Feruloyl esterase Fae1 is required specifically for host colonisation by the rice-blast fungus Magnaporthe oryzae.

Akhil Thaker,Khyati Mehta,Rajesh Patkar

doi:10.1007/s00294-021-01213-z

Akhil Thaker, Khyati Mehta + Show 1 more

Open Access

https://doi.org/10.1007/s00294-021-01213-z

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Abstract

Plant cell wall acts as a primary barrier for microbial pathogens during infection. A cell wall-degrading enzyme thus may be a crucial virulence factor, as it may aid the pathogen in successful host invasion. Nine genes coding for feruloyl esterases (Fae), likely involved in plant cell wall degradation, have been annotated in the genome of the cereal-blast fungus Magnaporthe oryzae. However, role of anyFae in pathogenicity of M. oryzae remains hitherto under explored. Here, we identified FAE1 gene (MGG_08737) that was significantly upregulated during host penetration and subsequent colonisation stages of infection. Accordingly, while deletion of FAE1 in M. oryzae did not affect the vegetative growth and asexual development, the fae1Δ mutant showed significantly reduced pathogenesis on rice plants, mainly due to impaired host invasion and colonisation. Very few (< 10%) fae1Δ appressoria that formed the primary invasive hyphae failed to elaborate from the first invaded cell to the neighbouring plant cells. Interestingly, exogenously added glucose, as a simple carbon source, or ferulic acid, a product of theFae activity, significantly supported the invasive growth of the fae1Δ mutant. We show that the Fae1-based feruloyl esterase activity, by targeting the plant cell wall, plays an important role in accumulating ferulic acid and/or sugar molecules, as a likely energy source, to enable host invasion and colonisation by M. oryzae. Given its role in plant cell wall digestion and host colonisation, M. oryzae Fae1 could be a potential candidate for a novel antifungal strategy and a biotechnological application in biofuel production.

Highlights

Microbial phytopathogens encounter plant cell wall as a major obstruction while invading and successfully colonizing the host
We found in M. oryzae genome a total of nine putative feruloyl esterases that showed homology with either AoFaeB
The total enzyme activity in the intracellular fraction was less and remained largely unchanged even in the presence of the host leaf extract (Fig. 2C). These results indicate that most M. oryzae Fae are secretory and that their expression is induced by the host-derived factors suggesting a likely role for the cell wall degrading enzymes (CWDE) in blast fungal pathogenesis

Summary

Introduction

Microbial phytopathogens encounter plant cell wall as a major obstruction while invading and successfully colonizing the host. Typical plant cell wall is primarily composed of three polysaccharides namely cellulose (microfibrils), hemicellulose (xylan and xylan derivatives) and pectin, interconnected via ferulic acid bridges to form a rigid mesh-like structure (Harris and Hartley, 1977; Bunzel et al, 2001). The necrotrophic fungal pathogens use cell wall degrading enzymes (CWDE) to invade/colonise the plant tissue (Cosgrove, 2001); whereas the biotrophic or hemibiotrophic fungal pathogens, in addition to CWDE, depend on specialised host entry enabled by infection structures called as appressorium (Howard et al, 1991). A secreted feruloyl esterase A, encoded by MGG_01403.5, in M. oryzae is found to be expressed during post-penetration stage (72 hpi onwards) of rice infection, but does not play a significant role in pathogenesis of the fungus (Zheng et al, 2009). Our in silico analysis of these Fae highlights a likely diversification of the sequences in a host-specific manner

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