Skip to main content
SpringerLink
Log in

Effectors of Phytophthora pathogens are powerful weapons for manipulating host immunity

  • Review
  • Published:
Planta Aims and scope Submit manuscript

Abstract

Main conclusion

This article provides an overview of the interactions between Phytophthora effectors and plant immune system components, which form a cross-linked complex network that regulates plant pathogen resistance.

Abstract

Pathogens secrete numerous effector proteins into plants to promote infections. Several Phytophthora species (e.g., P. infestans, P. ramorum, P. sojae, P. capsici, P. cinnamomi, and P. parasitica) are notorious pathogens that are extremely damaging to susceptible plants. Analyses of genomic data revealed that Phytophthora species produce a large group of effector proteins, which are critical for pathogenesis. And, the targets and functions of many identified Phytophthora effectors have been investigated. Phytophthora effectors can affect various aspects of plant immune systems, including plant cell proteases, phytohormones, RNAs, the MAPK pathway, catalase, the ubiquitin proteasome pathway, the endoplasmic reticulum, NB-LRR proteins, and the cell membrane. Clarifying the effector–plant interactions is important for unravelling the functions of Phytophthora effectors during pathogenesis. In this article, we review the effectors identified in recent decades and provide an overview of the effector-directed regulatory network in plants following infections by Phytophthora species.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2

Similar content being viewed by others

References

  • Abramovitch RB, Janjusevic R, Stebbins CE, Martin GB (2006) Type III effector AvrPtoB requires intrinsic E3 ubiquitin ligase activity to suppress plant cell death and immunity. Proc Natl Acad Sci USA 103:2851–2856

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Armstrong MR, Whisson SC, Pritchard L, Bos JIB, Venter E, Avrova AO, Rehmany AP, Brooks K, Bohme U, Cherevach I, Hamlin N, White B, Fraser A, Lord A, Quail MA, Churcher C, Hall N, Berriman M, Huang S, Kamoun S, Beynon JL, Birch PRJ (2005) An ancestral oomycete locus contains late blight avirulence gene Avr3a, encoding a protein that is recognized in the host cytoplasm. Proc Natl Acad Sci USA 102:7766–7771

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Baulcombe D (2004) RNA silencing in plants. Nature 431:356–363

    Article  CAS  PubMed  Google Scholar 

  • Beakes GW, Glockling SL, Sekimoto S (2012) The evolutionary phylogeny of the oomycete “fungi”. Protoplasma 249:3–19

    Article  PubMed  Google Scholar 

  • Bertolotti A, Zhang Y, Hendershot LM, Harding HP, Ron D (2000) Dynamic interaction of BiP and ER stress transducers in the unfolded-protein response. Nat Cell Biol 2:326–332

    Article  CAS  PubMed  Google Scholar 

  • Boevink PC, Wang XD, McLellan H, He Q, Naqvi S, Armstrong MR, Zhang W, Hein I, Gilroy EM, Tian ZD, Birch PRJ (2016) A Phytophthora infestans RXLR effector targets plant PP1c isoforms that promote late blight disease. Nat Commun 7:10311

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Boller T, He SY (2009) Innate immunity in plants: an arms race between pattern recognition receptors in plants and effectors in microbial pathogens. Science 324:742–744

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bos JIB, Kanneganti TD, Young C, Cakir C, Huitema E, Win J, Armstrong MR, Birch PRJ, Kamoun S (2006) The C-terminal half of Phytophthora infestans RXLR effector AVR3a is sufficient to trigger R3a-mediated hypersensitivity and suppress INF1-induced cell death in Nicotiana benthamiana. Plant J 48:165–176

    Article  CAS  PubMed  Google Scholar 

  • Bos JIB, Armstrong MR, Gilroy EM, Boevink PC, Hein I, Taylor RM, Tian ZD, Engelhardt S, Vetukuri RR, Harrower B, Dixelius C, Bryan G, Sadanandom A, Whisson SC, Kamoun S, Birch PRJ (2010) Phytophthora infestans effector AVR3a is essential for virulence and manipulates plant immunity by stabilizing host E3 ligase CMPG1. Proc Natl Acad Sci USA 107:9909–9914

    Article  PubMed  PubMed Central  Google Scholar 

  • Bouwmeester K, de Sain M, Weide R, Gouget A, Klamer S, Canut H, Govers F (2011) The lectin receptor kinase LecRK-I.9 is a novel Phytophthora resistance component and a potential host target for a RXLR effector. PLoS Pathog 7:e1001327

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bozkurt TO, Schornack S, Win J, Shindo T, Ilyas M, Oliva R, Cano LM, Jones AME, Huitema E, Hoorn RALVD, Kamoun S (2011) Phytophthora infestans effector AVRblb2 prevents secretion of a plant immune protease at the haustorial interface. Proc Natl Acad Sci USA 108:20832–20837

    Article  PubMed  PubMed Central  Google Scholar 

  • Callis J (2014) The ubiquitination machinery of the ubiquitin system. Arabidopsis Book 12:e0174

    Article  PubMed  PubMed Central  Google Scholar 

  • Champouret N, Bouwmeester K, Rietman H, van der Lee T, Maliepaard C, Maliepaard C, Heupink A, van de Vondervoort PJ, Jacobsen E, Visser RG, van der Vossen EA, Govers F, Vleeshouwers VG (2009) Phytophthora infestans isolates lacking class I ipiO variants are virulent on Rpi-blb1 potato. Mol Plant Microbe Interact 22:1535–1545

