Alternative splicing as an evolvable regulatory layer in plant adaptation and evolution

Abstract

Alternative splicing (AS) is a pervasive post-transcriptional regulatory mechanism that expands transcriptomic and proteomic diversity by generating multiple isoforms from a single gene. Increasing evidence indicates that AS functions as an evolvable regulatory layer linking short-term phenotypic plasticity with long-term adaptive evolution in plants. In this review, we synthesize recent advances in the origin, evolution, and functional significance of AS across plant lineages, with particular emphasis on emerging discoveries in horticultural crops. Comparative analyses from green algae to angiosperms reveal widespread AS and substantial variation in its prevalence across plant lineages, with intron retention remaining a prominent splicing mode and splicing regulatory networks showing considerable diversification. Functionally, AS contributes to plant adaptation through three major regulatory dimensions: coordinating responses to abiotic stresses, reshaping plant–microbe interactions, and modulating developmental plasticity and trait formation. Through isoform switching, AS reprograms gene function, integrates environmental and developmental signals, and optimizes tradeoffs among growth, reproduction, and stress resistance. We further discuss how conserved AS programs maintain core developmental and stress-response pathways, whereas lineage-specific AS divergence contributes to ecological adaptation, domestication, and phenotypic diversification. Environmental cues, splicing quantitative trait loci, structural variation, and transposable elements collectively shape AS evolution across populations and species. Finally, we propose a conceptual framework in which transient AS-mediated plasticity provides a substrate for evolutionary innovation and fixation. Understanding the mechanistic and evolutionary basis of AS will not only advance our knowledge of plant adaptation but also facilitate isoform-informed breeding strategies for improving stress resilience and quality traits in horticultural crops.