Free Standard AU & NZ Shipping For All Book Orders Over $80!
Register      Login
Functional Plant Biology Functional Plant Biology Society
Plant function and evolutionary biology
RESEARCH FRONT

The role of oomycete effectors in plant–pathogen interactions

Adrienne R. Hardham A C and David M. Cahill B
+ Author Affiliations
- Author Affiliations

A Plant Science Division, Research School of Biology, College of Medicine, Biology and Environment, The Australian National University, Canberra, ACT 2601, Australia.

B School of Life and Environmental Sciences, Deakin University, Geelong Campus at Waurn Ponds, Vic. 3217, Australia.

C Corresponding author. Email: adrienne.hardham@anu.edu.au

Functional Plant Biology 37(10) 919-925 https://doi.org/10.1071/FP10073
Submitted: 1 April 2010  Accepted: 4 June 2010   Published: 23 September 2010

Abstract

Plants constantly come into contact with a diverse range of microorganisms that are potential pathogens, and they have evolved multi-faceted physical and chemical strategies to inhibit pathogen ingress and establishment of disease. Microbes, however, have developed their own strategies to counteract plant defence responses. Recent research on plant–microbe interactions has revealed that an important part of the infection strategies of a diverse range of plant pathogens, including bacteria, fungi and oomycetes, is the production of effector proteins that are secreted by the pathogen and that promote successful infection by manipulating plant structure and metabolism, including interference in plant defence mechanisms. Pathogen effector proteins may function either in the extracellular spaces within plant tissues or within the plant cell cytoplasm. Extracellular effectors include cell wall degrading enzymes and inhibitors of plant enzymes that attack invading pathogens. Intracellular effectors move into the plant cell cytoplasm by as yet unknown mechanisms where, in incompatible interactions, they may be recognised by plant resistance proteins but where, in compatible interactions, they may suppress the plant’s immune response. This article presents a brief overview of our current understanding of the nature and function of effectors produced by oomycete plant pathogens.

Additional keywords: enzyme inhibitors, pathogens, Phytophthora, plant–microbe interactions, plant–pathogen interactions.


Acknowledgements

Support from the Australian Research Council during the preparation of this review is acknowledged by both authors.


References


Allen RL, Meitz JC, Baumber RE, Hall SA, Lee SC, Rose LE, Beynon JL (2008) Natural variation reveals key amino acids in a downy mildew effector that alters recognition specificity by an Arabidopsis resistance gene. Molecular Plant Pathology 9, 511–523.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Armstrong MR, Whisson SC, Pritchard L, Bos JIB, Venter E , et al . (2005) An ancestral oomycete locus contains late blight avirulence gene Avr3a, encoding a protein that is recognized in the host cytoplasm. Proceedings of the National Academy of Sciences of the United States of America 102, 7766–7771.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Baureithel K, Felix G, Boller T (1994) Specific, high affinity binding of chitin fragments to tomato cells and membranes. The Journal of Biological Chemistry 269, 17 931–17 938.
PubMed |
open url image1

Bhattacharjee S, Hiller NL, Liolios K, Win J, Kanneganti TD, Young C, Kamoun S, Haldar K (2006) The malarial host-targeting signal is conserved in the Irish potato famine pathogen. PLoS Pathogens 2, e50.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Birch PRJ, Boevink PC, Gilroy EM, Hein I, Pritchard L, Whisson SC (2008) Oomycete RXLR effectors: delivery, functional redundancy and durable disease resistance. Current Opinion in Plant Biology 11, 373–379.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Birch PRJ, Armstrong M, Bos J, Boevink P, Gilroy EM , et al . (2009) Towards understanding the virulence functions of RXLR effectors of the oomycete plant pathogen Phytophthora infestans. Journal of Experimental Botany 60, 1133–1140.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Bittner-Eddy PD, Allen RL, Rehmany AP, Birch P, Beynon JL (2003) Use of suppression subtractive hybridization to identify downy mildew genes expressed during infection of Arabidopsis thaliana. Molecular Plant Pathology 4, 501–507.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Boddey JA, Moritz RL, Simpson RJ, Cowman AF (2009) Role of the Plasmodium export element in trafficking parasite proteins to the infected erythrocyte. Traffic (Copenhagen, Denmark) 10, 285–299.
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