    Article  CAS  PubMed  Google Scholar 

  • Chen ZX, Silva H, Klessig DF (1993) Active oxygen species in the induction of plant systemic acquired resistance by salicylic-acid. Science 262:1883–1886

    Article  CAS  PubMed  Google Scholar 

  • Chen Y, Liu ZY, Halterman DA (2012) Molecular determinants of resistance activation and suppression by Phytophthora infestans effector IPI-O. Plant Pathog 8:e1002595

    CAS  Google Scholar 

  • Cheng BP, Yu XL, Ma ZC, Dong SM, Dou DL, Wang YC, Zheng XB (2012) Phytophthora sojae effector Avh331 suppresses the plant defence response by disturbing the MAPK signalling pathway. Physiol Mol Plant Pathol 77:1–9

    Article  CAS  Google Scholar 

  • Chinchilla D, Bauer Z, Regenass M, Boller T, Felix G (2006) The Arabidopsis receptor kinase FLS2 binds flg22 and determines the specificity of flagellin perception. Plant Cell 18:465–476

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cole RA, Synek L, Zarsky V, Fowler JE (2005) SEC8, A subunit of the putative Arabidopsis exocyst complex, facilitates pollen germination and competitive pollen tube growth. Plant Physiol 138:2005–2018

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Couto D, Zipfel C (2016a) Regulation of pattern recognition receptor signalling in plants. Immunology 16:537–552

    CAS  PubMed  Google Scholar 

  • Couto D, Zipfel C (2016b) Regulation of pattern recognition receptor signalling in plants. Immunology 16:537–552

    CAS  PubMed  Google Scholar 

  • Dagdas YF, Belhaj K, Maqboo A, Chaparro-Garcia A, Pandey P, Petre B (2016) An effector of the Irish potato famine pathogen antagonizes a host autophagy cargo receptor. eLife 5:e10856

    Article  PubMed  PubMed Central  Google Scholar 

  • Dangl JL, Horvath DM, Staskawicz BJ (2013) Pivoting the plant immune system from dissection to deployment. Science 341:746–751

    Article  CAS  PubMed  Google Scholar 

  • Dodds PN, Rathjen JP (2010) Plant immunity: towards an integrated view of plant–pathogen interactions. Nat Rev Genet 11:539–548

    Article  CAS  PubMed  Google Scholar 

  • Dong X, Hong Z, Chatterjee J, Kim S, Verma DPS (2008) Expression of callose synthase genes and its connection with Npr1 signaling pathway during pathogen infection. Planta 229:87–98

    Article  CAS  PubMed  Google Scholar 

  • Dong SM, Yin WX, Kong GH, Yang XY, Qutob D, Chen QH, Kale SD, Sui YY, Zhang ZG, Dou DL, Zheng XB, Gijzen M, Tyler BM, Wang YC (2011) Phytophthora sojae avirulence effector Avr3b is a secreted NADH and ADP-ribose Pyrophosphorylase that modulates plant immunity. PLoS Pathog 7:e1002353

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dou D, Zhou JM (2012) Phytopathogen effectors subverting host immunity: different foes, similar battleground. Cell Host Microbe 12:484–495

    Article  CAS  PubMed  Google Scholar 

  • Du Y, Mpina MH, Birch PRJ, Bouwmeester K, Govers F (2015) Phytophthora infestans RXLR effector AVR1 interacts with exocyst component Sec5 to manipulate plant immunity. Plant Physiol 169:1975–1990

    CAS  PubMed  PubMed Central  Google Scholar 

  • Eitas TK, Dangl JL (2010) NB-LRR proteins: pairs, pieces, perception, partners, and pathways. Curr Opin Plant Biol 13:472–477

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Érsek T, Ribeiro OK (2010) An annotated list of new Phytophthora species described post 1996. Acta Phytopathol Hung 45:251–266

    Article  Google Scholar 

  • Evangelisti E, Govetto B, Minet-Kebdani N, Kuhn ML, Attard A, Ponchet M, Panabieres F, Gourgues M (2013) The Phytophthora parasitica RXLR effector penetration-specific effector 1 favours Arabidopsis thaliana infection by interfering with auxin physiology. New Phytol 199:476–489

    Article  CAS  PubMed  Google Scholar 

  • Fan GJ, Yang Y, Li TT, Lu WQ, Du Y, Qiang XY, Wen QJ, Shan WX (2018) A Phytophthora capsici RXLR effector targets and inhibits a plant PPIase to suppress endoplasmic reticulum-mediated immunity. Mol Plant 11:1067–1083

    Article  CAS  PubMed  Google Scholar 

  • Fawke S, Doumane M, Schornack S (2015) Oomycete interactions with plants: infection strategies and resistance principles. Microbiol Mol Biol Rev 79:263–280

    Article  PubMed  PubMed Central  Google Scholar 

  • Felix G, Duran JD, Volko S, Boller T (1999) Plants have a sensitive perception system for the most conserved domain of bacterial flagellin. Plant J 18:265–276

