Within-plant genetic drift to control virus adaptation

Benoit Moury
Pathologie Vegétale, INRA, Avignon, France

benoit.moury@inra.fr

Plant breeders usually choose the plant resistance genes according to their immediate efficiency and spectrum of action against pathogens. To promote resistance durability, it would be also desirable to choose them according to their effects on pathogen evolution. In this perspective, one standing question is: which pathogen evolutionary trait (or combination of traits) should be targeted by plant resistance genes in order to minimize pathogen adaptation?

                  We explored this question on the pepper (Capsicum annuum; family Solanaceae) – Potato virus Y (PVY; genus Potyvirus, family Potyviridae) system using an experimental evolution approach. We chose six pepper genotypes possessing the same major-effect resistance gene but carrying different genetic backgrounds. At the individual plant level, these genotypes exert contrasted effects on PVY initial fitness (measured as PVY load within the plant at the beginning of experimental evolution) and on selection and genetic drift effects in PVY populations.

The PVY evolutionary trajectories were highly contrasted and dependent on the pepper genotype. Most lineages did not show any significant fitness change, others showed a significant fitness gain or went to extinction. Almost all PVY fitness gains were due to the fixation of one or two amino acid substitutions in PVY VPg, the protein linked to the viral RNA, which is a ligand of the product of the plant major resistance gene.

                  We analysed the effects of PVY initial fitness (Fi), effective population size (Ne) and selection coefficient (S) during plant infection on the change of PVY fitness during experimental evolution. The two significant factors were Ne and the interaction Ne × Fi. High and significant PVY fitness gains were observed mostly when Ne was high and Fi was low, which could be explained by low genetic drift and more opportunities for large-effect beneficial mutations. Extinctions of PVY lineages were observed only when Ne and Fi were low, which could be explained by the combination of high genetic drift and low probability of de novo mutations due to low Fi.

                  Our study shows that it is possible for plant breeders to combine a high resistance efficiency and high resistance durability, even with strong selection exerted on virus populations by a major-effect resistance gene, by using plant genotypes where viruses have a low Ne during infection.

Recent publications:

1. Rousseau et al. (2019). Virus epidemics, plant-controlled population bottlenecks and the durability of plant resistance. Phil Tr Roy Soc B 374:20180263.

2. Rousseau et al. (2018). Impact of genetic drift, selection and accumulation level on virus adaptation to its host plants. Mol Plant Pathol 19:2575-2589.

3. Rousseau et al. (2017). Estimating virus effective population size and selection without neutral markers. PLoS Path 13:e1006702.