Acetylation of a fungal effector that translocates host PR1 facilitates virulence

Abstract

Pathogens utilize a panoply of effectors to manipulate plant defense. However, despite their importance, relatively little is actually known about regulation of these virulence factors. Here, we show that the effector FolSvp1, secreted from fungal pathogen Fusarium oxysporum f. sp. lycopersici (Fol) directly binds and translocates the tomato pathogenesis-related protein1, SlPR1, from the apoplast outside the plasma membrane to the host nucleus via its nuclear localization signal. Relocation of SlPR1 abolishes generation of the defense signaling peptide, CAPE1, from its C-terminus, and as a consequence, facilitates pathogen invasion of plants. The action of FolSvp1 requires covalent modification by acetylation for full virulence in host tomato tissues. The modification is catalyzed by the Fol FolArd1 lysine acetyltransferase prior to secretion. Addition of an acetyl group to one residue, K167, prevents ubiquitination-dependent degradation of FolSvp1 in both Fol and plant cells with different mechanisms, allowing it to function normally in fungal invasion. Either inactivation of FolSvp1 or removal of the acetyl group on K167 leads to impaired pathogenicity of Fol. These findings indicate that acetylation can regulate the stability of effectors of fungal plant pathogens with impact on virulence.

The secreted FolAsp aspartic protease facilitates the virulence of Fusarium oxysporum f. sp. lycopersici

“…FolAsp is believed to contain a predicted 19-amino-acid signal peptide at the N-terminus according to SignalP-5.0, 1 which indicates that FolAsp is a secreted protein ( Figure 1A ), in accordance with its existence in the Fol secretome ( Li et al, 2022 ). Here, we further performed a yeast signal trap assay to validate the secretory function of the signal peptide ( Yin et al, 2018 ).…”

“…As FolAsp was identified to be secreted, it might function in the apoplast. Though FolAsp was transiently expressed with its native N-terminal signal peptide, FolAsp might not be faithfully secreted in planta , as described previously ( Li et al, 2022 ).…”

“…For the subcellular localization of FolAsp in planta , the full coding sequence of FolAsp was PCR amplified using primer pairs FolAsp-pQB-F/R. The forward primer FolAsp1 SlPR1SP -PQB-F was used to generate an artificial form of FolAsp containing the tomato SlPR1 signal peptide (1–24 amino acids) instead of its endogenous signal peptide (1–19 amino acids) ( Li et al, 2022 ). These constructs were cloned into a pQB-V3 vector ( Chen et al, 2020 ) and then transferred to the C-terminal GFP-tagged pK7FWG2 ( Karimi et al, 2002 ) using Gateway LR Clonase Enzyme Mix (Invitrogen).…”

“…In our previous studies, we have identified 32 secreted effector candidates in Fol by mass spectrometry, which gives the first clues into the establishment of Fol early infection ( Li J. et al, 2020 ). To date, the FolSvp1 is characterized to contribute virulence by translocating a key defense protein PR1 to dampen the host defense ( Li et al, 2022 ). FoRnt2, a secreted ribonuclease T2 protein, contributes to the full virulence of F. oxysporum in tomato plants depending on its RNase activity ( Qian et al, 2022a ).…”

Comparative transcriptome profiling reveals the importance of GmSWEET15 in soybean susceptibility to Sclerotinia sclerotiorum

“…Compared with WT, gmsweet15 mutant showed more enriched biological processes at 24 hpi, such as upregulation of the secretory pathways and RAS/ARF protein signal transduction processes and inhibited tetrapyrrole metabolic process ( Figures 3K , L ). The mature processing and localization of PR1 seemed to be an important battlefield for pathogens in plants, and many effectors target this process ( Yang et al, 2018 ; Sung et al, 2021 ; Li et al, 2022 ). In addition to being responsible for the mature processing and secretion of antibacterial peptides such as PR1, some endoplasmic reticulum and membrane transporters are associated with disease resistance capacity ( Mao et al, 2017 ; Wang et al, 2021 ).…”