Gene drives in plants: opportunities and challenges for weed control and engineered resilience

Abstract

Plant species, populations and communities are under threat from climate change, invasive pathogens, weeds and habitat fragmentation. Despite considerable research effort invested in genome engineering for crop improvement, the development of genetic tools for the management of wild plant populations has rarely been given detailed consideration. Gene drive systems that allow direct genetic management of plant populations via the spread of fitness-altering genetic modifications could be of great utility. However, despite the rapid development of synthetic tools and their enormous promise, little explicit consideration has been given to their application in plants and, to date, they remain untested. This article considers the potential utility of gene drives for the management of wild plant populations, and examines the factors that might influence the design, spread and efficacy of synthetic drives. To gain insight into optimal ways to design and deploy synthetic drive systems, we investigate the diversity of mechanisms underlying natural gene drives and their dynamics within plant populations and species. We also review potential approaches for engineering gene drives and discuss their potential application to plant genomes. We highlight the importance of considering the impact of plant life-history and genetic architecture on the dynamics of drive, investigate the potential for different types of resistance evolution, and touch on the ethical, regulatory and social challenges ahead.

Introduction

Plants play key roles as primary producers and underpin the diversity and functioning of terrestrial ecosystems. However, many natural and agricultural ecosystem systems face critical challenges associated with invasive species, climate change and the evolution of herbicide resistance. Consequently, the development of tools to help manage wild plant populations is urgently needed. Recent conceptual and technological developments relating to the engineering of gene drives place us at the forefront of an era in which the engineering of specific traits of economic or conservation interest into wild plant populations has become feasible.

While genome engineering has been widely embraced as a tool for the genetic improvement of plant species of economic or cultural value, synthetic tools for the genetic management of wild populations have received relatively little attention. Gene drives are selfish genes that are able to distort segregation ratios during meiosis or gamete development. They are thus able to spread through populations, even when they impose a fitness cost on their host, and in principle may be engineered to deliver desirable genetic changes in wild populations. The applied potential of gene drives has been long recognized, but the molecular tools required to engineer them for specific species and purposes remained unavailable. Now, new conceptual insights, the development of new endonuclease-based (e.g. CRISPR) genome engineering technologies and proof of concept experiments in animals and fungi have led to a surge in interest for application to plants. However, little explicit consideration has been given to the context in which gene drives might be used to manipulate plant populations, how they function at the molecular–genetic level, nor to the eco-evolutionary processes that will influence their spread and impact. For drive to occur, there must be synergy between processes taking place at molecular, cellular, organismal and population scales. This point is of particular importance when assessing the utility of gene drive as tool for the management of wild plant populations, given plants encompass a diverse range of life histories, DNA repair mechanisms and cytogenetic arrangements.

More information:

Barrett LG, Legros M, Kumaran N, Glassop D, Raghu S, Gardiner DM. 2019 Gene drives in plants: opportunities and challenges for weed control and engineered resilience. Proc. R. Soc. B 286: 20191515. http://dx.doi.org/10.1098/rspb.2019.1515