Identification of beneficial and detrimental bacteria impacting sorghum responses to drought using multi-scale and multisystem microbiome comparisons

Authors

Mingsheng Qi, Donald Danforth Plant Science Center, St. Louis, MO, USA.
Jeffrey C. Berry, Donald Danforth Plant Science Center, St. Louis, MO, USA.
Kira W. Veley, Donald Danforth Plant Science Center, St. Louis, MO, USA.
Lily O'Connor, Donald Danforth Plant Science Center, St. Louis, MO, USA.
Omri M. Finkel, University of North Carolina at Chapel Hill
Isai Salas-González, University of North Carolina at Chapel Hill
Molly Kuhs, Donald Danforth Plant Science Center, St. Louis, MO, USA.
Julietta Jupe, Donald Danforth Plant Science Center, St. Louis, MO, USA.
Emily Holcomb, Donald Danforth Plant Science Center, St. Louis, MO, USA.
Tijana Glavina del Rio, Lawrence Berkeley National Laboratory, Berkeley, CA, USA
Cody Creech, University of Nebraska - LincolnFollow
Peng Liu, Iowa State University, Ames, IA, USA.
Susannah G. Tringe, Lawrence Berkeley National Laboratory, Berkeley, CA, USA
Jeffery L. Dangl, University of North Carolina at Chapel Hill
Daniel P. Schachtman, University of Nebraska-LincolnFollow
Rebecca S. Bart, Donald Danforth Plant Science Center, St. Louis, MO, USA.Follow

ORCID IDs

Mingsheng Qi http://orcid.org/0000-0003-2448-1227

Jeffrey C. Berry http://orcid.org/0000-0002-8064-9787

Kira W. Veley http://orcid.org/0000-0002-3109-5810

Lily O’Connor http://orcid.org/0000-0002-4337-3582

Omri M. Finkel http://orcid.org/0000-0003-4770-0402

Isai Salas-González http://orcid.org/0000-0002-0347-5058

Molly Kuhs http://orcid.org/0000-0001-5063-5694

Emily Holcomb http://orcid.org/0000-0003-1392-6438

Cody Creech http://orcid.org/0000-0002-5334-4814

Peng Liu http://orcid.org/0000-0002-2093-8018

Susannah G. Tringe http://orcid.org/0000-0001-6479-8427

Jeffery L. Dangl http://orcid.org/0000-0003-3199-8654

Daniel P. Schachtman http://orcid.org/0000-0003-1807-4369

Rebecca S. Bart http://orcid.org/0000-0003-1378-3481

Date of this Version

2022

Citation

The ISME Journal (2022) 16:1957–1969; https://doi.org/10.1038/s41396-022-01245-4

Comments

© The Author(s) 2022. Open Access This article is licensed under a Creative Commons Attribution 4.0 International License

A Correction (July 2023) is attached (below)

Abstract

Drought is a major abiotic stress limiting agricultural productivity. Previous field-level experiments have demonstrated that drought decreases microbiome diversity in the root and rhizosphere. How these changes ultimately affect plant health remains elusive. Toward this end, we combined reductionist, transitional and ecological approaches, applied to the staple cereal crop sorghum to identify key root-associated microbes that robustly affect drought-stressed plant phenotypes. Fifty-three Arabidopsis-associated bacteria were applied to sorghum seeds and their effect on root growth was monitored. Two Arthrobacter strains caused root growth inhibition (RGI) in Arabidopsis and sorghum. In the context of synthetic communities, Variovorax strains were able to protect plants from Arthrobacter-caused RGI. As a transitional system, high-throughput phenotyping was used to test the synthetic communities. During drought stress, plants colonized by Arthrobacter had reduced growth and leaf water content. Plants colonized by both Arthrobacter and Variovorax performed as well or better than control plants. In parallel, we performed a field trial wherein sorghum was evaluated across drought conditions. By incorporating data on soil properties into the microbiome analysis, we accounted for experimental noise with a novel method and were able to observe the negative correlation between the abundance of Arthrobacter and plant growth. Having validated this approach, we cross-referenced datasets from the high-throughput phenotyping and field experiments and report a list of bacteria with high confidence that positively associated with plant growth under drought stress. In conclusion, a three-tiered experimental system successfully spanned the lab-to-field gap and identified beneficial and deleterious bacterial strains for sorghum under drought.