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A multifaceted analysis reveals two distinct phases of chloroplast biogenesis during de-etiolation in Arabidopsis.

ABSTRACT: Light triggers chloroplast differentiation whereby the etioplast transforms into a photosynthesizing chloroplast and the thylakoid rapidly emerges. However, the sequence of events during chloroplast differentiation remains poorly understood. Using Serial Block Face Scanning Electron Microscopy (SBF-SEM), we generated a series of chloroplast 3D reconstructions during differentiation, revealing chloroplast number and volume and the extent of envelope and thylakoid membrane surfaces. Furthermore, we used quantitative lipid and whole proteome data to complement the (ultra)structural data, providing a time-resolved, multi-dimensional description of chloroplast differentiation. This showed two distinct phases of chloroplast biogenesis: an initial photosynthesis-enabling 'Structure Establishment Phase' followed by a 'Chloroplast Proliferation Phase' during cell expansion. Moreover, these data detail thylakoid membrane expansion during de-etiolation at the seedling level and the relative contribution and differential regulation of proteins and lipids at each developmental stage. Altogether, we establish a roadmap for chloroplast differentiation, a critical process for plant photoautotrophic growth and survival.

SUBMITTER: Pipitone R

PROVIDER: S-EPMC7906606 | biostudies-literature |

REPOSITORIES: biostudies-literature

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APYRASE1/2 mediate red light-induced de-etiolation growth in Arabidopsis seedlings.

Project description:In etiolated seedlings, red light (R) activates phytochrome and initiates signals that generate major changes at molecular and physiological levels. These changes include inhibition of hypocotyl growth and promotion of the growth of primary roots, apical hooks, and cotyledons. An earlier report showed that the sharp decrease in hypocotyl growth rapidly induced by R was accompanied by an equally rapid decrease in the transcript and protein levels of two closely related apyrases (APYs; nucleoside triphosphate-diphosphohydrolases) in Arabidopsis (Arabidopsis thaliana), APY1 and APY2, enzymes whose expression alters auxin transport and growth in seedlings. Here, we report that single knockouts of either APY inhibit R-induced promotion of the growth of primary roots, apical hooks, and cotyledons, and RNAi-induced suppression of APY1 expression in the background of apy2 inhibits R-induced apical hook opening. When R-irradiated primary roots and apical hook-cotyledons began to show a gradual increase in their growth relative to dark controls, they concurrently showed increased levels of APY protein, but in hook-cotyledon tissue, this occurred without parallel increases in their transcripts. In wild-type seedlings whose root growth is suppressed by the photosynthesis inhibitor 3-(3,4-dichlorophenyl)-1,1-dimethylurea, the R-induced increased APY expression in roots was also inhibited. In unirradiated plants, the constitutive expression of APY2 promoted both hook opening and changes in the transcript abundance of Small Auxin Upregulated RNA (SAUR), SAUR17 and SAUR50 that help mediate de-etiolation. These results provide evidence that the expression of APY1/APY2 is regulated by R and that APY1/APY2 participate in the signaling pathway by which phytochrome induces differential growth changes in different tissues of etiolated seedlings.

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<i>Arabidopsis</i> SPA2 represses seedling de-etiolation under multiple light conditions.

Project description:In Arabidopsis, phytochrome (phy) A, phyB, and cryptochrome 1 (cry1) are representative far-red, red, and blue light photoreceptors, respectively. Members of the SUPPRESSOR OF PHYA-105 (SPA) protein family (SPA1-SPA4) form E3 ubiquitin ligase complexes with CONSTITUTIVE PHOTOMORPHOGENIC1 (COP1), which mediates the degradation of photomorphogenesis-promoting factors to desensitize light signaling. SPA2 has been reported to promote seedling etiolation in the dark. However, the unique roles of SPA2 and its three functional domains in suppressing photomorphogenesis under different light conditions are largely unknown. Here, we demonstrate that overexpression of the full-length or the central coiled-coil and C-terminal WD-repeat domains of SPA2 cause hyper-etiolation phenotypes under several light conditions. The SPA2 central coiled-coil and C-terminal WD-repeat domains are necessary and sufficient for repressing seedling de-etiolation, cotyledon unfolding, and promoting hypocotyl negative gravitropism under several light conditions. Furthermore, phyA, phyB, cry1, and COP1 repress protein accumulation or nuclear translocation of SPA2 through direct interactions with its kinase-like and coiled-coil domains located in the N-terminus in response to far-red, red, and blue light treatments, respectively. Taken together, our results demonstrate that SPA2 functions under multiple light conditions; moreover, light-activated photoreceptors rapidly suppress SPA2 activity via direct interactions in response to different light treatments.

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Establishment of photosynthesis through chloroplast development is controlled by two distinct regulatory phases

Project description:A pluripotent inducible cell line was generated from Arabidopsis to address the limitations of traditional in planta dicot systems and to develop a well-controlled experimental setup where the individual regulatory check points of chloroplast development could be defined. Following light exposure, this cell line was shown to differentiate into photosynthetically active cells with functional chloroplasts providing an experimental system with a temporal gradient of chloroplast development. Using this unique cell line from the dicot Arabidopsis we could demonstrate that the development from a proplastid to a functional chloroplast, and thereby the establishment of photosynthesis, is dependent on a regulatory mechanism involving two distinct phases. First, light exposure triggers an initial change in gene expression, metabolite profile, chlorophyll accumulation and plastid structure. Secondly, a second signal, most likely triggered by activation of the chloroplast, is required for full transition to a functional chloroplast and the shift from heterotrophic to photoautotrophic metabolism.

