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La recherche sur les protéines effectrices a démarrées à partir du concept de Flor (1970) sur la relation gène pour gène. La grande majorité des travaux réalisés sur les effecteurs aujourd‟hui

concernent les effecteurs présents chez les microorganismes phytopathogènes, en lien avec

leur implication forte dans la virulence de ces microorganismes. Néanmoins, il existe

maintenant des microorganismes modèles non pathogènes étudiés pour leur capacité à utiliser

des protéines effectrices comme moyen de communication et stratégie d‟interaction. Outre les

champignons mycorhiziens L. bicolor et R. irregularis décrits dans le chapitre précédent, le

champignon Piriformospora indica, un champignon mutualiste endophyte de l‟ordre des

Sebacinales, possèdent lui aussi des protéines effectrices (Raffiqi et al, 2013 ; Akum et al,

2015) afin de promouvoir la symbiose mutualiste qu‟il met en place avec une très large

gamme d‟hôte (Qiang et al, 2012). Cette manipulation de l‟hôte végétal semble notamment

impacter les voies hormonales de régulation de l‟acide jasmonique et gibbérellique ainsi que

la voie de l‟auxine (Schaffer et al, 2009). Chez les champignons, seul L. bicolor et R.

irregularis sont rapporté comme utilisant des protéines effectrices ciblant respectivement les

voies de l‟acide jasmonique (Plett et al, 2014) et de l‟éthylène (Kloppholz et al, 2011). La

recherche sur les protéines effectrices ne se limite donc pas aux organismes pathogènes et

s‟intéresse aux mécanismes de translocation, à la localisation et aux fonctions des effecteurs,

en différenciant les effecteurs présents dans la zone apoplastique des effecteurs actifs dans le

cytoplasme. Il existe donc des similarités entre les microorganismes mutualistes et

phytopathogènes dans leur stratégie de colonisation de l‟hôte végétal. Il y a néanmoins un

manque de données concernant les effecteurs d‟organismes filamenteux, qu‟ils soient des

champignons ou des oomycètes, particulièrement ceux ayant un style de vie non pathogène.

Les recherches actuelles sur les champignons ectomycorhiziens étudient donc la diversité de

fonctions et de localisations d‟effecteurs candidats, dans le but d‟élucider les similitudes et

divergence existant entre les effecteurs de champignons mutualistes et les champignons

pathogènes.

Références

Akum, F. N., Steinbrenner, J., Biedenkopf, D., Imani, J., and Kogel, K.-H. 2015. The Piriformospora indica effector PIIN_08944 promotes the mutualistic Sebacinalean symbiosis. Front. Plant Sci. 6:1–12

Baptista, P., Martins, A., Pais, M. S., Tavares, R. M., & Lino-Neto, T. (2007). Involvement of reactive oxygen species during early stages of ectomycorrhiza establishment between Castanea sativa and Pisolithus tinctorius. Mycorrhiza, 17(3), 185–193. http://doi.org/10.1007/s00572-006-0091-4

Boch, J., and Bonas, U. 2010. Xanthomonas AvrBs3 family-type III effectors: discovery and function. Annu. Rev. Phytopathol. 48:419–36

Bogdanove, a. J., and Voytas, D. F. 2011. TAL Effectors: Customizable Proteins for DNA Targeting. Science (80). 333:1843–1846

Bozkurt, T. O., Schornack, S., Win, J., Shindo, T., Ilyas, M., Oliva, R., Cano, L. M., Jones, a. M. E., Huitema, E., van der Hoorn, R. a. L., and Kamoun, S. 2011. Phytophthora infestans effector AVRblb2 prevents secretion of a plant immune protease at the haustorial interface. Proc. Natl. Acad. Sci. 108:20832–20837 van den Burg, H. a, Harrison, S. J., Joosten, M. H. a J., Vervoort, J., and de Wit, P. J. G. M. 2006. Cladosporium

fulvum Avr4 protects fungal cell walls against hydrolysis by plant chitinases accumulating during infection. Mol. Plant. Microbe. Interact. 19:1420–1430

Caillaud, M. C., Piquerez, S. J. M., Fabro, G., Steinbrenner, J., Ishaque, N., Beynon, J., and Jones, J. D. G. 2012. Subcellular localization of the Hpa RxLR effector repertoire identifies a tonoplast-associated protein HaRxL17 that confers enhanced plant susceptibility. Plant J. 69:252–265

