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Research Project: Discovery of Plant Genetic Mechanisms Controlling Microbial Recruitment to the Root Microbiome

Location: Plant Gene Expression Center

Title: Holo-omics disentangle drought response and biotic interactions among plant, endophyte and pathogen

Author
item CHEN, PEILIN - Chinese Academy Of Sciences
item YU, QINGYI - Chinese Academy Of Sciences
item WANG, CONG - Chinese Academy Of Sciences
item MONTOYA, LILIAM - University Of California Berkeley
item WEST, PATRICK - University Of California Berkeley
item XU, LING - University Of California Berkeley
item VAROQUAUX, NELLE - University Of California Berkeley
item COLE, BENJAMIN - Joint Genome Institute
item HIXSON, KIM - Pacific Northwest National Laboratory
item KIM, YOUNG-MA - Pacific Northwest National Laboratory
item LIU, LING - Chinese Academy Of Sciences
item ZHANG, BAODAN - Chinese Academy Of Sciences
item ZHANG, JIE - Chinese Academy Of Sciences
item LI, BAIYANG - Chinese Academy Of Sciences
item PURDOM, ELIZABETH - University Of California Berkeley
item VOGEL, JOHN - Joint Genome Institute
item JANSSON, CHRISTER - Pacific Northwest National Laboratory
item HUTMACHER, ROBERT - Kearney Agricultural Center
item DAHLBERG, JEFFREY - Kearney Agricultural Center
item Coleman-Derr, Devin
item LEMAUX, PEGGY - University Of California Berkeley
item TAYLOR, JOHN - University Of California Berkeley
item GAO, CHENG - Chinese Academy Of Sciences

Submitted to: Nature
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 3/30/2025
Publication Date: 4/18/2025
Citation: Chen, P., Yu, Q., Wang, C., Montoya, L., West, P., Xu, L., Varoquaux, N., Cole, B., Hixson, K., Kim, Y., Liu, L., Zhang, B., Zhang, J., Li, B., Purdom, E., Vogel, J., Jansson, C., Hutmacher, R., Dahlberg, J., Coleman-Derr, D.A., Lemaux, P., Taylor, J., Gao, C. 2025. Holo-omics disentangle drought response and biotic interactions among plant, endophyte and pathogen. Nature. 246(6):2702–2717. https://doi.org/10.1111/nph.70155.
DOI: https://doi.org/10.1111/nph.70155

Interpretive Summary: In nature, the fitness of a macro-organism is inseparable from its fungal mycobiome, the abundant and diverse, beneficial, or harmful collection of fungi in its interior and on its surface. Well-known consequences of the fungal mycobiome on host plant fitness include both positive and negative alterations of responses to abiotic stresses, resource acquisition, and biotic stresses that include disease. These altered responses can promote or suppress plant growth. The realized impact of the fungal mycobiome on plant fitness is determined by the interactions among plants, beneficial fungi, and harmful fungi, and the impacts can change as these players adapt to changes in the abiotic environment. Here we explore how fungi respond to drought via changes in plant root metabolism.

Technical Abstract: Plant response to drought stress involves fungi and bacteria that live on and in plants and in the rhizosphere. Manipulation of these myco- and microbiomes has the potential to mitigate drought stress under global climate change, yet the stability of these microbiomes remains poorly understood. We address the entangled responses of pathogenic and endophytic fungi associated with sorghum when droughted through assembly of the most abundant fungal, endophyte genome from rhizospheric metagenomic sequence followed by comparison of its metatranscriptome with the host plant metabolome and transcriptome. The rise of endophyte abundance 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 endophyte and plant pathogenic fungi associates with a rise in expression of the endophyte’s biosynthetic gene clusters coding for secondary compounds. Among them is a siderophore suggesting iron as the resource limiting abundance of both endophyte and pathogens. Surprisingly, we found no evidence that reduction in relative abundance of pathogenic fungal is associated with plant hormones or immunity.