Evolution of gene regulation: Tx factors, but not enhancers, found in Capsaspora, but both found in Nematostella

The origin of all animals, from humans to sponges and comb jellies and socialists, can be traced back to a major event in evolutionary history: the transition to multi-cellularity. This transition was no doubt shaped by environmental changes––such as rising oxygen levels––and the evolution of cells that could consume other (smaller) cells. However, to fully understand what drove this seminal event, we must look to the genome. Writing in Cell, the major article [attached] investigates gene regulation in a microscopic cousin of animals, Capsaspora owczarzaki. The study indicates that Capsaspora represents a transi­tional state in evolution of gene-regulatory mechanisms, and provides a foundation for investigating how such mechanisms might have contributed to the origin of animals.

More than 600 million years ago, a series of genetic innovations allowed the progeni­tors of animals to exploit emerging environ­mental niches on a changing planet. These progenitors cannot be studied directly––so HOW CAN WE identify those genetic innova­tions that mattered most for animal origins? Most insights into pre-animal genomes have come from comparisons of extant animals and their close relatives, choanoflagellates and Capsaspora. Contrary to expecta­tion, these studies revealed that much of the animal genetic toolkit (including genes that encode cell-adhesion proteins––such as integrins and cadherins, and those for vital signalling proteins such as receptor tyrosine kinases) is also expressed in Capsaspora and choanoflagellates, indicating that many ‘animal’ genes pre-date animal origins.

Authors [below] show that changing chromatin states, differential long-intervening-noncoding RNA (lincRNA) expression, and dynamic cis-regulatory sites are associated with life cycle transitions in Capsaspora. Moreover, they demonstrate conservation of animal developmental transcription (Tx)-factor networks and extensive network interconnection in this pre-Metazoan organism. In contrast, however, Capsaspora lacks animal promoter types, and its regulatory sites are small, proximal, and lack signatures of animal enhancers. Overall, their data indicate that the emergence of animal multi-cellularity was associated with a major shift in genome cis-regulatory complexity––most notably the appearance of distal enhancer regulation.

Cell  2o16; 165: 1224–1237 [main article]  and  Nature  23 June 2o16; 534: 482–483 [News ‘n’ Viws]

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