An ancestral stomatal patterning module revealed in the non-vascular land plant Physcomitrella patens.

Robert S Caine,Julie E Gray,Andrew C Cuming,Caspar C Chater,David J Beerling,Yasuko Kamisugi,Andrew J Fleming

doi:10.1242/dev.135038

Robert S Caine, Julie E Gray + Show 5 more

Open Access

https://doi.org/10.1242/dev.135038

Copy DOI

Abstract

The patterning of stomata plays a vital role in plant development and has emerged as a paradigm for the role of peptide signals in the spatial control of cellular differentiation. Research in Arabidopsis has identified a series of epidermal patterning factors (EPFs), which interact with an array of membrane-localised receptors and associated proteins (encoded by ERECTA and TMM genes) to control stomatal density and distribution. However, although it is well-established that stomata arose very early in the evolution of land plants, until now it has been unclear whether the established angiosperm stomatal patterning system represented by the EPF/TMM/ERECTA module reflects a conserved, universal mechanism in the plant kingdom. Here, we use molecular genetics to show that the moss Physcomitrella patens has conserved homologues of angiosperm EPF, TMM and at least one ERECTA gene that function together to permit the correct patterning of stomata and that, moreover, elements of the module retain function when transferred to Arabidopsis. Our data characterise the stomatal patterning system in an evolutionarily distinct branch of plants and support the hypothesis that the EPF/TMM/ERECTA module represents an ancient patterning system.

Highlights

Stomata are microscopic pores present in the epidermis of all angiosperms and the majority of ferns and bryophytes
We show that P. patens has an epidermal patterning factors (EPFs)/TOO MANY MOUTHS (TMM)/ ERECTA module required for stomatal patterning fundamentally similar to that found in angiosperms and that elements of the module retain function when transferred to Arabidopsis
Because our data suggested that PpEPF1, PpTMM and PpERECTA1 all play a role in stomatal patterning in P. patens, we investigated whether they might represent conserved functions by introducing the P. patens genes into the appropriate Arabidopsis genetic background, i.e. could they complement the cognate angiosperm gene function in stomatal patterning? For this experiment, we focused on the putative EPF and TMM orthologues because the respective mutants in Arabidopsis have clear phenotypes with respect to stomatal density and patterning

Summary

Introduction

Stomata are microscopic pores present in the epidermis of all angiosperms and the majority of ferns and bryophytes. Received 15 January 2016; Accepted 26 May 2016 distribution is tightly regulated, both by endogenous developmental mechanisms that influence their number and pattern in different organs of the plant, and by modulation of these controls by a host of environmental factors (Chater et al, 2015; Geisler et al, 1998; Hunt and Gray, 2009; MacAlister et al, 2007) This spatial control of stomatal distribution, combined with the ease of scoring phenotype on the exposed epidermis, makes them an attractive system to investigate the control of patterning in plants, a major topic highlighted in the seminal work by Steeves and Sussex (1989)

Methods

Results

Conclusion