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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 under-standing of the cellular signaling networks that control carbon flux and acclimation to envi-ronmental stress remains incomplete. In this study, we used the Chlamydomonas reinhard-tii 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. Our results indicate that PP-InsPs participate in the regulation of carbon storage in the form of starch and their deficiency increases TAGs levels in the algal cells. They also impact chloroplast-specific lipid remodeling by modifying membrane composition and fluidity through fatty acid desatu-rations and glycerolipid composition. In addition, our findings suggest that PP-InsPs are in-volved in chloroplast-nucleus communication, where they coordinate transcriptional repres-sion 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 environmental cues such as high light. These data uncover a novel function of PP-InsPs in high light acclimation and potentially in chloroplast-nucleus communication, providing new insights that may help engineering more resilient and efficient strains.

INSTRUMENT(S): Liquid Chromatography MS - negative - reverse-phase

PROVIDER: MTBLS14720 | MetaboLights | 2026-06-09

REPOSITORIES: MetaboLights

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			Action	DRS
	a_MTBLS14720_LC-MS_negative_reverse-phase.txt	Txt
	i_Investigation.txt	Txt
	m_MTBLS14720_LC-MS_reverse-phase_metabolite_profiling_v2_maf.tsv	Tabular
	s_MTBLS14720.txt	Txt

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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.

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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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