Defects in leaf carbohydrate metabolism compromise acclimation to high light and lead to a high chlorophyll fluorescence phenotype in Arabidopsis thaliana

BMC Plant Biol. 2012 Jan 16;12:8. doi: 10.1186/1471-2229-12-8.

Abstract

Background: We have studied the impact of carbohydrate-starvation on the acclimation response to high light using Arabidopsis thaliana double mutants strongly impaired in the day- and night path of photoassimilate export from the chloroplast. A complete knock-out mutant of the triose phosphate/phosphate translocator (TPT; tpt-2 mutant) was crossed to mutants defective in (i) starch biosynthesis (adg1-1, pgm1 and pgi1-1; knock-outs of ADP-glucose pyrophosphorylase, plastidial phosphoglucomutase and phosphoglucose isomerase) or (ii) starch mobilization (sex1-3, knock-out of glucan water dikinase) as well as in (iii) maltose export from the chloroplast (mex1-2).

Results: All double mutants were viable and indistinguishable from the wild type when grown under low light conditions, but--except for sex1-3/tpt-2--developed a high chlorophyll fluorescence (HCF) phenotype and growth retardation when grown in high light. Immunoblots of thylakoid proteins, Blue-Native gel electrophoresis and chlorophyll fluorescence emission analyses at 77 Kelvin with the adg1-1/tpt-2 double mutant revealed that HCF was linked to a specific decrease in plastome-encoded core proteins of both photosystems (with the exception of the PSII component cytochrome b559), whereas nuclear-encoded antennae (LHCs) accumulated normally, but were predominantly not attached to their photosystems. Uncoupled antennae are the major cause for HCF of dark-adapted plants. Feeding of sucrose or glucose to high light-grown adg1-1/tpt-2 plants rescued the HCF- and growth phenotypes. Elevated sugar levels induce the expression of the glucose-6-phosphate/phosphate translocator2 (GPT2), which in principle could compensate for the deficiency in the TPT. A triple mutant with an additional defect in GPT2 (adg1-1/tpt-2/gpt2-1) exhibited an identical rescue of the HCF- and growth phenotype in response to sugar feeding as the adg1-1/tpt-2 double mutant, indicating that this rescue is independent from the sugar-triggered induction of GPT2.

Conclusions: We propose that cytosolic carbohydrate availability modulates acclimation to high light in A. thaliana. It is conceivable that the strong relationship between the chloroplast and nucleus with respect to a co-ordinated expression of photosynthesis genes is modified in carbohydrate-starved plants. Hence carbohydrates may be considered as a novel component involved in chloroplast-to-nucleus retrograde signaling, an aspect that will be addressed in future studies.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Acclimatization*
  • Arabidopsis / genetics
  • Arabidopsis / metabolism*
  • Arabidopsis / radiation effects
  • Arabidopsis Proteins / genetics
  • Arabidopsis Proteins / metabolism
  • Carbohydrate Metabolism*
  • Cell Nucleus / genetics
  • Cell Nucleus / metabolism
  • Chlorophyll / metabolism
  • Chloroplasts / metabolism
  • Chloroplasts / ultrastructure
  • Crosses, Genetic
  • Cytosol / metabolism
  • Electron Transport
  • Fluorescence
  • Gene Expression Regulation, Plant
  • Gene Knockout Techniques
  • Genes, Plant
  • Glucose-1-Phosphate Adenylyltransferase / genetics
  • Glucose-1-Phosphate Adenylyltransferase / metabolism
  • Glucose-6-Phosphate Isomerase / genetics
  • Glucose-6-Phosphate Isomerase / metabolism
  • Light*
  • Microscopy, Electron, Transmission
  • Phenotype
  • Phosphoglucomutase / genetics
  • Phosphoglucomutase / metabolism
  • Photosynthesis
  • Plant Leaves / metabolism*
  • Plant Leaves / radiation effects
  • Starch / biosynthesis

Substances

  • Arabidopsis Proteins
  • Chlorophyll
  • Starch
  • ADP-glucose pyrophosphorylase, Arabidopsis
  • Glucose-1-Phosphate Adenylyltransferase
  • Glucose-6-Phosphate Isomerase
  • Phosphoglucomutase