Abstract
An Arabidopsis thaliana double mutant (adg1-1/tpt-2) defective in the day- and night-path of photoassimilate export from the chloroplast due to a knockout in the triose phosphate/phosphate translocator (TPT; tpt-2) and a lack of starch [mutation in ADP glucose pyrophosphorylase (AGPase); adg1-1] exhibits severe growth retardation, a decrease in the photosynthetic capacity, and a high chlorophyll fluorescence (HCF) phenotype under high light conditions. These phenotypes could be rescued when the plants were grown on sucrose (Suc) or glucose (Glc). Here we address the question whether Glc-sensing hexokinase1 (HXK1) defective in the Glc insensitive 2 (gin2-1) mutant is involved in the sugar-dependent rescue of adg1-1/tpt-2. Triple mutants defective in the TPT, AGPase, and HXK1 (adg1-1/tpt-2/gin2-1) were established as homozygous lines and grown together with Col-0 and Landsberg erecta (Ler) wild-type plants, gin2-1, the adg1-1/tpt-2 double mutant, and the adg1-1/tpt-2/gpt2-1 triple mutant [additionally defective in the glucose 6-phosphate/phosphate translocator 2 (GPT2)] on agar in the presence or absence of 50 mM of each Glc, Suc, or fructose (Fru). The growth phenotype of the double mutant and both triple mutants could be rescued to a similar extent only by Glc and Suc, but not by Fru. All three sugars were capable of rescuing the HCF and photosynthesis phenotype, irrespectively of the presence or absence of HXK1. Quantitative RT-PCR analyses of sugar-responsive genes revealed that plastidial HXK (pHXK) was up-regulated in adg1-1/tpt-2 plants grown on sugars, but showed no response in adg1-1/tpt-2/gin2-1. It appears likely that soluble sugars are directly taken up by the chloroplasts and enter further metabolism, which consumes ATP and NADPH from the photosynthetic light reaction and thereby rescues the photosynthesis phenotype of the double mutant. The implication of sugar turnover and probably signaling inside the chloroplasts for the concept of retrograde signaling is discussed.
Highlights
Plants are exposed to a variety of environmental factors including stresses such as excessive light or drought
GENERATION AND PROPERTIES OF HOMOZYGOUS adg1-1/tpt-2/ gin2-1 TRIPLE MUTANTS The gin2-1 mutant (Moore et al, 2003), which had been isolated from an EMS mutagenized A. thaliana population in the Landsberg erecta (Ler) background, contains a translational stop codon after position 1296 downstream of the start codon leading to a non-functional protein
There was no additional visible phenotype of the triple mutant compared to the double mutant, when plants were grown on soil or on Murashige– Skoog (MS) agar plates in the absence of sugars
Summary
Plants are exposed to a variety of environmental factors including stresses such as excessive light or drought. Studies on mutant and wild-type plants revealed at least six possible signals chloroplasts might emit to trigger yet unknown signaling pathways or cascades The list of these signals comprises (i) tetrapyrroles as intermediates of chlorophyll and heme biosynthesis (Surpin et al, 2002; Beck, 2005), (ii) chloroplast-generated redox signals (Pfannschmidt et al, 1999), (iii) reactive oxygen species (ROS; Kim et al, 2008; Foyer and Noctor, 2009; Miller et al, 2009; Triantaphylidès and Havaux, 2009), (iv) plastid gene expression (Ahlert et al, 2003), (v) the production of abscisic acid (ABA) as response to an enhanced xanthophyll cycle (Baier et al, 2004; Baier and Dietz, 2005), and chloroplast-derived metabolite signals including carbohydrates (Smeekens, 1998, 2000; Rolland et al, 2002, 2006; Bräutigam et al, 2009), which accumulate as a consequence of photosynthetic CO2 assimilation
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