Abstract

Stomata are specialized pores in the epidermis of the aerial parts of a plant, where stomatal guard cells close and open to regulate gas exchange with the atmosphere and restrict excessive water vapor from the plant. The production and patterning of the stomatal lineage cells in higher plants are influenced by the activities of the widely-used mitogen-activated protein kinase (MAPK) signaling components. The phenotype caused by the loss-of-function mutations suggested pivotal roles of the canonical MAPK pathway in the suppression of stomatal formation and regulation of stomatal patterning in Arabidopsis, whilst the cell type-specific manipulation of individual MAPK components revealed the existence of a positive impact on stomatal production. Among a large number of putative MAPK substrates in plants, the nuclear transcription factors SPEECHLESS (SPCH) and SCREAM (SCRM) are targets of MAPK 3 and 6 (MPK3/6) in the inhibition of stomatal formation. The polarity protein BREAKING OF ASYMMETRY IN THE STOMATAL LINEAGE (BASL) is phosphorylated by MPK3/6 for localization and function in driving divisional asymmetries. Here, by functionally characterizing three MAPK SUBSTRATES IN THE STOMATAL LINEAGE (MASS) proteins, we establish that they are plasma membrane-associated, positive regulators of stomatal production. MPK6 can phosphorylate the MASS proteins in vitro and mutating the putative substrate sites interferes the subcellular partition and function of MASS in planta. Our fine-scale domain analyses identify critical subdomains of MASS2 required for specific subcellular localization and biological function, respectively. Furthermore, our data indicate that the MASS proteins may directly interact with the MAPKK Kinase YODA (YDA) at the plasma membrane. Thus, the deeply conserved MASS proteins are tightly connected with MAPK signaling in Arabidopsis to fine-tune stomatal production and patterning, providing a functional divergence of the YDA-MPK3/6 cascade in the regulation of plant developmental processes.

Highlights

  • The mitogen-activated protein kinase (MAPK) cascades are central signaling pathways that regulate a wide range of cellular processes in plant growth, development and stress responses [1,2,3]

  • We report that a group of new MAPK substrates, the MAPK SUBSTRATES IN THE STOMATAL LINEAGE (MASS) proteins, function at the plasma membrane to regulate stomatal production and patterning in Arabidopsis

  • The output of MAPK signaling in the regulation of stomatal development is diverged by differentially localized substrates, suggesting that the concerted activities of MAPK substrates fine-tune stomatal development to improve plant adaptability to the changing environment

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Summary

Introduction

The mitogen-activated protein kinase (MAPK) cascades are central signaling pathways that regulate a wide range of cellular processes in plant growth, development and stress responses [1,2,3]. They function downstream of the cell-surface receptors to deliver and amplify extracellular stimuli that trigger a myriad of cytoplasmic and nuclear responses [4]. Several key factors are modified and regulated by MAPKs. The stomatal lineage initiation is controlled by the bHLH transcription factors SPEECHLESS (SPCH) [9, 10] and its partners SCREAM/ICE1 (SCRM/ICE1) and SCRM2 [11]. Recent studies showed that SCRM/ICE1 physically bridges MAPKs and SPCH to initiate the stomata lineage [14]

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