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

Shuai Cao, Longfei Wang, Tongwen Han, Wenxue Ye, Yang Liu, Yi Sun, Stephen P. Moose, Qingxin Song, Z. Jeffrey Chen

Research output: Contribution to journalArticlepeer-review


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.

Original languageEnglish (US)
Article number53
JournalGenome biology
Issue number1
StatePublished - Dec 2022


  • Backcrossing
  • DNA methylation
  • Epialleles
  • Hybrid
  • Maize
  • Paramutation
  • Small RNA
  • Transgenerational inheritance

ASJC Scopus subject areas

  • Ecology, Evolution, Behavior and Systematics
  • Genetics
  • Cell Biology


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