Nonproteinaceous effectors: the <i>terra incognita</i> of plant–fungal interactions

Collemare, Jérôme; O’Connell, Richard J.; Lebrun, Marc

doi:10.1111/nph.15785

Cited by 79 publications

(71 citation statements)

References 67 publications

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“…Independent of their lifestyles, all phytopathogenic fungi secrete virulence factors, also known as effectors, to aid in the establishment and development of infection within their host(s) (Cook et al, 2015;Lo Presti et al, 2015). Fungal effectors consist of a diverse group of molecules, including toxic secondary metabolites, enzymatic proteins, nonenzymatic proteins, and small interfering RNA molecules (Howlett, 2006;Stergiopoulos and de Wit, 2009;Weiberg et al, 2013;Collemare et al, 2019). Many fungal effectors discovered previously are small, cysteine-rich proteins that are secreted during host infection (Stergiopoulos and de Wit, 2009).…”

Section: Introductionmentioning

confidence: 99%

Conservation and expansion of a necrosis‐inducing small secreted protein family from host‐variable phytopathogens of the Sclerotiniaceae

Denton‐Giles

McCarthy

Sehrish

et al. 2020

Molecular Plant Pathology

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Fungal effector proteins facilitate host‐plant colonization and have generally been characterized as small secreted proteins (SSPs). We classified and functionally tested SSPs from the secretomes of three closely related necrotrophic phytopathogens: Ciborinia camelliae, Botrytis cinerea, and Sclerotinia sclerotiorum. Alignment of predicted SSPs identified a large protein family that share greater than 41% amino acid identity and that have key characteristics of previously described microbe‐associated molecular patterns (MAMPs). Strikingly, 73 of the 75 SSP family members were predicted within the secretome of the host‐specialist C. camelliae with single‐copy homologs identified in the secretomes of the host generalists S. sclerotiorum and B. cinerea. To explore the potential function of this family of SSPs, 10 of the 73 C. camelliae proteins, together with the single‐copy homologs from S. sclerotiorum (SsSSP3) and B. cinerea (BcSSP2), were cloned and expressed as recombinant proteins. Infiltration of SsSSP3 and BcSSP2 into host tissue induced rapid necrosis. In contrast, only one of the 10 tested C. camelliae SSPs was able to induce a limited amount of necrosis. Analysis of chimeric proteins consisting of domains from both a necrosis‐inducing and a non‐necrosis‐inducing SSP demonstrated that the C‐terminus of the S. sclerotiorum SSP is essential for necrosis‐inducing function. Deletion of the BcSSP2 homolog from B. cinerea did not affect growth or pathogenesis. Thus, this research uncovered a family of highly conserved SSPs present in diverse ascomycetes that exhibit contrasting necrosis‐inducing functions.

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Section: Introductionmentioning

confidence: 99%

Conservation and expansion of a necrosis‐inducing small secreted protein family from host‐variable phytopathogens of the Sclerotiniaceae

Denton‐Giles

McCarthy

Sehrish

et al. 2020

Molecular Plant Pathology

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“…1; Dodds & Rathjen, 2010; Thomma et al , 2011). Alongside proteinaceous effectors, many phytopathogens also secrete other effectors (including small RNAs and secondary metabolites) to enable host colonization (reviewed by Collemare et al , 2019). In this Tansley insight article, we focus only on proteinaceous effectors.…”

Section: Introductionmentioning

confidence: 99%

Exploring folds, evolution and host interactions: understanding effector structure/function in disease and immunity

2020

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Summary Over the past decade, tremendous progress has been made in plant pathology, broadening our understanding of how pathogens colonize their hosts. To manipulate host cell physiology and subvert plant immune responses, pathogens secrete an array of effector proteins. A co‐evolutionary arms‐race drives the pathogen to constantly reinvent its effector repertoire to undermine plant immunity. In turn, hosts develop novel immune receptors to maintain effector recognition and mount defences. Understanding how effectors promote disease and how they are perceived by the plant's defence network persist as major subjects in the study of plant–pathogen interactions. Here, we focus on recent advances (over roughly the last two years) in understanding structure/function relationships in effectors from bacteria and filamentous plant pathogens. Structure/function studies of bacterial effectors frequently uncover diverse catalytic activities, while structure‐informed similarity searches have enabled cataloguing of filamentous pathogen effectors. We also suggest how such advances have informed the study of plant–pathogen interactions.

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“…Necrotrophic fungi secrete phytotoxic secondary metabolites to kill the host tissues and suppress plant-defense responses (Osbourn, 2001;Keller et al, 2005;Muria-Gonzalez et al, 2015;Pusztahelyi et al, 2015;Collemare et al, 2019). These metabolites are secreted into infected plants and either act as virulence factors, i.e.…”

Section: Phytotoxic Fungal Metabolitesmentioning

confidence: 99%

“…Thus, this vesicular-mediated secretion could provide a route for fungal export of metabolites that is distinct from efflux by membrane transporters. It is anticipated that vesicular-mediated secretion in plant pathogenic fungi will become an active topic of research in the near future (Collemare et al, 2019). Conventional export/secretion of secondary metabolites seems to operate in plant pathogenic fungi as they possess several ABC and MFS transporters (Amnuaykanjanasin and Daub, 2009;Coleman and Mylonakis, 2009).…”

Section: Export Mechanisms Of Fungal Small Compoundsmentioning

confidence: 99%

The Multiple Facets of Plant–Fungal Interactions Revealed Through Plant and Fungal Secretomics

2020

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The plant secretome is usually considered in the frame of proteomics, aiming at characterizing extracellular proteins, their biological roles and the mechanisms accounting for their secretion in the extracellular space. In this review, we aim to highlight recent results pertaining to secretion through the conventional and unconventional protein secretion pathways notably those involving plant exosomes or extracellular vesicles. Furthermore, plants are well known to actively secrete a large array of different molecules from polymers (e.g. extracellular RNA and DNA) to small compounds (e.g. ATP, phytochemicals, secondary metabolites, phytohormones). All of these play pivotal roles in plant-fungi (or oomycetes) interactions, both for beneficial (mycorrhizal fungi) and deleterious outcomes (pathogens) for the plant. For instance, recent work reveals that such secretion of small molecules by roots is of paramount importance to sculpt the rhizospheric microbiota. Our aim in this review is to extend the definition of the plant and fungal secretomes to a broader sense to better understand the functioning of the plant/microorganisms holobiont. Fundamental perspectives will be brought to light along with the novel tools that should support establishing an environment-friendly and sustainable agriculture.

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Nonproteinaceous effectors: the terra incognita of plant–fungal interactions

Cited by 79 publications

References 67 publications

Conservation and expansion of a necrosis‐inducing small secreted protein family from host‐variable phytopathogens of the Sclerotiniaceae

Conservation and expansion of a necrosis‐inducing small secreted protein family from host‐variable phytopathogens of the Sclerotiniaceae

Exploring folds, evolution and host interactions: understanding effector structure/function in disease and immunity

The Multiple Facets of Plant–Fungal Interactions Revealed Through Plant and Fungal Secretomics

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