Mutations in the SLAC1 anion channel slow stomatal opening and severely reduce K+ uptake channel activity via enhanced cytosolic [Ca2+] and increased Ca2+ sensitivity of K+ uptake channels

New Phytol. 2013 Jan;197(1):88-98. doi: 10.1111/nph.12008. Epub 2012 Nov 5.

Abstract

The Arabidopsis guard cell anion channel SLAC1 is essential for stomatal closure in response to various endogenous and environmental stimuli. Interestingly, here we reveal an unexpected impairment of slac1 alleles on stomatal opening. We report that mutations in SLAC1 unexpectedly slow stomatal opening induced by light, low CO(2) and elevated air humidity in intact plants and that this is caused by the severely reduced activity of inward K(+) (K(+)(in)) channels in slac1 guard cells. Expression of channels and transporters involved in stomatal opening showed small but significant reductions in transcript levels in slac1 guard cells; however, this was deemed insufficient to explain the severely impaired K(+)(in) channel activity in slac1. We further examined resting cytosolic Ca(2+) concentration ([Ca(2+)](cyt)) and K(+)(in) channel sensitivity to [Ca(2+)](cyt) in slac1. These experiments showed higher resting [Ca(2+)](cyt) in slac1 guard cells and that reducing [Ca(2+)](cyt) to < 10 nM rapidly restored the activity of K(+)(in) channels in slac1 closer to wild-type levels. These findings demonstrate an unanticipated compensatory feedback control in plant stomatal regulation, which counteracts the impaired stomatal closing response of slac1, by down-regulating stomatal opening mechanisms and implicates enhanced [Ca(2+)](cyt) sensitivity priming as a mechanistic basis for the down-regulated K(+)(in) channel activity.

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

  • Abscisic Acid / pharmacology
  • Alleles
  • Arabidopsis / drug effects
  • Arabidopsis / genetics
  • Arabidopsis / metabolism
  • Arabidopsis Proteins / genetics
  • Arabidopsis Proteins / metabolism*
  • Calcium / metabolism*
  • Carbon Dioxide / metabolism
  • Cell Membrane / enzymology
  • Cytosol / metabolism*
  • Gene Expression Regulation, Plant
  • Light
  • Membrane Proteins / genetics
  • Membrane Proteins / metabolism*
  • Mutation*
  • Patch-Clamp Techniques
  • Plant Cells / metabolism
  • Plant Epidermis / drug effects
  • Plant Epidermis / metabolism
  • Plant Stomata / drug effects
  • Plant Stomata / metabolism*
  • Potassium Channels, Inwardly Rectifying / metabolism*
  • Protoplasts / metabolism

Substances

  • Arabidopsis Proteins
  • Membrane Proteins
  • Potassium Channels, Inwardly Rectifying
  • SLAC1 protein, Arabidopsis
  • Carbon Dioxide
  • Abscisic Acid
  • Calcium