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Pectin methylesterase gene AtPMEPCRA contributes to physiological adaptation to simulated and spaceflight microgravity in Arabidopsis.

ABSTRACT: Pectin is biosynthesized in a highly methylated form and is partially de-methylated by pectin methylesterase (PME) activity. Plant PMEs play a critical role in cell wall remodeling in many physiological processes. Here, we studied Arabidopsis seedlings, which had been exposed to simulated or actual microgravity. Simulated microgravity inhibited total PME activity in Arabidopsis seedlings. We identified that AtPMEPCRA expression played a major role in the microgravity-induced inhibition of PME activity. atpmepcra mutants did not exhibit the enlarged leaf area of Arabidopsis seedlings observed under spaceflight microgravity. The downregulation of AtPMEPCRA expression in response to microgravity was due, in part, to changes in methylation patterns. The sexual offspring of the plants grown during spaceflight retained the methylation changes at AtPMEPCRA locus for one generation and thus contribute to the physiological adaptation to microgravity among F₁ offspring seed generation. We conclude that AtPMEPCRA contributes to the spaceflight-induced transgenerational responses in Arabidopsis.

SUBMITTER: Xu P

PROVIDER: S-EPMC9118689 | biostudies-literature | 2022 May

REPOSITORIES: biostudies-literature

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Pectin methylesterase gene <i>AtPMEPCRA</i> contributes to physiological adaptation to simulated and spaceflight microgravity in Arabidopsis.

Xu Peipei P Chen Haiying H Hu Jinbo J Pang Xiaocheng X Jin Jing J Cai Weiming W

iScience 20220429 5

Pectin is biosynthesized in a highly methylated form and is partially de-methylated by pectin methylesterase (PME) activity. Plant PMEs play a critical role in cell wall remodeling in many physiological processes. Here, we studied Arabidopsis seedlings, which had been exposed to simulated or actual microgravity. Simulated microgravity inhibited total PME activity in Arabidopsis seedlings. We identified that <i>AtPMEPCRA</i> expression played a major role in the microgravity-induced inhibition of ...[more]

PMID: 35602950

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Project description:Experimentation on the International Space Station has reached the stage where repeated and nuanced transcriptome studies are beginning to illuminate the structural and metabolic differences between plants grown in space compared to plants on the Earth. Genes that are important in establishing the spaceflight responses are being identified, their roles in spaceflight physiological adaptation are increasingly understood, and the fact that different genotypes adapt differently is recognized. However, the basic question of whether these spaceflight responses are actually required for survival has yet to be posed, and the fundamental notion that spaceflight responses may be non-adaptive has yet to be explored. Therefore the experiments presented here were designed to ask if portions of the plant spaceflight response can be genetically removed without causing loss of spaceflight survival and without causing increased stress responses. The CARA experiment compared the spaceflight transcriptome responses in the root tips of two Arabidopsis ecotypes, Col-0 and WS, as well as that of a PhyD mutant of Col-0. When grown with the ambient light of the ISS, phyD plants displayed a significantly reduced spaceflight transcriptome response compared to Col-0, suggesting that altering the activity of a single gene can actually improve spaceflight adaptation by reducing the transcriptome cost of physiological adaptation. The WS genotype showed an even simpler spaceflight transcriptome response in the ambient light of the ISS, more broadly indicating that the plant genotype can be manipulated to reduce the cost of spaceflight adaptation, as measured by transcriptional response. These differential genotypic responses suggest that genetic manipulation could further reduce, or perhaps eliminate the metabolic cost of spaceflight adaptation. When plants were germinated and then left in the dark on the ISS, the WS genotype actually mounted a larger transcriptome response than Col-0, suggesting that the in-space light environment affects physiological adaptation, which implies that manipulating the local habitat can also substantially impact the metabolic cost of spaceflight adaptation.