Caillaud, M.-C., Wirthmueller, L., Sklenar, J., Findlay, K., Piquerez, S. J. M., Jones, A. M. E., Robatzek, S., Jones, J. D. G., and Faulkner, C. 2014. The Plasmodesmal Protein PDLP1 Localises to

Haustoria-Associated Membranes during Downy Mildew Infection and Regulates Callose Deposition. PLoS Pathog. 10:e1004496

Cui, F., Wu, S., Sun, W., Coaker, G., Kunkel, B., He, P., and Shan, L. 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

Fesel, P. H., and Zuccaro, A. 2015. B-glucan: Crucial component of the fungal cell wall and elusive MAMP in plants. Fungal Genet. Biol.

Fester, T., & Hause, G. (2005). Accumulation of reactive oxygen species in arbuscular mycorrhizal roots.

Mycorrhiza, 15(5), 373–379. http://doi.org/10.1007/s00572-005-0363-4

Giraldo, M. C., and Valent, B. 2013. Filamentous plant pathogen effectors in action. Nat. Rev. Microbiol. 11:800–14

de Jonge, R., van Esse, H. P., Kombrink, A., Shinya, T., Desaki, Y., Bours, R., van der Krol, S., Shibuya, N., Joosten, M. H. a J., and Thomma, B. P. H. J. 2010. Conserved fungal LysM effector Ecp6 prevents chitin-triggered immunity in plants. Science. 329:953–955

Kale, S. D., Gu, B., Capelluto, D. G. S., Dou, D., Feldman, E., Rumore, A., Arredondo, F. D., Hanlon, R., Fudal, I., Rouxel, T., Lawrence, C. B., Shan, W., and Tyler, B. M. 2010. External Lipid PI3P Mediates Entry of Eukaryotic Pathogen Effectors into Plant and Animal Host Cells. Cell. 142:284–295

Kaschani, F., Shabab, M., Bozkurt, T., Shindo, T., Schornack, S., Gu, C., Ilyas, M., Win, J., Kamoun, S., and van der Hoorn, R. A. L. 2010. An effector-targeted protease contributes to defense against Phytophthora infestans and is under diversifying selection in natural hosts. Plant Physiol. 154:1794–804

Kay, S., Hahn, S., Marois, E., Hause, G., and Bonas, U. 2007. A bacterial effector acts as a plant transcription factor and induces a cell size regulator. Science. 318:648–651

Kazan, K., and Lyons, R. 2014. Intervention of Phytohormone Pathways by Pathogen Effectors. Plant Cell. 26:2285–2309

Khang, C. H., Berruyer, R., Giraldo, M. C., Kankanala, P., Park, S.-Y., Czymmek, K., Kang, S., and Valent, B. 2010. Translocation of Magnaporthe oryzae effectors into rice cells and their subsequent cell-to-cell movement. Plant Cell. 22:1388–1403

Kloppholz, S., Kuhn, H., and Requena, N. 2011. A Secreted Fungal Effector of Glomus intraradices Promotes Symbiotic Biotrophy. Curr. Biol. 21:1204–1209

Li, Y., Moore, R., Guinn, M., and Bleris, L. 2012. Transcription activator-like effector hybrids for conditional control and rewiring of chromosomal transgene expression. Sci. Rep. 2:897

Liu, W., Rudis, M. R., Peng, Y., Mazarei, M., Millwood, R. J., Yang, J. P., Xu, W., Chesnut, J. D., and Stewart, C. N. 2014. Synthetic TAL effectors for targeted enhancement of transgene expression in plants. Plant Biotechnol. J. 12:436–446

Malinovsky, F. G., Fangel, J. U., and Willats, W. G. T. 2014. The role of the cell wall in plant immunity. Front. Plant Sci. 5:178

Manning, V. A., Chu, A. L., Scofield, S. R., and Ciuffetti, L. M. 2010. Intracellular expression of a host-selective toxin, ToxA, in diverse plants phenocopies silencing of a ToxA-interacting protein, ToxABP1. New Phytol. 187:1034–1047

