Pathogenic fungi neutralize plant‐derived ROS via Srpk1 deacetylation

Abstract

In response to infection, plants can induce the production of reactive oxygen species (ROS) to restrict pathogen invasion. In turn, adapted pathogens have evolved a counteracting mechanism of enzymatic ROS detoxification, but how it is activated remains elusive. Here, we show that in the tomato vascular wilt pathogen Fusarium oxysporum f. sp. lycopersici ( Fol ) this process is initiated by deacetylation of the FolSrpk1 kinase. Upon ROS exposure, Fol decreases FolSrpk1 acetylation on the K304 residue by altering the expression of the acetylation‐controlling enzymes. Deacetylated FolSrpk1 disassociates from the cytoplasmic FolAha1 protein, thus enabling its nuclear translocation. Increased accumulation of FolSrpk1 in the nucleus allows for hyperphosphorylation of its phosphorylation target FolSr1 that subsequently enhances transcription of different types of antioxidant enzymes. Secretion of these enzymes removes plant‐produced H 2 O 2 , and enables successful Fol invasion. Deacetylation of FolSrpk1 homologs has a similar function in Botrytis cinerea and likely other fungal pathogens. These findings reveal a conserved mechanism for initiation of ROS detoxification upon plant fungal infection.

Sir2‐mediated cytoplasmic deacetylation facilitates pathogenic fungi infection in host plants

“…Fungal strains and culture conditions Fusarium oxysporum f. sp. lycopersici strain 4287 (Fol ) and B05.10 of Botrytis cinerea were used in this study (Yang et al, 2022;Zhang et al, 2023). Strains were grown on potato dextrose agar (PDA).…”

“…In phytopathogenic fungi like F. oxysporum and Botrytis cinerea, although several acetylated proteins outside the nuclei have been identified (J. Yang et al, 2022;Zhang et al, 2023), the enzymes that write or erase Kac of nonhistone proteins remain unclear.…”

Suppressing plant defense: Scavenge the ROS!

“…Hyperphosphorylated FolSr1 then regulates the transcription of antioxidant enzymes which are translated and secreted out of the fungal cell to detoxify host‐produced ROS. The figure was modified from the figure shown in Zhang et al (2023). ROS, reactive oxygen species.…”

“…Several other phytopathogenic fungi have a corresponding K304 site and NLS present in their Srpk1, suggesting a similar mechanism of ROS detoxification and suppression of plant defense. In this article, we have presented our views on how future studies can be synthesized based on the pathway deciphered by Zhang et al (2023, https://doi.org/10.15252/embj.2022112634).…”

“…The molecular mechanism behind the activation of ROS detoxifying enzymes in fungal pathogens in response to host ROS production has remained elusive. Zhang et al (2023) have recently deciphered the mechanism behind this longstanding question (Figure 1). Fusarium oxysporum f. sp.…”