    Article  CAS  PubMed  Google Scholar 

  • Fellbrich G, Romanski A, Varet A, Blume B, Brunner F, Engelhardt S, Felix G, Kemmerling B, Krzymowska M, Nürnberger T (2002) NPP1, a Phytophthora-associated trigger of plant defense in parsley and Arabidopsis. Plant J 32:375–390

    Article  CAS  PubMed  Google Scholar 

  • Galan JE, Lara-Tejero M, Marlovits TC, Wagner S (2014) Bacterial type III secretion systems: specialized nanomachines for protein delivery into target cells. Annu Rev Microbiol 68:415–438

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gaulin E, Dramé N, Lafitte C, Torto-Alalibo T, Martinez Y, Torregrosa C (2006) Cellulose binding domains of a Phytophthora cell wall protein are novel pathogen-associated molecular patterns. Plant Cell 18:1766–1777

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gouget A, Senchou V, Govers F, Sanson A, Barre A, Rouge′ P, Pont-Lezica R, Canut H (2006) Lectin receptor kinases participate in protein-protein interactions to mediate plasma membrane-cell wall adhesions in Arabidopsis. Plant Physiol 140:81–90

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Grünwald NJ, Goss EM, Press CM (2008) Phytophthora ramorum: a pathogen with a remarkably wide host-range causing sudden oak death on oaks and ramorum blight on woody ornamentals. Mol Plant Pathol 9:729–740

    Article  PubMed  PubMed Central  Google Scholar 

  • Haas BJ, Kamoun S, Zody MC, Jiang RHY, Handsaker RE, Cano LM, Grabherr M et al (2009) Genome sequence and analysis of the Irish potato famine pathogen Phytophthora infestans. Nature 461:393–398

    Article  CAS  PubMed  Google Scholar 

  • Habib H, Majid K (2007) Plant protease inhibitors: a defense strategy in plants. Biotechnol Mol Biol Rev 2:068–085

    Google Scholar 

  • Hála M, Cole R, Synek L, Drdová E, Pecenková T, Nordheim A, Lamkemeyer T, Madlung J, Hochholdinger F, Fowler JE, Zársky V (2008) An exocyst complex functions in plant cell growth in Arabidopsis and tobacco. Plant Cell 20:1330–1345

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hausbeck MK, Lamour KH (2004) Phytophthora capsici on vegetable crops: research progress and management challenges. Plant Dis 88:1292–1303

    Article  PubMed  Google Scholar 

  • He CC, Bartholomew CR, Zhou WB, Klionsky DJ (2009) Assaying autophagic activity in transgenic GFP-Lc3 and GFP-Gabarap zebrafish embryos. Autophagy 5:520–526

    Article  CAS  PubMed  Google Scholar 

  • 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. Proc Natl Acad Sci USA 104:12217–12222

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hetz C (2012) The unfolded protein response: controlling cell fate decisions under ER stress and beyond. Nat Rev Mol Cell Biol 13:89–102

    Article  CAS  PubMed  Google Scholar 

  • Huang J, Yang M, Lu L, Zhang X (2016) Diverse functions of small RNAs in different plant-pathogen communications. Front Microbiol. https://doi.org/10.3389/fmicb.2016.01552

    Article  PubMed  PubMed Central  Google Scholar 

  • Huang J, Gu LF, Zhang Y, Yan TX, Kong GH, Kong L, Guo BD, Qiu M, Wang Y, Jing MF, Xing WM, Ye WW, Wu Z, Zhang ZG, Zheng XB, Gijzen M, Wang YC, Dong SM (2017) An oomycete plant pathogen reprograms host pre-mRNA splicing to subvert immunity. Nat Commun 8:2051

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jiang RH, Tripathy S, Govers F, Tyler BM (2008) RXLR effector reservoir in two Phytophthora species is dominated by a single rapidly evolving super family with more than 700 members. Proc Natl Acad Sci USA 105:4874–4879

    Article  PubMed  PubMed Central  Google Scholar 

  • Jing MF, Guo BD, Li HY, Yang B, Wang HN, Kong GH, Zhao Y, Xu HW, Wang Y, Ye WW, Dong SM, Qiao YL, Tyler BM, Ma WB, Wang YC (2016) A Phytophthora sojae effector suppresses endoplasmic reticulum stress-mediated immunity by stabilizing plant binding immunoglobulin Proteins. Nat Commun 7:11685

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Jones JDG, Dangl JL (2006) The plant immune system. Nature 444:323–329

    Article  CAS  PubMed  Google Scholar 

  • Jorda L, Coego A, Conejero V, Vera PA (1999) Genomic cluster containing four differentially regulated subtilisin-like processing protease genes is in tomato plants. J Biol Chem 274:2360–2365

    Article  CAS  PubMed  Google Scholar 

  • Jwa NS, Hwang BK (2017) Convergent evolution of pathogen effectors toward reactive oxygen species signaling networks in plants. Front Plant Sci 8:01687

    Article  Google Scholar 

  • Kamoun S, van West P, de Jong AJ, de Groot KE, Vleeshouwers VG, Govers F (1997) A gene encoding a protein elicitor of Phytophthora infestans is down-regulated during infection of potato. Mol Plant Microbe Interact 10:13–20

    Article  CAS  PubMed  Google Scholar 

  • Kamoun S, van West P, Vleeshouwers VG, de Groot KE, Govers F (1998) Resistance of Nicotiana benthamiana to Phytophthora infestans is mediated by the recognition of the elicitor protein INF1. Plant Cell 10:1413–1426

