The origin and evolution of stomata

James W. Clark*, Brogan J. Harris, Alexander J. Hetherington, Natalia Hurtado-Castano, Robert A. Brench, Stuart Casson, Tom A. Williams, Julie E. Gray, Alistair M. Hetherington

*Corresponding author for this work

Research output: Contribution to journalReview article (Academic Journal)peer-review

30 Citations (Scopus)

Abstract

The acquisition of stomata is one of the key innovations that led to the colonisation of the terrestrial environment by the earliest land plants. However, our understanding of the origin, evolution and the ancestral function of stomata is incomplete. Phylogenomic analyses indicate that, firstly, stomata are ancient structures, present in the common ancestor of land plants, prior to the divergence of bryophytes and tracheophytes and, secondly, there has been reductive stomatal evolution, especially in the bryophytes (with complete loss in the liverworts). From a review of the evidence, we conclude that the capacity of stomata to open and close in response to signals such as ABA, CO2 and light (hydroactive movement) is an ancestral state, is present in all lineages and likely predates the divergence of the bryophytes and tracheophytes. We reject the hypothesis that hydroactive movement was acquired with the emergence of the gymnosperms. We also conclude that the role of stomata in the earliest land plants was to optimise carbon gain per unit water loss. There remain many other unanswered questions concerning the evolution and especially the origin of stomata. To address these questions, it will be necessary to: find more fossils representing the earliest land plants, revisit the existing early land plant fossil record in the light of novel phylogenomic hypotheses and carry out more functional studies that include both tracheophytes and bryophytes.

Original languageEnglish
Pages (from-to)R539-R553
JournalCurrent Biology
Volume32
Issue number11
DOIs
Publication statusPublished - 6 Jun 2022

Bibliographical note

Funding Information:
The authors wish to acknowledge support from the Leverhulme trust (RPG-2019-004). B.J.H. and R.A.B. are grateful, respectively, to the New Phytol. Foundation and the UK BBSRC (BB/M011151/1) for the award of postgraduate studentships. T.A.W. and J.E.G. are supported by Royal Society University Research and Leverhulme Trust Senior Research Fellowships (URF/R/201024 and SRF∖R1∖21000149). A.J.H. was funded by a UK Research and Innovation Future Leaders Fellowship (MR/T018585/1). The authors are grateful to three anonymous reviewers who provided constructive and authoritative comments during the peer review process.

Funding Information:
The authors wish to acknowledge support from the Leverhulme trust (RPG-2019-004). B.J.H. and R.A.B. are grateful, respectively, to the New Phytol. Foundation and the UK BBSRC (BB/M011151/1) for the award of postgraduate studentships. T.A.W. and J.E.G. are supported by Royal Society University Research and Leverhulme Trust Senior Research Fellowships (URF/R/201024 and SRF∖R1∖21000149). A.J.H. was funded by a UK Research and Innovation Future Leaders Fellowship (MR/T018585/1). The authors are grateful to three anonymous reviewers who provided constructive and authoritative comments during the peer review process. The authors declare no competing interests.

Publisher Copyright:
© 2022 Elsevier Inc.

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