Lacking chloroplasts in guard cells of crumpled leaf attenuates stomatal opening: both guard cell chloroplasts and mesophyll contribute to guard cell ATP levels

Plant Cell Environ. 2014 Sep;37(9):2201-10. doi: 10.1111/pce.12297. Epub 2014 Mar 12.

Abstract

Controversies regarding the function of guard cell chloroplasts and the contribution of mesophyll in stomatal movements have persisted for several decades. Here, by comparing the stomatal opening of guard cells with (crl-ch) or without chloroplasts (crl-no ch) in one epidermis of crl (crumpled leaf) mutant in Arabidopsis, we showed that stomatal apertures of crl-no ch were approximately 65-70% those of crl-ch and approximately 50-60% those of wild type. The weakened stomatal opening in crl-no ch could be partially restored by imposing lower extracellular pH. Correspondingly, the external pH changes and K(+) accumulations following fusicoccin (FC) treatment were greatly reduced in the guard cells of crl-no ch compared with crl-ch and wild type. Determination of the relative ATP levels in individual cells showed that crl-no ch guard cells contained considerably lower levels of ATP than did crl-ch and wild type after 2 h of white light illumination. In addition, guard cell ATP levels were lower in the epidermis than in leaves, which is consistent with the observed weaker stomatal opening response to white light in the epidermis than in leaves. These results provide evidence that both guard cell chloroplasts and mesophyll contribute to the ATP source for H(+) extrusion by guard cells.

Keywords: Arabidopsis; mesophyll cells; white light.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adenosine Triphosphate / metabolism*
  • Arabidopsis / drug effects
  • Arabidopsis / physiology*
  • Arabidopsis / radiation effects
  • Arabidopsis Proteins / genetics*
  • Arabidopsis Proteins / metabolism
  • Chloroplasts / drug effects
  • Chloroplasts / metabolism*
  • Chloroplasts / radiation effects
  • Circadian Rhythm / drug effects
  • Circadian Rhythm / physiology
  • Extracellular Space / metabolism
  • Glycosides / pharmacology
  • Hydrogen-Ion Concentration
  • Light
  • Mesophyll Cells / drug effects
  • Mesophyll Cells / metabolism*
  • Mesophyll Cells / radiation effects
  • Plant Stomata / cytology*
  • Plant Stomata / drug effects
  • Plant Stomata / physiology*
  • Plant Stomata / radiation effects
  • Potassium / metabolism

Substances

  • ARC6 protein, Arabidopsis
  • Arabidopsis Proteins
  • CRUMPLED LEAF protein, Arabidopsis
  • Glycosides
  • fusicoccin
  • Adenosine Triphosphate
  • Potassium