The decrotonylase FoSir5 facilitates mitochondrial metabolic state switching in conidial germination of Fusarium oxysporum

  1. Ning Zhang
  2. Limin Song
  3. Yang Xu
  4. Xueyuan Pei
  5. Ben F Luisi
  6. Wenxing Liang  Is a corresponding author
  1. Qingdao Agricultural University, China
  2. University of Cambridge, United Kingdom

Abstract

Fusarium oxysporum is one of the most important pathogenic fungi with a broad range of plant and animal hosts. The first key step of its infection cycle is conidial germination, but there is limited information available on the molecular events supporting this process. We show here that germination is accompanied by a sharp decrease in expression of FoSir5, an ortholog of the human lysine deacetylase SIRT5. We observe that FoSir5 decrotonylates a subunit of the fungal pyruvate dehydrogenase complex (FoDLAT) at K148, resulting in inhibition of the activity of the complex in mitochondria. Moreover, FoSir5 decrotonylates histone H3K18, leading to a downregulation of transcripts encoding enzymes of aerobic respiration pathways. Thus, the activity of FoSir5 coordinates regulation in different organelles to steer metabolic flux through respiration. As ATP content is positively related to fungal germination, we propose that FoSir5 negatively modulates conidial germination in F. oxysporum through its metabolic impact. These findings provide insights into the multifaceted roles of decrotonylation, catalysed by FoSir5, that support conidial germination in F. oxysporum.

Data availability

The RNA-seq raw reads are available in NCBI Sequence Read Archive (SRA) database with the accession number of PRJNA687117.

Article and author information

Author details

  1. Ning Zhang

    Key Lab of Integrated Crop Pest Management of Shandong Province, College of Plant Health and Medicine, Qingdao Agricultural University, Qingdao, China
    Competing interests
    The authors declare that no competing interests exist.
  2. Limin Song

    Key Lab of Integrated Crop Pest Management of Shandong Province, College of Plant Health and Medicine, Qingdao Agricultural University, Qingdao, China
    Competing interests
    The authors declare that no competing interests exist.
  3. Yang Xu

    Key Lab of Integrated Crop Pest Management of Shandong Province, College of Plant Health and Medicine, Qingdao Agricultural University, Qingdao, China
    Competing interests
    The authors declare that no competing interests exist.
  4. Xueyuan Pei

    Department of Biochemistry, University of Cambridge, Cambridge, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
  5. Ben F Luisi

    Department of Biochemistry, University of Cambridge, Cambridge, United Kingdom
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-1144-9877
  6. Wenxing Liang

    Key Lab of Integrated Crop Pest Management of Shandong Province, College of Plant Health and Medicine, Qingdao Agricultural University, Qingdao, China
    For correspondence
    wliang1@qau.edu.cn
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-3791-4901

Funding

National Natural Science Foundation of China (31972213)

  • Wenxing Liang

National Natural Science Foundation of China (32102149)

  • Ning Zhang

Shandong Provincial Natural Science Foundation (ZR2019BC070)

  • Ning Zhang

Shandong Provincial Natural Science Foundation (ZR2020KC003)

  • Wenxing Liang

Shandong Province 'Double-Hundred Talen Plan' (WST2018008)

  • Wenxing Liang

Taishan Scholar Construction Foundation of Shandong Province (tshw20130963)

  • Wenxing Liang

Wellcome Trust (200873/Z/16/Z)

  • Xueyuan Pei
  • Ben F Luisi

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

Reviewing Editor

  1. Weiwei Dang, Baylor College of Medicine, United States

Version history

  1. Received: November 15, 2021
  2. Preprint posted: November 30, 2021 (view preprint)
  3. Accepted: December 15, 2021
  4. Accepted Manuscript published: December 20, 2021 (version 1)
  5. Version of Record published: January 5, 2022 (version 2)

Copyright

© 2021, Zhang et al.

This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.

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  1. Ning Zhang
  2. Limin Song
  3. Yang Xu
  4. Xueyuan Pei
  5. Ben F Luisi
  6. Wenxing Liang
(2021)
The decrotonylase FoSir5 facilitates mitochondrial metabolic state switching in conidial germination of Fusarium oxysporum
eLife 10:e75583.
https://doi.org/10.7554/eLife.75583

Share this article

https://doi.org/10.7554/eLife.75583

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