Abstract

Significance Plant stomata are produced through divisions and differentiation of stem cells, termed meristemoids. During stomatal development, we see diverse patterns of meristemoid behavior among land plant lineages. However, both the ecological significance and the diversification processes of this diversity remain mostly unknown. Here we report that the ecologically diverse genus Callitriche shows unprecedented intrageneric diversity in meristemoid behavior. While meristemoids in terrestrial species of Callitriche undergo a series of asymmetric divisions before differentiation, those in amphibious species skip the divisions and directly differentiate into stomata. The simple shift in the expression times of two key transcription factors underlies these different patterns. This study provides important insights into the evolution and ecological significance of stomatal patterning.

Highlights

  • Stomata, the gas exchange structures of plants, are formed by the division and differentiation of stem cells, or meristemoids

  • C. japonica belongs to the ancestral clade, while C. terrestris is a more derived species that is phylogenetically closest to C. palustris among the three newly analyzed species [26, 27] (Fig. 2A)

  • As reported previously, stomatal development in C. palustris occurred in restricted development phases (∼500 to 1,000 μm leaf primordium length), and that this was the case in another amphibious species, C. stagnalis

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Summary

Introduction

The gas exchange structures of plants, are formed by the division and differentiation of stem cells, or meristemoids. This plasticity in stomatal development has long been known for amphibious species from broad lineages [19,20,21,22], the molecular basis is still largely unexplored To investigate this phenomenon, we previously described the process of leaf and stomatal development in the amphibious plant Callitriche palustris L. under highly reproducible conditions [23]. The transcription factor FAMA regulates the symmetric division of a GMC to produce a pair of GCs [1] These key transcription factors, collectively termed SMF (SPCH/ MUTE/FAMA) proteins, form a single clade in the bHLH family and are broadly conserved in land plant lineages [4, 5]. Recent studies have shown that SMF orthologs have conserved functions in the stomatal development of other model land plant species, such as rice [6], maize [6, 7], Brachypodium distachyon [8, 9], tomato [10], and Physcomitrium patens [11]

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