Epigenetic management of self and non-self: lessons from 40 years of transgenic plants

Plant varieties exhibiting unstable or variegated phenotypes, or showing virus recovery have long remained a mystery. It is only with the development of transgenic plants 40 years ago that the epigenetic features underlying these phenomena were elucidated. Indeed, the study of transgenic plants that did not express the introduced sequences revealed that transgene loci sometimes undergo transcriptional gene silencing (TGS) or post-transcriptional gene silencing (PTGS) by activating epigenetic defenses that naturally control transposable elements, duplicated genes or viruses. Even when they do not trigger TGS or PTGS spontaneously, stably expressed transgenes driven by viral promoters set apart from endogenous genes in their epigenetic regulation. As a result, transgenes driven by viral promoters are capable of undergoing systemic PTGS throughout the plant, whereas endogenous genes can only undergo local PTGS in cells where RNA quality control is impaired. Together, these results indicate that the host genome distinguishes self from non-self at the epigenetic level, allowing PTGS to eliminate non-self, and preventing PTGS to become systemic and kill the plant when it is locally activated against deregulated self.