Autocrine regulation of stomatal differentiation potential by EPF1 and ERECTA-LIKE1 ligand-receptor signaling

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Abstract

Development of stomata, valves on the plant epidermis for optimal gas exchange and water control, is fine-tuned by multiple signaling peptides with unique, overlapping, or antagonistic activities. EPIDERMAL PATTERNING FACTOR1 (EPF1) is a founding member of the secreted peptide ligands enforcing stomatal patterning. Yet, its exact role remains unclear. Here, we report that EPF1 and its primary receptor ERECTA-LIKE1 (ERL1) target MUTE, a transcription factor specifying the proliferation-to-differentiation switch within the stomatal cell lineages. In turn, MUTE directly induces ERL1. The absolute co-expression of ERL1 and MUTE, with the co-presence of EPF1, triggers autocrine inhibition of stomatal fate. During normal stomatal development, this autocrine inhibition prevents extra symmetric divisions of stomatal precursors likely owing to excessive MUTE activity. Our study reveals the unexpected role of self-inhibition as a mechanism for ensuring proper stomatal development and suggests an intricate signal buffering mechanism underlying plant tissue patterning.

DOI: http://dx.doi.org/10.7554/eLife.24102.001

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SCREAM/ICE1 and SCREAM2 specify three cell-state transitional steps leading to arabidopsis stomatal differentiation.

Masahiro M Kanaoka, Lynn Pillitteri, Hiroaki Fujii … (2008)

Differentiation of specialized cell types in multicellular organisms requires orchestrated actions of cell fate determinants. Stomata, valves on the plant epidermis, are formed through a series of differentiation events mediated by three closely related basic-helix-loop-helix proteins: SPEECHLESS (SPCH), MUTE, and FAMA. However, it is not known what mechanism coordinates their actions. Here, we identify two paralogous proteins, SCREAM (SCRM) and SCRM2, which directly interact with and specify the sequential actions of SPCH, MUTE, and FAMA. The gain-of-function mutation in SCRM exhibited constitutive stomatal differentiation in the epidermis. Conversely, successive loss of SCRM and SCRM2 recapitulated the phenotypes of fama, mute, and spch, indicating that SCRM and SCRM2 together determined successive initiation, proliferation, and terminal differentiation of stomatal cell lineages. Our findings identify the core regulatory units of stomatal differentiation and suggest a model strikingly similar to cell-type differentiation in animals. Surprisingly, map-based cloning revealed that SCRM is INDUCER OF CBF EXPRESSION1, a master regulator of freezing tolerance, thus implicating a potential link between the transcriptional regulation of environmental adaptation and development in plants.

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Termination of asymmetric cell division and differentiation of stomata.

Lynn Pillitteri, Daniel Sloan, Naomi Bogenschutz … (2007)

Stomata consist of a pair of guard cells that mediate gas and water-vapour exchange between plants and the atmosphere. Stomatal precursor cells-meristemoids-possess a transient stem-cell-like property and undergo several rounds of asymmetric divisions before further differentiation. Here we report that the Arabidopsis thaliana basic helix-loop-helix (bHLH) protein MUTE is a key switch for meristemoid fate transition. In the absence of MUTE, meristemoids abort after excessive asymmetric divisions and fail to differentiate stomata. Constitutive overexpression of MUTE directs the entire epidermis to adopt guard cell identity. MUTE has two paralogues: FAMA, a regulator of guard cell morphogenesis, and SPEECHLESS (SPCH). We show that SPCH directs the first asymmetric division that initiates stomatal lineage. Together, SPCH, MUTE and FAMA bHLH proteins control stomatal development at three consecutive steps: initiation, meristemoid differentiation and guard cell morphogenesis. Our findings highlight the roles of closely related bHLHs in cell type differentiation in plants and animals.

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Stomagen positively regulates stomatal density in Arabidopsis.

