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Inositol Pyrophosphates Mediate Chloroplast Lipid Remodeling and Nuclear Gene Repression during High-Light Acclimation in Chlamydomonas reinhardtii

ABSTRACT: Microalgae are photosynthetic organisms capable of autotrophic growth. Their applicability in multiple industrial fields has been largely studied, thanks to their ability to fixate CO2 into high added value organic products like fatty acids and carotenoids. However, our understanding of the cellular signaling networks that control carbon flux and acclimation to environmental stress remains incomplete. In this study, we used the Chlamydomonas reinhardtii mutant strain vip1-1, which carries a loss-of-function mutation in the hexakisphosphate kinase responsible for the synthesis of inositol pyrophosphates InsP7 and InsP8 (PP-InsPs), to investigate the role of these molecules during high-light acclimation. We show that PP-InsPs participate in chloroplast-specific lipid remodeling by modifying membrane composition and fluidity through fatty acid desaturations and glycerolipid composition. In addition, our findings suggest that PP-InsPs are involved in chloroplast-nucleus communication, where they act as transcriptional repressors of photosynthesis associated nuclear genes (PhANGs), fatty acid desaturases and lipid synthases, contributing to cellular acclimation to high light. We also found that PP-InsPs modulating effect extended to protein synthesis and accumulation of Calvin-Benson-Bassham cycle intermediates. Therefore, we propose that PP-InsPs function as integratory molecules that balance carbon allocation between storage and structural pools, in response to envirnomental cues such as high light. This uncovers a novel function of PP-InsPs in high light acclimation and potentially in chloroplast-nucleus communication, providing new insights that may help engineer more resilient and efficient strains.

ORGANISM(S): Chlamydomonas reinhardtii

PROVIDER: GSE315948 | GEO | 2026/05/31

REPOSITORIES: GEO

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Project description:Ascorbate (vitamin C) is an important antioxidant in leaves with multiple functions in photosynthesis and its levels are tightly regulated by light quality. The majority of work to date has focussed on regulation of ascorbate levels via biosynthesis. However, the pathway of ascorbate degradation, which is localised in the apoplast may additionally play a significant role. The degradative pathway begins with ascorbate oxidation by the enzyme ascorbate oxidase (AO) and hence we have examined the impact of manipulation of ascorbate oxidase activity on the content of ascorbate and the acclimation of photosynthesis to changing light levels. Leaf ascorbate content was highly light dependent in Nicotiana tobaccum being double in high compared with low light conditions. In contrast ascorbate oxidase activity was not altered by changing light levels. Transgenic tobacco lines with reduced or enhanced AO activity exhibited no morphological phenotype and photosynthesis under high light was similarly impaired irrespective of the measured AO activity. However further investigation between AO activity and leaf acclimation to changing light intensity revealed a suite of metabolic and transcriptome changes indicating a role for the apoplastic ascorbate pool in chloroplast to nucleus communication. In all genotypes, transcripts associated with ascorbate synthesis and recycling were less abundant following transition from high to low light. However transcripts associated with glutathione recycling, light harvesting, reaction centre function and the Calvin cycle were all increased in abundance. Following the transition from high to low light increases in leaf threonate, an ascorbate degradation product, were proportional to AO activity. A number of chloroplast synthesised amino acids were significantly increased both during high light and following transfer back to LL for 12 h. Similarly, several primary carbohydrates and TCA intermediates were significantly enhanced following high light treatment. In addition to light effects, AO activity had a significant impact on ï¢-alanine, aspartate and threonine. Intriguingly, a large number of fatty acids were reduced in antisense AO and wild-type plants immediately after high light stress however the content of these compounds were significantly increased in overexpressing sense lines. We conclude that AO mediated turnover plays an important role in adjusting cellular ascorbate content to photosynthetic need in a fluctuating light environment and that light mediated signals rapidly adjust that the apoplastic ascorbate pool.

Project description:The triose-phosphate/phosphate translocator (TPT) of the chloroplast inner envelope membrane mediates the counter-exchange of stromal triose phosphates derived from CO2 fixation with cytosolic phosphate, thus providing the cytosol with precursors for sucrose synthesis. We have isolated an Arabidopsis mutant (tpt-1) in which the gene encoding TPT is disrupted by a T-DNA insertion. During growth in low light tpt-1 plants are phenotypically normal, but in high light photosynthesis is inhibited and growth is retarded relative to wildtype. This mutant compensates for the absence of TPT by diverting photosynthate into starch which is hydrolysed and exported from the chloroplast as glucose that is subsequently phosphorylated by hexokinase. In low light the capacity of the pathway of starch synthesis is sufficient to accommodate the normal rate of CO2 fixation, but in high light it is unable to match the potential rate of CO2 fixation. Consequently, in high light-grown plants there are measurable effects on the redoxstate of several components. Thus, the tpt-1 mutation influences the carbohydrate status within the cell, alters the form in which carbon is received by the cytosol, and changes the redox signals that are important in photosynthetic acclimation. Method: Plants will be grown in a 8h light:16h dark regime at both 400 and 100 Âµmol PAR m-2 s-1. Total RNA will be extracted from pools of individual illuminated leaves from at least eight plants at growth stage 3.70. Leaves will be harvested 2 h into the photoperiod to maximise differences between plant lines in the expression of genes of photosynthesis and carbohydrate metabolism. We anticipate that expression of many genes will be affected by the absence of TPT and by changes in light intensity. However, by comparing differences in transcript levels between wildtype and TPT mutant grown in high light with the differences that occur in plants grown in low light we will discriminate between genes whose expression is affected by changes in the pattern of carbohydrate metabolism and those influenced by redox poise of the thylakoid photochemical components. These comparisons will also highlight genes affected by recently identified regulatory interactions between sugar-sensing and redox-sensing. A genome-wide expression study will establish the extent to which gene expression is altered by the absence of TPT in leaves, and will provide the basis for more detailed analysis of a selected range of transcripts whose levels of expression differ between plant lines.

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Inositol Pyrophosphates Mediate Chloroplast Lipid Remodeling and Nuclear Gene Repression during High-Light Acclimation in Chlamydomonas reinhardtii

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