Holo‐omics disentangle drought response and biotic interactions among plant, endophyte and pathogen
Holo-omics provide a novel opportunity to study the interactions among fungi from different functional guilds in host plants in field conditions. We address the entangled responses of plant pathogenic and endophytic fungi associated with sorghum when droughted through the assembly of the most abundant fungal, endophyte genome from rhizospheric metagenomic sequences followed by a comparison of its metatranscriptome with the host plant metabolome and transcriptome. The rise in relative abundance of endophytic Acremonium persicinum (operational taxonomic unit 5 (OTU5)) in drought co-occurs with a rise in fungal membrane dynamics and plant metabolites, led by ethanolamine, a key phospholipid membrane component. The negative association between endophytic A. persicinum (OTU5) and plant pathogenic fungi co-occurs with a rise in expression of the endophyte's biosynthetic gene clusters coding for secondary compounds. Endophytic A. persicinum (OTU5) and plant pathogenic fungi are negatively associated under preflowering drought but not under postflowering drought, likely a consequence of variation in fungal fitness responses to changes in the availability of water and niche space caused by plant maturation over the growing season. Our findings suggest that the dynamic biotic interactions among host, beneficial and harmful microbiota in a changing environment can be disentangled by a blending of field observation, laboratory validation, holo-omics and ecological modelling.
Authors
- Christer Jansson (ORCID: https://orcid.org/0000-0001-9548-093X)
- Qingyi Yu (ORCID: https://orcid.org/0000-0001-5393-5764)
- Nelle Varoquaux (ORCID: https://orcid.org/0000-0002-8748-6546)
- Kim Hixson (ORCID: https://orcid.org/0000-0003-3915-7040)
- Peggy G. Lemaux (ORCID: https://orcid.org/0000-0002-2842-4724)
- Elizabeth Purdom (ORCID: https://orcid.org/0000-0001-9455-7990)
- Patrick T. West (ORCID: https://orcid.org/0000-0001-8039-7535)
- Peng‐Lei Chen (ORCID: https://orcid.org/0009-0006-1613-3352)
- Benjamin Cole (ORCID: https://orcid.org/0000-0001-9652-624X)
- Cheng Da Gao (ORCID: https://orcid.org/0000-0003-2522-7909)
- John P. Vogel (ORCID: https://orcid.org/0000-0003-1786-2689)
- Baodan Zhang (ORCID: https://orcid.org/0000-0001-5602-5459)
- Devin Coleman‐Derr (ORCID: https://orcid.org/0000-0002-6282-1731)
- Ling Xu
- Liliam Montoya (ORCID: https://orcid.org/0000-0002-9311-9398)
- Ling Liu (ORCID: https://orcid.org/0000-0001-7912-568X)
- Cong Wang (ORCID: https://orcid.org/0000-0002-3408-2118)
- Jie Zhang (ORCID: https://orcid.org/0009-0002-4482-8611)
- Young‐Mo Kim (ORCID: https://orcid.org/0000-0002-8972-7593)
- Baiyang Li (ORCID: https://orcid.org/0009-0003-2404-4569)
- John W. Taylor (ORCID: https://orcid.org/0000-0002-5794-7700)
- Robert B. Hutmacher
- Jeffery Dahlberg
Institutions
- Agricultural Research Service (US)
- Pacific Northwest National Laboratory (US)
- Joint Genome Institute (US)
- Chinese Academy of Sciences (CN)
- University of Nebraska at Kearney (US)
- Institute of Microbiology (CN)
- Plant Gene Expression Center (US)
- University of Chinese Academy of Sciences (CN)
- China Agricultural University (CN)
- University of California, Davis (US)
- University of California, Berkeley (US)
Publication Details
- Journal
- New Phytologist
- Published
- 2025-04-18
- DOI
- https://doi.org/10.1111/nph.70155
- Citations
- 6
- Primary Topic
- Plant Pathogens and Fungal Diseases
- Type
- article
- Field-Weighted Citation Impact
- 6.91
Funders
- U.S. Department of Energy
- Joint Genome Institute
- National Natural Science Foundation of China
- Chinese Academy of Sciences
- Office of Science
- National Key Research and Development Program of China
- Biological and Environmental Research