Project description:The Heat Shock Factor A2 (HsfA2), as a part of the HSF network, is essential to the plant’s response to almost any environmental stress and to the cellular homeostatic control mechanisms. Plant cell cultures disabled in HsfA2 function were grown aboard the International Space Station (ISS) in order to ascertain whether or not they use the same terrestrially effective systems to adapt to the novel environment of spaceflight. Cultured lines of Arabidopsis thaliana derived from wild type (WT) cultivar Col-0 and from a knock-out line deficient in the gene encoding HSFA2 (HSFA2 KO) were launched to the ISS on SpaceX-2 as part of the Cellular Expression Logic (CEL) experiment of the BRIC17 spaceflight mission and were fixed in-flight after 10 days on orbit. Microarray gene expression data were analyzed using a two-part comparative approach. First, differentially expressed genes were identified between the environments (spaceflight to ground) within cells of the same genotype, which represented physiological adaptation to the spaceflight environment. Second, gene expression profiles were identified between the genotypes (HSFA2 KO to WT) within the same environment, defining genes uniquely required by the two genotypes in the ground and spaceflight adapted states. The physiological state of the cells as a result of disabling a gene has tremendous control over the mechanisms induced to adapt to the environment of spaceflight. The HsfA2 demonstrated a role in the physiological adaptation to the spaceflight environment since the cells disabled in the HsfA2 gene used substantially different genes to achieve the spaceflight adapted state than the WT cells. The endoplasmic reticulum (ER) stress and unfolded protein response (UPR) define the HSFA2 KO cells’ physiological state regardless of the environment and likely result from the deficiency in the chaperone-mediated protein folding machinery. HsfA2 seems to have a universal stress response role but also specific roles in the physiological adaptation to spaceflight through cell wall remodeling, signal perception and transduction and starch biosynthesis. Implementation of knock-out cells identified a set of genes with a required expression level in order for a cell to achieve a spaceflight-adapted state. The HSFA2 KO cells helped to unravel the HsfA2-dependent genes of the adaption of wild type cells to the environment of spaceflight.

Project description:BackgroundPectin methylesterases (PMEs) catalyze the demethylesterification of homogalacturonans in the cell wall; their activity is regulated in part by pectin methylesterase inhibitors (PMEIs). PME activity may result in either rigidification or loosening of the cell wall, depending on the mode of demethylesterification. The activity of PMEs in the middle lamella is expected to affect intrusive elongation of phloem fibers, and their adhesion to adjacent cells. Length and extractability of phloem fibers are qualities important for their industrial uses in textiles and composites. As only three flax PMEs had been previously described, we were motivated to characterize the PME and PMEI gene families of flax.ResultsWe identified 105 putative flax PMEs (LuPMEs) and 95 putative PMEIs (LuPMEIs) within the whole-genome assembly. We found experimental evidence for the transcription of 77/105 LuPMEs and 83/95 LuPMEIs, and surveyed the transcript abundance of these in 12 different tissues and stages of development. Six major monophyletic groups of LuPMEs could be defined based on the inferred relationships of flax genes and their presumed orthologs from other species. We searched the LuPMEs and LuPMEIs for conserved residues previously reported to be important for their tertiary structure and function. In the LuPMEs, the most highly conserved residues were catalytic residues while in the LuPMEIs, cysteines forming disulfude bridges between helices α2 and α3 were most highly conserved. In general, the conservation of critical residues was higher in the genes with evidence of transcript expression than in those for which no expression was detected.ConclusionsThe LuPMEs and LuPMEIs comprise large families with complex patterns of transcript expression and a wide range of physical characteristics. We observed that multiple PMEs and PMEIs are expressed in partially overlapping domains, indicative of several genes acting redundantly during most processes. The potential for functional redundancy was highlighted also by the phylogenetic analyses. We were able to identify a subset of PME and PMEIs that appeared particularly relevant to fiber development, which may provide a basis for the improvement of key traits in industrial feedstocks and a better understanding of the physiological roles of PMEs and PMEIs in general.

Dataset Information

Pectin methylesterase gene AtPMEPCRA contributes to physiological adaptation to simulated and spaceflight microgravity in Arabidopsis.

Publications

Pectin methylesterase gene <i>AtPMEPCRA</i> contributes to physiological adaptation to simulated and spaceflight microgravity in Arabidopsis.

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