Genetic Alterations of the Putrescine Metabolic Pathway in Arabidopsis thaliana Lead to Attenuated Morphological and Transcriptomic Responses to the Spaceflight Conditions of the International Space Station

This study investigates the impact of altering the polyamine (putrescine, Put) metabolic pathway on plant responses to spaceflight conditions in Arabidopsis thaliana . By engineering lines with modified Put synthesis and degradation pathways, we observed distinct transcriptional and phenotypic responses to spaceflight. Put-accumulating plants including an ARGININE DECARBOXYLASE -over-expressing ( OxPtADC) line and Copper-AMINE OXIDASE3 ( cuao3) knockdown mutants, exhibited fewer differentially expressed genes (DEGs) than the wild type, suggesting that increased Put accumulation may mitigate some stress effects associated with spaceflight. Gene Ontology (GO) enrichment analysis revealed significant changes in biological processes related to spaceflight responses, particularly hypoxia, oxidative stress, and photosynthesis, with Put-modified genotypes showing simplified patterns of expression responses to spaceflight. Specifically, fewer hypoxia-related, and oxidative stress response genes, including those associated with ROS metabolism and cell wall modification, were responsive to spaceflight in the Put-accumulation lines than in the wild type. Similarly, fewer photosynthesis-associated genes were down-regulated under spaceflight conditions in Put-accumulation lines. Morphologically, ISS-grown seedlings exhibited an increase in petiole length, a phenotype previously associated with seedling exposure to hypoxia. This petiole-length response was notably reduced in the OxPtADC and cuao3 genotypes. These findings suggest that manipulating the Put metabolic pathway may enhance plant adaptation to spaceflight conditions, facilitating their incorporation in bioregenerative life-support systems for space-exploration missions.