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kaschani F, Van Der Hoorn RAL (2011) A model of the C14-EPIC complex indicates hot spots for a protease-inhibitor arms race in the oomycete-potato interaction. Plant Signal Behav 6:1109–1112

    Article  CAS  Google Scholar 

  • Kaschani F, Shabab M, Bozkurt T, Shindo T, Schornack S, Gu C, Hoorn RALVD (2010) An effector-targeted protease contributes to defense against Phytophthora infestans and is under diversifying selection in natural hosts. Plant Physiol 154:1794–1804

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kim I, Xu W, Reed JC (2008) Cell death and endoplasmic reticulum stress: disease relevance and therapeutic opportunities. Nat Rev Drug Discov 7:1013–1030

    Article  CAS  PubMed  Google Scholar 

  • King SRF, McLellan H, Boevink PC, Armstrong MR, Bukharova T, Sukarta O, Win J, Kamoun S, Birch PRJ, Banfield MJ (2014) Phytophthora infestans RXLR Effector PexRD2 interacts with host MAPKKKe to suppress plant immune signaling. Plant Cell 26:1345–1359

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kruger J, Thomas CM, Golstein C, Dixon MS, Smoker M, Tang SJ, Mulder L, Jones JDG (2002) A tomato cysteine protease required for Cf-2-Dependent disease resistance and suppression of autonecrosis. Science 296:744–747

    Article  PubMed  Google Scholar 

  • Lamour KH, Mudge J, Gobena D, Hurtado-Gonzales OP, Schmutz J, Kuo A, Miller NA, Rice BJ, Raffaele S, Cano LM, Bharti AK, Donahoo RS, Finley S, Huitema E, Hulvey J, Platt D, Salamov A, Savidor A, Sharma R, Stam R, Storey D, Thines M, Win J, Haas BJ, Dinwiddie DL, Jenkins J, Knight JR, Affourtit JP, Han CS, Chertkov O, Lindquist EA, Detter C, Grigoriev IV, Kamoun S, Kingsmore SF (2012) Genome sequencing and mapping reveal loss of heterozygosity as a mechanism for rapid adaptation in the vegetable pathogen Phytophthora capsici. MPMI 25:1350–1360

    Article  CAS  PubMed  Google Scholar 

  • Lee HA, Yeom SI (2015) Plant NB-LRR proteins: tightly regulated sensors in a complex manner. Brief Funct Genom 14:233–242

    Article  CAS  Google Scholar 

  • Li Y, Chen L, Mu J, Zuo J (2013) Lesion simulating disease1 interacts with catalases to regulate hypersensitive cell death in Arabidopsis. Plant Physiol 163:1059–1070

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li Q, Zhang MX, Shen DY, Liu TL, Chen YY, Zhou JM, Dou DL (2016) A Phytophthora sojae effector PsCRN63 forms homo-/hetero-dimers to suppress plant immunity via an inverted association manner. Sci Rep 6:26951

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Liu TL, Ye WW, Ru YY, Yang XY, Gu B, Tao K, Lu S, Dong SM, Zheng XB, ShanWX Wang YC, Dou DL (2011) Two host cytoplasmic effectors are required for pathogenesis of Phytophthora sojae by suppression of host defenses. Plant Physiol 155:490–501

    Article  CAS  PubMed  Google Scholar 

  • Liu TL, Song TQ, Zhang X, Yuan HB, Su LM, Li WL, Xu J, Liu SH, Chen LL, Chen TZ, Zhang MX, Gu LC, Zhang BL, Dou DL (2014) Unconventionally secreted effectors of two filamentous pathogens target plant salicylate biosynthesis. Nat Commun 5:4686

    Article  CAS  PubMed  Google Scholar 

  • Liu H, Ma X, Yu HQ, Fang DH, Li YP, Wang X, Wang W, Dong Y, Xiao BG (2016) Genomes and virulence difference between two physiological races of Phytophthora nicotianae. GigaScience 5:3. https://doi.org/10.1186/s13742-016-0108-7

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Luna E, Pastor V, Robert J, Flors V, Mauch-Mani B, Ton J (2011) Callose deposition: a multifaceted plant defense response. MPMI 24:183–193

    Article  CAS  PubMed  Google Scholar 

  • Ma Z, Zhu L, Song T, Wang Y, Zhang Q, Xia Y, Qiu M, Lin Y, Li H, Kong L, Fang Y, Ye W, Wang Y, Dong S, Zheng X, Tyler BM, Wang Y (2017) A paralogous decoy protects Phytophthora sojae apoplastic effector PsXEG1 from a host inhibitor. Science 355:710–714

    Article  CAS  PubMed  Google Scholar 

  • Mafurah JJ, Ma HF, Zhang MX, Xu J, He F, Ye T, Shen DY, Chen YY, Rajput NA, Dou DL, Eugenin EA (2015) A virulence essential CRN effector of Phytophthora capsici suppresses host defense and induces cell death in plant nucleus. PLOS ONE 10:e0127965

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • McLellan H, Boevink PC, Armstrong MR, Pritchard L, Gomez S, Morales J, Whisson SC, Beynon JL, Birch PRJ (2013) An RxLR effector from Phytophthora infestans prevents re-localisation of two plant NAC transcription factors from the endoplasmic reticulum to the nucleus. PLoS Pathog 9:e1003670

