Evolution of chloroplast retrograde signaling facilitates green plant adaptation to land

Chenchen Zhao, Yuanyuan Wang, Kai Xun Chan, D. Blaine Marchant, Peter J. Franks, David Randall, Estee E. Tee, Guang Chen, Sunita Ramesh, Su Yin Phua, Ben Zhang, Adrian Hills, Fei Dai, Dawei Xue, Matthew Gilliham, Steve Tyerman, Eviatar Nevo, Feibo Wu, Guoping Zhang, Gane K.-S. WongJames H. Leebens-Mack, Michael Melkonian, Michael R. Blatt, Pamela S. Soltis, Douglas E. Soltis, Barry J. Pogson, Zhong-Hua Chen

Research output: Contribution to journalArticlepeer-review

45 Citations (Scopus)

Abstract

Chloroplast retrograde signaling networks are vital for chloroplast biogenesis, operation, and signaling, including excess light and drought stress signaling. To date, retrograde signaling has been considered in the context of land plant adaptation, but not regarding the origin and evolution of signaling cascades linking chloroplast function to stomatal regulation. We show that key elements of the chloroplast retrograde signaling process, the nucleotide phosphatase (SAL1) and 3'-phosphoadenosine-5'-phosphate (PAP) metabolism, evolved in streptophyte algae-the algal ancestors of land plants. We discover an early evolution of SAL1-PAP chloroplast retrograde signaling in stomatal regulation based on conserved gene and protein structure, function, and enzyme activity and transit peptides of SAL1s in species including flowering plants, the fern Ceratopteris richardii, and the moss Physcomitrella patens. Moreover, we demonstrate that PAP regulates stomatal closure via secondary messengers and ion transport in guard cells of these diverse lineages. The origin of stomata facilitated gas exchange in the earliest land plants. Our findings suggest that the conquest of land by plants was enabled by rapid response to drought stress through the deployment of an ancestral SAL1-PAP signaling pathway, intersecting with the core abscisic acid signaling in stomatal guard cells.

Original languageEnglish
Pages (from-to)5015-5020
Number of pages6
JournalProceedings of the National Academy of Sciences of the United States of America
Volume116
Issue number11
DOIs
Publication statusPublished - 25 Feb 2019
Externally publishedYes

Bibliographical note

This open access article is distributed under Creative Commons Attribution-NonCommercial-NoDerivatives License 4.0 (CC BY-NC-ND).

Keywords

  • Comparative genomics
  • Green plant evolution
  • Signal transduction
  • Stomata
  • Water stress

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