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Evolutionarily conserved hierarchical gene regulatory networks for plant salt stress response

Nature Plants volume 7, pages 787–799 (2021)Cite this article

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Abstract

Plant cells constantly alter their gene expression profiles to respond to environmental fluctuations. These continuous adjustments are regulated by multi-hierarchical networks of transcription factors. To understand how such gene regulatory networks (GRNs) have stabilized evolutionarily while allowing for species-specific responses, we compare the GRNs underlying salt response in the early-diverging and late-diverging plants Marchantia polymorpha and Arabidopsis thaliana. Salt-responsive GRNs, constructed on the basis of the temporal transcriptional patterns in the two species, share common trans-regulators but exhibit an evolutionary divergence in cis-regulatory sequences and in the overall network sizes. In both species, WRKY-family transcription factors and their feedback loops serve as central nodes in salt-responsive GRNs. The divergent cis-regulatory sequences of WRKY-target genes are probably associated with the expansion in network size, linking salt stress to tissue-specific developmental and physiological responses. The WRKY modules and highly linked WRKY feedback loops have been preserved widely in other plants, including rice, while keeping their binding-motif sequences mutable. Together, the conserved trans-regulators and the quickly evolving cis-regulatory sequences allow salt-responsive GRNs to adapt over a long evolutionary timescale while maintaining some consistent regulatory structure. This strategy may benefit plants as they adapt to changing environments.

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Fig. 1: Temporal dynamics of M. polymorpha and A. thaliana transcriptome during salt treatment.
Fig. 2: Gene regulatory networks of salt-responsive transcriptional modulators.
Fig. 3: Salt-response phenotypes of WRKY knockout mutants in M. polymorpha and A. thaliana.
Fig. 4: Distinct pCREs for salt-response genes in Arabidopsis and M. polymorpha.
Fig. 5: Hierarchical regulation of WRKYs in M. polymorpha.
Fig. 6: WRKY-regulatory modes in different plant species.

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Data availability

All experimental data, transcriptome data, R codes and genetic materials presented in this study are available on request. All transcriptome datasets collected in this study are openly available in the NCBI GEO repository (GSE153103, https://www.ncbi.nlm.nih.gov/geo/).

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Acknowledgements

This work was financially supported by the Singapore-MIT Alliance for Research and Technology Program (SMART) and by Industry Alignment Fund—Prepositioning Program (IAF-PP).

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Authors and Affiliations

  1. Temasek Life Sciences Laboratory, National University of Singapore, Singapore, Singapore

    Ting-Ying Wu, HonZhen Goh, Shalini Krishnamoorthi & Daisuke Urano

  2. Department of Plant Biology, Michigan State University, East Lansing, MI, USA

    Christina B. Azodi

  3. Biotechnology Center in Southern Taiwan, Academia Sinica, Tainan, Taiwan

    Ming-Jung Liu

  4. Agricultural Biotechnology Research Center, Academia Sinica, Taipei, Taiwan

    Ming-Jung Liu

  5. Department of Biological Sciences, National University of Singapore, Singapore, Singapore

    Daisuke Urano

  6. Singapore-MIT Alliance for Research and Technology, Singapore, Singapore

    Daisuke Urano

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Contributions

T.Y.W. led the project design, the data collection and interpretation and the drafting of manuscript. C.A. and M.J.L. performed cis-regulatory element analysis and wrote the manuscript. D.U. conceived the project and wrote the manuscript. H.G. and S.K. prepared genetic mutants and collected experimental data. All authors contributed to finalizing the manuscript.

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Correspondence to Ting-Ying Wu or Daisuke Urano.

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Supplementary Information

Supplementary Figs. 1–14.

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Supplementary Data 1

Supporting dataset for A. thaliana.

Supplementary Data 2

Supporting dataset for M. polymorpha.

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Wu, TY., Goh, H., Azodi, C.B. et al. Evolutionarily conserved hierarchical gene regulatory networks for plant salt stress response. Nat. Plants 7, 787–799 (2021). https://doi.org/10.1038/s41477-021-00929-7

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