What causes opposing actions of brassinosteroids on stomatal development?

During the past few years, our understanding of stomatal development and patterning has been advanced by the cloning of a large number of genes in Arabidopsis (Arabidopsis thaliana). These genes encode peptide ligands (epidermal patterning factor, or EPF), and receptor proteins (TOO MANY MOUTHS [TMM] and the ERECTA family [ERf] of receptor-like kinases [ER, ERL1, and ERL2]; Nadeau and Sack, 2002; Shpak et al., 2005; Torii, 2012). Genes functioning downstream of these receptors include those encoding the mitogen-activated protein kinase (MAPK) module, which consists of the MAPK kinase kinase YODA (YDA); the MAPK kinases MKK4, MKK5, MKK7, and MKK9; and the MAPKs MPK3 and MPK6 (Bergmann et al., 2004; Wang et al., 2007; Lampard et al., 2009). MPK3 and MPK6 phosphorylate and inactivate the basic helix-loophelix transcriptional factor SPEECHLESS (SPCH), blocking the initiation of stomatal development (MacAlister et al., 2007; Pillitteri et al., 2007; Lampard et al., 2008). It is well known that the interaction of signaling pathways permits the fine tuning of cellular activities needed to carry out complex developmental processes. However, despite the progress made in studies on the stomatal signaling pathway, our understanding of its interaction with other signaling pathway remains very limited. One of the most well characterized signal transduction pathways in plant biology is the pathway regulated by brassinosteroids (BRs; Kim and Wang, 2010). These plant regulators are perceived by the Leu-rich-repeat receptor-like kinase BRASSINOSTEROID INSENSITIVE1 (BRI1; He et al., 2000). Direct binding of BRs to BRI1 results in the activation of a small family of kinases known as BRASSINOSTEROID SIGNALING KINASEs (Tang et al., 2008). Downstream components of bacterial spore kinases include the GLYCOGEN SYNTHASE KINASE3 (GSK3)-like BRASSINOSTEROID INSENSITIVE2 (BIN2) kinase (Li and Nam, 2002) and two protein phosphatases, BRI1 SUPPRESSOR1 (BSU1; Mora-García et al., 2004) and PROTEIN PHOSPHATASE2A (PP2A; Tang et al., 2011), which control the phosphorylation states of a family of transcription factors including BRI1-EMS-SUPPRESSOR1 (BES1; Yin et al., 2002) and BRASSINAZOLE RESISTANT1 (BZR1; He et al., 2005). BR signaling leads to the inactivation of BIN2, and PP2A-mediated dephosphorylation and the activation of BZR1 and BES1 (He et al., 2002; Kim and Wang, 2010; Tang et al., 2011). Two works have revealed that BRs control stomatal production through regulating proteins that function in the stomatal pathway (Gudesblat et al., 2012a; Kim et al., 2012). However, while one of these studies showed that BRs repress stomatal development by alleviating the BIN2-mediated inhibition of YDA (Kim et al., 2012; Fig. 1A), the other study concluded that these plant regulators promote stomatal formation by inhibiting the BIN2mediated phosphorylation of SPCH (Gudesblat et al., 2012a; Fig. 1B). A number of recent papers (Casson and Hetherington, 2012; Kong et al., 2012), including one published by the authors of one of the original articles (Gudesblat et al., 2012b), highlighted this apparent discrepancy and looked for its possible sources. In this article, I examine data from the cotyledon and hypocotyl separately and propose that BRs have opposite effects on the formation of stomata in these plant organs. I also look for the reasons behind such responses and propose that the TMM action, dampening excessive signal to ERf from the peptide ligands CHALLAH (CHAL) and EPFLIKE5 (EPFL5) in hypocotyls, may be responsible for the organ-specific effects of BRs.