title: Molecular Framework of a Regulatory Circuit Initiating Two-Dimensional Spatial Patterning of Stomatal Lineage.
abstract: Stomata, valves on the plant epidermis, are critical for plant growth and survival, and the presence of stomata impacts the global water and carbon cycle. Although transcription factors and cell-cell signaling components regulating stomatal development have been identified, it remains unclear as to how their regulatory interactions are translated into two-dimensional patterns of stomatal initial cells. Using molecular genetics, imaging, and mathematical simulation, we report a regulatory circuit that initiates the stomatal cell-lineage. The circuit includes a positive feedback loop constituting self-activation of SCREAMs that requires SPEECHLESS. This transcription factor module directly binds to the promoters and activates a secreted signal, EPIDERMAL PATTERNING FACTOR2, and the receptor modifier TOO MANY MOUTHS, while the receptor ERECTA lies outside of this module. This in turn inhibits SPCH, and hence SCRMs, thus constituting a negative feedback loop. Our mathematical model accurately predicts all known stomatal phenotypes with the inclusion of two additional components to the circuit: an EPF2-independent negative-feedback loop and a signal that lies outside of the SPCH•SCRM module. Our work reveals the intricate molecular framework governing self-organizing two-dimensional patterning in the plant epidermis.
authors.affiliation: Howard Hughes Medical Institute, University of Washington, Seattle, Washington, United States of America; Department of Biology, University of Washington, Seattle, Washington, United States of America.
authors.forename: Robin J
authors.initials: RJ
authors.lastname: Horst
authors.affiliation: National Institute for Basic Biology, Okazaki, Aichi, Japan.
authors.forename: Hironori
authors.initials: H
authors.lastname: Fujita
authors.affiliation: Howard Hughes Medical Institute, University of Washington, Seattle, Washington, United States of America; Department of Biology, University of Washington, Seattle, Washington, United States of America.
authors.forename: Jin Suk
authors.initials: JS
authors.lastname: Lee
authors.affiliation: Department of Biology, University of Washington, Seattle, Washington, United States of America.
authors.forename: Amanda L
authors.initials: AL
authors.lastname: Rychel
authors.affiliation: Department of Biology, University of Washington, Seattle, Washington, United States of America.
authors.forename: Jacqueline M
authors.initials: JM
authors.lastname: Garrick
authors.affiliation: National Institute for Basic Biology, Okazaki, Aichi, Japan.
authors.forename: Masayoshi
authors.initials: M
authors.lastname: Kawaguchi
authors.affiliation: Department of Biology, University of Washington, Seattle, Washington, United States of America.
authors.forename: Kylee M
authors.initials: KM
authors.lastname: Peterson
authors.affiliation: Howard Hughes Medical Institute, University of Washington, Seattle, Washington, United States of America; Department of Biology, University of Washington, Seattle, Washington, United States of America.
authors.forename: Keiko U
authors.initials: KU
authors.lastname: Torii
mesh_terms: D017360:Arabidopsis / Q000235:genetics* / Q000254:growth & development; D029681:Arabidopsis Proteins / Q000037:antagonists & inhibitors / Q000235:genetics*; D051792:Basic Helix-Loop-Helix Proteins / Q000037:antagonists & inhibitors / Q000235:genetics*; D002450:Cell Communication / Q000235:genetics*; D019070:Cell Lineage / Q000235:genetics; D003198:Computer Simulation; D004268:DNA-Binding Proteins / Q000235:genetics; D018506:Gene Expression Regulation, Plant; D008962:Models, Theoretical; D054046:Plant Stomata / Q000235:genetics / Q000254:growth & development*; D017346:Protein Serine-Threonine Kinases / Q000235:genetics; D011956:Receptors, Cell Surface / Q000235:genetics; D015398:Signal Transduction / Q000235:genetics; D014157:Transcription Factors / Q000235:genetics
chemical_list: D029681:Arabidopsis Proteins; D051792:Basic Helix-Loop-Helix Proteins; D004268:DNA-Binding Proteins; D017346:Protein Serine-Threonine Kinases; D011956:Receptors, Cell Surface; D014157:Transcription Factors; C542689:EPF2 protein, Arabidopsis; C538823:ICE2 protein, Arabidopsis; C517480:SPEECHLESS protein, Arabidopsis; C459090:too many mouths protein, Arabidopsis; C457763:ER protein, Arabidopsis