Evolution of chloroplast retrograde signaling facilitates green plant adaptation to land

Zhao, C. et al. (2019) Evolution of chloroplast retrograde signaling facilitates green plant adaptation to land. Proceedings of the National Academy of Sciences of the United States of America, 116(11), pp. 5015-5020. (doi: 10.1073/pnas.1812092116) (PMID:30804180) (PMCID:PMC6421419)

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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.

Item Type:Articles
Keywords:Water stress, Signal transduction, Stomata, Comparative genomics, Green Plant Evolution
Status:Published
Refereed:Yes
Glasgow Author(s) Enlighten ID:Blatt, Professor Michael
Authors: Zhao, C., Wang, Y., Chan, K. X., Marchant, D. B., Franks, P. J., Randall, D., Tee, E. E., Chen, G., Ramesh, S., Phua, S. Y., Zhang, B., Hills, A., Dai, F., Xue, D., Gilliham, M., Tyerman, S., Nevo, E., Wu, F., Zhang, G., Wong, G. K.-S., Leebens-Mack, J. H., Melkonian, M., Blatt, M. R., Soltis, P. S., Soltis, D. E., Pogson, B. J., and Chen, Z.-H.
College/School:College of Medical Veterinary and Life Sciences > Institute of Molecular Cell and Systems Biology
Journal Name:Proceedings of the National Academy of Sciences of the United States of America
Publisher:National Academy of Sciences
ISSN:0027-8424
ISSN (Online):1091-6490
Copyright Holders:Copyright © 2019 The Authors
First Published:First published in PNAS 116(11):5015-5020
Publisher Policy:Reproduced under a Creative Commons License

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