How sugars might coordinate chloroplast and nuclear gene expression during acclimation to high light intensities.

The concept of retrograde control of nuclear gene expression assumes the generation of signals inside the chloroplasts, which are either released from or sensed inside of the organelle. In both cases, downstream signaling pathways lead eventually to a differential regulation of nuclear gene expression and the production of proteins required in the chloroplast. This concept appears reasonable as the majority of the over 3000 predicted plastidial proteins are encoded by nuclear genes. Hence, the nucleus needs information on the status of the chloroplasts, such as during acclimation responses, which trigger massive changes in the protein composition of the thylakoid membrane and in the stroma. Here, we propose an additional control mechanism of nuclear- and plastome-encoded photosynthesis genes, taking advantage of pathways involved in sugar- or hormonal signaling. Sugars are major end products of photosynthesis and their contents respond very sensitively to changes in light intensities. Based on recent findings, we ask the question as to whether the carbohydrate status outside the chloroplast can be directly sensed within the chloroplast stroma. Sugars might synchronize the responsiveness of both genomes and thereby help to coordinate the expression of plastome- and nuclear-encoded photosynthesis genes in concert with other, more specific retrograde signals.

The essential role of sugar metabolism in the acclimation response of Arabidopsis thaliana to high light intensities.

Retrograde signals from chloroplasts are thought to control the expression of nuclear genes associated with plastidial processes such as acclimation to varying light conditions. Arabidopsis mutants altered in the day and night path of photoassimilate export from the chloroplasts served as tools to study the involvement of carbohydrates in high light (HL) acclimation. A double mutant impaired in the triose phosphate/phosphate translocator (TPT) and ADP-glucose pyrophosphorylase (AGPase) (adg1-1/tpt-2) exhibits a HL-dependent depletion in endogenous carbohydrates combined with a severe growth and photosynthesis phenotype. The acclimation response of mutant and wild-type plants has been assessed in time series after transfer from low light (LL) to HL by analysing photosynthetic performance, carbohydrates, MgProtoIX (a chlorophyll precursor), and the ascorbate/glutathione redox system, combined with microarray-based transcriptomic and GC-MS-based metabolomic approaches. The data indicate that the accumulation of soluble carbohydrates (predominantly glucose) acts as a short-term response to HL exposure in both mutant and wild-type plants. Only if carbohydrates are depleted in the long term (e.g. after 2 d) is the acclimation response impaired, as observed in the adg1-1/tpt-2 double mutant. Furthermore, meta-analyses conducted with in-house and publicly available microarray data suggest that, in the long term, reactive oxygen species such as H2O2 can replace carbohydrates as signals. Moreover, a cross-talk exists between genes associated with the regulation of starch and lipid metabolism. The involvement of genes responding to phytohormones in HL acclimation appears to be less likely. Various candidate genes involved in retrograde control of nuclear gene expression emerged from the analyses of global gene expression.

The Mysterious Rescue of adg1-1/tpt-2 - an Arabidopsis thaliana Double Mutant Impaired in Acclimation to High Light - by Exogenously Supplied Sugars.

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.