Ambivalent roles of nonsense-mediated mRNA decay in heat stress tolerance

RNA homeostasis is essential for gene regulation and cellular survival; however, how RNA degradation pathways contribute to stress adaptation remains incompletely understood. Here, we investigated the role of the nonsense-mediated mRNA decay (NMD) in regulating heat stress (HS) memory in a long-term acquired thermotolerance assay. NMD-deficient Arabidopsis thaliana mutants upf1-5 and upf3-1 exhibited a biphasic phenotype: they displayed transiently elevated heat tolerance during early recovery but became more sensitive to heat during late recovery. Genetic analysis of upf3;hsfa2 and upf3;hsfa3 double mutants demonstrated that the early heat tolerance occurs independently of both HsfA2 and HsfA3 HS-memory transcription factors. Under non-treated conditions, the upf3-1 transcriptome exhibited baseline priming of heat-shock responsive transcripts, likely accounting for the initial heat tolerance. Further transcriptome profiling revealed that upf3-1 mutants exhibited reduced levels of the functional HsfA2 isoform (HsfA2-I) and attenuated expression of the HsfA2-dependent thermomemory regulon following the triggering stress. NMD deficiency also upregulated immune-response genes while repressing developmental and cell-wall-associated pathways. Together, impaired HsfA2-dependent thermomemory and a compromised growth defense balance underlies the late heat sensitivity of NMD deficient plants. Overall, NMD acts as a dual-action post-transcriptional regulator that coordinates the transition from stress response to growth resumption.