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.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

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. The Plant Journal 48, 165–176.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Boudjeko T, Andème-Onzighi C, Vicré M, Balangé A-P, Ndoumou DO, Driouich A (2006) Loss of pectin is an early event during infection of cocoyam roots by Pythium myriotylum. Planta 223, 271–282.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Boudsocq M, Willmann MR, McCormack M, Lee H, Shan L, He P, Bush J, Cheng S-H, Sheen J (2010) Differential innate immune signalling via Ca2+sensor protein kinases. Nature 464, 418–422.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Brunner F, Rosahl S, Lee J, Rudd JJ, Geiler C, Kauppinen S, Rasmussen G, Scheel D, Nürnberger T (2002) Pep-13, a plant defense-inducing pathogen-associated pattern from Phytophthora transglutaminases. The EMBO Journal 21, 6681–6688.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Catanzariti A-M, Jones DA (2010) Effector proteins of extracellular fungal plant pathogens that trigger host resistance. Functional Plant Biology 37, 901–906.
Crossref | GoogleScholarGoogle Scholar | open url image1

Chinnapun D, Tian M, Day B, Churngchow N (2009) Inhibition of a Hevea brasiliensis protease by a Kazal-like serine protease inhibitor from Phytophthora palmivora. Physiological and Molecular Plant Pathology 74, 27–33.
Crossref | GoogleScholarGoogle Scholar | open url image1

Costanzo S, Ospina-Giraldo MD, Deahl KL, Baker CJ, Jones RW (2006) Gene duplication event in family 12 glucosyl hydrolase from Phytophthora spp. Fungal Genetics and Biology 43, 707–714.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Côté F, Roberts KA, Hahn MG (2000) Identification of high-affinity binding sites for the hepta-β-glucoside elicitor in membranes of the model legumes Medicago truncatula and Lotus japonicus. Planta 211, 596–605.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

de Koning-Ward TF, Gilson PR, Boddey JA, Rug M, Smith BJ , et al . (2009) A newly discovered protein export machine in malaria parasites. Nature 459, 945–949.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Dou D, Kale SD, Wang X, Chen Y, Wang Q , et al . (2008a) Conserved C-terminal motifs required for avirulence and suppression of cell death by Phytophthora sojae effector Avr1b. The Plant Cell 20, 1118–1133.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Dou D, Kale SD, Wang X, Jiang RHY, Bruce NA, Arredondo FD, Zhang X, Tyler BM (2008b) RXLR-mediated entry of Phytophthora sojae effector Avr1b into soybean cells does not require pathogen-encoded machinery. The Plant Cell 20, 1930–1947.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Ellis J, Catanzariti A-M, Dodds J (2006) The problem of how fungal and oomycete avirulence proteins enter plant cells. Trends in Plant Science 11, 61–63.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

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. The Plant Journal 32, 375–390.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Feng B-Z, Li P, Wang H, Zhang X-G (2010) Functional analysis of Pcpme6 from oomycete plant pathogen Phytophthora capsici. Microbial Pathogenesis 49, 23–31.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Gaulin E, Dramé N, Lafitte C, Torto-Alalibo T, Martinez Y , et al . (2006) Cellulose binding domains of a Phytophthora cell wall protein are novel pathogen-associated molecular patterns. The Plant Cell 18, 1766–1777.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Götesson A, Marshall JS, Jones DA, Hardham AR (2002) Characterization and evolutionary analysis of a large polygalacturonase gene family in the oomycete plant pathogen Phytophthora cinnamomi. Molecular Plant – Microbe Interactions 15, 907–921.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Grant MR, Jones JDG (2009) Hormone dis(harmony) moulds plant health and disease. Science 324, 750–752.
Crossref | PubMed |
open url image1

