Conserved Fungal LysM Effector Ecp6 Prevents Chitin-Triggered Immunity in Plants

Jonge, Ronnie de; Esse, H. Peter van; Kombrink, Anja; Shinya, Tomonori; Desaki, Yoshitake; Bours, Ralph; Krol, Sander van der; Shibuya, Naoto; Joosten, M.H.A.J.; Thomma, B.P.H.J.

doi:10.1126/science.1190859

Cited by 659 publications

(634 citation statements)

References 25 publications

(38 reference statements)

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“…1a, Supplementary Table 5). In other plant pathogens, these are involved in modifying fungal cell wall composition and/or capturing chitin residues to mask chitin-triggered immune signals and evade detection by the host plants [21][22][23][24][25] , suggesting similar roles in Armillaria.…”

Section: Resultsmentioning

confidence: 99%

Genome expansion and lineage-specific genetic innovations in the forest pathogenic fungi Armillaria

et al. 2017

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T he genus Armillaria causes root rot disease in both gymnoand angiosperms, in forests, parks, and even vineyards in more than 500 host plant species 1 across the world. Most Armillaria species are facultative necrotrophs, which, after colonizing and killing the root cambium, transition to a saprobic phase, decomposing dead woody tissues of the host. As saprotrophs, Armillaria spp. are white rot (WR) fungi, which can efficiently decompose all components of plant cell walls, including lignin, (hemi-)cellulose and pectin 2 . They produce fleshy fruiting bodies (honey mushrooms) that appear in large clumps around infected plants and produce sexual spores. The vegetative phase of Armillaria is predominantly diploid rather than dikaryotic like most basidiomycetes.Individuals of Armillaria can reach immense sizes and include the 'humongous fungus' , one of the largest terrestrial organisms on Earth 3 , measuring up to 965 hectares and 600 tons 4 , and can display a mutation rate ≅ 3 orders of magnitude lower than most filamentous fungi 5 . Individuals reach this immense size via growing rhizomorphs, dark mycelial strings 1-4 mm wide that allow the fungus to bridge gaps between food sources or host plants 1,6 (hence the name shoestring root rot). Rhizomorphs develop through the aggregation and coordinated parallel growth of hyphae, similar to some fruiting body tissues 7,8 . As migratory and exploratory organs, rhizomorphs can grow approximately 1 m yr −1 and cross several metres underground in search for new hosts, although roles in uptake and longrange translocation of nutrients have also been proposed 1,9,10 . Root contact by rhizomorphs is the main mode of infection by the fungus, which makes the prevention of recurrent infection in Armillariacontaminated areas particularly difficult 1 . Despite their huge impact on forestry, horticulture and agriculture, the genetics of the pathogenicity of Armillaria species is poorly understood. The only -omics data published so far have highlighted a substantial repertoire of plant cell wall degrading enzymes (PCWDE) and secreted proteins, among others, in A. mellea and A. solidipes 11,12 , while analyses of the genomes of other pathogenic basidiomycetes (such as Moniliophthora 13,14 , Heterobasidion 15 and Rhizoctonia 16 ) identified genes coding for PCWDEs, secreted and effector proteins or secondary metabolism (SM) as putative pathogenicity factors. However, the lifecycle and unique dispersal strategy of Armillaria prefigure other evolutionary routes to pathogenicity, which, along with other potential genomic factors (such as transposable elements 17 ) are not yet known.Here, we investigate genome evolution and the origin of pathogenicity in Armillaria using comparative genomics, transcriptomics

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Section: Resultsmentioning

confidence: 99%

Genome expansion and lineage-specific genetic innovations in the forest pathogenic fungi Armillaria

et al. 2017

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“…However, functional homologs of Ecp6 were found in Zymoseptoria tritici (Mg3LysM) and Magnaporthe oryzae (Slp1) (De Jonge et al 2010; Marshall et al 2011; Mentlak et al 2012). Interestingly, the Mg3LysM effector of Z. tritici unites the abilities of both Avr4 and Ecp6 to sequester chitin oligomers and protect fungal cells from hydrolysis (Marshall et al 2011).…”

