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A member of the CONSTANS-Like protein family is a putative regulator of reactive oxygen species homeostasis and spaceflight physiological adaptation.

ABSTRACT: A feature of the physiological adaptation to spaceflight in Arabidopsis thaliana (Arabidopsis) is the induction of reactive oxygen species (ROS)-associated gene expression. The patterns of ROS-associated gene expression vary among Arabidopsis ecotypes, and the role of ROS signalling in spaceflight acclimation is unknown. What could differences in ROS gene regulation between ecotypes on orbit reveal about physiological adaptation to novel environments? Analyses of ecotype-dependent responses to spaceflight resulted in the elucidation of a previously uncharacterized gene (OMG1) as being ROS-associated. The OMG1 5' flanking region is an active promoter in cells where ROS activity is commonly observed, such as in pollen tubes, root hairs, and in other tissues upon wounding. qRT-PCR analyses revealed that upon wounding on Earth, OMG1 is an apparent transcriptional regulator of MYB77 and GRX480, which are associated with the ROS pathway. Fluorescence-based ROS assays show that OMG1 affects ROS production. Phylogenetic analysis of OMG1 and closely related homologs suggests that OMG1 is a distant, unrecognized member of the CONSTANS-Like protein family, a member that arose via gene duplication early in the angiosperm lineage and subsequently lost its first DNA-binding B-box1 domain. These data illustrate that members of the rapidly evolving COL protein family play a role in regulating ROS pathway functions, and their differential regulation on orbit suggests a role for ROS signalling in spaceflight physiological adaptation.

SUBMITTER: Sng NJ

PROVIDER: S-EPMC6348315 | biostudies-literature | 2019 Feb

REPOSITORIES: biostudies-literature

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A member of the CONSTANS-Like protein family is a putative regulator of reactive oxygen species homeostasis and spaceflight physiological adaptation.

Sng Natasha J NJ Kolaczkowski Bryan B Ferl Robert J RJ Paul Anna-Lisa AL

AoB PLANTS 20181215 1

A feature of the physiological adaptation to spaceflight in Arabidopsis thaliana (Arabidopsis) is the induction of reactive oxygen species (ROS)-associated gene expression. The patterns of ROS-associated gene expression vary among Arabidopsis ecotypes, and the role of ROS signalling in spaceflight acclimation is unknown. What could differences in ROS gene regulation between ecotypes on orbit reveal about physiological adaptation to novel environments? Analyses of ecotype-dep ...[more]

PMID: 30705745

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Project description:Scientific access to spaceflight and especially the International Space Station has revealed that physiological adaptation to spaceflight is accompanied or enabled by changes in gene expression that significantly alter the transcriptome of cells in spaceflight. A wide range of experiments have shown that plant physiological adaptation to spaceflight involves gene expression changes that alter cell wall and other metabolisms. However, while transcriptome profiling aptly illuminates changes in gene expression that accompany spaceflight adaptation, mutation analysis is required to illuminate key elements required for that adaptation. Here we report how transcriptome profiling was used to gain insight into the spaceflight adaptation role of Altered response to gravity 1 (Arg1), a gene known to affect gravity responses in plants on Earth. The study compared expression profiles of cultured lines of Arabidopsis thaliana derived from wild-type (WT) cultivar Col-0 to profiles from a knock-out line deficient in the gene encoding ARG1 (ARG1 KO), both on the ground and in space. The cell lines were launched on SpaceX CRS-2 as part of the Cellular Expression Logic (CEL) experiment of the BRIC-17 spaceflight mission. The cultured cell lines were grown within 60 mm Petri plates in Petri Dish Fixation Units (PDFUs) that were housed within the Biological Research In Canisters (BRIC) hardware. Spaceflight samples were fixed on orbit. Differentially expressed genes were identified between the two environments (spaceflight and comparable ground controls) and the two genotypes (WT and ARG1 KO). Each genotype engaged unique genes during physiological adaptation to the spaceflight environment, with little overlap. Most of the genes altered in expression in spaceflight in WT cells were found to be Arg1-dependent, suggesting a major role for that gene in the physiological adaptation of undifferentiated cells to spaceflight. Key Words: ARG1-Spaceflight-Gene expression-Physiological adaptation-BRIC. Astrobiology 17, 1077-1111.

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:KRIT1 is a gene responsible for Cerebral Cavernous Malformations (CCM), a major cerebrovascular disease characterized by abnormally enlarged and leaky capillaries that predispose to seizures, focal neurological deficits, and fatal intracerebral hemorrhage. Comprehensive analysis of the KRIT1 gene in CCM patients has suggested that KRIT1 functions need to be severely impaired for pathogenesis. However, the molecular and cellular functions of KRIT1 as well as CCM pathogenesis mechanisms are still research challenges. We found that KRIT1 plays an important role in molecular mechanisms involved in the maintenance of the intracellular Reactive Oxygen Species (ROS) homeostasis to prevent oxidative cellular damage. In particular, we demonstrate that KRIT1 loss/down-regulation is associated with a significant increase in intracellular ROS levels. Conversely, ROS levels in KRIT1(-/-) cells are significantly and dose-dependently reduced after restoration of KRIT1 expression. Moreover, we show that the modulation of intracellular ROS levels by KRIT1 loss/restoration is strictly correlated with the modulation of the expression of the antioxidant protein SOD2 as well as of the transcriptional factor FoxO1, a master regulator of cell responses to oxidative stress and a modulator of SOD2 levels. Furthermore, we show that the KRIT1-dependent maintenance of low ROS levels facilitates the downregulation of cyclin D1 expression required for cell transition from proliferative growth to quiescence. Finally, we demonstrate that the enhanced ROS levels in KRIT1(-/-) cells are associated with an increased cell susceptibility to oxidative DNA damage and a marked induction of the DNA damage sensor and repair gene Gadd45alpha, as well as with a decline of mitochondrial energy metabolism. Taken together, our results point to a new model where KRIT1 limits the accumulation of intracellular oxidants and prevents oxidative stress-mediated cellular dysfunction and DNA damage by enhancing the cell capacity to scavenge intracellular ROS through an antioxidant pathway involving FoxO1 and SOD2, thus providing novel and useful insights into the understanding of KRIT1 molecular and cellular functions.

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.

Dataset Information

A member of the CONSTANS-Like protein family is a putative regulator of reactive oxygen species homeostasis and spaceflight physiological adaptation.

Publications

A member of the CONSTANS-Like protein family is a putative regulator of reactive oxygen species homeostasis and spaceflight physiological adaptation.

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