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

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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 any Fae 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 the Fae 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.

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Fig. 1
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source for M. oryzae. Vegetative growth of the WT M. oryzae on basal medium (BM) with or without 0.01% ferulic acid as the sole carbon source. The images were taken at 10 dpi

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source enabling successful host invasion and colonisation by the blast fungal pathogen

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Acknowledgements

We acknowledge late Prof. Bharat B. Chattoo for his guidance and providing sophisticated laboratory facility at the Bharat Chattoo Genome Research Centre (BCGRC). We also fondly remember late Dr. Johannes Manjrekar for the useful scientific discussions during the course of this work. We thank Naweed Naqvi (Temasek Lifesciences Laboratory, Singapore) for providing backbone vector pFGL1010. AT was supported by UGC-BSR-RFSMS (F.7-128/2007-BSR, dtd-02.09.2014), University Grants Commission, Government of India (GoI); and KM acknowledges the intramural University Research Scholarship from The M. S. University of Baroda. This work was supported by the Ramalingaswami Fellowship (BT/RLF/Re-entry/32/2014), DBT, GoI, awarded to RP. We also acknowledge the funding support (EMR/2017/005303) from SERB, GoI. We thank the BCGRC group at MSU for useful discussions.

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  1. Bharat Chattoo Genome Research Centre, Department of Microbiology and Biotechnology Centre, The Maharaja Sayajirao University of Baroda, Vadodara, Gujarat, India, 390002

    Akhil Thaker, Khyati Mehta & Rajesh Patkar

  2. Department of Biosciences and Bioengineering, Indian Institute of Technology Bombay, Powai, Mumbai, Maharashtra, India, 400076

    Rajesh Patkar

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  1. Akhil Thaker
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  2. Khyati Mehta
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Conceptualization: AT and RP; methodology: AT and RP; validation: AT and KM; formal analysis: AT; investigation: AT and KM; resources: RP; writing—original draft: AT and KM; writing—review and editing: RP; supervision: RP; project administration: RP; funding acquisition: RP.

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Correspondence to Rajesh Patkar.

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Thaker, A., Mehta, K. & Patkar, R. Feruloyl esterase Fae1 is required specifically for host colonisation by the rice-blast fungus Magnaporthe oryzae. Curr Genet 68, 97–113 (2022). https://doi.org/10.1007/s00294-021-01213-z

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