Cis–trans controls and regulatory novelty accompanying allopolyploidization

Abstract

Summary Allopolyploidy is a prevalent process in plants, having important physiological, ecological and evolutionary consequences. Transcriptomic responses to genomic merger and doubling have been demonstrated in many allopolyploid systems, encompassing a diversity of phenomena including homoeolog expression bias, genome dominance, expression‐level dominance and revamping of co‐expression networks. Notwithstanding the foregoing, there remains a need to develop a conceptual framework that will stimulate a deeper understanding of these diverse phenomena and their mechanistic interrelationships. Here we introduce considerations relevant to this framework with a focus on cis–trans interactions among duplicated genes and alleles in hybrids and allopolyploids. By extending classic allele‐specific expression analysis to the allopolyploid level, we distinguish the distinct effects of progenitor regulatory interactions from the novel intergenomic interactions that arise from genome merger and allopolyploidization. This perspective informs experiments designed to reveal the molecular genetic basis of gene regulatory control, and will facilitate the disentangling of genetic from epigenetic and higher‐order effects that impact gene expression. Finally, we suggest that the extended cis–trans model may help conceptually unify several presently disparate hallmarks of allopolyploid evolution, including genome‐wide expression dominance and biased fractionation, and lead to a new level of understanding of phenotypic novelty accompanying polyploidy.

Current research frontiers in plant epigenetics: an introduction to a Virtual Issue

“…Similarly, it has been shown that the dominant genome can be targeted by less silencing in comparison to the parental level, while the recessive genome retains the parental level of silencing (reviewed in Bird et al , 2018). The ‘TE model’ of subgenome‐specific bias and its influence on cis–trans interactions and homoeologue expression are discussed in a recent paper by Hu & Wendel (2019). In addition to the ‘TE model’, a transcription factor model is also highlighted as a strong candidate in shaping the fate of the divergent subgenomes (Hu & Wendel, 2019).…”

“…The ‘TE model’ of subgenome‐specific bias and its influence on cis–trans interactions and homoeologue expression are discussed in a recent paper by Hu & Wendel (2019). In addition to the ‘TE model’, a transcription factor model is also highlighted as a strong candidate in shaping the fate of the divergent subgenomes (Hu & Wendel, 2019).…”

Reduced chromatin accessibility underlies gene expression differences in homologous chromosome arms of hexaploid wheat and diploidAegilops tauschii

“…Enrichment of promoter motifs in these 87 DEGs (Additional File 6) is consistent with a model in which transcriptional regulation from the AABB genomes may differentially regulate DD genes during later stages of grain development. Such emergent patterns of cis-trans interactions in polyploid genomes have been modelled (Bottani et al 2018;Hu and Wendel 2018) .…”

Homoeologous gene expression and co-expression network analyses and evolutionary inference in allopolyploids

“…Quantification of homoeolog expression is particularly interesting, given the various patterns of duplicate gene expression possible in polyploid species (reviewed in [12]), the interactions among homoeologs in a gene network context [6,14], and the phenomenon of unbalanced homoeolog expression bias together with its potential long-term consequences for fractionation [72][73][74]. A number of previous studies have explored the bioinformatics of homoeolog expression profiling [68][69][70][71]; however, both the fundamental issue of read ambiguity and the downstream inferences regarding polyploid expression evolution have not been addressed.…”

“…Polyploidy in plants is far more prevalent than once thought, acting historically and more recently to shape the genomes of all angiosperms and most other groups of plants [8][9][10][11]. One realization that has emerged in the last decade is that polyploidy is accompanied by massive transcriptomic responses, as reviewed [12][13][14]. These responses are many and varied, including biased homoeolog expression, conditionspecific differential homoeolog usage, transgressive expression levels, and expression level dominance.…”