Shigeo S Sugano, Tomoo Shimada, Yu Imai … (2010)

Stomata in the epidermal tissues of leaves are valves through which passes CO(2), and as such they influence the global carbon cycle. The two-dimensional pattern and density of stomata in the leaf epidermis are genetically and environmentally regulated to optimize gas exchange. Two putative intercellular signalling factors, EPF1 and EPF2, function as negative regulators of stomatal development in Arabidopsis, possibly by interacting with the receptor-like protein TMM. One or more positive intercellular signalling factors are assumed to be involved in stomatal development, but their identities are unknown. Here we show that a novel secretory peptide, which we designate as stomagen, is a positive intercellular signalling factor that is conserved among vascular plants. Stomagen is a 45-amino-rich peptide that is generated from a 102-amino-acid precursor protein designated as STOMAGEN. Both an in planta analysis and a semi-in-vitro analysis with recombinant and chemically synthesized stomagen peptides showed that stomagen has stomata-inducing activity in a dose-dependent manner. A genetic analysis showed that TMM is epistatic to STOMAGEN (At4g12970), suggesting that stomatal development is finely regulated by competitive binding of positive and negative regulators to the same receptor. Notably, STOMAGEN is expressed in inner tissues (the mesophyll) of immature leaves but not in the epidermal tissues where stomata develop. This study provides evidence of a mesophyll-derived positive regulator of stomatal density. Our findings provide a conceptual advancement in understanding stomatal development: inner photosynthetic tissues optimize their function by regulating stomatal density in the epidermis for efficient uptake of CO(2).

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Sheila McCormick: Role: Reviewing editor

Journal

Journal ID (nlm-ta): eLife

Journal ID (iso-abbrev): Elife

Journal ID (hwp): eLife

Journal ID (publisher-id): eLife

Title: eLife

Publisher: eLife Sciences Publications, Ltd

ISSN (Electronic): 2050-084X

Publication date (Electronic, pub): 07 March 2017

Publication date Collection: 2017

Volume: 6

Electronic Location Identifier: e24102

Affiliations

[1 ]Howard Hughes Medical Institute, University of Washington , Seattle, United States

[2 ]deptDepartment of Biology , University of Washington , Seattle, United States

[3 ]deptGraduate School of Bioagricultural Sciences/Institute of Transformative Biomolecules (WPI-ITbM) , Nagoya University , Nagoya, Japan

[4]University of California-Berkeley , United States

[5]University of California-Berkeley , United States

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ktorii@ 123456u.washington.edu

Author information

Xingyun Qi http://orcid.org/0000-0003-1261-1362

Jonathan H Dang http://orcid.org/0000-0002-0458-4010

Alex K Hofstetter http://orcid.org/0000-0002-3709-9783

Keiko U Torii http://orcid.org/0000-0002-6168-427X

Article

Publisher ID: 24102

DOI: 10.7554/eLife.24102

PMC ID: 5358980

PubMed ID: 28266915

SO-VID: 01c684f6-b9c7-464e-a31e-95bea85b8f46

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This article is distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use and redistribution provided that the original author and source are credited.

History

Date received : 09 December 2016

Date accepted : 06 March 2017

Funding

Funded by: FundRef http://dx.doi.org/10.13039/100000011, Howard Hughes Medical Institute;

Award Recipient : Keiko U Torii

Funded by: FundRef http://dx.doi.org/10.13039/100000936, Gordon and Betty Moore Foundation;

Award ID: GBMF3035

Award Recipient : Keiko U Torii

Funded by: FundRef http://dx.doi.org/10.13039/100000001, National Science Foundation;

Award ID: MCB-0855659

Award Recipient : Keiko U Torii

The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.

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elife-xml-version 2.5

Author impact statement The stomatal precursor cell uses autocrine peptide-receptor kinase signaling to self-inhibit its differentiation potential in order to ensure proper stomatal development on the plant epidermis.

ScienceOpen disciplines: Life sciences

Keywords: peptide signaling,receptor kinase,stomatal development,cell fate,a. thaliana

Data availability:

ScienceOpen disciplines: Life sciences

Keywords: peptide signaling, receptor kinase, stomatal development, cell fate, a. thaliana

Autocrine regulation of stomatal differentiation potential by EPF1 and ERECTA-LIKE1 ligand-receptor signaling

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Most cited references 40

SCREAM/ICE1 and SCREAM2 specify three cell-state transitional steps leading to arabidopsis stomatal differentiation.

Termination of asymmetric cell division and differentiation of stomata.

Stomagen positively regulates stomatal density in Arabidopsis.

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