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.

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

  • 2,779
    views
  • 652
    downloads
  • 32
    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. Ecology
    Luis Abdala-Roberts, Adriana Puentes ... Kailen A Mooney
    Review Article

    Global change is causing unprecedented degradation of the Earth’s biological systems and thus undermining human prosperity. Past practices have focused either on monitoring biodiversity decline or mitigating ecosystem services degradation. Missing, but critically needed, are management approaches that monitor and restore species interaction networks, thus bridging existing practices. Our overall aim here is to lay the foundations of a framework for developing network management, defined here as the study, monitoring, and management of species interaction networks. We review theory and empirical evidence demonstrating the importance of species interaction networks for the provisioning of ecosystem services, how human impacts on those networks lead to network rewiring that underlies ecosystem service degradation, and then turn to case studies showing how network management has effectively mitigated such effects or aided in network restoration. We also examine how emerging technologies for data acquisition and analysis are providing new opportunities for monitoring species interactions and discuss the opportunities and challenges of developing effective network management. In summary, we propose that network management provides key mechanistic knowledge on ecosystem degradation that links species- to ecosystem-level responses to global change, and that emerging technological tools offer the opportunity to accelerate its widespread adoption.

    1. Ecology
    2. Evolutionary Biology
    Vendula Bohlen Šlechtová, Tomáš Dvořák ... Joerg Bohlen
    Research Article

    Eurasia has undergone substantial tectonic, geological, and climatic changes throughout the Cenozoic, primarily associated with tectonic plate collisions and a global cooling trend. The evolution of present-day biodiversity unfolded in this dynamic environment, characterised by intricate interactions of abiotic factors. However, comprehensive, large-scale reconstructions illustrating the extent of these influences are lacking. We reconstructed the evolutionary history of the freshwater fish family Nemacheilidae across Eurasia and spanning most of the Cenozoic on the base of 471 specimens representing 279 species and 37 genera plus outgroup samples. Molecular phylogeny using six genes uncovered six major clades within the family, along with numerous unresolved taxonomic issues. Dating of cladogenetic events and ancestral range estimation traced the origin of Nemacheilidae to Indochina around 48 mya. Subsequently, one branch of Nemacheilidae colonised eastern, central, and northern Asia, as well as Europe, while another branch expanded into the Burmese region, the Indian subcontinent, the Near East, and northeast Africa. These expansions were facilitated by tectonic connections, favourable climatic conditions, and orogenic processes. Conversely, aridification emerged as the primary cause of extinction events. Our study marks the first comprehensive reconstruction of the evolution of Eurasian freshwater biodiversity on a continental scale and across deep geological time.