Arms Race: Diverse Effector Proteins with Conserved Motifs

Overview

Journal Plant Signal Behav

Specialty Biology

Date 2019 Jan 10

PMID 30621489

Citations 31

Authors

Liping Liu

Le Xu

Qie Jia

Rui Pan

Ralf Oelmuller

Wenying Zhang

Chu Wu

Affiliations

Soon will be listed here.

Abstract

Effector proteins play important roles in the infection by pathogenic oomycetes and fungi or the colonization by endophytic and mycorrhizal fungi. They are either translocated into the host plant cells via specific translocation mechanisms and function in the host's cytoplasm or nucleus, or they reside in the apoplast of the plant cells and act at the extracellular host-microbe interface. Many effector proteins possess conserved motifs (such as the RXLR, CRN, LysM, RGD, DELD, EAR, RYWT, Y/F/WXC or CFEM motifs) localized in their N- or C-terminal regions. Analysis of the functions of effector proteins, especially so-called "core effectors", is crucial for the understanding of pathogenicity/symbiosis mechanisms and plant defense strategies, and helps to develop breeding strategies for pathogen-resistant cultivars, and to increase crop yield and quality as well as abiotic stress resistance. This review summarizes current knowledge about these effector proteins with the conversed motifs and their involvement in pathogenic or mutualistic plant/fungal interactions.

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References

Bos J, Armstrong M, Gilroy E, Boevink P, Hein I, Taylor R . Phytophthora infestans effector AVR3a is essential for virulence and manipulates plant immunity by stabilizing host E3 ligase CMPG1. Proc Natl Acad Sci U S A. 2010; 107(21):9909-14. PMC: 2906857. DOI: 10.1073/pnas.0914408107. View

Yaeno T, Li H, Chaparro-Garcia A, Schornack S, Koshiba S, Watanabe S . Phosphatidylinositol monophosphate-binding interface in the oomycete RXLR effector AVR3a is required for its stability in host cells to modulate plant immunity. Proc Natl Acad Sci U S A. 2011; 108(35):14682-7. PMC: 3167543. DOI: 10.1073/pnas.1106002108. View

Plett J, Kemppainen M, Kale S, Kohler A, Legue V, Brun A . A secreted effector protein of Laccaria bicolor is required for symbiosis development. Curr Biol. 2011; 21(14):1197-203. DOI: 10.1016/j.cub.2011.05.033. View

Cui F, Wu S, Sun W, Coaker G, Kunkel B, He P . The Pseudomonas syringae type III effector AvrRpt2 promotes pathogen virulence via stimulating Arabidopsis auxin/indole acetic acid protein turnover. Plant Physiol. 2013; 162(2):1018-29. PMC: 3668037. DOI: 10.1104/pp.113.219659. View

Bartolome R, Pelaez-Garcia A, Gomez I, Torres S, Fernandez-Acenero M, Escudero-Paniagua B . An RGD motif present in cadherin 17 induces integrin activation and tumor growth. J Biol Chem. 2014; 289(50):34801-14. PMC: 4263880. DOI: 10.1074/jbc.M114.600502. View

Sanchez-Vallet A, Saleem-Batcha R, Kombrink A, Hansen G, Valkenburg D, Thomma B . Fungal effector Ecp6 outcompetes host immune receptor for chitin binding through intrachain LysM dimerization. Elife. 2013; 2:e00790. PMC: 3700227. DOI: 10.7554/eLife.00790. View

Levesque C, Brouwer H, Cano L, Hamilton J, Holt C, Huitema E . Genome sequence of the necrotrophic plant pathogen Pythium ultimum reveals original pathogenicity mechanisms and effector repertoire. Genome Biol. 2010; 11(7):R73. PMC: 2926784. DOI: 10.1186/gb-2010-11-7-r73. View

Djamei A, Schipper K, Rabe F, Ghosh A, Vincon V, Kahnt J . Metabolic priming by a secreted fungal effector. Nature. 2011; 478(7369):395-8. DOI: 10.1038/nature10454. View

Dangl J, Horvath D, Staskawicz B . Pivoting the plant immune system from dissection to deployment. Science. 2013; 341(6147):746-51. PMC: 3869199. DOI: 10.1126/science.1236011. View

10.

Bouwmeester K, Meijer H, Govers F . At the Frontier; RXLR Effectors Crossing the Phytophthora-Host Interface. Front Plant Sci. 2012; 2:75. PMC: 3355728. DOI: 10.3389/fpls.2011.00075. View

11.

Larkan N, Lydiate D, Parkin I, Nelson M, Epp D, Cowling W . The Brassica napus blackleg resistance gene LepR3 encodes a receptor-like protein triggered by the Leptosphaeria maculans effector AVRLM1. New Phytol. 2012; 197(2):595-605. DOI: 10.1111/nph.12043. View

12.

Johnson M, Garrett C, Bond J, Coggan K, Wolfgang M, Redinbo M . Pseudomonas aeruginosa PilY1 binds integrin in an RGD- and calcium-dependent manner. PLoS One. 2012; 6(12):e29629. PMC: 3248442. DOI: 10.1371/journal.pone.0029629. View

13.

Gilroy E, Taylor R, Hein I, Boevink P, Sadanandom A, Birch P . CMPG1-dependent cell death follows perception of diverse pathogen elicitors at the host plasma membrane and is suppressed by Phytophthora infestans RXLR effector AVR3a. New Phytol. 2011; 190(3):653-66. DOI: 10.1111/j.1469-8137.2011.03643.x. View

14.

Bateman A, Bycroft M . The structure of a LysM domain from E. coli membrane-bound lytic murein transglycosylase D (MltD). J Mol Biol. 2000; 299(4):1113-9. DOI: 10.1006/jmbi.2000.3778. View

15.

de Jonge R, Thomma B . Fungal LysM effectors: extinguishers of host immunity?. Trends Microbiol. 2009; 17(4):151-7. DOI: 10.1016/j.tim.2009.01.002. View

16.

Ambawat S, Sharma P, Yadav N, Yadav R . MYB transcription factor genes as regulators for plant responses: an overview. Physiol Mol Biol Plants. 2014; 19(3):307-21. PMC: 3715649. DOI: 10.1007/s12298-013-0179-1. View

17.

Bos J, Kanneganti T, Young C, Cakir C, Huitema E, Win J . 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. 2006; 48(2):165-76. DOI: 10.1111/j.1365-313X.2006.02866.x. View

18.

Hurlburt N, Chen L, Stergiopoulos I, Fisher A . Structure of the Cladosporium fulvum Avr4 effector in complex with (GlcNAc)6 reveals the ligand-binding mechanism and uncouples its intrinsic function from recognition by the Cf-4 resistance protein. PLoS Pathog. 2018; 14(8):e1007263. PMC: 6128652. DOI: 10.1371/journal.ppat.1007263. View

19.

Limpens E, Franken C, Smit P, Willemse J, Bisseling T, Geurts R . LysM domain receptor kinases regulating rhizobial Nod factor-induced infection. Science. 2003; 302(5645):630-3. DOI: 10.1126/science.1090074. View

20.

Vetukuri R, Tripathy S, Malar C M, Panda A, Kushwaha S, Chawade A . Draft Genome Sequence for the Tree Pathogen Phytophthora plurivora. Genome Biol Evol. 2018; 10(9):2432-2442. PMC: 6152947. DOI: 10.1093/gbe/evy162. View