Journal
PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA
Volume 116, Issue 11, Pages 5015-5020Publisher
NATL ACAD SCIENCES
DOI: 10.1073/pnas.1812092116
Keywords
comparative genomics; water stress; green plant evolution; signal transduction; stomata
Categories
Funding
- Australian Research Council [DE1401011143, CE140100008, DP150104007]
- National Natural Science Foundation of China [31571578, 31620103912]
- University of Florida Genetics Institute
- UK Biotechnology and Biological Sciences Research Council
- BBSRC [BB/F001630/1, BB/L001276/1, BB/N01832X/1, BB/M001601/1, BB/D001528/1, BB/F001673/1, BB/K015893/1, BB/M01133X/1, BB/H024867/1, BB/N006909/1, BB/L019205/1, BB/I024496/1, BB/H009817/1, BB/P011586/1] Funding Source: UKRI
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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.
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