Extracellular Vesicles from Fusarium graminearum Contain Protein Effectors Expressed during Infection of Corn

Abstract

Fusarium graminearum (Fgr) is a devastating filamentous fungal pathogen that causes diseases in cereals, while producing mycotoxins that are toxic for humans and animals, and render grains unusable. Low efficiency in managing Fgr poses a constant need for identifying novel control mechanisms. Evidence that fungal extracellular vesicles (EVs) from pathogenic yeast have a role in human disease led us to question whether this is also true for fungal plant pathogens. We separated EVs from Fgr and performed a proteomic analysis to determine if EVs carry proteins with potential roles in pathogenesis. We revealed that protein effectors, which are crucial for fungal virulence, were detected in EV preparations and some of them did not contain predicted secretion signals. Furthermore, a transcriptomic analysis of corn (Zea mays) plants infected by Fgr revealed that the genes of some of the effectors were highly expressed in vivo, suggesting that the Fgr EVs are a mechanism for the unconventional secretion of effectors and virulence factors. Our results expand the knowledge on fungal EVs in plant pathogenesis and cross-kingdom communication, and may contribute to the discovery of new antifungals.

The development of extracellular vesicle markers for the fungal phytopathogen Colletotrichum higginsianum

“…EVs are frequently observed by TEM at the interface between plant and fungal cells (Ivanov et al., 2019; Micali et al., 2011; Roth et al., 2019). Recent studies also suggest that EVs from fungal phytopathogens carry protein effectors and phytotoxic compounds (Bleackley et al., 2019; Garcia‐Ceron et al., 2021; Garcia‐Ceron et al., 2021).…”

“…vasinfectum ; EVs of the latter were also associated with an unidentified purple‐coloured phytotoxic metabolite (Bleackley et al., 2019; Silva et al., 2014). Proteins involved in toxin synthesis were also identified in EVs from Fusarium graminearum (Garcia‐Ceron et al., 2021). Combined, these findings suggest that EVs may represent a common mechanism among fungal phytopathogens for the export, or even extracellular synthesis, of biologically active metabolites.…”

“…More recent studies have examined EVs from Zymoseptoria tritici (septoria leaf blotch in wheat), Fusarium oxysporum f. sp . vasinfectum ( Fusarium wilt disease in cotton), Ustilago maydis (maize smut) and Fusarium graminearum ( Fusarium stalk rot) (Bleackley et al., 2019; Garcia‐Ceron et al., 2021; Garcia‐Ceron et al., 2021; Hill & Solomon, 2020). EVs from these phytopathogens resemble other fungal EVs in their size and contents.…”

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

“…Finally, more research is required to better understand how secreted GH proteins, such as the BcCrh1 GH16 protein from B. cinerea ( Bi et al, 2021 ), enter plant cells. Here, one line of enquiry could involve the delivery of these proteins by extracellular vesicles (EVs), given that fungal EV cargo often contains CAZymes, such as GHs with a signal peptide (e.g., Garcia-Ceron et al, 2021 ).…”

Associative and Physical Mapping of Markers Related to Fusarium in Maize Resistance, Obtained by Next-Generation Sequencing (NGS)

“…Their presence in the feed is also a great threat to the health and life of animals, especially pigs and poultry, because they cause increased sensitivity to infectious agents that under standard conditions, without the additional action of toxin-producing fungal metabolites, would not be able to cause disease. In addition, they negatively affect production results [ 7 ].…”