Section: Fungal Potential Against Host Immune Systemmentioning

confidence: 99%

Chitin and chitin-related compounds in plant–fungal interactions

Pusztahelyi

2018

Mycology

153

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Chitin is the second abundant polysaccharide in the world after cellulose. It is a vital structural component of the fungal cell wall but not for plants. In plants, fungi are recognised through the perception of conserved microbe-associated molecular patterns (MAMPs) to induce MAMP-triggered immunity (MTI). Chitin polymers and their modified form, chitosan, induce host defence responses in both monocotyledons and dicotyledons. The plants’ response to chitin, chitosan, and derived oligosaccharides depends on the acetylation degree of these compounds which indicates possible biocontrol regulation of plant immune system. There has also been a considerable amount of recent research aimed at elucidating the roles of chitin hydrolases in fungi and plants as chitinase production in plants is not considered solely as an antifungal resistance mechanism. We discuss the importance of chitin forms and chitinases in the plant–fungal interactions and their role in persistent and possible biocontrol.Abbreviations ET, ethylene; GAP, GTPase-activating protein; GEF, GDP/GTP exchange factor; JA, jasmonic acid; LysM, lysin motif; MAMP, microbe-associated molecular pattern; MTI, MAMP-triggered immunity; NBS, nucleotide-binding site; NBS-LRR, nucleotide-binding site leucine-rich repeats; PM, powdery mildew; PR, pathogenesis-related; RBOH, respiratory burst oxidase homolog; RLK, receptor-like kinase; RLP, receptor-like protein; SA, salicylic acid; TF, transcription factor.

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“…Classic examples include the effectors of the dothidiomycete leaf mold fungus Cladosporium fulvum Avr2, Avr4, and ECP6, which target various extracellular processes of the host plant tomato (van den Burg et al 2006;Bolton et al 2008;van Esse et al 2008). Whereas Avr2 is an inhibitor of tomato apoplastic cysteine proteases, ECP6 interferes with the perception of C. fulvum cell wall chitin by tomato cell surface immune receptors (de Jonge et al 2010). Other microbes deliver their effectors inside plant cells, typically through specialized structures (Fig.…”

Section: Effectors Traffic To Different Cellular Compartments In Planmentioning

confidence: 99%

“…Some common themes are starting to emerge. Effectors from diverse pathogenic species of bacteria, oomycetes, fungi, and insects have been reported to suppress an overlapping set of PTI signaling pathways (Gimenez-Ibanez et al 2009;Bos et al 2010;de Jonge et al 2010;Wang et al 2011). Both bacterial and oomycete plant pathogens target vesicle trafficking pathways to interfere with focal immunity, although the exact mechanisms are yet to emerge Lindeberg et al 2012).…”

Section: Effectors From Unrelated Pathogens Converge On the Same Hostmentioning

confidence: 99%

Effector Biology of Plant-Associated Organisms: Concepts and Perspectives

Win

Chaparro-Garcia

Belhaj

et al. 2012

Cold Spring Harbor Symposia on Quantitative Biology

357

329

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Every plant is closely associated with a variety of living organisms. Therefore, deciphering how plants interact with mutualistic and parasitic organisms is essential for a comprehensive understanding of the biology of plants. The field of plant-biotic interactions has recently coalesced around an integrated model. Major classes of molecular players both from plants and their associated organisms have been revealed. These include cell surface and intracellular immune receptors of plants as well as apoplastic and host-cell-translocated (cytoplasmic) effectors of the invading organism. This article focuses on effectors, molecules secreted by plant-associated organisms that alter plant processes. Effectors have emerged as a central class of molecules in our integrated view of plant-microbe interactions. Their study has significantly contributed to advancing our knowledge of plant hormones, plant development, plant receptors, and epigenetics. Many pathogen effectors are extraordinary examples of biological innovation; they include some of the most remarkable proteins known to function inside plant cells. Here, we review some of the key concepts that have emerged from the study of the effectors of plant-associated organisms. In particular, we focus on how effectors function in plant tissues and discuss future perspectives in the field of effector biology.

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Conserved Fungal LysM Effector Ecp6 Prevents Chitin-Triggered Immunity in Plants

Cited by 659 publications

References 25 publications

Genome expansion and lineage-specific genetic innovations in the forest pathogenic fungi Armillaria

Genome expansion and lineage-specific genetic innovations in the forest pathogenic fungi Armillaria

Chitin and chitin-related compounds in plant–fungal interactions

Effector Biology of Plant-Associated Organisms: Concepts and Perspectives

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