The ubiquitous position effect, synergistic effect of recent generated tandem duplicated genes in grapevine, and their co-response and overactivity to biotic stress

Abstract

Tandem gene duplication is an important process in plant adaptive evolution, but the generation mechanism and expression characteristics of tandem duplicated (TD) genes and their roles in plant stress response have not been rigorously investigated. Here, we take grapevine (V. vinifera) as an example to show that recent large-scale tandem gene duplication, mediated by long terminal repeat retrotransposons, promotes the expansion of specific gene families involved in response to biotic stress, biosynthesis of various secondary metabolites and adaptive evolution. More importantly, compared with interspersed duplicated genes, TD genes exhibit a position and synergistic effect, and multifaceted overactivity and play key roles in response to biotic stress caused by pathogens such as P. viticola (downy mildew) and Erysiphe necator (powdery mildew). The higher co-expression level of TD genes is not only reflected in the co-response to biotic stress, but also universal in various tissues and developmental stages. This may be related to a higher level of co-regulation and a higher transcription factor regulatory efficiency, as well as sequence similarity within gene clusters. Moreover, most TD genes are expressed asymmetrically, while maintaining a relative balance, which may be beneficial for the retention and functional differentiation of the TD genes. These findings not only advance our understanding of the evolution of the V. vinifera genome and the evolution dynamics of the TD genes which has often been overlooked, but also provide guidance for the directional selection in breeding work.

Keywords

• tandem gene duplication
• long terminal repeat retrotransposons
• position effect
• synergistic effect
• co-regulation
• evolution dynamics
• vitis vinifera