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Melech-Bonfil S, Sessa G (2010) Tomato MAPKKKe is a positive regulator of cell-death signaling networks associated with plant immunity. Plant J 64:379–391

    Article  CAS  PubMed  Google Scholar 

  • Mellersh DG, Heath MC (2001) Plasma membrane-cell wall adhesion is required for expression of plant defense responses during fungal penetration. Plant Cell 13:413–424

    CAS  PubMed  PubMed Central  Google Scholar 

  • Meng X, Zhang S (2013) MAPK cascades in plant disease resistance signaling. Annu Rev Phytopathol 51:245–266

    Article  CAS  PubMed  Google Scholar 

  • Meng YL, Zhang Q, Ding W, Shan WX (2014) Phytophthora parasitica: a model oomycete plant pathogen. Mycology 5:43–51

    Article  CAS  PubMed  Google Scholar 

  • Moreno AA, Mukhtar MS, Blanco F, Boatwright JL, Moreno I, Jordan MR, Chen YN, Brandizzi F, Dong XN, Orellana A, Pajerowska-Mukhtar KM (2012) IRE1/bZIP60-mediated unfolded protein response plays distinct roles in plant immunity and abiotic stress responses. PLoS One. https://doi.org/10.1371/journal.pone.0031944

    Article  PubMed  PubMed Central  Google Scholar 

  • Mosolov VV, Valueva TA (2005) Proteinase inhibitors and their function in plants: a review. Appl Biochem Microbiol 4:227–246

    Article  CAS  Google Scholar 

  • Mukhtar MS, Carvunis AR, Dreze M, Epple P, Steinbrenner J, Moore J, Tasan M, Galli M, Hao T, Nishimura MT, Pevzner SJ, Donovan SE, Ghamsari L, Santhanam B, Romero V, Poulin MM, Gebreab F, Gutierrez BJ, Tam S, Monachello D, Boxem M, Harbort CJ, McDonald N, Gai L, Chen H, He Y, Vandenhaute J, Roth FP, Hill DE, Ecker JR, Vidal M, Beynon J, Braun P, Dangl JL (2011) Independently evolved virulence effectors converge ontohubs in a plant immune system network. Science 333:596–601

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nekrasov V, Li J, Batoux M, Roux M, Chu ZH, Lacombe S, Rougon A, Bittel P, Kiss-Papp M, Chinchilla D, van Esse HP, Jorda L, Schwessinger B, Nicaise V, Thomma BPHJ, Molina A, Jones JDG, Zipfel C (2009) Control of the pattern-recognition receptor EFR by an ER protein complex in plant immunity. EMBO J 28:3428–3438

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Nishimura MT, Stein M, Hou BH, Vogel JP, Edwards H, Somerville SC (2003) Loss of a callose synthase results in salicylic acid-dependent disease resistance. Science 301:969–972

    Article  CAS  PubMed  Google Scholar 

  • Panstruga R, Dodds PN (2009) Terrific protein traffic: the mystery of effector protein delivery by filamentous plant pathogens. Science 324:748–750

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Petrov VD, Van Breusegem F (2012) Hydrogen peroxide: a central hub for information flow in plant cells. AoB Plants 1:pls14

    Google Scholar 

  • Pieterse CM, Van der Does D, Zamioudis C, Leon-Reyes A, Van Wees SC (2012) Hormonal modulation of plant immunity. Annu Rev Cell Dev Biol 28:489–521

    Article  CAS  PubMed  Google Scholar 

  • Pitzschke A, Schikora A, Hirt H (2009) MAPK cascade signalling networks in plant defence. Curr Opin Plant Biol 12:421–426

    Article  CAS  PubMed  Google Scholar 

  • Qiang XY, Zechmann B, Reitz MU, Kogel KH, Schafer P (2012) The mutualistic fungus piriformospora indica colonizes Arabidopsis roots by inducing an endoplasmic reticulum stress-triggered caspase-dependent cell death. Plant Cell 24:794–809

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Qiao YL, Lui L, Xiong Q, Flores C, Wong J, Shi JX, Wang XB, Liu XG, Xiang QJ, Jiang SS, Zhang FC, Wang YC, Judelson HS, Chen XM, Ma WB (2013) Oomycete pathogens encode RNA silencing suppressors. Nat Genet 45:330–333

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Qiao Y, Shi J, Zhai Y, Hou Y, Ma W (2015) Phytophthora effector targets a novel component of small RNA pathway in plants to promote infection. Proc Natl Acad Sci 112:5850–5855

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Qutob D, Kemmerling B, Brunner F, Küfner I, Engelhardt S, Gust AA, Luberacki B, Seitz HU, Stahl D, Rauhut T, Glawischnig E, Schween G, Lacombe B, Watanabe N, Lam E, Schlichting R, Scheel D, Nau K, Dodt G, Hubert D, Gijzen M, Nürnberger T (2006) Phytotoxicity and innate immune responses induced by Nep1-like proteins. Plant Cell 18:3721–3744

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rajput NA, Zhang M, Ru Y, Liu T, Xu J, Liu L, Mafurah JJ, Dou D (2014) Phytophthora sojae effector PsCRN70 suppresses plant defenses in Nicotiana benthamiana. PLoS One 9:e98114

