A dynamic rhizosphere interplay between tree roots and soil bacteria under drought stress

Abstract

Root exudates are thought to play an important role in plant-microbial interactions. In return for nutrition, soil bacteria can increase the bioavailability of soil nutrients. However, root exudates typically decrease in situations such as drought, calling into question the efficacy of solvation and bacteria-dependent mineral uptake in such stress. Here we tested the hypothesis of exudate-driven microbial priming on Cupressus saplings grown in forest soil in custom-made rhizotron boxes. A 1-month imposed drought and concomitant inoculations with a mix of Bacillus subtilis and Pseudomonas stutzeri, bacteria species isolated from the forest soil, were applied using factorial design. Direct bacteria counts and visualization by confocal microscopy showed that both bacteria associated with Cupressus Interestingly, root exudation rates increased 2.3-fold with bacteria under drought, as well as irrigation. Forty four metabolites in exudates were significantly different in concentration between irrigated and drought trees, including phenolic acid compounds and quinate. When adding these metabolites as carbon and nitrogen sources to bacterial cultures of both bacterial species, 8 of 9 metabolites stimulated bacterial growth. Importantly, soil phosphorous bioavailability was maintained only in inoculated trees, mitigating drought-induced decrease in leaf phosphorus and iron. Our observations of increased root exudation rate when drought and inoculation regimes were combined, support the idea of root recruitment of beneficial bacteria, especially under water stress.

Data availability

Data Sharing DeclarationAll data related to the study are reported in the manuscript and Supplementary Information. Source Data files 1-6 are included in the submission.

Article and author information

Author details

  1. Yaara Oppenheimer-Shaanan

    Department of Plant and Environmental Sciences, Weizmann Institute of Science, Rehovot, Israel
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-7005-3074
  2. Gilad Jakoby

    Department of Plant and Environmental Sciences, Weizmann Institute of Science, Rehovot, Israel
    Competing interests
    The authors declare that no competing interests exist.
  3. Maya L Starr

    Department of Plant and Environmental Sciences, Weizmann Institute of Science, Rehovot, Israel
    Competing interests
    The authors declare that no competing interests exist.
  4. Romiel Karliner

    Department of Plant and Environmental Sciences, Weizmann Institute of Science, Rehovot, Israel
    Competing interests
    The authors declare that no competing interests exist.
  5. Gal Eilon

    Department of Plant and Environmental Sciences, Weizmann Institute of Science, Rehovot, Israel
    Competing interests
    The authors declare that no competing interests exist.
  6. Maxim Itkin

    Department of Plant and Environmental Sciences, Weizmann Institute of Science, Rehovot, Israel
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0003-1348-2814
  7. Sergey Malitsky

    Department of Plant and Environmental Sciences, Weizmann Institute of Science, Rehovot, Israel
    Competing interests
    The authors declare that no competing interests exist.
  8. Tamir Klein

    Department of Plant and Environmental Sciences, Weizmann Institute of Science, Rehovot, Israel
    For correspondence
    tamir.klein@weizmann.ac.il
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-3882-8845

Funding

Edith and Natan Goldenberg Career Development Chair

  • Tamir Klein

Mary and Tom Beck (Canadian Center for Alternative Energy Research)

  • Tamir Klein

Larson Charitable Foundation New Scientist Fund

  • Tamir Klein

Angel mFaivovich Foundation for Ecological Research

  • Tamir Klein

Yotam project

  • Tamir Klein

Dana and Yossie Hollander

  • Tamir Klein

Estate of Emile Mimran

  • Tamir Klein

Estate of Helen Nichunsky

  • Tamir Klein

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

Reviewing Editor

  1. Meredith C Schuman, University of Zurich, Switzerland

Version history

  1. Preprint posted: August 25, 2021 (view preprint)
  2. Received: April 22, 2022
  3. Accepted: July 17, 2022
  4. Accepted Manuscript published: July 20, 2022 (version 1)
  5. Version of Record published: August 17, 2022 (version 2)

Copyright

© 2022, Oppenheimer-Shaanan 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.

Metrics

  • 2,145
    views
  • 541
    downloads
  • 21
    citations

Views, downloads and citations are aggregated across all versions of this paper published by eLife.

Download links

A two-part list of links to download the article, or parts of the article, in various formats.

Downloads (link to download the article as PDF)

Open citations (links to open the citations from this article in various online reference manager services)

Cite this article (links to download the citations from this article in formats compatible with various reference manager tools)

  1. Yaara Oppenheimer-Shaanan
  2. Gilad Jakoby
  3. Maya L Starr
  4. Romiel Karliner
  5. Gal Eilon
  6. Maxim Itkin
  7. Sergey Malitsky
  8. Tamir Klein
(2022)
A dynamic rhizosphere interplay between tree roots and soil bacteria under drought stress
eLife 11:e79679.
https://doi.org/10.7554/eLife.79679

Share this article

https://doi.org/10.7554/eLife.79679

Further reading

    1. Computational and Systems Biology
    2. Ecology
    Kazushi Tsutsui, Ryoya Tanaka ... Keisuke Fujii
    Research Article

    Collaborative hunting, in which predators play different and complementary roles to capture prey, has been traditionally believed to be an advanced hunting strategy requiring large brains that involve high-level cognition. However, recent findings that collaborative hunting has also been documented in smaller-brained vertebrates have placed this previous belief under strain. Here, using computational multi-agent simulations based on deep reinforcement learning, we demonstrate that decisions underlying collaborative hunts do not necessarily rely on sophisticated cognitive processes. We found that apparently elaborate coordination can be achieved through a relatively simple decision process of mapping between states and actions related to distance-dependent internal representations formed by prior experience. Furthermore, we confirmed that this decision rule of predators is robust against unknown prey controlled by humans. Our computational ecological results emphasize that collaborative hunting can emerge in various intra- and inter-specific interactions in nature, and provide insights into the evolution of sociality.

    1. Ecology
    2. Evolutionary Biology
    Théo Constant, F Stephen Dobson ... Sylvain Giroud
    Research Article

    Seasonal animal dormancy is widely interpreted as a physiological response for surviving energetic challenges during the harshest times of the year (the physiological constraint hypothesis). However, there are other mutually non-exclusive hypotheses to explain the timing of animal dormancy, that is, entry into and emergence from hibernation (i.e. dormancy phenology). Survival advantages of dormancy that have been proposed are reduced risks of predation and competition (the ‘life-history’ hypothesis), but comparative tests across animal species are few. Using the phylogenetic comparative method applied to more than 20 hibernating mammalian species, we found support for both hypotheses as explanations for the phenology of dormancy. In accordance with the life-history hypotheses, sex differences in hibernation emergence and immergence were favored by the sex difference in reproductive effort. In addition, physiological constraint may influence the trade-off between survival and reproduction such that low temperatures and precipitation, as well as smaller body mass, influence sex differences in phenology. We also compiled initial evidence that ectotherm dormancy may be (1) less temperature dependent than previously thought and (2) associated with trade-offs consistent with the life-history hypothesis. Thus, dormancy during non-life-threatening periods that are unfavorable for reproduction may be more widespread than previously thought.