scholarly journals Sex-specific evolution of a Drosophila sensory system via interacting cis- and trans-regulatory changes

2022 ◽  
Author(s):  
David M Luecke ◽  
Gavin R Rice ◽  
Artyom Kopp

The evolution of gene expression via cis-regulatory changes is well established as a major driver of phenotypic evolution. However, relatively little is known about the influence of enhancer architecture and intergenic interactions on regulatory evolution. We address this question by examining chemosensory system evolution in Drosophila. D. prolongata males show a massively increased number of chemosensory bristles compared to females and males of sibling species. This increase is driven by sex-specific transformation of ancestrally mechanosensory organs. Consistent with this phenotype, the Pox neuro transcription factor (Poxn), which specifies chemosensory bristle identity, shows expanded expression in D. prolongata males. Poxn expression is controlled by non-additive interactions among widely dispersed enhancers. Although some D. prolongata Poxn enhancers show increased activity, the additive component of this increase is slight, suggesting most changes in Poxn expression are due to epistatic interactions between Poxn enhancers and trans-regulatory factors. Indeed, the expansion of D. prolongata Poxn enhancer activity is only observed in cells that express doublesex (dsx), the gene that controls sexual differentiation in Drosophila and also shows increased expression in D. prolongata males due to cis-regulatory changes. Although expanded dsx expression may contribute to increased activity of D. prolongata Poxn enhancers, this interaction is not sufficient to explain the full expansion of Poxn expression, suggesting that cis-trans interactions between Poxn, dsx, and additional unknown genes are necessary to produce the derived D. prolongata phenotype. Overall, our results demonstrate the importance of epistatic gene interactions for evolution, particularly when pivotal genes have complex regulatory architecture.

2019 ◽  
Vol 10 (1) ◽  
Author(s):  
Ying Bao ◽  
Guanjing Hu ◽  
Corrinne E. Grover ◽  
Justin Conover ◽  
Daojun Yuan ◽  
...  

AbstractCis and trans regulatory divergence underlies phenotypic and evolutionary diversification. Relatively little is understood about the complexity of regulatory evolution accompanying crop domestication, particularly for polyploid plants. Here, we compare the fiber transcriptomes between wild and domesticated cotton (Gossypium hirsutum) and their reciprocal F1 hybrids, revealing genome-wide (~15%) and often compensatory cis and trans regulatory changes under divergence and domestication. The high level of trans evolution (54%–64%) observed is likely enabled by genomic redundancy following polyploidy. Our results reveal that regulatory variation is significantly associated with sequence evolution, inheritance of parental expression patterns, co-expression gene network properties, and genomic loci responsible for domestication traits. With respect to regulatory evolution, the two subgenomes of allotetraploid cotton are often uncoupled. Overall, our work underscores the complexity of regulatory evolution during fiber domestication and may facilitate new approaches for improving cotton and other polyploid plants.


2016 ◽  
Author(s):  
Rafael F Guerrero ◽  
Matthew W Hahn ◽  
Leonie C Moyle ◽  
Amanda L Posto

Understanding the genetic basis for changes in transcriptional regulation is an important aspect of understanding phenotypic evolution. Using interspecific introgression lines, we infer the mechanisms of divergence in genome-wide patterns of gene expression between the nightshades Solanum pennellii and S. lycopersicum (domesticated tomato). We find that cis- and trans-regulatory changes have had qualitatively similar contributions to divergence in this clade, unlike results from other systems. Additionally, expression data from four tissues (shoot apex, ripe fruit, pollen, and seed) suggest that introgressed regions in these hybrid lines tend to be down-regulated, while background (non-introgressed) genes tend to be up-regulated. Finally, we find no evidence for an association between the magnitude of differential expression in NILs and previously determined sterility phenotypes. Our results contradict previous predictions of the predominant role of cis- over trans-regulatory divergence between species, and do not support a major role for gross genome-wide misregulation in reproductive isolation between these species.


Author(s):  
Timothy Fuqua ◽  
Jeff Jordan ◽  
Maria Elize van Breugel ◽  
Aliaksandr Halavatyi ◽  
Christian Tischer ◽  
...  

AbstractGene regulatory changes underlie much of phenotypic evolution. However, the evolutionary potential of regulatory evolution is unknown, because most evidence comes from either natural variation or limited experimental perturbations. Surveying an unbiased mutation library for a developmental enhancer in Drosophila melanogaster using an automated robotics pipeline, we found that most mutations alter gene expression. Our results suggest that regulatory information is distributed throughout most of a developmental enhancer and that parameters of gene expression—levels, location, and state—are convolved. The widespread pleiotropic effects of most mutations and the codependency of outputs may constrain the evolvability of developmental enhancers. Consistent with these observations, comparisons of diverse drosophilids reveal mainly stasis and apparent biases in the phenotypes influenced by this enhancer. Developmental enhancers may encode a much higher density of regulatory information than has been appreciated previously, which may impose constraints on regulatory evolution.Quote“Rock, robot rockRock, robot rockRock, robot rock”Daft Punk (2005)


FEBS Letters ◽  
2009 ◽  
Vol 583 (24) ◽  
pp. 3959-3965 ◽  
Author(s):  
Dawn Anne Thompson ◽  
Aviv Regev

