DNA methylation remodeling in F1 hybrids

Abstract

SUMMARYF1 hybrids derived from a cross between two inbred parental lines often display widespread changes in DNA methylation patterns relative to their parents. To which extent these changes drive non‐additive gene expression levels and phenotypic heterosis in F1 individuals is not fully resolved. Current mechanistic models propose that DNA methylation remodeling in hybrids is the result of epigenetic interactions between parental alleles via small interfering RNA (sRNA). These models have strong empirical support but are limited to genomic regions where the two parental lines differ in DNA methylation status. However, most remodeling events occur in parental regions with similar methylation patterns, and seem to be strongly conditioned by distally acting factors, even in isogenic hybrid systems. The molecular basis of these distal interactions is currently unknown, and will likely emerge as an active area of research in the future. Despite these gaps in our molecular understanding, parental DNA methylation states are statistically associated with heterosis, independent of genetic information, and may serve as biomarkers in crop breeding.

High- or Low-Yielding F2 Progeny of Wheat Is Result of Specific TaCKX Gene Coexpression Patterns in Association with Grain Yield in Paternal Parent

“…Such nonadditive gene expression levels associated with phenotypic heterosis in F 1 plants have already been reported and reviewed [ 29 , 30 , 31 , 32 , 33 ]. These deviations from the general role are the result of different factors, such as epigenetic regulation by transcription factors [ 34 , 35 , 36 , 37 , 38 ], the balance of gene dosage [ 39 , 40 ], small interfering RNAs (sRNA) [ 36 , 41 ], histone modifications [ 42 ], R-loop formation [ 43 ], or distally acting factors [ 31 ]. Furthermore, noncoding RNAs have been described as regulators of the development of shoots and grains in barley [ 44 ] and dominant epigenetic regulators of early meiotic stages in wheat, ensuring reproductive success [ 45 ].…”

Editorial: Interspecific hybridization in plant biology, volume II

“…Hybrid breeding exploits dominance effects by breeding for inbred parents whose F 1 progeny will have positive heterosis ( Kakoulidou and Johannes, 2023 ; Legarra et al., 2023 ). To evaluate and select for heterosis, hybrid breeding typically uses self-pollinated or double-haploid inbred lines, followed by progeny evaluation in heterotic pools ( Labroo et al., 2021 ).…”

Mapping parental DMRs predictive of local and distal methylome remodeling in epigenetic F1 hybrids

“…Such remodeling events can lead to non-additive gene expression changes and are mechanistically well understood. However, most of the remodeling events in hybrids do not occur in parental differentially methylated regions (DMRs) ( Greaves et al, 2012 ; Zhang et al, 2016 ; Lauss et al, 2018 ; Li et al, 2018 ; Ma et al, 2021 ; Kakoulidou & Johannes, 2023 ). Instead, they emerge in regions where the two parents are similarly methylated, and can involve both methylation gains and losses.…”