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Introns and alternative splicing in choanoflagellates


The first organisms to evolve were unicellular, and the vast majority of life has remained so for billions of years. Complex forms of multicellularity, requiring increased levels of cell adhesion, cell signaling and gene regulation, have evolved in only a few eukaryotic lineages. The comparison of genomes from choanoflagellates, the closest relatives of metazoans, with genomes from metazoans may reveal genomic changes underlying metazoan origins. I used this approach to investigate the evolution of introns during the origin of metazoans.

By analyzing the genome of the first choanoflagellate to be sequenced, Monosiga brevicollis, I found that its intron density rivals that of genes in intron-rich metazoans. Many intron positions are conserved between choanoflagellates and metazoans, implying that their shared unicellular ancestor was also intron-rich. In my analysis of the M. brevicollis genome, I made the unexpected discovery that, unlike most choanoflagellate genes, the longest genes contain relatively few introns. Indeed, one M. brevicollis gene contains the longest stretch of intron-free coding sequence known to date. I also found a similar trend in the genome of a basal metazoan, the sponge A. queenslandica. However, most long genes in other metazoans are not depleted of introns, revealing a difference in gene structure between eumetazoans and their closest relatives that may have implications for how these genes are regulated.

The results of these analyses led me to investigate the evolution of alternative splicing during the emergence of metazoans. Intron-rich metazoan genes undergo complex patterns of developmentally regulated alternative splicing. My analysis of intron evolution revealed that the unicellular ancestor of metazoans was also intron-rich, raising the possibility that alternative splicing was common before the transition to multicellularity. To test this, I used transcriptome sequencing to detect alternative splicing in choanoflagellates and the early branching metazoan, Hydra magnipapillata. I found that alternative splicing, especially the skipping of entire exons, occurs less frequently in choanoflagellates than in H. magnipapillata. Increased alternative splicing of already intron-rich genes may thus represent an augmentation of gene regulation that evolved during the origin of metazoans.

My analyses suggest that metazoans evolved from an intron-rich unicellular ancestor, setting the stage for complex patterns of alternative splicing to evolve during the transition to multicellularity. The connection between gene structure and alternative splicing provides an example of how non-coding features of eukaryotic genomes can impact the evolution of regulatory and morphological complexity.

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