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

Abstract

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.

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

“…As nutrients in the subcuticular environment are likely to be scarce throughout host colonization, it is anticipated that V. inaequalis meets a portion of its nutritional requirements through the degradation of the pectin-rich layer located between the cuticle and epidermal cells of apple using these enzymes [83]. Related to this, it is well known that fungal GH28 enzymes can be recognized as MAMPs, while host cell wall fragments released as a consequence of GH28 hydrolytic activity can be recognized as damaged-associated molecular patterns (DAMPs), by PRRs, to activate the plant immune system [7]. With this in mind, a subset of the ECs encoded by genes that peaked in expression during mid-late infection may function to suppress plant defences responses initiated by these GH28 enzymes.…”

A conserved enzyme of smut fungi facilitates cell-to-cell movement in the plant bundle sheath

“…It has been shown in many cases that fungal-derived extracellular GH family members and glucan-binding proteins play important roles in host penetration. While necrotrophs have relatively higher number and variation in their PCWDE repertoires to directly macerate and kill their host cells for nutrient acquisition, biotrophs fine-tune their limited number of PCWDEs to detoxify antimicrobial compounds, to acquire nutrients or to sequester MAMP molecules to prevent induction of host immunity (Bradley et al ., 2022). For example, some of GH3 and GH10 family members are involved in detoxification of host-specific avenacin and α-tomatine, antimicrobial secondary metabolites from oat and tomato, respectively (Bowyer et al ., 1995; Osbourn, 1996; Ökmen et al ., 2013).…”

“…In this regard, some filamentous phytopathogens use both mechanical force and enzymatic activities to breach this first layer of defense. While a specialized dome-like structure, the appressorium, provides mechanical force for direct penetration, each pathogen has an arsenal of plant cell wall degrading enzymes (PCWDEs) that break down the host cell wall for host penetration or nutrient acquisition (Bradley et al ., 2022). Plant pathogens show a wide range of variation in their PCWDEs repertoire including glycoside hydrolases (GHs), which determines their virulence, pathogenic life-styles and host specificity (Ospina-Giraldo et al ., 2010; Zhao et al ., 2013; Hane et al ., 2019).…”

“…The presence of a putative PCWDE among the organ-specific effectors might reflect differences in cell wall composition of leaves compared to tassel tissues. Many previously published reports demonstrate the importance of pathogen-derived PCWDEs in plant microbe interactions (Bradley et al ., 2022). While some glycoside hydrolases are involved in host penetration and nutrient acquisition by degrading plant cell wall components, others are involved in detoxification of antimicrobial secondary metabolites or hydrolyzing MAMP molecules (Bradley et al ., 2022).…”

“…Many previously published reports demonstrate the importance of pathogen-derived PCWDEs in plant microbe interactions (Bradley et al ., 2022). While some glycoside hydrolases are involved in host penetration and nutrient acquisition by degrading plant cell wall components, others are involved in detoxification of antimicrobial secondary metabolites or hydrolyzing MAMP molecules (Bradley et al ., 2022). For example, xylanases have been shown recently to be involved in proliferation of U. maydis during plant infection (Moreno-Sánchez et al ., 2021).…”