2018-05-12 | E-MTAB-5777 | biostudies-arrayexpress

GENOMES UNCOUPLED1 plays a key role during the de-etiolation process in Arabidopsis.

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Expression data from Arabidopsis during de-etiolation

Project description:Arabidopsis fc2-1 mutants fail to properly de-etiolate after a prolonged period in the dark. Our goal was to monitor whole genome expression during the first 2 hours of de-etiolation to determine the cuase of this growth arrest. In comparison with other mutants that also affect de-etiolation, we identified a subset of genes specifically regulated by FC2 function during de-etiolation.

2015-08-06 | GSE71764 | GEO

Autophagy mutants show delayed chloroplast development during de-etiolation in carbon limiting conditions

Project description:Autophagy is a conserved catabolic process that plays an essential role under nutrient starvation condition and influences different developmental processes. We observed that seedlings of autophagy mutants (atg2, atg5, atg7, and atg9) germinated in the dark showed delayed chloroplast development following illumination. The delayed chloroplast development was characterized by a decrease in photosynthetic and chlorophyll biosynthetic proteins, lower chlorophyll content, reduced chloroplast size, and increased levels of proteins involved in lipid biosynthesis. Confirming the biological impact of these differences, photosynthetic performance was impaired in autophagy mutants 12h post illumination. We observed that while gene expression for photosynthetic machinery during de-etiolation was largely unaffected in atg mutants, several genes involved in photosystem assembly were transcriptionally downregulated. We also investigated if the delayed chloroplast development could be explained by lower lipid import to the chloroplast or lower triglyceride (TAG) turnover. We observed that the limitations in the chloroplast lipid import imposed by trigalactosyldiacylglycerol1 are unlikely to explain the delay in chloroplast development. However, we found that lower TAG mobility in the triacylglycerol lipase mutant sugardependent1 significantly affected de-etiolation. Moreover, we showed that lower levels of carbon resources exacerbated the slow-greening phenotype whereas higher levels of carbon resources had an opposite effect. This work suggests a lack of autophagy machinery limits chloroplast development during de-etiolation, and this is exacerbated by limited lipid turnover (lipophagy) that physically or energetically restrains chloroplast development.

2021-08-04 | GSE156677 | GEO

Tissue specific light response during Arabidopsis de-etiolation

Project description:The time between seed germination and the development of the first true leaves is crucial for plants success. Depending on the environmental light conditions a plant must decide which developmental program to use. If light is limited, the seedling will use etiolated growth characterized by an elongated hypocotyl and tightly-closed, underdeveloped cotyledons, thus allowing it to reach a light source as quickly as possible. In contrast, seedlings that are grown in unlimited light will use de-etiolation growth, that is characterized by inhibited hypocotyl growth and unhooked, unfolded and fully expanded cotyledons. These seedlings become photosynthetic and increase their chances for reproduction. Interestingly, the outcome of the light signal varies between the seedling’s different organs, e.g. hypocotyl growth is inhibited by light whereas cotyledon expansion is induced. Separating the cotyledons and hypocotyls of de-etiolated seedlings during their first 12 hours of white light exposure, enabled us to perform individual transcriptome analyses of each organ and to examine what causes this variation in light responsiveness.

2020-04-20 | GSE132861 | GEO

Mutant-Based Model of Two Independent Pathways for Carotenoid-Mediated Chloroplast Biogenesis in Arabidopsis Embryos.

Project description:Chloroplasts are essential for autonomous plant growth, and their biogenesis is a complex process requiring both plastid and nuclear genome. One of the essential factors required for chloroplast biogenesis are carotenoids. Carotenoids are synthesized in plastids, and it was shown that plastid localized methylerythritol 4-phosphate (MEP) pathway provides substrates for their biosynthesis. Here, we propose a model, using results of our own mutant analysis combined with the results of others, that a MEP-independent pathway, likely a mevalonate (MVA)-dependent pathway, provides intermediates for chloroplast biogenesis in Arabidopsis embryos. The pattern of this chloroplast biogenesis differs from the MEP-dependent chloroplast biogenesis. In MEP-dependent chloroplast biogenesis, chloroplasts are formed rather uniformly in the whole embryo, with stronger chlorophyll accumulation in cotyledons. In a MEP-independent pathway, chloroplasts are formed predominantly in the hypocotyl and in the embryonic root. We also show that this pattern of chlorophyll accumulation is common to MEP pathway mutants as well as to the mutant lacking geranylgeranyl diphosphate synthase 11 (GGPPS11) activity in plastids but expressing it in the cytosol (GGPPS11cyt). It was recently described that shorter GGPPS11 transcripts are present in Arabidopsis, and they can be translated into active cytosolic proteins. We therefore propose that the MEP-independent pathway for chloroplast biogenesis in Arabidopsis embryos is an MVA pathway that provides substrates for the synthesis of GGPP via GGPPS11cyt and this is then transported to plastids, where it is used for carotenoid biosynthesis and subsequently for chloroplast biogenesis mainly in the hypocotyl and in the embryonic root.

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Expression data from Arabidopsis during de-etiolation

2015-08-06 | E-GEOD-71764 | biostudies-arrayexpress

Proteomics of Arabidopsis seedlings during de-etiolation

Project description:Light triggers chloroplast differentiation whereby the etioplast transforms into a photosynthesizing chloroplast and the thylakoid rapidly emerges. However, the sequence of events during chloroplast differentiation remains poorly understood. Here we used whole-seedling proteome data to quantify changes in protein abundances during the course of de-etiolation within the first four days of light exposure. This data complements quantitative lipid and (ultra)structural data described in Pipitone et al. (doi: https://doi.org/10.1101/2020.08.30.274043).

2021-02-16 | PXD021518 | Pride

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