Abstract
BackgroundPlants adapted to diverse environments on Earth throughout their evolutionary history, and developed mechanisms to thrive in a variety of terrestrial habitats. When plants are grown in the novel environment of spaceflight aboard the International Space Station (ISS), an environment completely outside their evolutionary history, they respond with unique alterations to their gene expression profile. Identifying the genes important for physiological adaptation to spaceflight and dissecting the biological processes and pathways engaged by plants during spaceflight has helped reveal spaceflight adaptation, and has furthered understanding of terrestrial growth processes. However, the underlying regulatory mechanisms responsible for these changes in gene expression patterns are just beginning to be explored. Epigenetic modifications, such as DNA methylation at position five in cytosine, has been shown to play a role in the physiological adaptation to adverse terrestrial environments, and may play a role in spaceflight as well.ResultsWhole Genome Bisulfite Sequencing of DNA of Arabidopsis grown on the ISS from seed revealed organ-specific patterns of differential methylation compared to ground controls. The overall levels of methylation in CG, CHG, and CHH contexts were similar between flight and ground DNA, however, thousands of specifically differentially methylated cytosines were discovered, and there were clear organ-specific differences in methylation patterns. Spaceflight leaves had higher methylation levels in CHG and CHH contexts within protein-coding genes in spaceflight; about a fifth of the leaf genes were also differentially regulated in spaceflight, almost half of which were associated with reactive oxygen signaling.ConclusionsThe physiological adaptation of plants to spaceflight is likely nuanced by epigenomic modification. This is the first examination of differential genomic methylation from plants grown completely in the spaceflight environment of the ISS in plant growth hardware developed for informing exploration life support strategies. Yet even in this optimized plant habitat, plants respond as if stressed. These data suggest that gene expression associated with physiological adaptation to spaceflight is regulated in part by methylation strategies similar to those engaged with familiar terrestrial stress responses. The differential methylation maps generated here provide a useful reference for elucidating the layers of regulation of spaceflight responses.
Highlights
Plants adapted to diverse environments on Earth throughout their evolutionary history, and developed mechanisms to thrive in a variety of terrestrial habitats
This study examined the role of DNA methylation, in particular, 5mCyt, in spaceflight-grown plants with the expectation of elucidating functional linkages between epigenetics and spaceflight adaptation
Arabidopsis seedlings demonstrated near typical terrestrial growth patterns in the veggie hardware of International Space Station (ISS) The three plates of Arabidopsis plants showed near typical germination and plant growth within the Veggie hardware of the ISS
Summary
Plants adapted to diverse environments on Earth throughout their evolutionary history, and developed mechanisms to thrive in a variety of terrestrial habitats. The underlying regulatory mechanisms responsible for these changes in gene expression patterns are just beginning to be explored Epigenetic modifications, such as DNA methylation at position five in cytosine, has been shown to play a role in the physiological adaptation to adverse terrestrial environments, and may play a role in spaceflight as well. Plants physiologically adapt to spaceflight using strategies that mimic several aspects of familiar terrestrial environmental responses, even though the spaceflight response is distinct from any singular terrestrial response. Among those strategies are transcriptomic and proteomic alterations that are increasingly well defined as more experiments are conducted on the International Space Station (ISS). Of particular note is that there are substantial differences in gene expression patterns even among tissue sources of the same genotype; Arabidopsis leaves, hypocotyls, roots, and root tips all have markedly different spaceflight transcriptomes, as do undifferentiated cell cultures [13, 14, 16, 18]
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