Marshall, R., Kombrink, A., Motteram, J., Loza-Reyes, E., Lucas, J., Hammond-Kosack, K. E., Thomma, B. P. H. J., and Rudd, J. J. 2011. Analysis of two in planta expressed LysM effector homologs from the fungus Mycosphaerella graminicola reveals novel functional properties and varying contributions to virulence on wheat. Plant Physiol. 156:756–69

McLellan, H., Boevink, P. C., Armstrong, M. R., Pritchard, L., Gomez, S., Morales, J., Whisson, S. C., Beynon, J. L., and Birch, P. R. J. 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 Mentlak, T. a., Kombrink, a., Shinya, T., Ryder, L. S., Otomo, I., Saitoh, H., Terauchi, R., Nishizawa, Y.,

Shibuya, N., Thomma, B. P. H. J., and Talbot, N. J. 2012. Effector-Mediated Suppression of Chitin-Triggered Immunity by Magnaporthe oryzae Is Necessary for Rice Blast Disease. Plant Cell. 24:322–335 Monaghan, J., and Zipfel, C. 2012. Plant pattern recognition receptor complexes at the plasma membrane. Curr.

Opin. Plant Biol. 15:349–357

El Oirdi, M., El Rahman, T. A., Rigano, L., El Hadrami, A., Rodriguez, M. C., Daayf, F., Vojnov, A., and Bouarab, K. 2011. Botrytis cinerea manipulates the antagonistic effects between immune pathways to promote disease development in tomato. Plant Cell. 23:2405–2421

Petre, B., and Kamoun, S. 2014. How Do Filamentous Pathogens Deliver Effector Proteins into Plant Cells? J.M. McDowell, ed. PLoS Biol. 12:e1001801

Petre, B., Lorrain, C., Saunders, D. G. O., Win, J., Sklenar, J., Duplessis, S., and Kamoun, S. 2015a. Rust fungal effectors mimic host transit peptides to translocate into chloroplasts. Cell. Microbiol.

Petre, B., Saunders, D. G. O., and Sklenar, J. 2015b. Candidate Effector Proteins of the Rust Pathogen Melampsora larici-populina Target Diverse Plant Cell Compartments. Mol. Plant-Microbe Interact. 28:689–700

Plett, J. M., Daguerre, Y., Wittulsky, S., Vayssières, A., Deveau, A., Melton, S. J., Kohler, A., Morrell-Falvey, J. L., Brun, A., Veneault-Fourrey, C., and Martin, F. 2014. Effector MiSSP7 of the mutualistic fungus Laccaria bicolor stabilizes the Populus JAZ6 protein and represses jasmonic acid (JA) responsive genes. Proc. Natl. Acad. Sci. U. S. A. 111:8299–304

Plett, J. M., Kemppainen, M., Kale, S. D., Kohler, A., Legu??, V., Brun, A., Tyler, B. M., Pardo, A. G., and Martin, F. 2011. A secreted effector protein of laccaria bicolor is required for symbiosis development. Curr. Biol. 21:1197–1203

Qiang, X., Weiss, M., Kogel, K. H., and Schäfer, P. 2012. Piriformospora indica-a mutualistic basidiomycete with an exceptionally large plant host range. Mol. Plant Pathol. 13:508–518

Qiao, Y., Shi, J., Zhai, Y., Hou, Y., and Ma, W. 2015. Phytophthora effector targets a novel component of small RNA pathway in plants to promote infection. Proc. Natl. Acad. Sci. U. S. A. 112:5850–5

Rafiqi, M., Jelonek, L., Akum, N. F., Zhang, F., and Kogel, K.-H. 2013. Effector candidates in the secretome of Piriformospora indica, a ubiquitous plant-associated fungus. Front. Plant Sci. 4:1–5

Ramirez-Garcés, D., Camborde, L., Pel, M. J. C., Jauneau, A., Martinez, Y., Néant, I., Leclerc, C., Moreau, M., Dumas, B., and Gaulin, E. 2015. CRN13 candidate effectors from plant and animal eukaryotic pathogens are DNA-binding proteins which trigger host DNA damage response. New Phytol.

