Emerging principles of regulatory evolution

Abstract

Understanding the genetic and molecular mechanisms governing the evolution of morphology is a major challenge in biology. Because most animals share a conserved repertoire of body-building and -patterning genes, morphological diversity appears to evolve primarily through changes in the deployment of these genes during development. The complex expression patterns of developmentally regulated genes are typically controlled by numerous independent cis-regulatory elements (CREs). It has been proposed that morphological evolution relies predominantly on changes in the architecture of gene regulatory networks and in particular on functional changes within CREs. Here, we discuss recent experimental studies that support this hypothesis and reveal some unanticipated features of how regulatory evolution occurs. From this growing body of evidence, we identify three key operating principles underlying regulatory evolution, that is, how regulatory evolution: (i) uses available genetic components in the form of preexisting and active transcription factors and CREs to generate novelty; (ii) minimizes the penalty to overall fitness by introducing discrete changes in gene expression; and (iii) allows interactions to arise among any transcription factor and downstream CRE. These principles endow regulatory evolution with a vast creative potential that accounts for both relatively modest morphological differences among closely related species and more profound anatomical divergences among groups at higher taxonomical levels.pleiotropy ͉ cis-regulation ͉ transcription ͉ pigmentation ͉ body plan

Evolution of Double Positive Autoregulatory Feedback Loops in CYCLOIDEA2 Clade Genes Is Associated with the Origin of Floral Zygomorphy

“…Given that the same CYC binding sites are found in the zygomorphic lineages of both Asterids and Rosids, with no such site detected in their respective ancestral actinomorphic lineages, and the establishment of floral zygomorphy frequently involves the dorsal-specific activities of a pair of CYC2 genes, we suggest that the double positive autoregulatory feedback loops revealed in Lamiales might have become established independently in the Asterids and Rosids, in accordance with the independent origins of several major zygomorphic lineages in the core eudicots (Donoghue et al, 1998;Cubas, 2004;Jabbour et al, 2009). A growing amount of evidence shows that many polyploids experience extensive and rapid genomic alterations even within the first few generations, and changes in the architecture of gene regulatory networks and in particular functional changes within cis-regulatory elements are frequently associated with evolutionary innovations (Adams and Wendel, 2005;Moore and Purugganan, 2005;Soltis, 2005;Prud'homme et al, 2006Prud'homme et al, , 2007Wagner, 2008). Therefore, this neofunctionalization (i.e., the double positive autoregulatory feedback loops underlain by a key regulatory change in CYC2 clade genes) might have been subsequent to the second WGD event in angiosperms that provided novel opportunities for the evolutionary success of the core eudicots.…”

“…The independent evolution of morphological similarities is widespread in both animals and plants and usually involves repeated recruitment of the same kind of genes in independent lineages, such as Yellow genes for pigmentation traits in flies (Prud'homme et al, 2006(Prud'homme et al, , 2007Werner et al, 2010), Pitx1 genes for pelvic reduction in sticklebacks (Shapiro et al, 2006), and RPL (shl) genes for fruit shattering in Arabidopsis and rice (Arnaud et al, 2011). Natural selection usually biases these genes, especially certain regulatory regions that behave as genomic hotspots for phenotypic evolution (Papa et al, 2008;Arnaud et al, 2011).…”

Dynamic SPR monitoring of yeast nuclear protein binding to a cis-regulatory element

“…Transcription only proceeds when the occupancy of dozens of these cis-regulatory elements is in an appropriate state [1,2]. Comprehensive identification and monitoring of these cisregulatory elements could lead to a better understanding of fundamental biological processes like development [3] and evolution [4].…”

PEP1 regulates perennial flowering in Arabis alpina

“…Furthermore, not all perennials flower in response to vernalization and FLC is not a universal regulator of vernalization requirement 27 , supporting the idea that different mechanisms must regulate the perennial growth habit in other groups of plants. Species-specific traits can evolve through alterations in the expression patterns of regulatory genes 28 . The differences in histone modifications at FLC and PEP1 in A. thaliana and A. alpina, respectively, suggest that differences in chromatin regulation may be one of the mechanisms by which these alterations in gene expression patterns occur, thereby allowing diversification of rapidly evolving traits such as life history characters.…”