The Role of Glycoside Hydrolases in Phytopathogenic Fungi and Oomycetes Virulence

Rafiei, Vahideh; Vélëz, Heriberto; Tzelepis, Georgios

doi:10.3390/ijms22179359

Cited by 91 publications

(45 citation statements)

References 89 publications

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“…Another interesting PCWDE is a GH10 endoxylanase, which is encoded by a gene that is highly expressed during this mid-late infection stage. The importance of endoxylanases in virulence has been reported in some necrotrophic and hemibiotrophic fungi [85–88], and a GH10 endoxylanase from the necrotrophic fungus Valsa mali is important for colonization of apple [89]. Notably, the up-regulation of genes encoding PCWDEs during mid-late infection coincided with the up-regulation of genes encoding sugar and nitrogen-associated transporters.…”

Section: Discussionmentioning

confidence: 95%

TheVenturia inaequaliseffector repertoire is expressed in waves and is dominated by expanded families with predicted structural similarity to avirulence proteins from other plant-pathogenic fungi

Rocafort

Bowen

Hassing

et al. 2022

Preprint

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BackgroundScab, caused by the biotrophic fungus Venturia inaequalis, is the most economically important disease of apples worldwide. During infection, V. inaequalis occupies the subcuticular environment, where it secretes virulence factors, termed effectors, to promote host colonization. However, in the presence of corresponding host resistance proteins, these effectors are recognized as avirulence determinants to activate plant defences. To develop durable control strategies against scab, a better understanding of the molecular mechanisms underpinning subcuticular growth by V. inaequalis is required. Likewise, more information is needed on the role that effectors play in activating, suppressing or circumventing resistance protein-mediated defences.ResultsWe generated the first comprehensive RNA-seq transcriptome of V. inaequalis during colonization of apple. Analysis of this transcriptome revealed five in planta gene expression clusters or waves corresponding to three specific infection stages: early, mid and mid-late infection. Early infection was characterized by genes encoding plant cell wall-degrading enzymes (PCWDEs) and proteins associated with oxidative stress responses. Mid infection was characterized by genes encoding transporter proteins. Finally, mid-late infection was characterized by genes encoding PCWDEs and effector candidates (ECs), with most ECs belonging to expanded protein families. To gain insights into function, AlphaFold2 was used to predict the tertiary structures of proteinaceous ECs. Strikingly, many ECs were predicted to have structural similarity to avirulence proteins from other plant-pathogenic fungi, including members of the MAX, LARS, ToxA and FOLD structural effector families. In addition, several other ECs, including an EC family with amino acid similarity to the AvrLm6 effector from Leptosphaeria maculans, were predicted to adopt a KP6/ferredoxin-like fold. Thus, proteins with a KP6/ferredoxin-like fold may represent yet another structural family of effectors shared among plant-pathogenic fungi.ConclusionsOur study reveals the transcriptomic profile underpinning subcuticular growth by V. inaequalis, and reinforces the idea that fungal effectors share a limited number of structural folds. Importantly, our study also provides an enriched list of V. inaequalis ECs that can be investigated for roles in virulence and avirulence, and raises the possibility that apple resistance proteins can be engineered to recognize EC family folds or host components targeted by multiple EC family members.

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Section: Discussionmentioning

confidence: 95%

TheVenturia inaequaliseffector repertoire is expressed in waves and is dominated by expanded families with predicted structural similarity to avirulence proteins from other plant-pathogenic fungi

Rocafort

Bowen

Hassing

et al. 2022

Preprint

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“…Over recent years, it has become increasingly clear that secreted GH proteins of plant-associated fungi and oomycetes (i.e., those that are targeted extracellularly, but that lack a transmembrane domain or a glycophosphatidylinositol lipid modification site) play diverse roles in promoting host colonization and/or activating host immune responses (e.g., as effectors, MAMPs, or proteins that generate DAMPs; Kubicek et al, 2014 ; Rafiei et al, 2021 ; Figure 1 ; Supplementary Table 1 ). In this review, we highlight these roles, provide an overview of existing knowledge gaps and summarise future directions.…”

