Regulatory Divergence between Parental Alleles Determines Gene Expression Patterns in Hybrids

Abstract

Both hybridization and allopolyploidization generate novel phenotypes by conciliating divergent genomes and regulatory networks in the same cellular context. To understand the rewiring of gene expression in hybrids, the total expression of 21,025 genes and the allele-specific expression of over 11,000 genes were quantified in interspecific hybrids and their parental species, Coffea canephora and Coffea eugenioides using RNA-seq technology. Between parental species, cis- and trans-regulatory divergences affected around 32% and 35% of analyzed genes, respectively, with nearly 17% of them showing both. The relative importance of trans-regulatory divergences between both species could be related to their low genetic divergence and perennial habit. In hybrids, among divergently expressed genes between parental species and hybrids, 77% was expressed like one parent (expression level dominance), including 65% like C. eugenioides. Gene expression was shown to result from the expression of both alleles affected by intertwined parental trans-regulatory factors. A strong impact of C. eugenioides trans-regulatory factors on the upregulation of C. canephora alleles was revealed. The gene expression patterns appeared determined by complex combinations of cis- and trans-regulatory divergences. In particular, the observed biased expression level dominance seemed to be derived from the asymmetric effects of trans-regulatory parental factors on regulation of alleles. More generally, this study illustrates the effects of divergent trans-regulatory parental factors on the gene expression pattern in hybrids. The characteristics of the transcriptional response to hybridization appear to be determined by the compatibility of gene regulatory networks and therefore depend on genetic divergences between the parental species and their evolutionary history.

Segmental allotetraploidy generates extensive homoeologous expression rewiring and phenotypic diversity at the population level in rice

“…The preponderant trans ‐effects on orthologous expression differences between the parental subspecies is consistent with the scenario that the attenuated allelic expression difference in the F1 hybrids is due to strong common trans ‐regulation (Figures and ). Our results pointing to more prominent trans ‐ than cis ‐effects are contrasted with several previous studies of interspecific differences in gene expression, which found higher cis ‐ than trans ‐ (Shi et al., ) or similar cis ‐ and trans ‐regulatory divergence (Bell, Kane, Rieseberg, & Adams, ; Combes et al., ). Together, it suggests that the relative importance of cis ‐ versus trans ‐regulatory divergence in the evolution of gene expression differences between inter‐ and intraspecies can be significantly different.…”

“…However, we note that our RNA‐seq‐based genomewide assay of the same F1 hybrids and tetraploid rice plants of earlier generations (immediately following WGD, hence nonsegregating) produced virtually the same results (Xu et al., ). Moreover, several recent studies in diverse organismal systems also revealed significant attenuation of inherit parental expression divergence in interspecific F1 hybrids and/or allopolyploids (Bell et al., ; Combes et al., ; Cox et al., ; Shi et al., ). Therefore, it seems unlikely that our observation is due to biased selection of genes or their small number.…”

Contrasting Levels of Molecular Evolution on the Mouse X Chromosome

“…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.…”

Cis–trans controls and regulatory novelty accompanying allopolyploidization

“…These compensatory stabilizing regulatory processes may, however, give rise to immediate expression novelty following genomic merger, where different cis and trans factors contributed by two divergent diploids become united in a common nucleus. Although these regulatory patterns have been explored in various plant systems (Springer & Stupar, ; Chaudhary et al ., ; Shi et al ., ; Bell et al ., ; Lemmon et al ., ; Xu et al ., ; Combes et al ., ; He et al ., ), we point out here that the classic ASE model fails to adequately parse the various forms of cis–trans interactions that are created by allopolyploidy. As such, advancing our understanding of the molecular and regulatory basis of phenotypic innovations that emerge following allopolyploidization requires this model to be extended.…”