Core cellular and tissue-specific mechanisms enable desiccation tolerance in Craterostigma

Robert VanBuren*, Ching Man Wai, Valentino Giarola, Milan Župunski, Jeremy Pardo, Michael Kalinowski, Guido Grossmann, Dorothea Bartels*

*Corresponding author for this work

Research output: Contribution to journalArticlepeer-review

12 Scopus citations

Abstract

Resurrection plants can survive prolonged life without water (anhydrobiosis) in regions with seasonal drying. This desiccation tolerance requires the coordination of numerous cellular processes across space and time, and individual plant tissues face unique constraints related to their function. Here, we analyzed the complex, octoploid genome of the model resurrection plant Craterostigma (C. plantagineum), and surveyed spatial and temporal expression dynamics to identify genetic elements underlying desiccation tolerance. Homeologous genes within the Craterostigma genome have divergent expression profiles, suggesting the subgenomes contribute differently to desiccation tolerance traits. The Craterostigma genome contains almost 200 tandemly duplicated early light-induced proteins, a hallmark trait of desiccation tolerance, with massive upregulation under water deficit. We identified a core network of desiccation-responsive genes across all tissues, but observed almost entirely unique expression dynamics in each tissue during recovery. Roots and leaves have differential responses related to light and photoprotection, autophagy and nutrient transport, reflecting their divergent functions. Our findings highlight a universal set of likely ancestral desiccation tolerance mechanisms to protect cellular macromolecules under anhydrobiosis, with secondary adaptations related to tissue function.

Original languageEnglish (US)
Pages (from-to)231-245
Number of pages15
JournalPlant Journal
Volume114
Issue number2
DOIs
StatePublished - Apr 2023

Funding

This work is supported by NSF Grant MCB-1817347 (to RV). MK was a participant in the Plant Genomics Research Experience for Undergraduates Program funded by NSF | BIO | Division of Biological Infrastructure (NSF-DBI 1358474). GG was supported by the German Research Foundation (DFG Heisenberg Professorship; grant # GR4559/4-1) and Germany's Excellence Strategy (CEPLAS-EXC-2048/1 project ID 390686111). The authors thank members of the Water and Life Interface Institute (WALII), supported by NSF DBI grant # 2213983, for helpful discussions. The authors declare no competing financial interests. This work is supported by NSF Grant MCB‐1817347 (to RV). MK was a participant in the Plant Genomics Research Experience for Undergraduates Program funded by NSF | BIO | Division of Biological Infrastructure (NSF‐DBI 1358474). GG was supported by the German Research Foundation (DFG Heisenberg Professorship; grant # GR4559/4‐1) and Germany's Excellence Strategy (CEPLAS‐EXC‐2048/1 project ID 390686111). The authors thank members of the Water and Life Interface Institute (WALII), supported by NSF DBI grant # 2213983, for helpful discussions. The authors declare no competing financial interests.

Keywords

  • comparative genomics
  • craterostigma
  • desiccation tolerance
  • gene co-expression

ASJC Scopus subject areas

  • Genetics
  • Plant Science
  • Cell Biology

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