Origins and Evolution of Stomatal Development

Abstract

The fossil record suggests stomata-like pores were present on the surfaces of land plants over 400 million years ago. Whether stomata arose once or whether they arose independently across newly evolving land plant lineages has long been a matter of debate. In Arabidopsis, a genetic toolbox has been identified that tightly controls stomatal development and patterning. This includes the basic helix-loop-helix (bHLH) transcription factors SPEECHLESS (SPCH), MUTE, FAMA, and ICE/SCREAMs (SCRMs), which promote stomatal formation. These factors are regulated via a signaling cascade, which includes mobile EPIDERMAL PATTERNING FACTOR (EPF) peptides to enforce stomatal spacing. Mosses and hornworts, the most ancient extant lineages to possess stomata, possess orthologs of these Arabidopsis (Arabidopsis thaliana) stomatal toolbox genes, and manipulation in the model bryophyte Physcomitrella patens has shown that the bHLH and EPF components are also required for moss stomatal development and patterning. This supports an ancient and tightly conserved genetic origin of stomata. Here, we review recent discoveries and, by interrogating newly available plant genomes, we advance the story of stomatal development and patterning across land plant evolution. Furthermore, we identify potential orthologs of the key toolbox genes in a hornwort, further supporting a single ancient genetic origin of stomata in the ancestor to all stomatous land plants.

Diurnal Variation in Gas Exchange: The Balance between Carbon Fixation and Water Loss

“…However, it is less well established that considerable heterogeneity exists in stomatal characters and function over the leaf lamina. Stomatal density over the leaf lamina is determined by both cell differentiation and cell expansion (Poole et al, 1996(Poole et al, , 2000Lawson et al, 2002); however, stomatal spacing generally follows the basic one-cell spacing rule that results in stomata being separated by at least one epidermal cell (Geisler et al, 2000;Chater et al, 2017;Torii and Bergmann, 2017) to ensure proper guard cell function (Sachs, 2005). Spatial patterns of stomatal density have been illustrated in a number of different species (Smith et al, 1989;Poole et al, 1996;Lawson and Weyers, 1999), and the influence of environmental conditions on such patterning has been reported (Croxdale, 2000;Poole et al, 2000).…”

Small Pores with a Big Impact

“…We dedicate this Focus Issue to the memory of Fred Sack (Bergmann et al, 2017), whose pioneering studies of mutants in stomatal development, as well as his infectious humor and generosity, formed the cornerstone of much research that has followed over the past two decades. The Update review by Chater et al (2017) touches on some of the most recent developments on this topic. As an example of how this knowledge may be applied, again we point the reader to the research article by Hughes et al (2017).…”

<div class="page" title="Page 1"><div class="layoutArea"><div class="column">Structure, function and evolution of stomata from a bryological perspective</div></div></div>

“…Independent evolution or re-evolution of a structure has been documented in other organisms (Collin & Miglietta 2008). For stomata, this scenario seems unlikely due to similarities in development, guard cell architecture, anatomy of surrounding tissue, and shared stomata-related genes (Chater et al 2017). If stomata are homologous, there is also a possibility that those in bryophytes are highly derived and have lost the physiological functions attributed to tracheophyte stomata.…”

“…Reminiscent of stomata in true mosses that are also operculate, this restriction to the lower capsule region could be interpreted as plesiomorphic in mosses. A search of the draft genome of Sphagnum could not clearly identify stomata related genes (Chater et al 2017). Clarification of the homology of pseudostomata and bryophyte stomata may require transcriptomic studies integrated with physiological and structural data.…”

“…Key regulatory elements SCREAM and SMF (SPEACHLESS, MUTE, FAMA), signaling peptides and membrane receptors (EPF, TMM, ERECTA) are known to be present and involved in stomatal development in the moss Physcomitrella (MacAlister & Bergmann 2011, Cain et al 2016, Chater et al 2017. Othologs of these genes have been recently identified in the genome of Anthoceros (Chater et al 2017) Microscopic observations of other mosses and hornworts also point to regular separation of stomata ( Fig. 2), but some exceptions are perplexing such as Polytrichum where stomata are clustered in the apophysis and so close to each other that opening of the pore seems unlikely (Fig.…”