Journal Article

Evolution of chloroplast retrograde signaling facilitates green plant adaptation to land

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

2019

Overview

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.

• Publisher: National Academy of Sciences
• Subject: Abscisic acid / Adaptation / Adaptation, Physiological / Adenosine Diphosphate / Algae / Biological Evolution / Biological Sciences / Cascades / Ceratopteris richardii / Chloroplasts / Chloroplasts - metabolism / Drought / Embryophyta - physiology / Enzymatic activity / Enzyme activity / Evolution / Ferns / Flowering / Flowering plants / Gas exchange / Gene expression / Guard cells / Hydrogen Peroxide - metabolism / Ion Transport / Metabolism / Movement / Nitric Oxide - metabolism / Peptides / Phylogeny / Physcomitrella patens / Plant Stomata - physiology / Plants (botany) / Protein structure / Proteins / Retrograde transport / Signal Transduction / Signaling / Stomata / Structure-function relationships / Viridiplantae - physiology