Timely expression of the Arabidopsis stoma‐fate master regulator MUTE is required for specification of other epidermal cell types

Abstract

Summary Epidermal differentiation in Arabidopsis thaliana aerial organs involves stomatal lineage development. Lineages derive from meristemoids, which arise from asymmetric divisions of protodermal cells. Each meristemoid divides repeatedly in an inward spiral before it transits to a guard mother cell (GMC) that produces the stoma, leaving a trail of surrounding stomatal lineage ground cells (SLGCs) that eventually differentiate into endoreplicated pavement cells. MUTE is a bHLH transcription factor that is expressed in late meristemoids and drives their transition to GMCs. Loss‐of‐function mute mutants are stomata‐less dwarf plants with arrested lineages, in which stunted putative SLGCs surround a halted meristemoid. We analysed MUTE functions using a chemically inducible system for mute‐3 complementation based on conditional MUTE expression in its normal domain. Continuous induction from germination produced stomata‐bearing, normal‐sized plants with viable mute‐3 seeds. In 2‐week‐old mute‐3 cotyledons, meristemoids appeared to retain their identity and synchronously formed stomata in response to induced MUTE expression. However, arrested SLGCs were not complemented: many produced stomata, leading to stomatal clusters, and others remained unexpanded and diploid. In contrast, non‐lineage pavement cells, which are under‐endoreplicated in mute‐3, expanded and increased their ploidy level upon induction, showing that the lack of response of SLGCs is specific to this arrested cell type. Leaf phenotypic mosaics include wild‐type lineages and adjacent mute‐3 lineages, whose meristemoids and putative SLGCs remained arrested, indicating that the role of MUTE in SLGC fate is strictly lineage‐autonomous. These results show that timely MUTE expression is essential to prevent stomatal fate in SLGCs and to promote their differentiation as pavement cells.

Too many faces for TOO MANY MOUTHS?

“…Developmental windows have also been reported for stomatal lineage progression in relation to cell differentiation rather than division (Triviño et al, 2013). In agreement with the proposed role of TMM in maintaining meristemoid identity (Geisler et al, 2000;Bhave et al, 2009), loss of TMM function might lead to lineages losing their autonomy during the early stages of leaf primordium development, and a general repression of lineage differentiation might predominate as a result.…”

Transcriptional control of cell fate in the stomatal lineage

“…In the absence of MUTE, meristemoids fail to transition into GMCs and continue to divide asymmetrically [10]. A version of MUTE with an estrogen responsive promoter expressed in the normal MUTE spatial domain was used to determine how long mute meristemoids were competent to respond to the return of MUTE activity [41*]). When induced early, meristemoids were completely rescued and could progress to make GMCs and stomata.…”

MUTE Directly Orchestrates Cell State Switch and the Single Symmetric Division to Create Stomata

“…Among the stomatal transcription factors, MUTE is the only one whose overexpression confers constitutive differentiation of stomata with paired GCs (Pillitteri et al, 2008; Pillitteri et al, 2007; Trivino et al, 2013). Overexpression of SPCH and FAMA confers highly-divided stomatal-lineage cells and singular GCs, respectively (MacAlister et al, 2007; Ohashi-Ito and Bergmann, 2006).…”