cis‐andtrans‐Regulation inDrosophilaInterspecific Hybrids

Coolon, Joseph D.; Wittkopp, Patricia J.

doi:10.1002/9781118552872.ch3

Cited by 15 publications

(18 citation statements)

References 85 publications

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“…), where divergence between species is only slightly biased toward cis ‐acting mutations. By contrast, most studies in Drosophila suggest a stronger role of cis ‐regulation, but there is considerable variation in the results (reviewed in Coolon and Wittkopp ). In fact, divergence between D. mauritiana and D. simulans is mostly trans ‐regulatory (Meiklejohn et al.…”

Section: Discussionmentioning

confidence: 98%

Genome-wide patterns of regulatory divergence revealed by introgression lines

et al. 2016

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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 downregulated, while background (nonintrogressed) genes tend to be upregulated. 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.

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Section: Discussionmentioning

confidence: 98%

Genome-wide patterns of regulatory divergence revealed by introgression lines

et al. 2016

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“…For faster-X expression divergence, this would require that differences in transcript abundances are due to divergence in cis-regulatory elements and/or X-linked trans-regulatory elements (Kayserili et al 2012;Meisel et al 2012a;Meisel and Connallon 2013). Several studies suggest that divergence in transcript abundances is largely determined by evolution in cis (Wittkopp et al 2004;Landry et al 2005;Wittkopp et al 2008;Graze et al 2009;Goncalves et al 2012;Shi et al 2012;Shen et al 2014;Mack et al 2016), while other research indicates that trans-regulatory divergence is more common (Emerson et al 2010;McManus et al 2010;Schaefke et al 2013;Coolon et al 2014;Meiklejohn et al 2014;Combes et al 2015) or that the inferred mode of regulatory divergence is dependent on taxon and experimental design (Coolon and Wittkopp 2013;Guerrero et al 2016). The mechanisms underlying the evolution of DNA methylation are even more poorly understood, but levels of DNA methylation within a given genomic region appear strongly Faster-X sequence evolution also assumes that beneficial mutations are on average at least partially recessive (Charlesworth et al 1987), while theory (Gibson and Weir 2005) and several empirical studies (Lemos et al 2008;McManus et al 2010;Schaefke et al 2013) suggest that cis-regulatory elements should on average act additively.…”

Section: Regulatory Evolution and Spermatogenesismentioning

confidence: 99%

“…However, if selection on gene expression acts on standing genetic variation, as opposed to new mutations, then substitution rates are predicted to be lower on the X chromosome (Meisel and Connallon 2013), given lower levels of X-linked genetic diversity in mice (Geraldes et al 2008). The relative contribution of new mutations vs. standing genetic variation to adaptive regulatory divergence has not yet been explicitly addressed (Coolon and Wittkopp 2013).…”

Section: Regulatory Evolution and Spermatogenesismentioning

confidence: 99%

Contrasting Levels of Molecular Evolution on the Mouse X Chromosome

et al. 2016

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The mammalian X chromosome has unusual evolutionary dynamics compared to autosomes. Faster-X evolution of spermatogenic protein-coding genes is known to be most pronounced for genes expressed late in spermatogenesis, but it is unclear if these patterns extend to other forms of molecular divergence. We tested for faster-X evolution in mice spanning three different forms of molecular evolution-divergence in protein sequence, gene expression, and DNA methylation-across different developmental stages of spermatogenesis. We used FACS to isolate individual cell populations and then generated cell-specific transcriptome profiles across different stages of spermatogenesis in two subspecies of house mice (Mus musculus), thereby overcoming a fundamental limitation of previous studies on whole tissues. We found faster-X protein evolution at all stages of spermatogenesis and faster-late protein evolution for both X-linked and autosomal genes. In contrast, there was less expression divergence late in spermatogenesis (slower late) on the X chromosome and for autosomal genes expressed primarily in testis (testis-biased). We argue that slower-late expression divergence reflects strong regulatory constraints imposed during this critical stage of sperm development and that these constraints are particularly acute on the tightly regulated sex chromosomes. We also found slower-X DNA methylation divergence based on genome-wide bisulfite sequencing of sperm from two species of mice (M. musculus and M. spretus), although it is unclear whether slower-X DNA methylation reflects development constraints in sperm or other X-linked phenomena. Our study clarifies key differences in patterns of regulatory and protein evolution across spermatogenesis that are likely to have important consequences for mammalian sex chromosome evolution, male fertility, and speciation.KEYWORDS faster X evolution; gene expression; DNA methylation; fluorescence-activated cell sorting; postmeiotic sex chromosome repression (PSCR) T HE X chromosome plays a disproportionately large role in adaptation and speciation (Bachtrog et al. 2011;Ellegren 2011;Charlesworth 2013), but the underlying molecular and evolutionary drivers of these patterns remain unclear. On one hand, the X chromosome often shows strong signatures of evolutionary constraint. For example, the evolution of dosage compensation via epigenetic X-chromosome inactivation (XCI) in females (Lyon 1961(Lyon , 1962 imposes regulatory constraints that select for strong conservation of X-linked gene content in placental mammals (Ohno 1967;Kohn et al. 2004). On the other hand, these inherent constraints are punctuated by strong specialization in X-linked gene content (Emerson et al. 2004;Mueller et al. 2008Mueller et al. , 2013Potrzebowski et al. 2008;Zhang et al. 2010;Sin et al. 2012) and numerous examples of rapid X-linked evolution Singh 2003, 2006;Baines and Harr 2007;Kousathanas et al. 2014;Nam et al. 2015).The X chromosome is predicted to evolve faster than the autosomes if beneficial mutations...

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“…Our results are consistent with previous findings in Coffea (Combes et al 2015) and Arabidopsis (Shi et al 2012), where divergence between species is only slightly biased towards cis-acting mutations. By contrast, most studies in Drosophila suggest a stronger role of cis-regulation, but there is considerable variation in the results (reviewed in Coolon and Wittkopp 2013). In fact, divergence between D. mauritiana and D. simulans is mostly trans-regulatory (Meiklejohn et al 2014).…”

Section: Discussionmentioning

confidence: 99%

Genome-wide patterns of regulatory divergence revealed by introgression lines

Guerrero

Hahn

Moyle

et al. 2016

Preprint

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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.

show abstract

cis‐andtrans‐Regulation inDrosophilaInterspecific Hybrids

Cited by 15 publications

References 85 publications

Genome-wide patterns of regulatory divergence revealed by introgression lines

Genome-wide patterns of regulatory divergence revealed by introgression lines

Contrasting Levels of Molecular Evolution on the Mouse X Chromosome

Genome-wide patterns of regulatory divergence revealed by introgression lines

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