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Robert-Seilaniantz A, Grant M, Jones JDG (2011) Hormone crosstalk in plant disease and defense: more than just JASMONATE-SALICYLATE antagonism. Annu Rev Phytopathol 49:317–343

    Article  CAS  PubMed  Google Scholar 

  • Rodriguez MC, Petersen M, Mundy J (2010) Mitogenactivated protein kinase signaling in plants. Annu Rev Plant Biol 61:621–649

    Article  CAS  PubMed  Google Scholar 

  • Rose JKC, Ham KS, Darvill AG, Albersheim P (2002) Molecular cloning and characterization of glucanase inhibitor proteins: coevolution of a counterdefense mechanism by plant pathogens. Plant Cell 14:1–17

    Article  CAS  Google Scholar 

  • Rosebrock TR, Zeng LR, Brady JJ, Abramovitch RB, Xiao FM, Martin GB (2007) A bacterial E3 ubiquitin ligase targets a host protein kinase to disrupt plant immunity. Nature 448:370–374

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Saijo Y (2010) ER quality control of immune receptors and regulators in plants. Cell Microbiol 12:716–724

    Article  CAS  PubMed  Google Scholar 

  • Sarkies P, Miska EA (2014) Small RNAs break out: the molecular cell biology of mobile small RNAs. Nat Rev Mol Cell Biol 15:525–535

    Article  CAS  PubMed  Google Scholar 

  • Saunders DGO, Breen S, Win J, Schornack S, Hein I, Bozkurt TO, Champouret N, Vleeshouwers VGAA, Birch PRJ, Gilroy EM, Kamoun S (2012) Host protein BSL1 associates with Phytophthora infestans RXLR effector AVR2 and the solanum demissum immune receptor R2 to mediate disease resistance. Plant Cell 24:3420–3434

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Senchou V, Weide R, Carrascoa A, Bouyssoua H, Pont-Lezicaa R, Govers F, Canut H (2004) High affinity recognition of a Phytophthora protein by Arabidopsis via an RGD motif. Cell Mol Life Sci 61:502–509

    Article  CAS  PubMed  Google Scholar 

  • Sharpee WC, Dean RA (2016) Form and function of fungal and oomycete effectors. Fungal Biol Rev 30:62–73

    Article  Google Scholar 

  • Singer AU, Schulze S, Skarina T, Xu X, Cui H, Eschen-Lippold L, Egler M, Srikumar T, Raught B, Lee J, Scheel D, Savchenko A, Bonas U (2013) A pathogen type III effector with a novel E3 ubiquitin ligase architecture. PLoS Pathog 9:e1003121

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Song J, Win J, Tian M, Schornack S, Kaschani F, Muhammad I, Song J, Win J, Tian MY, Schornack S, Kaschani F, Ilyas M, van der Hoorn RAL, Kamoun S (2009) Apoplastic effectors secreted by two unrelated eukaryotic plant pathogens target the tomato defense protease Rcr3. Proc Natl Acad Sci USA 106:1654–1659

    Article  PubMed  PubMed Central  Google Scholar 

  • Song TQ, Ma ZC, Shen DY, Li Q, Li WL, Su LM, Ye TY, Zhang MX, Wang YC, Dou DL (2015) An oomycete CRN effector reprograms expression of plant HSP genes by targeting their promoters. PLOS Pathog 11:e1005348

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Taguchi F, Shimizu R, Inagaki Y, Toyoda K, Shiraishi T, Ichinose Y (2003) Posttranslational modification of flagellin determines the specificity of HR induction. Plant Cell Physiol 44:342–349

    Article  CAS  PubMed  Google Scholar 

  • Thaler JS, Humphrey PT, Whiteman NK (2012) Evolution of jasmonate and salicylate signal crosstalk. Trends Plant Sci 17:260–270

    Article  CAS  PubMed  Google Scholar 

  • Thines M, Lebeda A, Burdon JJ, Thrall P, Jege MJ (2014) Phylogeny and evolution of plant pathogenic oomycetes-a global overview. Eur J Plant Pathol 138:431–447

    Article  Google Scholar 

  • Tian M, Huitema E, Da Cunha L, Torto-Alalibo T, Kamoun S (2004) A Kazal-like extracellular serine protease inhibitor from Phytophthora infestans targets the tomato pathogenesis-related protease P69B. J Biol Chem 279:26370–26377

    Article  CAS  PubMed  Google Scholar 

  • Tian M, Benedetti B, Kamoun S (2005) A Second Kazal-like protease inhibitor from Phytophthora infestans inhibits and interacts with the apoplastic pathogenesis-related protease P69B of tomato. Plant Physiol 138:1785–1793

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tian M, Win J, Song J, van der Hoorn R, van der Knaap E, Kamoun S (2007) A Phytophthora infestans cystatin-like protein targets a novel tomato papain-like apoplastic protease. Plant Physiol 143:364–377

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tornero P, Conejero V, Vera P (1997) Identification of a new pathogen-induced member of the subtilisin-like processing protease family from plants. J Biol Chem 272:14412–14419

    Article  CAS  PubMed  Google Scholar 

  • Tyler BM (2007) Phytophthora sojae: root rot pathogen of soybean and model oomycete. Mol Plant Pathol 8:1–8

