Limitation of nocturnal import of ATP into Arabidopsis chloroplasts leads to photooxidative damage

Plant J. 2007 Apr;50(2):293-304. doi: 10.1111/j.1365-313X.2007.03049.x. Epub 2007 Mar 12.

Abstract

When grown in short day conditions and at low light, leaves of Arabidopsis plants with mutations in the genes encoding two plastidial ATP/ADP transporters (so-called null mutants) spontaneously develop necrotic lesions. Under these conditions, the mutants also display light-induced accumulation of H(2)O(2) and constitutive expression of genes for copper/zinc superoxide dismutase 2 and ascorbate peroxidase 1. In the light phase, null mutants accumulate high levels of phototoxic protoporphyrin IX but have only slightly reduced levels of Mg protoporphyrin IX. The physiological changes are associated with reduced magnesium-chelatase activity. Since the expression of genes encoding any of the three subunits of magnesium-chelatase is similar in wild type and null mutants, decreased enzyme activity is probably due to post-translational modification which might be due to limited availability of ATP in plastids during the night. Surprisingly, the formation of necrotic lesions was absent when null mutants were grown either in long days and low light intensity or in short days and high light intensity. We ascribe the lack of lesion phenotype to increased nocturnal ATP supply due to glycolytic degradation of starch which may lead to additional substrate-level phosphorylation in the stroma. Thus, nocturnal import of ATP into chloroplasts represents a crucial, previously unknown process that is required for controlled chlorophyll biosynthesis and for preventing photooxidative damage.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adenosine Triphosphate / metabolism*
  • Arabidopsis / genetics
  • Arabidopsis / metabolism*
  • Arabidopsis / radiation effects
  • Arabidopsis Proteins / genetics
  • Arabidopsis Proteins / metabolism
  • Ascorbate Peroxidases
  • Biological Transport / radiation effects
  • Chloroplasts / metabolism*
  • Circadian Rhythm
  • Gene Deletion
  • Gene Expression Regulation, Plant / radiation effects
  • Glycolysis / radiation effects
  • Hydrogen Peroxide / metabolism
  • Light*
  • Lyases / genetics
  • Lyases / metabolism
  • Mutation
  • Oxidative Stress
  • Peroxidases / genetics
  • Peroxidases / metabolism
  • Plant Leaves / genetics
  • Plant Leaves / metabolism
  • Plant Leaves / radiation effects
  • Protoporphyrins / genetics
  • Protoporphyrins / metabolism
  • Reactive Oxygen Species / metabolism
  • Reverse Transcriptase Polymerase Chain Reaction
  • Starch / metabolism
  • Superoxide Dismutase / genetics
  • Superoxide Dismutase / metabolism
  • Time Factors

Substances

  • Arabidopsis Proteins
  • Protoporphyrins
  • Reactive Oxygen Species
  • magnesium protoporphyrin
  • Adenosine Triphosphate
  • Starch
  • Hydrogen Peroxide
  • protoporphyrin IX
  • Peroxidases
  • Ascorbate Peroxidases
  • Superoxide Dismutase
  • superoxide dismutase 2
  • Lyases
  • magnesium chelatase