Dataset Information

Spatially patterned hydrogen peroxide orchestrates stomatal development in Arabidopsis.

ABSTRACT: Stomatal pores allow gas exchange between plant and atmosphere. Stomatal development is regulated by multiple intrinsic developmental and environmental signals. Here, we show that spatially patterned hydrogen peroxide (H₂O₂) plays an essential role in stomatal development. H₂O₂ is remarkably enriched in meristemoids, which is established by spatial expression patterns of H₂O₂-scavenging enzyme CAT2 and APX1. SPEECHLESS (SPCH), a master regulator of stomatal development, directly binds to the promoters of CAT2 and APX1 to repress their expression in meristemoid cells. Mutations in CAT2 or APX1 result in an increased stomatal index. Ectopic expression of CAT2 driven by SPCH promoter significantly inhibits the stomatal development. Furthermore, H₂O₂ activates the energy sensor SnRK1 by inducing the nuclear localization of the catalytic α-subunit KIN10, which stabilizes SPCH to promote stomatal development. Overall, these results demonstrate that the spatial pattern of H₂O₂ in epidermal leaves is critical for the optimal stomatal development in Arabidopsis.

SUBMITTER: Shi W

PROVIDER: S-EPMC9418256 | biostudies-literature | 2022 Aug

REPOSITORIES: biostudies-literature

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Spatially patterned hydrogen peroxide orchestrates stomatal development in Arabidopsis.

Shi Wen W Wang Lingyan L Yao Lianmei L Hao Wei W Han Chao C Fan Min M Wang Wenfei W Bai Ming-Yi MY

Nature communications 20220826 1

Stomatal pores allow gas exchange between plant and atmosphere. Stomatal development is regulated by multiple intrinsic developmental and environmental signals. Here, we show that spatially patterned hydrogen peroxide (H2O2) plays an essential role in stomatal development. H2O2 is remarkably enriched in meristemoids, which is established by spatial expression patterns of H2O2-scavenging enzyme CAT2 and APX1. SPEECHLESS (SPCH), a m ...[more]

PMID: 36028510

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Project description: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.

Dataset Information

Spatially patterned hydrogen peroxide orchestrates stomatal development in Arabidopsis.

Publications

Spatially patterned hydrogen peroxide orchestrates stomatal development in Arabidopsis.

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