Epigenetic transgenerational effects on RNAi in Arabidopsis

Abstract

Epigenetic states and even certain environmental responses in nematodes, mammals and seed plants can be inherited over successive generations. RNAi in plants is an epigenetic form of RNA degradation that is normally reset early in development. In contrast, competence, i.e., the susceptibility of a transgene for RNAi, is believed to be genetically determined and faithfully transmitted over many generations. Unexpectedly, we found that the same yellow fluorescent protein (YFP) transgene in a monogenic, homozygous line of Arabidopsis exhibited two epigenetic states of RNAi: type I, which is initiated in rosette leaves and is stable in later developmental stages, and, type II, which is initiated after floral induction and is unstable. The incidence of type I plants descended from type I parents decreased over three successive generations of self-fertilized plants. By the third generation, a substantial fraction of plants from type I parents exhibited either the type II phenotype or remained high-YFP expressing throughout sporophytic development, indicating that silencing had been completely lost. Similarly, plants descended from type II parents showed a progressive shift from the type II phenotype and a complete loss of silencing. These results show that the silencing types (or states) of parental plants have significant influence on both silencing determination and silencing types (or states) of their offspring, however, this influence fades through several generations of self; as regardless of the types of the parental lines, competence for RNA silencing tends to loss after generations. Thus, we propose that RNA silencing in plants can be the target of transgenerational effects. While the underlying mechanisms are still unknown, our findings in the Arabidopsis RNA silencing system complement the current understanding of heritable RNAi in C. elegans, that this phenomenon is likely a common mechanism in Eukaryote systems.