Grouffaud S, Van West P, Avrova AO, Birch PRJ, Whisson SC (2008) Plasmodium falciparum and Hyaloperonospora parasitica effector translocation motifs are functional in Phytophthora infestans. Microbiology 154, 3743–3751.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Haas BJ, Kamoun S, Zody MC, Jiang RHY, Handsaker RE , et al . (2009) Genome sequence and analysis of the Irish potato famine pathogen Phytophthora infestans. Nature 461, 393–398.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Halim VA, Hunger A, Macioszek V, Landgraf P, Nürnberger T, Scheel D, Rosahl S (2004) The oligopeptide elicitor Pep-13 induces salicylic acid-dependent and -independent defense reactions in potato. Physiological and Molecular Plant Pathology 64, 311–318.
Crossref | GoogleScholarGoogle Scholar | open url image1

Halim VA, Altmann S, Ellinger D, Eschen-Lippold L, Miersch O, Scheel D, Rosahl S (2009) PAMP-induced defense responses in potato require both salicylic acid and jasmonic acid. The Plant Journal 57, 230–242.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Ham K-S, Wu S-C, Darvill AG, Albersheim P (1997) Fungal pathogens secrete an inhibitor protein that distinguishes isoforms of plant pathogenesis-related endo-β-1,3-glucanases. The Plant Journal 11, 169–179.
Crossref | GoogleScholarGoogle Scholar | open url image1

Hatsch D, Phalip V, Petkovski E, Jeltsch J-M (2006) Fusarium graminearum on plant cell wall: no fewer than 30 xylanase genes transcribed. Biochemical and Biophysical Research Communications 345, 959–966.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Hein I, Gilroy EM, Armstrong MR, Birch PRJ (2009) The zig-zag-zig in oomycete–plant interactions. Molecular Plant Pathology 10, 547–562.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Hogenhout SA, Van der Hoorn RAL, Terauchi R, Kamoun S (2009) Emerging concepts in effector biology of plant-associated organisms. Molecular Plant – Microbe Interactions 22, 115–122.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Hwang IS, Hwang BK (2010) The pepper 9-lipoxygenase gene CaLOX1 functions in defence and cell death responses to microbial pathogens. Plant Physiology 152, 948–967.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Jiang RHY, Tyler BM, Govers F (2006) Comparative analysis of Phytophthora genes encoding secreted proteins reveals conserved synteny and lineage-specific gene duplications and deletions. Molecular Plant-Microbe Interactions 19, 1311–1321.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Jiang RHY, Tripathy S, Govers F, Tyler BM (2008) RXLR effector reservoir in two Phytophthora species is dominated by a single rapidly evolving superfamily with more than 700 members. Proceedings of the National Academy of Sciences of the United States of America 105, 4874–4879.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

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

Kamoun S (2006) A catalogue of the effector secretome of plant pathogenic oomycetes. Annual Review of Phytopathology 44, 41–60.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Kelley BS, Lee S-J, Damasceno CMB, Chakravarthy S, Kim B-D, Martin GB, Rose JKC (2010) A secreted effector protein (SNE1) from Phytophthora infestans is a broadly acting suppresor of programmed cell death. The Plant Journal 62, 357–366.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Kidd BN, Edgar CI, Kumar KK, Aitken EA, Schenk PM, Manners JM, Kazan K (2009) The mediator complex subunit PFT1 is a key regulator of jasmonate-dependent defence in Arabidopsis. The Plant Cell 21, 2237–2252.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Lamour KH, Win J, Kamoun S (2007) Oomycete genomics: new insights and future directions. FEMS Microbiology Letters 274, 1–8.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Liu Z, Bos JIB, Armstrong M, Whisson SC, da Cunha L , et al . (2005) Patterns of diversifying selection in the phytotoxin-like scr74 gene family of Phytophthora infestans. Molecular Biology and Evolution 22, 659–672.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