    Article  CAS  PubMed  Google Scholar 

  • Tyler BM, Tripathy S, Zhang XM, Dehal P, Jiang RHY, Aerts A, Arredondo FD, Baxter L, Bensasson D, Beynon JL, Chapman J, Damasceno CMB, Dorrance AE, Dou DL, Dickerman AW, Dubchak IL, Garbelotto M, Gijzen M, Gordon SG, Govers F, Grunwald NJ, Huang W, Ivors KL, Jones RW, Kamoun S, Krampis K, Lamour Lee MK, McDonald WH, Medina M, Nordberg EK, Maclean DJ, Ospina-Giraldo MD, Morris PF, Phuntumart V, Putnam NH, Rash S, Rose JKC, Sakihama Y, Salamov AA, Savidor A, Scheuring CF, Smith BM, Sobral BWS, Terry A, Torto-Alalibo TA, Win J, Xu ZY, Zhang HB, Grigoriev IV, Rokhsar DS, Boore JL (2006) Phytophthora genome sequences uncover evolutionary origins and mechanisms of pathogenesis. Science 313:1261–1266

    Article  CAS  PubMed  Google Scholar 

  • van Damme M, Bozkurt TO, Cakir C, Schornack S, Sklenar J, Jones AME, Kamoun S (2012) The Irish potato famine pathogen Phytophthora infestans translocates the CRN8 kinase into host plant cells. PLoS Pathog 8:e1002875

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Vance V, Vaucheret H (2001) RNA silencing in plants-defense and counter defense. Science 292:2277–2280

    Article  CAS  PubMed  Google Scholar 

  • Vetukuri RR, Whisson SC, Grenville-Briggs LJ (2017) Phytophthora infestans effector Pi14054 is a novel candidate suppressor of host silencing mechanisms. Eur J Plant Pathol 149:771–777

    Article  CAS  Google Scholar 

  • Voinnet O (2009) Origin, biogenesis, and activity of plant microRNAs. Cell 136:669–687

    Article  CAS  PubMed  Google Scholar 

  • Wang YJ, Li JF, Hou SG, Wang XW, Li YA, Ren DT, Chen S, Tang XY, Zhou JM (2010) A Pseudomonas syringae ADP-ribosyltransferase inhibits Arabidopsis mitogen-activated protein kinase kinases. Plant Cell 22:2033–2044

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang XD, Boevink P, McLellan H, Armstrong M, Bukharova T, Qin ZW, Birch PRJ (2015) A host KHRNA-binding protein is a susceptibility factor targeted by an RXLR effector to promote late blight disease. Mol Plant 8:1385–1395

    Article  CAS  PubMed  Google Scholar 

  • Wang SM, Boevink PC, Welsh L, Zhang RF, Whisson SC, Birch PRJ (2017) Delivery of cytoplasmic and apoplastic effectors from Phytophthora infestans haustoria by distinct secretion pathways. New Phytol 216:205–215

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang SM, Welsh L, Thorpe P, Whisson SC, Boevinkb PC, Birch PRJ (2018) The Phytophthora infestans haustorium is a site for secretion of diverse classes of infection-associated proteins. mBio. https://doi.org/10.1128/mBio.01216-18

    Article  PubMed  PubMed Central  Google Scholar 

  • Wang SM, McLellan H, Bukharova T, He Q, Murphy F, Shi JY, Sun SH, van Weymers P, Ren YJ, Thilliez G, Wang HX, Chen XW, Engelhardt S, Vleeshouwers V, Gilroy EM, Whisson SC, Hein I, Wang XD, Tian ZD, Birch PRJ, Boevink PC (2019) Phytophthora infestans RXLR effectors act in concert at diverse subcellular locations to enhance host colonization. J Exp Bot 70:343–356

    Article  PubMed  Google Scholar 

  • Whisson SC, Boevink PC, Moleleki L, Avrova AO, Morales JG, Gilroy EM, Armstrong MR, Grouffaud S, van West P, Chapman S, Hein I, Toth IK, Pritchard L, Birch PRJ (2007) A translocation signal for delivery of oomycete effector proteins into host plant cells. Nature 450:115–118

    Article  CAS  PubMed  Google Scholar 

  • Whisson SC, Boevink PC, Wang SM, Birch PRJ (2016) The cell biology of late blight disease. Curr Opin Microbiol 34:127–135

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Win J, Kamoun S (2007) Adaptive evolution has targeted the C-terminal domain of the RXLR effectors of plant pathogenic oomycetes. Plant Cell 19:2349–2369

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Win J, Krasileva KV, Kamoun S, Shirasu K, Staskawicz BJ, Banfield MJ (2012) Sequence divergent RXLR effectors share a structural fold conserved across plant pathogenic oomycete species. PLoS Pathog 8:e1002400

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Xiong Q, Ye WW, Choi D, Wong J, Qiao YL, Tao K, Wang YC, Ma WB (2014) Phytophthora suppressor of RNA silencing 2 is a conserved RxLR effector that promotes infection in soybean and Arabidopsis thaliana. MPMI 27:1379–1389

