Reciprocal allopolyploid grasses (Festuca × Lolium) display stable patterns of genome dominance

Abstract

Summary Allopolyploidization entailing the merger of two distinct genomes in a single hybrid organism, is an important process in plant evolution and a valuable tool in breeding programs. Newly established hybrids often experience massive genomic perturbations, including karyotype reshuffling and gene expression modifications. These phenomena may be asymmetric with respect to the two progenitors, with one of the parental genomes being “dominant.” Such “genome dominance” can manifest in several ways, including biased homoeolog gene expression and expression level dominance. Here we employed a k‐mer–based approach to study gene expression in reciprocal Festuca pratensis Huds. × Lolium multiflorum Lam. allopolyploid grasses. Our study revealed significantly more genes where expression mimicked that of the Lolium parent compared with the Festuca parent. This genome dominance was heritable to successive generation and its direction was only slightly modified by environmental conditions and plant age. Our results suggest that Lolium genome dominance was at least partially caused by its more efficient trans‐acting gene expression regulatory factors. Unraveling the mechanisms responsible for propagation of parent‐specific traits in hybrid crops contributes to our understanding of allopolyploid genome evolution and opens a way to targeted breeding strategies.

Both male and female meiosis contribute to non‐Mendelian inheritance of parental chromosomes in interspecific plant hybrids (Lolium × Festuca)

“…S2). Based on species‐specific k‐mers derived from the previous study (Glombik et al ., 2021), we were able to analyze the parental allele‐specific expression for 15 kinetochore genes. Out of these, 13 genes did not show significantly different expression between homoeologues; however, two genes ( NDC80 and NNF1 ) were expressed exclusively from a Lolium homoeologue in all nine samples of the three pollen development stages and three biological replicates.…”

“…In our previous study, we revealed that Festuca × Lolium hybrids used in this study displayed overall gene expression more frequently at the level of the Lolium parent; however, this was accomplished by overexpression of the Festuca allele. The study suggested that it is more likely that transcription factors from Lolium can manipulate the expression of Festuca alleles rather than transcription factors from Festuca modulating the expression of Lolium alleles (Glombik et al ., 2021). A study on a synthetic allopolyploid cotton revealed that the parental‐specific gene expression could be at least partially altered by developmental, environmental, and ecological conditions, such as during abiotic stress, even though the genome dominance seems to be deterministic (Dong & Adams, 2011; Glombik et al ., 2021).…”

“…Homoeologs with a log 2 fold‐change value > 1 and false discovery rate < 0.05 were defined as significantly differentially expressed. For a comparison of gene expression in somatic tissue, we performed the analysis also on F 1 hybrid RNA‐seq data from our previous study (Glombik et al ., 2021).…”

Genome Dominance in Allium Hybrids (A. cepa × A. roylei)

“…Most, if not all, allopolyploids retain the expression level of one (dominant) parent (so-called expression level dominance) and/or display a preferential expression from the alleles of the dominant genome (so-called homoeolog expression bias). Such dominance does not involve all the expressed genes, as some genes can be overexpressed from the submissive genome or display the overall expression at the level of the submissive parent ( Edger et al, 2017 ; Bird et al, 2018 ; Glombik et al, 2021 ).…”

Genetic architecture of inter-specific and -generic grass hybrids by network analysis on multi-omics data

“…However, genomic instability is often reported and a shift to the ryegrass genome over generations can happen in crosses with fescues (Kopecky et al 2017;Akiyama et al 2012). Additionally, homeolog expression bias and expression level dominance can be observed in such allopolyploids (Glombik et al 2021). Collectively, these phenomena may lead to distinct interactomes when hybridizations are performed across species, which can be analyzed through network reconstruction by leveraging high throughput omics data and appropriate statistical methods.…”