Differential Intron Retention is a Key Event of Alternative Splicing-Driven Transcriptome Adaptation to Environmental Stresses in Populus trichocarpa

Alternative splicing (AS) of precursor messenger RNAs (pre-mRNAs) is widespread across metazoan organisms. In plants the majority of intron-containing genes (42-61%) are alternatively spliced with intron retention (IR) being the prevalent class. The repertoire of AS can be modulated by various environmental stresses. We investigated the extent of abiotic stress-driven differential IR (DIR) events across principal tissue types of western poplar (Populus trichcarpa). Osmotic (dehydration or high salinity) or temperature (heat or cold) stresses triggered a broad range of DIR events in leaf, root, and xylem tissues. Each stress treatment induced a distinct set of stress-specific DIR events. The majority of transcripts harboring DIR events were unique between short-term and prolonged treatment phases.  However, several subsets of common DIR events were ubiquitously induced by two or more stress treatments. Among transcripts harboring multiple stress-regulated retained introns some DIR events occurred with high frequency across all treatments and tissues. Such highly responsive events were often observed in transcripts derived from genes regulating stress response. Stress-induced DIR events were present across key gene families regulating splicing, stress-response, plant development, cell wall metabolism, transcription, and circadian rhythms.