Stress and light spectral quality influence the transcriptome of a tomato crop on the International Space Station

BACKGROUND: Spaceflight introduces unique environmental stresses that challenge plant growth and development, necessitating an understanding of molecular responses to enable sustainable agriculture for long-duration missions. This study investigated the transcriptomic responses of tomato (Solanum lycopersicum cv. 'Red Robin') grown under red- and blue-rich light spectra aboard the International Space Station (ISS) and in ground controls at Kennedy Space Center. Using RNA sequencing, we analyzed leaf and adventitious root tissues to uncover gene expression changes driven by spaceflight conditions and light quality. RESULTS: Our results revealed significant transcriptomic alterations influenced by both spaceflight and lighting spectra. Differential gene expression analysis identified numerous up- and downregulated genes in flight samples compared to ground controls, with adventitious roots displaying pronounced transcriptional changes. Genes associated with stress responses, hormonal signaling, and metabolic pathways were prominently upregulated in spaceflight-grown tissues. Gene ontology and KEGG pathway enrichment analyses highlighted critical roles for oxidative stress response, secondary metabolite biosynthesis, and hormonal regulation. Additionally, red-rich lighting appeared to stabilize gene expression patterns, while blue-rich lighting induced greater variability across conditions. Notably, spaceflight exhibited extensive adventitious roots formation, with gene clusters enriched in antioxidant metabolism, cell wall remodeling, and stress adaptation processes. Leaf tissues demonstrated distinct transcriptional signatures under flight and ground conditions, with blue-rich lighting enhancing stress-responsive pathways and red-rich lighting favoring metabolic stability. CONCLUSIONS: This study provides novel insights into the molecular mechanisms underlying plant adaptation to spaceflight and variable lighting conditions, emphasizing the importance of tailored environmental control for optimizing crop production in space. These findings could have implications for developing resilient plant varieties suitable for extreme environments, both in extraterrestrial settings and on Earth.