Brassinosteroid regulates stomatal development by GSK3-mediated inhibition of a MAPK pathway

Nature. 2012 Feb 5;482(7385):419-22. doi: 10.1038/nature10794.

Abstract

Plants must coordinate the regulation of biochemistry and anatomy to optimize photosynthesis and water-use efficiency. The formation of stomata, epidermal pores that facilitate gas exchange, is highly coordinated with other aspects of photosynthetic development. The signalling pathways controlling stomata development are not fully understood, although mitogen-activated protein kinase (MAPK) signalling is known to have key roles. Here we demonstrate in Arabidopsis that brassinosteroid regulates stomatal development by activating the MAPK kinase kinase (MAPKKK) YDA (also known as YODA). Genetic analyses indicate that receptor kinase-mediated brassinosteroid signalling inhibits stomatal development through the glycogen synthase kinase 3 (GSK3)-like kinase BIN2, and BIN2 acts upstream of YDA but downstream of the ERECTA family of receptor kinases. Complementary in vitro and in vivo assays show that BIN2 phosphorylates YDA to inhibit YDA phosphorylation of its substrate MKK4, and that activities of downstream MAPKs are reduced in brassinosteroid-deficient mutants but increased by treatment with either brassinosteroid or GSK3-kinase inhibitor. Our results indicate that brassinosteroid inhibits stomatal development by alleviating GSK3-mediated inhibition of this MAPK module, providing two key links; that of a plant MAPKKK to its upstream regulators and of brassinosteroid to a specific developmental output.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't
  • Research Support, U.S. Gov't, Non-P.H.S.

MeSH terms

  • Arabidopsis / drug effects*
  • Arabidopsis / enzymology*
  • Arabidopsis / genetics
  • Arabidopsis / growth & development
  • Arabidopsis Proteins / antagonists & inhibitors
  • Arabidopsis Proteins / genetics
  • Arabidopsis Proteins / metabolism*
  • Brassinosteroids / pharmacology*
  • Glycogen Synthase Kinase 3 / antagonists & inhibitors
  • Glycogen Synthase Kinase 3 / genetics
  • Glycogen Synthase Kinase 3 / metabolism*
  • MAP Kinase Kinase Kinases / metabolism
  • MAP Kinase Signaling System / drug effects*
  • Mitogen-Activated Protein Kinase Kinases / metabolism
  • Nicotiana
  • Phosphorylation / drug effects
  • Plant Stomata / drug effects*
  • Plant Stomata / enzymology
  • Plant Stomata / genetics
  • Plant Stomata / growth & development*
  • Plants, Genetically Modified
  • Protein Kinases / genetics
  • Protein Kinases / metabolism*
  • Protein Serine-Threonine Kinases / genetics
  • Protein Serine-Threonine Kinases / metabolism
  • Receptors, Cell Surface / genetics
  • Receptors, Cell Surface / metabolism

Substances

  • Arabidopsis Proteins
  • Brassinosteroids
  • Receptors, Cell Surface
  • too many mouths protein, Arabidopsis
  • Protein Kinases
  • BIN2 protein, Arabidopsis
  • ER protein, Arabidopsis
  • Protein Serine-Threonine Kinases
  • MAP Kinase Kinase Kinases
  • YODA protein, Arabidopsis
  • Glycogen Synthase Kinase 3
  • MKK4 protein, Arabidopsis
  • Mitogen-Activated Protein Kinase Kinases