Acetylation of a fungal effector that translocates host PR1 facilitates virulence

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    The authors provided strong evidence that the Fusarium oxysporum effector protein FolSpv1 enhances virulence by targeting tomato SlPR1 and preventing the generation of the SlPR1-derived phytocytokine CAPE1, which otherwise positively regulates disease resistance in tomato plants. Strikingly, they show that FolSpv1 translocates SlPR1 from the apoplast back into the nucleus of tomato cell, suggesting a previously unknown mechanism employed by pathogenic microbes.

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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 Fol -Secreted Virulence-related Protein1 (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.

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  1. Author Response

    Reviewer #1 (Public Review):

    1. Fig 6E shows that CAPE1 is released only upon Fol infection. This appears to contradict with the notion that FolSpv1 prevents CAPE1 release. However, Fol strain overexpressing FolSpv1 prevented the release of CAPE1. It is necessary to compare WT and the mutant strain in which the FolSvp1 gene is deleted. One would expect that the mutant strain induces significantly more CAPE1 release. Similarly, mutant strain complemented with the nls1 construct needs to be tested to see whether nuclear localization is required for preventing CAPE1 release.

    Thank you for the good suggestions! According to the revision policy of eLife in response to COVID-19, we stated in the Discussion section that FolSpv1-mediated translocation of SlPR1 into the nucleus impedes CAPE1 release needs to be further …

  2. eLife assessment

    The authors provided strong evidence that the Fusarium oxysporum effector protein FolSpv1 enhances virulence by targeting tomato SlPR1 and preventing the generation of the SlPR1-derived phytocytokine CAPE1, which otherwise positively regulates disease resistance in tomato plants. Strikingly, they show that FolSpv1 translocates SlPR1 from the apoplast back into the nucleus of tomato cell, suggesting a previously unknown mechanism employed by pathogenic microbes.

  3. Reviewer #1 (Public Review):

    Pathogen effectors promote parasitism either in the apoplast or cytoplasm. Unexpectedly, the work described here suggests that FolSpv1 first interacts with SlPR1 in the apoplast and then translocates SlPR1 into the nucleus of tomato plant cells. The authors suggested that the FolSpv1-mediated translocation of SlPR1 into the nucleus prevented the generation of CAPE1, leading to compromised immunity in tomato plants. The study additionally showed that acetylation of FolSpv1 K167 protects the protein from ubiquitination and proteasome-mediated degradation in both the fungal cell and plant cell. Overexpression of SlPR1 or exogenous application of CAPE1 enhanced resistance to F. oxysporum, indicating that CAPE1 contributes to disease resistance to the pathogen in tomato plants. This is consistent with prior …

  4. Reviewer #2 (Public Review):

    In this work, the authors were trying to prove the model that the fungal pathogen Fusarium oxysporum f. sp. lycopersici (Fol) utilizes the acetyltransferase FolArd1 to induce the acetylation of the K167 residue of the effector protein FolSvp1. This acetylation prevents the K152, K258 and K284 ubiquitination-mediated degradation of FolSvp1 in Fol, and meanwhile inhibits the K167 ubiquitination-mediated degradation of FolSvp1 in tomato plants. In the host plants, FolSvp1 interacts specifically with the apoplastic defense protein SlPR1 and translocates it to the nucleus, which suppresses the SlPR1-derived CAPE1 peptide-induced fungal resistance. Overall, the experiments were well designed and the large amount of data justified most of their conclusions. The work sheds novel insight into the virulence mechanisms …