Rivas, S., and Genin, S. 2011. A Plethora of Virulence Strategies Hidden Behind Nuclear Targeting of Microbial Effectors. Front. Plant Sci. 2:1–20

Rivas-San Vicente, M., and Plasencia, J. 2011a. Salicylic acid beyond defence: Its role in plant growth and development. J. Exp. Bot. 62:3321–3338

Rivas-San Vicente, M., and Plasencia, J. 2011b. Salicylic acid beyond defence: Its role in plant growth and development. J. Exp. Bot. 62:3321–3338

Rovenich, H., Boshoven, J. C., and Thomma, B. P. H. J. 2014. Filamentous pathogen effector functions: Of pathogens, hosts and microbiomes. Curr. Opin. Plant Biol. 20:96–103

Sánchez-Vallet, A., Saleem-Batcha, R., Kombrink, A., Hansen, G., Valkenburg, D. J., Thomma, B. P. H. J., and Mesters, J. R. 2013. Fungal effector Ecp6 outcompetes host immune receptor for chitin binding through intrachain LysM dimerization. Elife. 2013

Schäfer, P., Pfiffi, S., Voll, L. M., Zajic, D., Chandler, P. M., Waller, F., Scholz, U., Pons-Kühnemann, J., Sonnewald, S., Sonnewald, U., and Kogel, K.-H. 2009. Phytohormones in plant root-Piriformospora indica mutualism. Plant Signal. Behav. 4:669–71

Schornack, S., van Damme, M., Bozkurt, T. O., Cano, L. M., Smoker, M., Thines, M., Gaulin, E., Kamoun, S., and Huitema, E. 2010. Ancient class of translocated oomycete effectors targets the host nucleus. Proc. Natl. Acad. Sci. U. S. A. 107:17421–17426

Shimizu, T., Nakano, T., Takamizawa, D., Desaki, Y., Ishii-Minami, N., Nishizawa, Y., Minami, E., Okada, K., Yamane, H., Kaku, H., and Shibuya, N. 2010. Two LysM receptor molecules, CEBiP and OsCERK1, cooperatively regulate chitin elicitor signaling in rice. Plant J. 64:204–214

Shinya, T., Motoyama, N., Ikeda, A., Wada, M., Kamiya, K., Hayafune, M., Kaku, H., and Shibuya, N. 2012. Functional characterization of CEBiP and CERK1 homologs in arabidopsis and rice reveals the presence of different chitin receptor systems in plants. Plant Cell Physiol. 53:1696–1706

Song, J., Win, J., Tian, M., Schornack, S., Kaschani, F., Ilyas, M., van der Hoorn, R. a L., and Kamoun, S. 2009. Apoplastic effectors secreted by two unrelated eukaryotic plant pathogens target the tomato defense protease Rcr3. Proc. Natl. Acad. Sci. U. S. A. 106:1654–1659

Song, T., Ma, Z., Shen, D., Li, Q., Li, W., Su, L., Ye, T., Zhang, M., Wang, Y., and Dou, D. 2015. An Oomycete CRN Effector Reprograms Expression of Plant HSP Genes by Targeting their Promoters. PLoS Pathog. 11 Tian, M., Benedetti, B., and 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. 138:1785–93

Tian, M., Huitema, E., Da Cunha, L., Torto-Alalibo, T., and 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

Tian, M., Win, J., Song, J., van der Hoorn, R., van der Knaap, E., and Kamoun, S. 2007. A Phytophthora infestans cystatin-like protein targets a novel tomato papain-like apoplastic protease. Plant Physiol. 143:364–77

Vargas, W. A., Sanz-Martín, J. M., Rech, G. E., Armijos-Jaramillo, V. D., Rivera, L. P., Echeverria, M. M., Díaz-Mínguez, J. M., Thon, M. R., and Sukno, S. A. 2015. A fungal effector with host nuclear localization and DNA-binding properties is required for maize anthracnose development. Mol. Plant. Microbe. Interact. Wawra, S., Djamei, A., Albert, I., Nürnberger, T., Kahmann, R., and van West, P. 2013. In Vitro Translocation

Experiments with RxLR-Reporter Fusion Proteins of Avr1b from Phytophthora sojae and AVR3a from Phytophthora infestans Fail to Demonstrate Specific Autonomous Uptake in Plant and Animal Cells. Mol. Plant. Microbe. Interact. 26:528–36

Yan, S., and Dong, X. 2014. Perception of the plant immune signal salicylic acid. Curr. Opin. Plant Biol. 20:64– 68

Chapitre II