    Article  CAS  PubMed  Google Scholar 

  • Yang ZT, Wang MJ, Sun L, Lu SJ, Bi DL, Sun L, Song ZT, Zhang SS, Zhou SF, Liu JX (2014a) The membrane-associated transcription factor NAC089 controls ER-stress-induced programmed cell death in plants. PLoS Genet 10:e1004243

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yang ZT, Lu SJ, Wang MJ, Bi DL, Sun L, Zhou SF, Song ZT, Liu JX (2014b) A plasma membrane-tethered transcription factor, NAC062/ANAC062/NTL6, mediates the unfolded protein response in Arabidopsis. Plant J 79:1033–1043

    Article  CAS  PubMed  Google Scholar 

  • Yang B, Wang QQ, Jing MF, Guo BD, Wu JW, Wang HN, Wang Y, Lin L, Wang Y, Ye W, Dong S, Wang Y (2017) Distinct regions of the Phytophthora essential effector Avh238 determine its function in cell death activation and plant immunity suppression. New Phytol 214:361–375

    Article  CAS  PubMed  Google Scholar 

  • Yoshioka H, Asai S, Yoshioka M, Kobayashi M (2009) Molecular mechanisms of generation for nitric oxide and reactive oxygen species, and role of the radical burst in plant immunity. Mol Cells 28:321e9

    Article  CAS  Google Scholar 

  • Yu XL, Tang JL, Wang QQ, Ye WW, Tao K, Duan SY, Lu CC, Yang XY, Dong SM, Zheng XB, Wang YC (2012) The RxLR effector Avh241 from Phytophthora sojae requires plasma membrane localization to induce plant cell death. New Phytol 196:247–260

    Article  CAS  PubMed  Google Scholar 

  • Zadoks JC (2008) The potato murrain on the European continent and the revolutions of 1848. Potato Res 51:5–45

    Article  Google Scholar 

  • Zhang J, Shao F, Li Y, Cui HT, Chen LJ, Li HT, Zou Y, Long CZ, Lan LF, Chai JJ, Chen S, Tang XY, Zhou JM (2007) A Pseudomonas syringae effector inactivates MAPKs to suppress PAMP-Induced immunity in plants. Cell Host Microbe 1:175–185

    Article  CAS  PubMed  Google Scholar 

  • Zhang MX, Li Q, Liu TL, Liu L, Shen DY, Zhu Y, Liu PH, Zhou JM, Dou DL (2015) Two cytoplasmic effectors of Phytophthora sojae regulate plant cell death via interactions with plant catalases. Plant Physiol 167:164–175

    Article  CAS  PubMed  Google Scholar 

  • Zhang W, Corwin JA, Copeland D, Feusier J, Eshbaugh R, Chen F, Atwell S, Kliebenstein DJ (2017) Plastic transcriptomes stabilize immunity to pathogen diversity: the jasmonic acid and salicylic acid networks within the Arabidopsis/Botrytis Pathosystem. Plant Cell 29:2727–2752

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zheng XZ, McLellan HZ, Fraiture MZ, Liu XY, Boevink PC, Gilroy EM, Chen Y, Kandel K, Sessa G, Birch PRJ, Brunner F (2014) Functionally redundant RXLR effectors from Phytophthora infestans act at different steps to suppress early flg22-triggered immunity. PLoS Pathog 10:e1004057

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Zhou BJ, Zeng LR (2017) Conventional and unconventional ubiquitination in plant immunity. Mol Plant Pathol 18:1313–1330

    Article  PubMed  PubMed Central  Google Scholar 

  • Zhu JK, Shi J, Singh U, Wyatt SE, Bressan RA, Hasegawa PM, Carpita NC (1993) Enrichment of vitronectin- and fibronectin-like proteins in NaCl adapted plant cells and evidence for their involvement in plasma membrane-cell wall adhesion. Plant J 3:637–646

    Article  CAS  PubMed  Google Scholar 

  • Zipfel C, Kunze G, Chinchilla D, Caniard A, Jones JD, Boller T, Felix G (2006) Perception of the bacterial PAMP EF-Tu by the receptor EFR restricts Agrobacterium mediated transformation. Cell 125:749–760

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

This work was supported by the Fundamental Research Funds for the Chinese Academy of Agricultural Sciences (Grant no. 1610232016018), the Agricultural Science and Technology Innovation Program of the Chinese Academy of Agricultural Sciences (Grant no. ASTIP-TRIC04), and the China National Tobacco Corp. Yunnan Science and Technology Project: Construction of Tobacco Genome Breeding Platform (Grant no. 2017YN05). We declare no conflict of interest.

Author information

Authors and Affiliations

  1. Key Laboratory of Tobacco Pest Monitoring, Controlling and Integrated Management, Tobacco Research Institute, Chinese Academy of Agricultural Sciences, No. 11 Forth Longitudinal Keyuan Rd, Laoshan District, Qingdao, 266101, People’s Republic of China

    Wenjing Wang

  2. Yunnan Academy of Tobacco Agricultural Sciences, Kunming, 650021, People’s Republic of China

    Fangchan Jiao

Authors
  1. Wenjing Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Fangchan Jiao
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Wenjing Wang.

Additional information

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Wang, W., Jiao, F. Effectors of Phytophthora pathogens are powerful weapons for manipulating host immunity. Planta 250, 413–425 (2019). https://doi.org/10.1007/s00425-019-03219-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00425-019-03219-x

Keywords

Search

Navigation