Autocrine regulation of stomatal differentiation potential by EPF1 and ERECTA-LIKE1 ligand-receptor signaling

Abstract

Development of stomata, valves on the plant epidermis for optimal gas exchange and water control, is fine-tuned by multiple signaling peptides with unique, overlapping, or antagonistic activities. EPIDERMAL PATTERNING FACTOR1 (EPF1) is a founding member of the secreted peptide ligands enforcing stomatal patterning. Yet, its exact role remains unclear. Here, we report that EPF1 and its primary receptor ERECTA-LIKE1 (ERL1) target MUTE, a transcription factor specifying the proliferation-to-differentiation switch within the stomatal cell lineages. In turn, MUTE directly induces ERL1. The absolute co-expression of ERL1 and MUTE, with the co-presence of EPF1, triggers autocrine inhibition of stomatal fate. During normal stomatal development, this autocrine inhibition prevents extra symmetric divisions of stomatal precursors likely owing to excessive MUTE activity. Our study reveals the unexpected role of self-inhibition as a mechanism for ensuring proper stomatal development and suggests an intricate signal buffering mechanism underlying plant tissue patterning.DOI: http://dx.doi.org/10.7554/eLife.24102.001

Reducing Stomatal Density in Barley Improves Drought Tolerance without Impacting on Yield

“…In Arabidopsis, this cellular transition step is under the control of the transcription factor MUTE (Fig. 8) whose activity promotes expression of the receptor-like kinase ERECTA-LIKE1, which in turn mediates EPF1 signaling and the subsequent autocrine inhibition of MUTE (Qi et al, 2017). Barley MUTE may be regulated by HvEPF1 by a similar autocrine pathway and/or by phosphorylation as grass MUTE genes (unlike Arabidopsis MUTE) encode potential MAP kinase phosphorylation sites (Liu et al, 2009).…”

“…Both peptides act extracellularly within the aerial epidermal cell layer to suppress stomatal development through activation of an intracellular MAP kinase signaling pathway (Bergmann et al, 2004;Wang et al, 2007;Lampard et al, 2008). Although their functions somewhat overlap, EPF2 acts earliest in stomatal development to restrict entry of cells into the stomatal lineage, while EPF1 acts later to orient subsequent divisions of meristemoid cells and enforce stomatal spacing through the "one-cellspacing" rule via the inhibition of MUTE expression (Hara et al, 2007;Qi et al, 2017). Manipulation of the expression levels of these peptides in Arabidopsis has led to significant improvements in drought tolerance and WUE in experiments conducted in controlledenvironment plant growth rooms (Doheny-Adams et al, 2012;Hepworth et al, 2015).…”

Origins and Evolution of Stomatal Development

“…1, G and H). Arabidopsis was the original workbench used for studying stomatal genetics and continues to provide much insight into how stomata develop and function (Yang and Sack, 1995;Chater et al, 2015;Han and Torii, 2016;Qi et al, 2017). Such advances have identified many of the key genetic players responsible for permitting entry into the stomatal lineage, the formation of the meristemoid, and the subsequent divisions and transitions that lead to the formation of stomata (Zhao and Sack, 1999;Ohashi-Ito and Bergmann, 2006;Hara et al, 2007;MacAlister et al, 2007;Pillitteri et al, 2007;Kanaoka et al, 2008;Hunt et al, 2010;Sugano et al, 2010).…”

“…1H; Hara et al, 2009;Hunt and Gray, 2009;Hunt et al, 2010;Kondo et al, 2010;Sugano et al, 2010;Lee et al, 2012Lee et al, , 2015. Later in the stomatal lineage, EPF1 interacts with ERECTAs (primarily ERL1), again possibly overseen by TMM, to prevent GMC transitioning (Hara et al, 2007;Lee et al, 2012;Jewaria et al, 2013;Qi et al, 2017). This prevents neighboring cells from becoming stomata and promotes appropriate stomatal patterning and spacing.…”

“…Conversely, in grasses, no such amplifying divisions are apparent, as the asymmetric entry division leads directly to a GMC (and a SLGC; Liu et al, 2009;Luo et al, 2012;Raissig et al, 2016). Moreover, the function of EPF1-like peptides also appears divergent between Arabidopsis and grasses, as Arabidopsis EPF1 predominantly regulates the transition from meristemoid to GMC (Hunt and Gray, 2009;Han and Torii, 2016;Qi et al, 2017), another ontogenetic step not seen in grasses (Liu et al, 2009;Luo et al, 2012). Clearly, understanding how EPF/Ls regulate stomatal development in grasses will not only expand our understanding of stomatal developmental ontogeny, but might also provide crop researchers with invaluable new stomatal phenotypes with which to study biotic and abiotic stresses in socioeconomically important species.…”