High-Temperature-Responsive Poplar lncRNAs Modulate Target Gene Expression via RNA Interference and Act as RNA Scaffolds to Enhance Heat Tolerance

High-temperature stress is a threat to plant development and survival. Long noncoding RNAs (lncRNAs) participate in plant stress responses, but their functions in the complex stress response network remain unknown. Poplar contributes to terrestrial ecological stability. In this study, we identified 204 high-temperature-responsive lncRNAs in an abiotic stress-tolerant poplar (Populus simonii) species using strand-specific RNA sequencing (ssRNA-seq). Mimicking overexpressed and repressed candidate lncRNAs in poplar was used to illuminate their regulation pattern on targets using nano sheet mediation. These lncRNAs were predicted to target 185 genes, of which 100 were cis genes and 119 were trans genes. Gene Ontology enrichment analysis showed that anatomical structure morphogenesis and response to stress and signaling were significantly enriched. Among heat-responsive LncRNAs, TCONS_00202587 binds to upstream sequences via its secondary structure and interferes with target gene transcription. TCONS_00260893 enhances calcium influx in response to high-temperature treatment by interfering with a specific variant/isoform of the target gene. Heterogeneous expression of these two lncRNA targets promoted photosynthetic protection and recovery, inhibited membrane peroxidation, and suppressed DNA damage in Arabidopsis under heat stress. These results showed that lncRNAs can regulate their target genes by acting as potential RNA scaffolds or through the RNA interference pathway.