Zhao, Chenchen, Wang, Yuanyuan, Chan, Kai Xun ORCID: 0000-0003-3554-7228, Marchant, D. Blaine, Franks, Peter J., Randall, David, Tee, Estee E., Chen, Guang, Ramesh, Sunita ORCID: 0000-0003-2230-4737, Phua, Su Yin, Zhang, Ben, Hills, Adrian, Dai, Fei, Xue, Dawei ORCID: 0000-0001-9904-7615, Gilliham, Matthew ORCID: 0000-0003-0666-3078, Tyerman, Steve, Nevo, Eviatar, Wu, Feibo ORCID: 0000-0001-8797-3398, Zhang, Guoping, Wong, Gane K. -S., Leebens-Mack, James H., Melkonian, Michael, Blatt, Michael R., Soltis, Pamela S., Soltis, Douglas E., Pogson, Barry J. and Chen, Zhong-Hua ORCID: 0000-0002-7531-320X (2019). Evolution of chloroplast retrograde signaling facilitates green plant adaptation to land. Proc. Natl. Acad. Sci. U. S. A., 116 (11). S. 5015 - 5021. WASHINGTON: NATL ACAD SCIENCES. ISSN 0027-8424

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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: Journal Article
Creators:
CreatorsEmailORCIDORCID Put Code
Zhao, ChenchenUNSPECIFIEDUNSPECIFIEDUNSPECIFIED
Wang, YuanyuanUNSPECIFIEDUNSPECIFIEDUNSPECIFIED
Chan, Kai XunUNSPECIFIEDorcid.org/0000-0003-3554-7228UNSPECIFIED
Marchant, D. BlaineUNSPECIFIEDUNSPECIFIEDUNSPECIFIED
Franks, Peter J.UNSPECIFIEDUNSPECIFIEDUNSPECIFIED
Randall, DavidUNSPECIFIEDUNSPECIFIEDUNSPECIFIED
Tee, Estee E.UNSPECIFIEDUNSPECIFIEDUNSPECIFIED
Chen, GuangUNSPECIFIEDUNSPECIFIEDUNSPECIFIED
Ramesh, SunitaUNSPECIFIEDorcid.org/0000-0003-2230-4737UNSPECIFIED
Phua, Su YinUNSPECIFIEDUNSPECIFIEDUNSPECIFIED
Zhang, BenUNSPECIFIEDUNSPECIFIEDUNSPECIFIED
Hills, AdrianUNSPECIFIEDUNSPECIFIEDUNSPECIFIED
Dai, FeiUNSPECIFIEDUNSPECIFIEDUNSPECIFIED
Xue, DaweiUNSPECIFIEDorcid.org/0000-0001-9904-7615UNSPECIFIED
Gilliham, MatthewUNSPECIFIEDorcid.org/0000-0003-0666-3078UNSPECIFIED
Tyerman, SteveUNSPECIFIEDUNSPECIFIEDUNSPECIFIED
Nevo, EviatarUNSPECIFIEDUNSPECIFIEDUNSPECIFIED
Wu, FeiboUNSPECIFIEDorcid.org/0000-0001-8797-3398UNSPECIFIED
Zhang, GuopingUNSPECIFIEDUNSPECIFIEDUNSPECIFIED
Wong, Gane K. -S.UNSPECIFIEDUNSPECIFIEDUNSPECIFIED
Leebens-Mack, James H.UNSPECIFIEDUNSPECIFIEDUNSPECIFIED
Melkonian, MichaelUNSPECIFIEDUNSPECIFIEDUNSPECIFIED
Blatt, Michael R.UNSPECIFIEDUNSPECIFIEDUNSPECIFIED
Soltis, Pamela S.UNSPECIFIEDUNSPECIFIEDUNSPECIFIED
Soltis, Douglas E.UNSPECIFIEDUNSPECIFIEDUNSPECIFIED
Pogson, Barry J.UNSPECIFIEDUNSPECIFIEDUNSPECIFIED
Chen, Zhong-HuaUNSPECIFIEDorcid.org/0000-0002-7531-320XUNSPECIFIED
URN: urn:nbn:de:hbz:38-153921
DOI: 10.1073/pnas.1812092116
Journal or Publication Title: Proc. Natl. Acad. Sci. U. S. A.
Volume: 116
Number: 11
Page Range: S. 5015 - 5021
Date: 2019
Publisher: NATL ACAD SCIENCES
Place of Publication: WASHINGTON
ISSN: 0027-8424
Language: English
Faculty: Unspecified
Divisions: Unspecified
Subjects: no entry
Uncontrolled Keywords:
KeywordsLanguage
NEGATIVE REGULATOR; TRANSIT PEPTIDES; ABSCISIC-ACID; GUARD-CELL; HIGH LIGHT; DROUGHT; ORIGIN; TOLERANCE; REVEALS; STRESSMultiple languages
Multidisciplinary SciencesMultiple languages
Refereed: Yes
URI: http://kups.ub.uni-koeln.de/id/eprint/15392

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