Temporal network analysis identifies early physiological and transcriptomic indicators of mild drought in Brassica rapa

  1. Kathleen Greenham  Is a corresponding author
  2. Carmela Rosaria Guadagno  Is a corresponding author
  3. Malia A Gehan
  4. Todd C Mockler
  5. Cynthia Weinig  Is a corresponding author
  6. Brent E Ewers
  7. C. Robertson McClung  Is a corresponding author
  1. Dartmouth College, United States
  2. University of Wyoming, United States
  3. Donald Danforth Plant Science Center, United States

Abstract

The dynamics of local climates make development of agricultural strategies challenging. Yield improvement has progressed slowly, especially in drought-prone regions where annual crop production suffers from episodic aridity. Underlying drought responses are circadian and diel control of gene expression that regulate daily variations in metabolic and physiological pathways. To identify transcriptomic changes that occur in the crop Brassica rapa during initial perception of drought, we applied a co-expression network approach to associate rhythmic gene expression changes with physiological responses. Coupled analysis of transcriptome and physiological parameters over a two-day time course in control and drought-stressed plants provided temporal resolution necessary for correlation of network modules with dynamic changes in stomatal conductance, photosynthetic rate, and photosystem II efficiency. This approach enabled the identification of drought-responsive genes based on their differential rhythmic expression profiles in well-watered versus droughted networks and provided new insights into the dynamic physiological changes that occur during drought.

Data availability

The following data sets were generated

Article and author information

Author details

  1. Kathleen Greenham

    Department of Biological Sciences, Dartmouth College, Hanover, United States
    For correspondence
    kathleen.m.greenham@dartmouth.edu
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0001-7681-5263
  2. Carmela Rosaria Guadagno

    Department of Botany and Program in Ecology, University of Wyoming, Laramie, United States
    For correspondence
    cguadagn@uwyo.edu
    Competing interests
    The authors declare that no competing interests exist.
  3. Malia A Gehan

    Donald Danforth Plant Science Center, St. Louis, United States
    Competing interests
    The authors declare that no competing interests exist.
  4. Todd C Mockler

    Donald Danforth Plant Science Center, St. Louis, United States
    Competing interests
    The authors declare that no competing interests exist.
  5. Cynthia Weinig

    Department of Botany and program in Ecology, University of Wyoming, Laramie, United States
    For correspondence
    cweinig@uwyo.edu
    Competing interests
    The authors declare that no competing interests exist.
  6. Brent E Ewers

    Department of Botany and Program in Ecology, University of Wyoming, Laramie, United States
    Competing interests
    The authors declare that no competing interests exist.
  7. C. Robertson McClung

    Department of Biological Sciences, Dartmouth College, Hanover, United States
    For correspondence
    mcclung@dartmouth.edu
    Competing interests
    The authors declare that no competing interests exist.
    ORCID icon "This ORCID iD identifies the author of this article:" 0000-0002-7875-3614

Funding

National Science Foundation (IOS-1202779)

  • Kathleen Greenham

Rural Development Administration (SSAC PJ01106904)

  • C. Robertson McClung

National Science Foundation (IOS-1025965)

  • Todd C Mockler
  • Cynthia Weinig
  • Brent E Ewers
  • C. Robertson McClung

National Science Foundation (IOS-1547796)

  • Cynthia Weinig
  • Brent E Ewers
  • C. Robertson McClung

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

Copyright

© 2017, Greenham 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

  • 5,908
    views
  • 1,035
    downloads
  • 93
    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. Kathleen Greenham
  2. Carmela Rosaria Guadagno
  3. Malia A Gehan
  4. Todd C Mockler
  5. Cynthia Weinig
  6. Brent E Ewers
  7. C. Robertson McClung
(2017)
Temporal network analysis identifies early physiological and transcriptomic indicators of mild drought in Brassica rapa
eLife 6:e29655.
https://doi.org/10.7554/eLife.29655

Share this article

https://doi.org/10.7554/eLife.29655

Further reading

    1. Plant Biology
    Zigmunds Orlovskis, Archana Singh ... Saskia A Hogenhout
    Research Article

    Obligate parasites often trigger significant changes in their hosts to facilitate transmission to new hosts. The molecular mechanisms behind these extended phenotypes - where genetic information of one organism is manifested as traits in another - remain largely unclear. This study explores the role of the virulence protein SAP54, produced by parasitic phytoplasmas, in attracting leafhopper vectors. SAP54 is responsible for the induction of leaf-like flowers in phytoplasma-infected plants. However, we previously demonstrated that the insects were attracted to leaves and the leaf-like flowers were not required. Here, we made the surprising discovery that leaf exposure to leafhopper males is required for the attraction phenotype, suggesting a leaf response that distinguishes leafhopper sex in the presence of SAP54. In contrast, this phytoplasma effector alongside leafhopper females discourages further female colonization. We demonstrate that SAP54 effectively suppresses biotic stress response pathways in leaves exposed to the males. Critically, the host plant MADS-box transcription factor short vegetative phase (SVP) emerges as a key element in the female leafhopper preference for plants exposed to males, with SAP54 promoting the degradation of SVP. This preference extends to female colonization of male-exposed svp null mutant plants over those not exposed to males. Our research underscores the dual role of the phytoplasma effector SAP54 in host development alteration and vector attraction - integral to the phytoplasma life cycle. Importantly, we clarify how SAP54, by targeting SVP, heightens leaf vulnerability to leafhopper males, thus facilitating female attraction and subsequent plant colonization by the insects. SAP54 essentially acts as a molecular ‘matchmaker’, helping male leafhoppers more easily locate mates by degrading SVP-containing complexes in leaves. This study not only provides insights into the long reach of single parasite genes in extended phenotypes, but also opens avenues for understanding how transcription factors that regulate plant developmental processes intersect with and influence plant-insect interactions.

    1. Microbiology and Infectious Disease
    2. Plant Biology
    Nyasha Charura, Ernesto Llamas ... Alga Zuccaro
    Research Article

    Programmed cell death occurring during plant development (dPCD) is a fundamental process integral for plant growth and reproduction. Here, we investigate the connection between developmentally controlled PCD and fungal accommodation in Arabidopsis thaliana roots, focusing on the root cap-specific transcription factor ANAC033/SOMBRERO (SMB) and the senescence-associated nuclease BFN1. Mutations of both dPCD regulators increase colonization by the beneficial fungus Serendipita indica, primarily in the differentiation zone. smb-3 mutants additionally exhibit hypercolonization around the meristematic zone and a delay of S. indica-induced root-growth promotion. This demonstrates that root cap dPCD and rapid post-mortem clearance of cellular corpses represent a physical defense mechanism restricting microbial invasion of the root. Additionally, reporter lines and transcriptional analysis revealed that BFN1 expression is downregulated during S. indica colonization in mature root epidermal cells, suggesting a transcriptional control mechanism that facilitates the accommodation of beneficial microbes in the roots.