Global transcriptome analyses provide evidence that chloroplast redox state contributes to intracellular as well as long-distance signalling in response to stress and acclimation in Arabidopsis

Photosynth Res. 2016 Jun;128(3):287-312. doi: 10.1007/s11120-016-0245-y. Epub 2016 Mar 28.

Abstract

Global transcriptome analyses were used to assess the interactive effects of short-term stress versus long-term acclimation to high light (HL), low temperature (LT) and excitation pressure in Arabidopsis. Microarray analyses indicated that exposure to stress resulted in two times as many modulated transcripts in both, high-light-treated and low-temperature-treated plants, compared to plants that were fully acclimated to either one of these conditions. We showed that 10.9 % of all transcripts were regulated in the same way by both stress conditions, and hence, were categorized as excitation pressure regulated, rather than regulated by either high-light or low-temperature stress per se. This group of chloroplast redox-sensitive genes included various photosynthetic genes as well as genes known to be associated with cold acclimation (cbf3, cor15A, cor15B) and gibberellic acid (GA) metabolism and signalling (ga2ox1, gai). Chemical inhibition of the photosynthetic electron transport by either DCMU or DBMIB indicated that although the plastoquinone pool contributes significantly to redox regulation of the transcriptome (8.6 %), it appears that PSI represents the major source of redox signals (89 %), whereas PSII appears to contribute only 3.1 %. A comparison of the gene expression profiles between stress and acclimated plants indicated that 10 % of the genes induced by a short, 1-h stress were also associated with long-term acclimation to high excitation pressure. This included the APETALA2/ETHYLENE-RESPONSIVE-BINDING PROTEIN family, the MYB domain- and MYB-related transcription factor family as well as the GRAS transcription factor family important in GA signalling confirming that acclimation to stress is a time-nested phenomenon. We suggest that acclimation to photosynthetic redox imbalance extends beyond the chloroplast and the leaf cell to systemic ROS signalling. This is discussed in terms of the control of plant phenotype through regulation of the nuclear encoded cbf regulon and GA metabolism.

Keywords: Acclimation; Arabidopsis; Chloroplast redox signalling; Cold; Excitation pressure; High-light; Stress.

MeSH terms

  • Acclimatization
  • Arabidopsis / genetics*
  • Arabidopsis / physiology
  • Arabidopsis / radiation effects
  • Arabidopsis Proteins / genetics*
  • Arabidopsis Proteins / physiology
  • Chloroplasts / metabolism
  • Cold Temperature
  • Electron Transport
  • Gene Expression Profiling
  • Gene Expression Regulation, Plant*
  • Gibberellins / metabolism
  • Light
  • Oligonucleotide Array Sequence Analysis
  • Oxidation-Reduction
  • Photosynthesis
  • Photosystem I Protein Complex / metabolism
  • Photosystem II Protein Complex / metabolism
  • Plant Growth Regulators / metabolism
  • Plant Leaves / genetics
  • Plant Leaves / physiology
  • Signal Transduction*
  • Stress, Physiological

Substances

  • Arabidopsis Proteins
  • Gibberellins
  • Photosystem I Protein Complex
  • Photosystem II Protein Complex
  • Plant Growth Regulators
  • gibberellic acid