Small RNAs mediate transgenerational inheritance of genome-wide trans-acting epialleles in maize

Abstract

Background Hybridization and backcrossing are commonly used in animal and plant breeding to induce heritable variation including epigenetic changes such as paramutation. However, the molecular basis for hybrid-induced epigenetic memory remains elusive. Results Here, we report that hybridization between the inbred parents B73 and Mo17 induces trans-acting hypermethylation and hypomethylation at thousands of loci; several hundreds (~ 3%) are transmitted through six backcrossing and three selfing generations. Notably, many transgenerational methylation patterns resemble epialleles of the nonrecurrent parent, despite > 99% of overall genomic loci are converted to the recurrent parent. These epialleles depend on 24-nt siRNAs, which are eliminated in the isogenic hybrid Mo17xB73:mop1-1 that is defective in siRNA biogenesis. This phenomenon resembles paramutation-like events and occurs in both intraspecific (Mo17xB73) and interspecific (W22xTeosinte) hybrid maize populations. Moreover, siRNA abundance and methylation levels of these epialleles can affect expression of their associated epigenes, many of which are related to stress responses. Conclusion Divergent siRNAs between the hybridizing parents can induce trans-acting epialleles in the hybrids, while the induced epigenetic status is maintained for transgenerational inheritance during backcross and hybrid breeding, which alters epigene expression to enhance growth and adaptation. These genetic and epigenetic principles may apply broadly from plants to animals.

Frequent spontaneous structural rearrangements promote rapid genome diversification in a Brassica napus F1 generation

“…Although they could theoretically be due to spontaneous somatic mutations, these tend to be smaller in size than the large chromosomal segments seen here. Genomic features being inherited in unexpected patterns in early generations have been reported in the form of paramutations in maize, green pea, barley grass and Arabidopsis (Lolle et al, 2005;Hollick, 2017;Adu-Yeboah et al, 2021;Bente et al, 2021;Pereira and Leitão, 2021;Cao et al, 2022), and as selfish genetic elements in rice (Lolle et al, 2005;Hollick, 2017;Yu et al, 2018). In all cases, the reported mutations were limited to a gene-size scale and not to larger genomic features.…”

Transgressive and parental dominant gene expression and cytosine methylation during seed development inBrassica napushybrids

“…7). Studies linking methylation and expression and evaluating epialleles have proved beneficial in detecting heterotic patterns in other crops like maize, rice and Arabidopsis (Greaves et al, 2015; Cao et al, 2022; Wang and Wang, 2022). In addition, 112635 CpG islands were detected in all assigned chromosomes in the Express 617 reference genome, with an average length of 363 bp and strong differences in frequency in centromeric regions of different chromosomes (Table S35).…”

“…Furthermore, Rong et al (2021) reported the enrichment of transposable elements in imprinted genes in B. napus located in 5 kbp flanking regions. Cao et al (2022) analyzed imprinted genes in six backcrossing generations of maize as well as in three selfing generations derived from the 6 th backcross. It was proposed that the divergence between TEs derived from 24-nt siRNAs in the parental maize genomes might have led to transgenerational inheritance of imprinted genes.…”

Recent Advances in DNA Methylation and Their Potential Breeding Applications in Plants

“…When reciprocal hybrids and their parents are examined, embryos and endosperm experience synchronized significant alterations in the DNA methylome, which is thought to be the cause of heterosis of immature seed-related characteristics [268]. During soybean seed development, DNA methylation is altered differently in different cytosine contexts: CHH increases significantly throughout the seed and drops precipitously within the germinating seedling, whereas only minor changes in the global level of CG/CHG occur during the same developmental period [173,272]. Furthermore, in Arabidopsis, loss of CHH and CHG methylation has no effect on seed development, and the key genes for soybean seed development are found in non-methylated genomic regions [272].…”

“…During soybean seed development, DNA methylation is altered differently in different cytosine contexts: CHH increases significantly throughout the seed and drops precipitously within the germinating seedling, whereas only minor changes in the global level of CG/CHG occur during the same developmental period [173,272]. Furthermore, in Arabidopsis, loss of CHH and CHG methylation has no effect on seed development, and the key genes for soybean seed development are found in non-methylated genomic regions [272]. According to the information above, methylation profiles produced during seed development may have other functions.…”