McLeod A, Smart CD, Fry WE (2003) Characterization of 1,3-β-glucanase and 1,3;1,4-β-glucanase genes from Phytophthora infestans. Fungal Genetics and Biology 38, 250–263.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Meijer HJG, van de Vondervoort PJI, Yin QY, de Koster CG, Klis FM, Govers F, de Groot PWJ (2006) Identification of cell wall-associated proteins from Phytophthora ramorum. Molecular Plant – Microbe Interactions 19, 1348–1358.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Misas-Villamil JC, Van der Hoorn RAL (2008) Enzyme–inhibitor interactions at the plant–pathogen interface. Current Opinion in Plant Biology 11, 380–388.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Nicastro G, Orsomando G, Ferrari E, Manconi L, Desario F , et al . (2009) Solution structure of the phytotoxic protein PcF: the first characterized member of the Phytophthora PcF toxin family. Protein Science 18, 1786–1791.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Niture SK (2008) Comparative biochemical and structural characterizations of fungal polygalacturonases. Biologia 63, 1–19.
Crossref | GoogleScholarGoogle Scholar | open url image1

Oh CS, Pedley KF, Martin GB (2010) Tomato 14–3-3 protein 7 positively regulates immunity associated programmed cell death by enhancing protein abundance and signalling ability of MAPKKKα. The Plant Cell 22, 260–272.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Oliva R, Win J, Raffaele S, Boutemy L, Bozkurt TO , et al . (2010) Recent developments in effector biology of filamentous plant pathogens. Cellular Microbiology 12, 705–715.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Orsomando G, Lorenzi M, Raffaelli N, Rizza MD, Mezzetti B, Ruggieri S (2001) Phytotoxic protein PcF, purification, characterization, and cDNA sequencing of a novel hydroxyproline-containing factor secreted by the strawberry pathogen Phytophthora cactorum. The Journal of Biological Chemistry 276, 21 578–21 584.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Osman H, Mikes V, Milat M-L, Ponchet M, Marion D, Prangé T, Maume BF, Vauthrin S, Blein J-P (2001) Fatty acids bind to the fungal elicitor cryptogein and compete with sterols. FEBS Letters 489, 55–58.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Qutob D, Kamoun S, Gijzen M (2002) Expression of a Phytophthora sojae necrosis-inducing protein occurs during transition from biotrophy to necrotrophy. The Plant Journal 32, 361–373.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Rehmany AP, Gordon A, Rose LE, Allen RL, Armstrong MR, Whisson SC, Kamoun S, Tyler BM, Birch PRJ, Beynon JL (2005) Differential recognition of highly divergent downy mildew avirulence gene alleles by RPP1 resistance genes from two Arabidopsis lines. The Plant Cell 17, 1839–1850.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Rooney HCE, van ‘t Klooster JW, Van der Hoorn RAL, Joosten MHAJ, Jones JDG, de Witt PJGM (2005) Cladosporium Avr2 inhibits tomato Rcr3 protease required for Cf-2-dependent disease resistance. Science 308, 1783–1786.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Rose JKC, Ham K-S, Darvill AG, Albersheim P (2002) Molecular cloning and characterization of glucanase inhibitor proteins: coevolution of a counterdefence mechanism by plant pathogens. The Plant Cell 14, 1329–1345.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Schornack S, Huitema E, Cano LM, Bozkurt TO, Oliva R , et al . (2009) Ten things to know about oomycete effectors. Molecular Plant Pathology 10, 795–803.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Shang Y, Li X, Cui H, He P, Thilmony R, Chinamanani S, Zwiesler-Vollick J, Goplan S, Tang X, Zhou J-M (2006) RAR1, a central player in plant immunity, is targeted by Pseudomonas syringae effector AvrB. Proceedings of the National Academy of Sciences of the United States of America 103, 19 200–19 205.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Sohn KH, Lei R, Nemri A, Jones JDG (2007) The downy mildew effector proteins ATR1 and ATR13 promote disease susceptibility in Arabidopsis thaliana. The Plant Cell 19, 4077–4090.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

