Evolutionary conservation of ABA signaling for stomatal closure

Shengguan Cai, Guang Chen, Yuanyuan Wang, Yuqing Huang, D. Blaine Marchant, Yizhou Wang, Qian Yang, Fei Dai, Adrian Hills, Peter J. Franks, Eviatar Nevo, Douglas E. Soltis, Pamela S. Soltis, Emily Sessa, Paul G. Wolf, Dawei Xue, Guoping Zhang, Barry J. Pogson, Michael R. Blatt, Zhong Hua Chen

Research output: Contribution to journalArticlepeer-review

Abstract

Abscisic acid (ABA)-driven stomatal regulation reportedly evolved after the divergence of ferns, during the early evolution of seed plants approximately 360 million years ago. This hypothesis is based on the observation that the stomata of certain fern species are unresponsive to ABA, but exhibit passive hydraulic control. However, ABA-induced stomatal closure was detected in some mosses and lycophytes. Here, we observed that a number of ABA signaling and membrane transporter protein families diversified over the evolutionary history of land plants. The aquatic ferns Azolla filiculoides and Salvinia cucullata have representatives of 23 families of proteins orthologous to those of Arabidopsis (Arabidopsis thaliana) and all other land plant species studied. Phylogenetic analysis of the key ABA signaling proteins indicates an evolutionarily conserved stomatal response to ABA. Moreover, comparative transcriptomic analysis has identified a suite of ABAresponsive genes that differentially expressed in a terrestrial fern species, Polystichum proliferum. These genes encode proteins associated with ABA biosynthesis, transport, reception, transcription, signaling, and ion and sugar transport, which fit the general ABA signaling pathway constructed from Arabidopsis and Hordeum vulgare. The retention of these key ABA-responsive genes could have had a profound effect on the adaptation of ferns to dry conditions. Furthermore, stomatal assays have shown the primary evidence for ABA-induced closure of stomata in two terrestrial fern species P. proliferum and Nephrolepis exaltata. In summary, we report, to our knowledge, new molecular and physiological evidence for the presence of active stomatal control in ferns.

Original languageEnglish
Pages (from-to)732-747
Number of pages16
JournalPlant Physiology
Volume174
Issue number2
DOIs
StatePublished - Jun 2017

Bibliographical note

Funding Information:
This work was funded by the National Natural Science Foundation of China (grants nos. 31571578 and 31620103912), the Chinese 1000-Plan Project, the Fundamental Research Funds for the Central Universities, the Australian Research Council Discovery Projects and Discovery Early Career Researcher Award Programs (grant no. DE1401011143), the UK Biotechnology and Biological Sciences Research Council, and the University of Florida Genetics Institute.

Publisher Copyright:
© 2017 American Society of Plant Biologists. All Rights Reserved.

ASJC Scopus subject areas

  • Physiology
  • Genetics
  • Plant Science

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