Swift microbiome-mediated phenotype transfer from transgenic plants.

Abstract

The expression of an organism's genes determines its own characteristics in any given environment. In this study, we demonstrate that the phenotypic traits of genetically modified transgenic Arabidopsis thaliana plants, designed for nutrient efficiency and enhanced yield, can be naturally and readily transferred to neighboring wild-type plants. Our findings reveal that the transgenic plants significantly influence the populational, compositional, and functional traits of their root-associated microbiome (RAM), resulting in a larger population, with distinct composition and high functional potential compared to wild-type plants, regardless of soil type. This phenomenon appears to stem from altered metabolite exudation patterns, which enhance root recruitment. Notably, the RAM plays a dual role: it not only contributes to the robust phenotype of the transgenic plants but also facilitates the transfer of these traits to adjacent wild-type plants. Upon transplanting wild-type plants into the presence of transgenics, we observed the induction of transgenic-like phenotypes. Metagenomic and compositional analyses indicate that this transfer is linked to an increase in 2,3-butanediol (2,3-BD) fermenting bacteria. Furthermore, exposure to 2,3-BD alone was sufficient to elicit transgenic phenotypes in wild-type plants. These results suggest that factors external to plant tissues, such as root-associated bacteria and their volatile metabolic products, play a crucial role in the transferability of plant phenotypes to neighboring plants. Our findings underscore the importance of evaluating microbiome interactions in the context of transgenic organisms and open new avenues for alternative agricultural practices that may reduce reliance on genetic modification.