Section: Introductionmentioning

confidence: 99%

Secreted Glycoside Hydrolase Proteins as Effectors and Invasion Patterns of Plant-Associated Fungi and Oomycetes

et al. 2022

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During host colonization, plant-associated microbes, including fungi and oomycetes, deliver a collection of glycoside hydrolases (GHs) to their cell surfaces and surrounding extracellular environments. The number and type of GHs secreted by each organism is typically associated with their lifestyle or mode of nutrient acquisition. Secreted GHs of plant-associated fungi and oomycetes serve a number of different functions, with many of them acting as virulence factors (effectors) to promote microbial host colonization. Specific functions involve, for example, nutrient acquisition, the detoxification of antimicrobial compounds, the manipulation of plant microbiota, and the suppression or prevention of plant immune responses. In contrast, secreted GHs of plant-associated fungi and oomycetes can also activate the plant immune system, either by acting as microbe-associated molecular patterns (MAMPs), or through the release of damage-associated molecular patterns (DAMPs) as a consequence of their enzymatic activity. In this review, we highlight the critical roles that secreted GHs from plant-associated fungi and oomycetes play in plant–microbe interactions, provide an overview of existing knowledge gaps and summarize future directions.

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“…Among the down‐regulated genes, genes coding for putative glycoside hydrolases (GH) belonging to families 17 and 18 ( DN13345 and DN17665 ) were identified (Figure 2b , Table S2 ). The family GH17 includes enzymes with 1,3‐β‐glucosidase (EC 3.2.1.39), lichenase (EC 3.2.1.73), and exo‐1,3‐glucanase (EC 3.2.1.58) activities, while the GH18 family includes fungal enzymes with chitinolytic activity and endo‐β‐ N ‐acetyl‐glycosaminidases (ENGases) (Rafiei et al, 2021 ; Tzelepis & Karlsson, 2019 ). Furthermore, down‐regulation of a gene coding for a putative hydrophobin ( DN10012 ) was also observed (Figure 2b , Table S2 ).…”

Section: Resultsmentioning

confidence: 99%

A Verticillium longisporum pleiotropic drug transporter determines tolerance to the plant host β‐pinene monoterpene

Rafiei

Ruffino

Hodén

et al. 2021

Molecular Plant Pathology

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Plant roots exude a plethora of chemical compounds into the rhizosphere, the soil environment surrounding the root system. These compounds include ions, free oxygen, water, enzymes, and a diverse array of secondary metabolites that play important roles in microbe attraction to the roots (Bais et al., 2006;Hosseini et al., 2013). In the rhizosphere, plant roots interact with a variety of organisms such as insects, nematodes, and a vast range of microorganisms, such as fungi, bacteria, and protozoans. These interactions can be beneficial, pathogenic, or neutral for the plant (Campos-Soriano et al., 2012;Pineda et al., 2010;Zamioudis & Pieterse, 2012). Regarding the pathogenic interactions between plants and microbes, plant roots secrete antimicrobial compounds to defend themselves (Bais et al., 2006;Bednarek et al., 2005).Terpenes, a class of volatile secondary metabolites, constitute a major portion of root exudates (Bais et al., 2006). They are

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The Role of Glycoside Hydrolases in Phytopathogenic Fungi and Oomycetes Virulence

Cited by 91 publications

References 89 publications

TheVenturia inaequaliseffector repertoire is expressed in waves and is dominated by expanded families with predicted structural similarity to avirulence proteins from other plant-pathogenic fungi

TheVenturia inaequaliseffector repertoire is expressed in waves and is dominated by expanded families with predicted structural similarity to avirulence proteins from other plant-pathogenic fungi

Secreted Glycoside Hydrolase Proteins as Effectors and Invasion Patterns of Plant-Associated Fungi and Oomycetes

A Verticillium longisporum pleiotropic drug transporter determines tolerance to the plant host β‐pinene monoterpene

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