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.

Keywords: ecology; evolution; genetic management; life-history; meiotic drive; resistance.

Figure 1.

Example of mechanisms facilitating pre-gametic drive during female meiosis, modelled on Maize Ab10 [36]. During meiosis, the drive element (shown in red) can induce non-random chromosome segregation to the cell that ultimately develops into the female gamete. Non-drive alleles are relegated to the polar bodies (along with one of the drive alleles), and segregation ratios in gametes are strongly skewed towards the drive allele. (Online version in colour.)

Figure 2.

Example of mechanisms facilitating post-gametic drive (i.e. gamete killers). In (a), the drive acts by producing a trans-acting toxin and a cis-acting antidote. Non-drive alleles are killed by the toxin, whereas drive alleles are ‘rescued’ by the antidote. In (b), the drive acts via direct interference with gametes carrying non-self alleles, for example, by producing a molecule that is only harmful to gametes carrying the non-drive allele. (Online version in colour.)

Figure 3.

Impact of seed bank structure on the dynamics of a gene drive carrying a recessive lethal cargo. The model of gene drive dynamics in seed banks is presented in electronic supplementary material, text S1. This figure presents the frequency of the drive allele D in the population (a) and the reduction in the mean fitness of the population (b) following the introduction of the recessive lethal gene drive in the population at time 0 (initial frequency of 5%). ν represents the yearly seed germination rate (and consequently the average time spent in the seed bank is 1/ν). Genotype-specific fitness is set as c_DD = 0, c_Dd = 1, c_dd = 1. (Online version in colour.)