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Suarez-Fernandez, MAuthorMaestre-Guillén, AAuthorDe Francesco, AAuthorMeile, LAuthorSanchez-Vallet, ACorresponding Author

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March 25, 2025
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Sas3-mediated histone acetylation regulates effector gene activation in a fungal plant pathogen

Publicated to:Mbio. 14 (5): - 2023-10-01 14(5), DOI: 10.1128/mbio.01386-23

Authors: Suarez-Fernandez, M; Alvarez-Aragón, R; Pastor-Mediavilla, A; Maestre-Guillén, A; del Olmo, I; De Francesco, A; Meile, L; Sánchez-Vallet, A

Affiliations

UAM, Ctr Biol Mol Severo Ochoa, CSIC - Author
Univ Alicante, Dept Marine Sci & Appl Biol - Author
Univ Politecn Madrid UPM, Ctr Biotecnol & Genom Plantas CBGP, Inst Nacl Invest & Tecnol Agr & Alimentaria INIA, Consejo Super Invest Cient CSIC - Author

Abstract

Effector proteins are secreted by plant pathogens to enable host colonization. Typically, effector genes are tightly regulated, have very low expression levels in axenic conditions, and are strongly induced during host colonization. Chromatin remodeling contributes to the activation of effector genes in planta by still poorly known mechanisms. In this work, we investigated the role of histone acetylation in effector gene derepression in plant pathogens. We used Zymoseptoria tritici, a major pathogen of wheat, as a model to determine the role of lysine acetyltransferases (KATs) in plant infection. We showed that effector gene activation is associated with chromatin remodeling, featuring increased acetylation levels of histone H3 lysine 9 (H3K9) and 14 (H3K14) in effector loci. We functionally characterized the role of Z. tritici KATs and demonstrated their distinct contributions to growth, development, and infection. Sas3 is required for host colonization and pycnidia production and is involved in the acetylation of H3K9 and H3K14 in effector loci and, consequently, in effector gene activation during plant infection. We propose that Sas3-mediated histone acetylation is required for the spatiotemporal activation of effector genes and the virulence of Z. tritici. IMPORTANCE Pathogen infections require the production of effectors that enable host colonization. Effectors have diverse functions and are only expressed at certain stages of the infection cycle. Thus, effector genes are tightly regulated by several mechanisms, including chromatin remodeling. Here, we investigate the role of histone acetylation in effector gene activation in the fungal wheat pathogen Zymoseptoria tritici. We demonstrate that lysine acetyltransferases (KATs) are essential for the spatiotemporal regulation of effector genes. We show that the KAT Sas3 is involved in leaf symptom development and pycnidia formation. Importantly, our results indicate that Sas3 controls histone acetylation of effector loci and is a regulator of effector gene activation during stomatal penetration. Overall, our work demonstrates the key role of histone acetylation in regulating gene expression associated with plant infection.

Keywords

AcetylationAcetyltransferaseChromatinChromatin assembly and disassemblyChromatin remodelingEffector gene activationH3 acetylationHistone acetylationHistonesMethylationPlant diseasesProteinResistanceSas3TranscriptionTranscriptional activationWheatZinc-fingerZymoseptoria triticiZymoseptoria-tritici

Quality index

Bibliometric impact. Analysis of the contribution and dissemination channel

The work has been published in the journal Mbio due to its progression and the good impact it has achieved in recent years, according to the agency WoS (JCR), it has become a reference in its field. In the year of publication of the work, 2023, it was in position 28/161, thus managing to position itself as a Q1 (Primer Cuartil), in the category Microbiology.

From a relative perspective, and based on the normalized impact indicator calculated from World Citations provided by WoS (ESI, Clarivate), it yields a value for the citation normalization relative to the expected citation rate of: 1.17. This indicates that, compared to works in the same discipline and in the same year of publication, it ranks as a work cited above average. (source consulted: ESI Nov 14, 2024)

This information is reinforced by other indicators of the same type, which, although dynamic over time and dependent on the set of average global citations at the time of their calculation, consistently position the work at some point among the top 50% most cited in its field:

  • Field Citation Ratio (FCR) from Dimensions: 2.62 (source consulted: Dimensions Sep 2025)

Specifically, and according to different indexing agencies, this work has accumulated citations as of 2025-09-18, the following number of citations:

  • WoS: 6
  • Scopus: 6

Impact and social visibility

From the perspective of influence or social adoption, and based on metrics associated with mentions and interactions provided by agencies specializing in calculating the so-called "Alternative or Social Metrics," we can highlight as of 2025-09-18:

  • The use, from an academic perspective evidenced by the Altmetric agency indicator referring to aggregations made by the personal bibliographic manager Mendeley, gives us a total of: 18.
  • The use of this contribution in bookmarks, code forks, additions to favorite lists for recurrent reading, as well as general views, indicates that someone is using the publication as a basis for their current work. This may be a notable indicator of future more formal and academic citations. This claim is supported by the result of the "Capture" indicator, which yields a total of: 18 (PlumX).

With a more dissemination-oriented intent and targeting more general audiences, we can observe other more global scores such as:

  • The Total Score from Altmetric: 18.05.
  • The number of mentions on the social network Facebook: 2 (Altmetric).
  • The number of mentions on the social network X (formerly Twitter): 29 (Altmetric).

It is essential to present evidence supporting full alignment with institutional principles and guidelines on Open Science and the Conservation and Dissemination of Intellectual Heritage. A clear example of this is:

  • The work has been submitted to a journal whose editorial policy allows open Open Access publication.

Leadership analysis of institutional authors

There is a significant leadership presence as some of the institution’s authors appear as the first or last signer, detailed as follows: First Author (ALVAREZ ARAGON, ROCIO) and Last Author (SÁNCHEZ VALLET, ANDREA).

the author responsible for correspondence tasks has been SÁNCHEZ VALLET, ANDREA.