Stomata on the plant epidermis control gas and water exchange and are formed by MAPK-dependent processes. Although the contribution of MAP KINASE3 (MPK3) and MPK6 (MPK3/MPK6) to the control of stomatal patterning and differentiation in Arabidopsis () has been examined extensively, how they are inactivated and regulate distinct stages of stomatal development is unknown. Here, we identify a dual-specificity phosphatase, MAP KINASE PHOSPHATASE1 (MKP1), which promotes stomatal cell fate transition by controlling MAPK activation at the early stage of stomatal development. Loss of function of creates clusters of small cells that fail to differentiate into stomata, resulting in the formation of patches of pavement cells. We show that MKP1 acts downstream of YODA (a MAPK kinase kinase) but upstream of MPK3/MPK6 in the stomatal signaling pathway and that MKP1 deficiency causes stomatal signal-induced MAPK hyperactivation in vivo. By expressing MKP1 in the three discrete cell types of stomatal lineage, we further identified that MKP1-mediated deactivation of MAPKs in early stomatal precursor cells directs cell fate transition leading to stomatal differentiation. Together, our data reveal the important role of MKP1 in controlling MAPK signaling specificity and cell fate decision during stomatal development.

Peptide signaling has emerged as a key component of plant growth and development, including stomatal patterning, which is critical for plant productivity and survival. Although exciting progress has been made in understanding EPIDERMAL PATTERNING FACTOR (EPF) signaling in Arabidopsis, the mechanisms by which EPF peptides control different stomatal patterns and morphologies in grasses is poorly understood. Here, by examining expression patterns, overexpression transgenics, and cross-species complementation, the antagonistic stomatal ligands orthologous to Arabidopsis AtEPF2 and AtSTOMAGEN/AtEPFL9 peptides were identified in Triticum aestivum(wheat) and the grass model organism Brachypodium distachyon. Application of bioactive BdEPF2 peptides inhibited stomatal initiation, but not the progression or differentiation of stomatal precursors in Brachypodium. Additionally, the inhibitory roles of these EPF peptides during grass stomatal development were suppressed by the contrasting positive action of the BdSTOMAGEN peptide in a dose-dependent manner. These results not only demonstrate how conserved EPF peptides that control different stomatal patterns exist in nature but also suggest new strategies to improve crop yield through the utilization of plant-derived antagonistic peptides that optimize stomatal density on the plant epidermis.

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The MAPK signaling cascade is universal among eukaryotes and mediates a variety of environmental and developmental responses. Two Arabidopsis MAPKs, MPK3 and MPK6, have been shown to be activated by various stimuli and suggested as a convergence point of different signaling pathways. It is known that these MAPKs, MPK3/MPK6, control the discrete stages of stomatal development in Arabidopsis, but how they are regulated and how the same MAPK components can achieve signaling specificity is largely unknown. We recently demonstrated that MAP Kinase Phosphatase 1 (MKP1) promotes stomatal differentiation by suppressing activation of MPK3/MPK6 in the stomatal lineage. By expressing MKP1 in discrete stomatal precursor cell types, we further identified that MKP1 plays an important role at the early stage of stomatal development for the cell fate transition leading to stomatal differentiation. While MKP1 was previously known as a key regulator of environmental stress responses, our data illustrate a novel role of MKP1 in plant development: it acts as one of the specificity-determining regulators of MAPK signaling to enforce proper stomatal development in Arabidopsis.

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