2016 ◽  
Vol 113 (36) ◽  
pp. 10115-10120 ◽  
Author(s):  
Noritaka Adachi ◽  
Molly Robinson ◽  
Aden Goolsbee ◽  
Neil H. Shubin

The diversification of paired appendages has been a major factor in the evolutionary radiation of vertebrates. Despite its importance, an understanding of the origin of paired appendages has remained elusive. To address this problem, we focused on T-box transcription factor 5 (Tbx5), a gene indispensable for pectoral appendage initiation and development. Comparison of gene expression in jawless and jawed vertebrates reveals that the Tbx5 expression in jawed vertebrates is derived in having an expression domain that extends caudal to the heart and gills. Chromatin profiling, phylogenetic footprinting, and functional assays enabled the identification of a Tbx5 fin enhancer associated with this apomorphic pattern of expression. Comparative functional analysis of reporter constructs reveals that this enhancer activity is evolutionarily conserved among jawed vertebrates and is able to rescue the finless phenotype of tbx5a mutant zebrafish. Taking paleontological evidence of early vertebrates into account, our results suggest that the gain of apomorphic patterns of Tbx5 expression and regulation likely contributed to the morphological transition from a finless to finned condition at the base of the vertebrate lineage.


2021 ◽  
Vol 22 (1) ◽  
Author(s):  
Colin T. Waters ◽  
Stephen S. Gisselbrecht ◽  
Yuliya A. Sytnikova ◽  
Tiziana M. Cafarelli ◽  
David E. Hill ◽  
...  

AbstractUnderstanding the contributions of transcription factor DNA binding sites to transcriptional enhancers is a significant challenge. We developed Quantitative enhancer-FACS-Seq for highly parallel quantification of enhancer activities from a genomically integrated reporter in Drosophila melanogaster embryos. We investigate the contributions of the DNA binding motifs of four poorly characterized TFs to the activities of twelve embryonic mesodermal enhancers. We measure quantitative changes in enhancer activity and discover a range of epistatic interactions among the motifs, both synergistic and alleviating. We find that understanding the regulatory consequences of TF binding motifs requires that they be investigated in combination across enhancer contexts.


2018 ◽  
Author(s):  
Timothy B. Sackton ◽  
Phil Grayson ◽  
Alison Cloutier ◽  
Zhirui Hu ◽  
Jun S. Liu ◽  
...  

The relative roles of regulatory and protein evolution in the origin and loss of convergent phenotypic traits is a core question in evolutionary biology. Here we combine phylogenomic, epigenomic and developmental data to show that convergent evolution of regulatory regions, but not protein-coding genes, is associated with flightlessness in palaeognathous birds, a classic example of a convergent phenotype. Eleven new genomes, including a draft genome from an extinct moa, resolve palaeognath phylogeny and show that the incidence of independent, convergent accelerations among 284,000 conserved non-exonic elements is significantly more frequent in ratites than other bird lineages. Ratite-specific acceleration of conserved regions and measures of open chromatin across eight tissues in the developing chick identify candidate regulatory regions that may have modified or lost function in ratites. Enhancer activity assays conducted in the early developing chicken forelimb confirm that volant versions of a conserved element in the first intron of the TEAD1 gene display conserved enhancer activity, whereas an accelerated flightless version fails to drive reporter gene expression. Our results show that convergent molecular changes associated with loss of flight are largely regulatory in nature.


1972 ◽  
Vol 14 (1) ◽  
pp. 49-55 ◽  
Author(s):  
K. S. Bains ◽  
K. S. Gill ◽  
K. L. Sehgal

Grain protein and Pelshenke value in 8 × 8 diallel crosses and after eliminating the interacting arrays were genetically analysed. All the dominance variation for grain protein was due to epistatic interactions. The dominance component for Pelshenke value was considerably inflated by epistasis. For both characters, the dominance component was affected more by the epistatic bias than the additive component of genetic variance, resulting in considerably low narrow-sense heritability estimates. Covariance between grain protein and Pelshenke value was primarily due to additive gene effects and was attributed to pleiotropic relationships in the absence of genetic linkage. An ambidirectional trend of dominance with an asymmetric distribution of dominant and recessive alleles among the cultivars was observed for grain protein, whereas preponderance of the dominant decreasing genes with more isodirectional gene distribution was operative for Pelshenke value. Correlated responses of these quality traits to selection due to high additive genetic correlation and degree of co-inheritance in relation to their gene action is stressed.


Science ◽  
2019 ◽  
Vol 364 (6435) ◽  
pp. 74-78 ◽  
Author(s):  
Timothy B. Sackton ◽  
Phil Grayson ◽  
Alison Cloutier ◽  
Zhirui Hu ◽  
Jun S. Liu ◽  
...  

A core question in evolutionary biology is whether convergent phenotypic evolution is driven by convergent molecular changes in proteins or regulatory regions. We combined phylogenomic, developmental, and epigenomic analysis of 11 new genomes of paleognathous birds, including an extinct moa, to show that convergent evolution of regulatory regions, more so than protein-coding genes, is prevalent among developmental pathways associated with independent losses of flight. A Bayesian analysis of 284,001 conserved noncoding elements, 60,665 of which are corroborated as enhancers by open chromatin states during development, identified 2355 independent accelerations along lineages of flightless paleognaths, with functional consequences for driving gene expression in the developing forelimb. Our results suggest that the genomic landscape associated with morphological convergence in ratites has a substantial shared regulatory component.


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