Aberrant regulation of RNA splicing in sunflower hybrids may underlie intrinsic incompatibilities

Authors: Chris C R Smith, Loren H Rieseberg, Brent S Hulke, Nolan C Kane

Publication Date: September 8, 2020

Abstract: Alternative spicing is an integral part of gene expression in multicellular organisms that allows for diverse mRNA transcripts and proteins to be produced from a single gene. However, most existing analyses have focused on macro-evolution, with only limited research on splice site evolution over shorter term, micro-evolutionary time scales. Here we examine splicing evolution that has occurred during domestication and observe 45 novel splice forms with strongly transgressive isoform compositions, representing 0.24% of analyzed transcripts. We identify loci associated with variation in the levels of these splice forms, finding that many novel transcripts were regulated by multiple alleles with non-additive interactions. A subset of these interactions involved the expression of individual spliceosome components. These overdominant and epistatic interactions often resulted in alteration in the protein-coding regions of the transcripts, resulting in frameshifts and truncations. By associating the splice variation in these genes with size and growth rate measurements, we found that none of the individual splice variants affected these plant traits significantly, but the cumulative expression of all aberrant transcripts did show a significant reduction in growth rate associated with higher proportions of disrupted transcripts. This demonstrates the importance of co-evolution of the different spliceosomal components and their regulators and suggests that these genes may contribute to evolution of reproductive isolation as Bateson-Dobzhansky-Muller incompatibility loci.

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