Abstract
Background: Plants subjected to the novel environment of spaceflight show transcriptomic changes that resemble aspects of several terrestrial abiotic stress responses. Under investigation here is whether epigenetic modulations, similar to those that occur in terrestrial stress responses, have a functional role in spaceflight physiological adaptation. The Advanced Plant Experiment-04 – Epigenetic Expression experiment examined the role of cytosine methylation in spaceflight adaptation. The experiment was conducted onboard the International Space Station, and evaluated the spaceflight-altered, genome-wide methylation profiles of two methylation-regulating gene mutants [methyltransferase 1 (met1-7) and elongator complex subunit 2 (elp2-5)] along with a wild-type Col-0 control.Results: The elp2-5 plants suffered in their physiological adaptation to spaceflight in that their roots failed to extend away from the seed and the overall development of the plants was greatly impaired in space. The met1-7 plants suffered less, with their morphology affected by spaceflight in a manner similar to that of the Col-0 controls. The differentially expressed genes (DEGs) in spaceflight were dramatically different in the elp2-5 and met1-7 plants compared to Col-0, indicating that the disruptions in these mutants resulted in a reprogramming of their spaceflight responses, especially in elp2-5. Many of the genes comprising the spaceflight transcriptome of each genotype were differentially methylated in spaceflight. In Col-0 the majority of the DEGs were representative of the now familiar spaceflight response, which includes genes associated with cell wall remodeling, pathogen responses and ROS signaling. However, the spaceflight transcriptomes of met1-7 and elp2-5 each presented patterns of DEGs that are almost completely different than Col-0, and to each other. Further, the DEGs of the mutant genotypes suggest a more severe spaceflight stress response in the mutants, particularly in elp2-5.Conclusion: Arabidopsis physiological adaptation to spaceflight results in differential DNA methylation in an organ-specific manner. Disruption of Met1 methyltransferase function does not dramatically affect spaceflight growth or morphology, yet met1-7 reprograms the spaceflight transcriptomic response in a unique manner. Disruption of elp2-5 results in poor development in spaceflight grown plants, together with a diminished, dramatically reprogrammed transcriptomic response.
Highlights
Plants cope with environmental changes by reprogramming gene expression and metabolic processes necessary for growth, development, and survival (e.g., Hirayama and Shinozaki, 2010; Sewelam et al, 2014; Lopez-Ruiz et al, 2020)
Col-0 and met1-7 exhibited a typical growth morphology of Arabidopsis grown in Veggie during spaceflight (Figure 1A)
For both Col-0 and met1-7 the spaceflight (FT) roots adopt a slightly randomized growth habit compared to the ground controls (GCs), yet extend well away from the site of germination and the stem, and are generally negatively phototropic in response to the “vertical” orientation of the plates relative to the light source in the Veggie growth habitat
Summary
Plants cope with environmental changes by reprogramming gene expression and metabolic processes necessary for growth, development, and survival (e.g., Hirayama and Shinozaki, 2010; Sewelam et al, 2014; Lopez-Ruiz et al, 2020). The adaptability of a genotype to changing environmental conditions is determined by its genome and gene activity, both of which are in turn influenced by epigenetic factors such as DNA methylation (e.g., Dowen et al, 2012; Zhang et al, 2018). The APEX-04 EPEX spaceflight experiment investigated the role of specific epigenomic changes in determining the physiological adaptation of plants to the spaceflight environment. DNA methylation profiles within a genome are dynamic and complex, yet integral to plant growth, development, and stress responses (reviewed in: Bartels et al, 2018). Genome-wide DNA methylation and gene expression alterations occurred in plants grown for part of their life cycle in a satellite experiment (Xu et al, 2018). Under investigation here is whether epigenetic modulations, similar to those that occur in terrestrial stress responses, have a functional role in spaceflight physiological adaptation. The experiment was conducted onboard the International Space Station, and evaluated the spaceflight-altered, genome-wide methylation profiles of two methylation-regulating gene mutants [methyltransferase 1 (met1-7) and elongator complex subunit 2 (elp2-5)] along with a wild-type Col-0 control
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