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

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. 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 plus 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, defective in siRNA biogenesis. This phenomenon resembles paramutation-like events and occurs in both intraspecific and interspecific hybrid maize populations. Moreover, siRNA abundance and methylation levels of these epialleles may affect expression of epigenes. Divergent siRNAs between the parents can induce trans-acting epialleles in hybrids, while the induced epigenetic status is maintained for transgenerational inheritance during backcross and hybrid breeding, which alters gene expression to enhance growth and adaptation to stresses. These genetic and epigenetic principles may apply broadly from plants to animals.