cell Host & Microbe 7(4), 290–301.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Zipfel C, Kunze G, Chinchilla D, Caniard A, Jones J, Boller T, Felix G (2006) Perception of the bacterial PAMP EF-Tu by the receptor EFR restricts Agrobacterium-mediated transformation. Cell 125, 749–760.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1