Transcription factor control of asymmetric cell divisions that establish the stomatal lineage

Abstract

The establishment of new cell lineages during development often requires a symmetry-breaking event. An asymmetric division in the epidermis of plants initiates a lineage that ultimately produces stomatal guard cells. Stomata are pores in the epidermis that serve as the main conduits for gas exchange between plants and the atmosphere; they are critical for photosynthesis and exert a major influence on global carbon and water cycles. Recent studies implicated intercellular signalling in preventing the inappropriate production of stomatal complexes. Genes required to make stomata, however, remained elusive. Here we report the identification of a gene, SPEECHLESS (SPCH), encoding a basic helix-loop-helix (bHLH) transcription factor that is necessary and sufficient for the asymmetric divisions that establish the stomatal lineage in Arabidopsis thaliana. We demonstrate that SPCH and two paralogues are successively required for the initiation, proliferation and terminal differentiation of cells in the stomatal lineage. The stomatal bHLHs define a molecular pathway sufficient to create one of the key cell types in plants. Similar molecules and regulatory mechanisms are used during muscle and neural development, highlighting a conserved use of closely related bHLHs for cell fate specification and differentiation.

Arabidopsis homeodomain-leucine zipper IV proteins promote stomatal development and ectopically induce stomata beyond the epidermis

“…Among them, MUTE and SCRM are capable of converting the aerial shoot epidermis into stomata when ectopically overexpressed or stabilized (Kanaoka et al, 2008;Pillitteri et al, 2008). By contrast, ectopic overexpressions of SPCH and FAMA confer excessive asymmetric entry divisions and the formation of guard cell-like cells, respectively (MacAlister et al, 2007;Ohashi-Ito and Bergmann, 2006;Pillitteri et al, 2007). Importantly, the ability of MUTE and SCRM to trigger stomatal differentiation is limited to the epidermis.…”

“…The stomatal cell-state transitions are specified by combinatorial activities of five basic helix-loop-helix (bHLH) proteins, SPEECHLESS (SPCH), MUTE, FAMA, SCREAM (SCRM, also known as ICE1) and SCRM2 (Kanaoka et al, 2008;MacAlister et al, 2007;Ohashi-Ito and Bergmann, 2006;Pillitteri et al, 2007). These bHLH proteins are necessary and sufficient for specifying each stomatal precursor state.…”

Generation of Signaling Specificity in Arabidopsis by Spatially Restricted Buffering of Ligand–Receptor Interactions

“…For epf1 epf2 and STO-MAGEN RNAi analysis, nine plants were analyzed per genotype/independent line for all measurements (except STOMAGEN RNAi pedicels; eight plants per line were examined). MUTEpro:nucGFP (MacAlister et al, 2007) in Col was used as a BASTA-resistant control to compare with STOMAGEN RNAi lines. For rescue of chal cll2 by CLL2pro:CLL1 (and the CLL2pro:GFP control), 12 independent T1s were analyzed for height, and 11 independent T1s were analyzed for pedicel and internode length.…”

A Tale of Two Systems: Peptide Ligand-Receptor Pairs in Plant Development

“…It is expressed in most protodermal cells and later its expression levels in pavement cells are gradually decreased, although its expression is maintained in stomatal lineage cells for these cells to undergo stomatal differentiation (MacAlister et al 2007;Pillitteri et al 2007). Interestingly, expression patterns of EPF2, an inhibitor of entry asymmetric division, are overlapped with SPCH, and SPCH is required for EPF2 expression (Hara et al 2009).…”