Origin and function of stomata in the moss Physcomitrella patens

Abstract

Stomata are microscopic valves on plant surfaces that originated over 400 million years ago and facilitated the greening of Earth’s continents by permitting efficient shoot-atmosphere gas exchange and plant hydration1. However, the core genetic machinery regulating stomatal development in non-vascular land plants is poorly understood2–4 and their function has remained a matter of debate for a century5. Here, we show that genes encoding the two basic helix-loop-helix proteins PpSMF1 and PpSCRM1 in the moss Physcomitrella patens are orthologous to transcriptional regulators of stomatal development in the flowering plant Arabidopsis thaliana and essential for stomata formation in moss. Targeted knock-out P. patens mutants lacking either PpSMF1 or PpSCRM1 develop gametophytes indistinguishable from wild-type plants but mutant sporophytes lacking stomata. Protein-protein interaction assays reveal heterodimerisation between PpSMF1 and PpSCRM1 which, together with moss-angiosperm gene complementations6, suggests deep functional conservation of the heterodimeric SMF1 and SCRM1 unit required to activate transcription for moss stomatal development, as in A. thaliana7. Moreover, stomata-less sporophytes of ΔPpSMF1 and ΔPpSCRM1 mutants exhibited delayed dehiscence, implying stomata might have promoted dehiscence in the first complex land plant sporophytes.

Evolution of the Stomatal Regulation of Plant Water Content

“…Evidence of highly conserved stomatal developmental genetics among land plants (Vatén and Bergmann, 2012;Caine et al, 2016) appears to support the long-held notion of conserved stomatal function (Haberlandt, 1886;Paton and Pearce, 1957;Ziegler, 1987;Chater et al, 2011). However, a recent combination of molecular and whole plant experiments by Chater et al (2016) suggests a divergent functional role for stomata in bryophytes. All that is required to transform the function of guard cells from passive to functionally ABA sensitive is the relocation or concentration of an ancestral and highly conserved ABA signaling pathway into the guard cells .…”

“…If the function of the earliest stomata was the same as in vascular plants, facilitating the dynamic optimization of water use against carbon gain (Cowan, 1977), then common elements of the stomatal control process likely evolved with these first stomata. This angiosperm-centric hypothesis has been long held as the best explanation for stomatal evolution (Haberlandt, 1886;Paton and Pearce, 1957;Ziegler, 1987;Chater et al, 2011), but has been recently challenged by key differences in the general behavior and apparent role of early stomata as well as recent molecular and physiological evidence indicating a highly divergent functional role for stomata in these most basal stomatabearing land plants (Haig, 2013;Pressel et al, 2014;Field et al, 2015;Chater et al, 2016;Renzaglia et al, 2017).…”

Origins and Evolution of Stomatal Development

“…Our thinking is inevitably pigeon-holed, however, because Arabidopsis is a dicot angiosperm of the Brassicaceae family, and the caveat remains that apparent "deviations" from what we observe in Arabidopsis stomata may turn out to be more appropriate models for land plants as a whole. Nevertheless, several recent stomatal evolution studies strongly support Arabidopsis's continuing role in informing our thinking Chater et al, 2016;Raissig et al, 2016Raissig et al, , 2017 Figure 1. The evolution and origin of stomata in land plants.…”

Stomatal Function across Temporal and Spatial Scales: Deep-Time Trends, Land-Atmosphere Coupling and Global Models

“…Stomata first appeared more than 410 million years ago in rudimentary terrestrial plants Raven, 2002;Chater et al, 2016). From then on, they have significantly influenced the fluxes of carbon, water, and energy at the land surface (Berry et al, 2010).…”