Mobility connects: transposable elements wire new transcriptional networks by transferring transcription factor binding motifs

Abstract

Transposable elements (TEs) constitute major fractions of plant genomes. Their potential to be mobile provides them with the capacity to cause major genome rearrangements. Those effects are potentially deleterious and enforced the evolution of epigenetic suppressive mechanisms controlling TE activity. However, beyond their deleterious effects, TE insertions can be neutral or even advantageous for the host, leading to long-term retention of TEs in the host genome. Indeed, TEs are increasingly recognized as major drivers of evolutionary novelties by regulating the expression of nearby genes. TEs frequently contain binding motifs for transcription factors and capture binding motifs during transposition, which they spread through the genome by transposition. Thus, TEs drive the evolution and diversification of gene regulatory networks by recruiting lineage-specific targets under the regulatory control of specific transcription factors. This process can explain the rapid and repeated evolution of developmental novelties, such as C4 photosynthesis and a wide spectrum of stress responses in plants. It also underpins the convergent evolution of embryo nourishing tissues, the placenta in mammals and the endosperm in flowering plants. Furthermore, the gene regulatory network underlying flower development has also been largely reshaped by TE-mediated recruitment of regulatory elements; some of them being preserved across long evolutionary timescales. In this review, we highlight the potential role of TEs as evolutionary toolkits in plants by showcasing examples of TE-mediated evolutionary novelties.

Epigenetic inheritance mediates phenotypic diversity in natural populations

“…Plant TEs are generally methylated in all sequence contexts -CG, CHG, and CHH (H being A, T, or C) 3,4,7,8 . TE methylation induces silencing 7 , confers genome stability 6,9 , and can influence the expression of neighbouring genes [10][11][12][13][14][15] . Gene body methylation (gbM) occurs only in the CG context 3,4,16 , although genes can also feature TE-like methylation in all contexts (teM) 17,18 .…”

The Evolutionary Volte-Face of Transposable Elements: From Harmful Jumping Genes to Major Drivers of Genetic Innovation

“…Nowadays, it is well-accepted that TE exaptation has been a major driver for several genetic and morphological innovations throughout evolution [ 25 , 135 ]. There are many examples depicting TE exaptation events as major contributors to essential evolutionary transitions, such as the elaboration of the vertebrate adaptive immune system [ 151 , 152 , 153 ], or the development of the embryo-nourishing tissues that are the mammalian placenta and the seed endosperm [ 154 , 155 ].…”

Domestication and microbiome

“…In this way TEs stimulate the evolution and diversification of gene regulatory networks and supply targets to regulate genes transcription. This phenomenon can explain fast and frequent evolution of new phenotypic features – for example convergent evolution of embryo nourishing tissues, the placenta in mammals, and the endosperm in flowering plants (Qiu and Kohler, 2020).…”