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. Proceedings of the National Academy of Sciences of the United States of America 106, 1654–1659.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Sun WX, Jia YJ, Feng BZ, O’Neill NR, Zhu XP, Xie BY, Zhang XG (2009) Functional analysis of Pcipg2 from the straminopilous plant pathogen Phytophthora capsici. Genesis 47, 535–544.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Tian M, Kamoun S (2005) A two disulfide bridge Kazal domain from Phytophthora exhibits stable inhibitory activity against serine proteases of the subtilisin family. BMC Biochemistry 6, 15.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

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. The Journal of Biological Chemistry 279, 26 370–26 377.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

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 Physiology 138, 1785–1793.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Tian MY, 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 Physiology 143, 364–377.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Tomassini A, Sella L, Raiola A, D’Ovidio R, Favaron F (2009) Characterization and expression of Fusarium graminearum endo-polygalacturonases in vitro and during wheat infection. Plant Pathology 58, 556–564.
Crossref | GoogleScholarGoogle Scholar | open url image1

Torto TA, Rauser L, Kamoun S (2002) The pipg1 gene of the oomycete Phytophthora infestans encodes a fungal-like endopolygalacturonase. Current Genetics 40, 385–390.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Torto TA, Li S, Styer A, Huitema E, Testa A, Gow NAR, Van West P, Kamoun S (2003) EST mining and functional expression assays identify extracellular effector proteins from the plant pathogen Phytophthora. Genome Research 13, 1675–1685.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Torto-Alalibo T, Tian M, Gajendran K, Waugh ME, Van West P, Kamoun S (2005) Expressed sequence tags from the oomycete fish pathogen Saprolegnia parasitica reveal putative virulence factors. BMC Microbiology 5, 46.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Tyler BM, Tripathy S, Zhang XM, Dehal P, Jiang RHY , et al . (2006) Phytophthora genome sequences uncover evolutionary origins and mechanisms of pathogenesis. Science 313, 1261–1266.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Veit S, Worle JM, Nürnberger T, Koch W, Seitz HU (2001) A novel protein elicitor (PaNie) from Pythium aphanidermatum induces multiple defense responses in carrot, Arabidopsis, and tobacco. Plant Physiology 127, 832–841.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Whisson SC, Boevink P, Moleleki L, Avrova AO, Morales JG , et al . (2007) A translocation signal for delivery of oomycete effector proteins into host plant cells. Nature 450, 115–118.
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, 2349–2354.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Win J, Morgan W, Bos J, Krasileva KV, Cano LM, Chaparro-Garcia A, Ammar R, Staskawicz BJ, Kamoun S (2007) Adaptive evolution has targeted the C-terminal domain of the RXLR effectors of plant pathogenic oomycetes. The Plant Cell 19, 2349–2369.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Wu C-H, Yan H-Y, Liou R-F (2008) Functional characterization of a gene family encoding polygalacturonase in Phytophthora parasitica. Molecular Plant-Microbe Interactions 21, 480–489.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Yan H-Z, Liou R-F (2005) Cloning and analysis of pppg1, an inducible endopolygalacturonase gene from the oomycete plant pathogen Phytophthora parasitica. Fungal Genetics and Biology 42, 339–350.
Crossref | PubMed |
open url image1

Yang H, Yang S, Hua J (2007) The Arabidopsis BAP1 and BAP2 genes are general inhibitors of programmed cell death. Plant Physiology 145, 135–146.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

York WS, Qin Q, Rose JKC (2004) Proteinaceous inhibitors of endo-β-glucanases. Biochimica et Biophysica Acta 1696, 223–233.
PubMed |
open url image1

Zipfel C (2009) Early molecular events in PAMP-triggered immunity. Current Opinion in Plant Biology 12, 414–420.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1

Zipfel C, Robatzek S, Navarro L, Oakeley EJ, Jones JDG, Felix G, Boller T (2004) Bacterial disease resistance in Arabidopsis through flagellin perception. Nature 428, 764–767.
Crossref | GoogleScholarGoogle Scholar | PubMed | open url image1