On epigenetics and epistasis: hybrids and their non-additive interactions

Abstract

Hybrid seeds have been a key component of greatly increasing the yield of many important crops, foremost of maize. If the parents are properly chosen, non-additive interactions between diverged genomes can lead to strongly superior performance of the F1 progeny, known as heterosis. While many different explanations have been advanced, a consensus for the causes of genome-wide positive epistasis in hybrids has not emerged. In this issue of The EMBO Journal, Shivaprasad and colleagues describe a new mechanism that can account for heterosis often being a genome-wide phenomenon. These authors show that small RNA (sRNA) loci of tomato can exhibit transgressive activity, which can in turn lead to epigenetic and gene expression changes within hybrid progeny. This is particularly exciting because many sRNAs are produced from non-coding regions or transposable elements (TEs), which diverge more quickly than protein-coding genes and thus provide more opportunity for unexpected genetic interactions. Epistasis is defined as a non-additive genetic interaction, where the interaction may be described as transgressive if the hybrid progeny is in some way either superior to the better or inferior to the worse parent. Transgression has been previously suggested to facilitate hybrid niche specialization and is particularly important in crop breeding (i.e., when hybrid yields are higher than those of either parent). sRNAs play an important role in gene and genome regulation. MicroRNAs (miRNAs) and trans-acting small interfering RNAs (tasiRNAs) regulate coding transcript levels, while small interfering RNAs (siRNAs) guide DNA methylation and stable chromatin modifications predominantly at TEs and other repeat sequences. These epigenetic marks keep TEs repressed, thereby limiting potentially detrimental transposition events. Epigenetic and sRNA differences between and within species are relatively poorly described compared with genetic and transcriptome variation. Nonetheless, since genomic differences are overrepresented within TEs and repeat elements, which are controlled by siRNAs, one might expect that divergent epigenetic modifications could make major contributions to hybrid phenotypes. In agreement, TEs can be activated in interspecific hybrids, accompanied by changes in DNA methylation (Michalak, 2009), and TEs have been proposed to contribute to transgressive phenotypes