Dynamic plastid redox signals integrate gene expression and metabolism to induce distinct metabolic states in photosynthetic acclimation in Arabidopsis.

Plants possess acclimation responses in which structural reconfigurations adapt the photosynthetic apparatus to fluctuating illumination. Long-term acclimation involves changes in plastid and nuclear gene expression and is controlled by redox signals from photosynthesis. The kinetics of these signals and the adjustments of energetic and metabolic demands to the changes in the photosynthetic apparatus are currently poorly understood. Using a redox signaling system that preferentially excites either photosystem I or II, we measured the time-dependent impact of redox signals on the transcriptome and metabolome of Arabidopsis thaliana. We observed rapid and dynamic changes in nuclear transcript accumulation resulting in differential and specific expression patterns for genes associated with photosynthesis and metabolism. Metabolite pools also exhibited dynamic changes and indicate readjustments between distinct metabolic states depending on the respective illumination. These states reflect reallocation of energy resources in a defined and reversible manner, indicating that structural changes in the photosynthetic apparatus during long-term acclimation are additionally supported at the level of metabolism. We propose that photosynthesis can act as an environmental sensor, producing retrograde redox signals that trigger two parallel adjustment loops that coordinate photosynthesis and metabolism to adapt plant primary productivity to the environment.

Redox regulation and antioxidative defence in Arabidopsis leaves viewed from a systems biology perspective.

Redox regulation is a central control element in cell metabolism. It is employed to adjust photosynthesis and the antioxidant defence system of leaves to the prevailing environment. During recent years progress has been made in describing the redox-dependent alterations in metabolism, the thiol/disulfide proteome, the redox-dependent and cross-talking signalling pathways and the target genes of redox regulation. Some transcription factors have been identified as proteins that perform thiol/disulfide transitions linked to the redox-regulation of specific plant promoters. In addition first mathematical models have been designed to simulate antioxidant defence and predict its response. Taken together, a profound experimental data set has been generated which allows to approach a systems biology type of understanding of antioxidant defence in photosynthesising cells in the near future. Since oxidative stress is likely to limit plant growth under stress, such a systematic understanding of antioxidant defence will help to define novel targets for breeding stress-tolerant plants.

Regulation of gene expression by photosynthetic signals triggered through modified CO2 availability.

BACKGROUND: To coordinate metabolite fluxes and energy availability, plants adjust metabolism and gene expression to environmental changes through employment of interacting signalling pathways. RESULTS: Comparing the response of Arabidopsis wild-type plants with that of the mutants adg1, pgr1 and vtc1 upon altered CO2-availability, the regulatory role of the cellular energy status, photosynthetic electron transport, the redox state and concentration of ascorbate and glutathione and the assimilatory force was analyzed in relation to the transcript abundance of stress-responsive nuclear encoded genes and psaA and psbA encoding the reaction centre proteins of photosystem I and II, respectively. Transcript abundance of Bap1, Stp1, psaA and psaB was coupled with seven metabolic parameters. Especially for psaA and psaB, the complex analysis demonstrated that the assumed PQ-dependent redox control is subordinate to signals linked to the relative availability of 3-PGA and DHAP, which define the assimilatory force. For the transcripts of sAPx and Csd2 high correlations with the calculated redox state of NADPH were observed in pgr1, but not in wild-type, suggesting that in wild-type plants signals depending on thylakoid acidification overlay a predominant redox-signal. Strongest correlation with the redox state of ascorbate was observed for 2CPA, whose transcript abundance regulation however was almost insensitive to the ascorbate content demonstrating dominance of redox regulation over metabolite sensing. CONCLUSION: In the mutants, signalling pathways are partially uncoupled, demonstrating dominance of metabolic control of photoreaction centre expression over sensing the redox state of the PQ-pool. The balance between the cellular redox poise and the energy signature regulates sAPx and Csd2 transcript abundance, while 2CPA expression is primarily redox-controlled.

The antioxidant status of photosynthesizing leaves under nutrient deficiency: redox regulation, gene expression and antioxidant activity in Arabidopsis thaliana.

Redox signals provide important information on plant metabolism during development and in dependence on environmental parameters and trigger compensatory responses and antioxidant defence. The aim of the study was to characterize the redox and antioxidant status of photosynthesizing leaves under N, P and S deficiency on a comparative basis. Therefore, redox signals, indicators of the cellular redox environment and parameters of antioxidant defence were determined and related to general growth parameters, namely (1) transcript levels of all chloroplast encoded genes; (2) ascorbate and glutathione; (3) activities of catalase (CAT) and ascorbate peroxidase (APX); and (4) transcript amounts of eight peroxiredoxins, three catalases and three ascorbate peroxidases. The results reveal distinct patterns of redox responses dependent on the type of nutrient deficiency. (1) Nitrogen deprivation caused up-regulation of psbA, psbC, petA, petG and clpP transcripts, down-regulation of psbG, psbK and ndhA, a five-fold increase in ascorbic acid, a severe drop in CAT and APX activities, although cat1 mRNA levels were increased in young and old leaves. (2) With the exception of psbA and psaJ transcripts, P-starvation induced a general trend to decreased mRNA abundance of plastome genes; ascorbate and glutathione levels were increased, as was the activity of APX and CAT. In accordance with that result, transcripts of all cat genes and stromal apx, as well as prxIIC, prxIID, were elevated under P deprivation. (3) Sulphur depletion increased transcripts of petA, petB, petD, petG, ndhJ and rpo-genes. mRNAs of psbG, psbK, atpA, atpB, atpE and atpF were decreased. Glutathione levels dropped to less than 25% of control, in parallel activities of APX were stimulated in young leaves. Transcripts of many antioxidant enzymes were unaltered or decreased, only cat2 mRNA was increased. It is concluded that N-, P- and S-nutrient deprivation trigger distinct redox changes and induce oxidative stress with a rather defined pattern in the context of nutrient-specific alterations in metabolism.