Gene expression divergence following gene and genome duplications in spatially resolved plant transcriptomes

Abstract

Gene and genome duplications expand genetic repertoires and facilitate functional innovation. Segmental or whole-genome duplications generate duplicates with similar and somewhat redundant expression profiles across multiple tissues, while other modes of duplication create genes that show increased divergence, leading to functional innovations. How duplicates diverge in expression across cell types in a single tissue remains elusive. Here, we used high-resolution spatial transcriptomic data from Arabidopsis thaliana, Glycine max, Phalaenopsis aphrodite, Zea mays, and Hordeum vulgare to investigate the evolution of gene expression following gene duplication. We found that genes originating from segmental or whole-genome duplications display increased expression levels, expression breadths, spatial variability, and number of co-expression partners. Duplication mechanisms that preserve cis-regulatory landscapes typically generate paralogs with more preserved expression profiles, but such differences generated by mode of duplication fade or disappear over time. Paralogs originating from large-scale (including whole-genome) duplications display redundant or overlapping expression profiles, indicating functional redundancy or sub-functionalization, while most small-scale duplicates diverge asymmetrically, consistent with neofunctionalization. Expression divergence also depends on gene functions, with dosage-sensitive genes displaying highly preserved expression profiles and genes involved in more specialized processes diverging more rapidly. Our findings offer a spatially resolved view of expression divergence following duplication, elucidating the tempo and mode of gene expression evolution, and helping understand how gene and genome duplications shape cell identities.