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Impact of genetic drift, selection and accumulation level on virus adaptation to its host plants.

ABSTRACT: The efficiency of plant major resistance genes is limited by the emergence and spread of resistance-breaking mutants. Modulation of the evolutionary forces acting on pathogen populations constitutes a promising way to increase the durability of these genes. We studied the effect of four plant traits affecting these evolutionary forces on the rate of resistance breakdown (RB) by a virus. Two of these traits correspond to virus effective population sizes (Ne ) at either plant inoculation or during infection. The third trait corresponds to differential selection exerted by the plant on the virus population. Finally, the fourth trait corresponds to within-plant virus accumulation (VA). These traits were measured experimentally on Potato virus Y (PVY) inoculated to a set of 84 pepper doubled-haploid lines, all carrying the same pvr23 resistance gene, but having contrasting genetic backgrounds. The lines showed extensive variation for the rate of pvr23 RB by PVY and for the four other traits of interest. A generalized linear model showed that three of these four traits, with the exception of Ne at inoculation, and several pairwise interactions between them had significant effects on RB. RB increased with increasing values of Ne during plant infection or VA. The effect of differential selection was more complex because of a strong interaction with VA. When VA was high, RB increased as the differential selection increased. An opposite relationship between RB and differential selection was observed when VA was low. This study provides a framework to select plants with appropriate virus evolution-related traits to avoid or delay RB.

SUBMITTER: Rousseau E

PROVIDER: S-EPMC6638063 | biostudies-literature | 2018 Dec

REPOSITORIES: biostudies-literature

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Impact of genetic drift, selection and accumulation level on virus adaptation to its host plants.

Rousseau Elsa E Tamisier Lucie L Fabre Frederic F Simon Vincent V Szadkowski Marion M Bouchez Olivier O Zanchetta Catherine C Girardot Gregory G Mailleret Ludovic L Grognard Frederic F Palloix Alain A Moury Benoit B

Molecular plant pathology 20181025 12

The efficiency of plant major resistance genes is limited by the emergence and spread of resistance-breaking mutants. Modulation of the evolutionary forces acting on pathogen populations constitutes a promising way to increase the durability of these genes. We studied the effect of four plant traits affecting these evolutionary forces on the rate of resistance breakdown (RB) by a virus. Two of these traits correspond to virus effective population sizes (N<sub>e</sub> ) at either plant inoculatio ...[more]

PMID: 30074299

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Project description:Manipulating evolutionary forces imposed by hosts on pathogens like genetic drift and selection could avoid the emergence of virulent pathogens. For instance, increasing genetic drift could decrease the risk of pathogen adaptation through the random fixation of deleterious mutations or the elimination of favorable ones in the pathogen population. However, no experimental proof of this approach is available for a plant-pathogen system. We studied the impact of pepper (Capsicum annuum) lines carrying the same major resistance gene but contrasted genetic backgrounds on the evolution of Potato virus Y (PVY). The pepper lines were chosen for the contrasted levels of genetic drift (inversely related to Ne, the effective population size) they exert on PVY populations, as well as for their contrasted resistance efficiency (inversely related to the initial replicative fitness, Wi, of PVY in these lines). Experimental evolution was performed by serially passaging 64 PVY populations every month on six contrasted pepper lines during seven months. These PVY populations exhibited highly divergent evolutionary trajectories, ranging from viral extinctions to replicative fitness gains. The sequencing of the PVY VPg cistron, where adaptive mutations are likely to occur, allowed linking these replicative fitness gains to parallel adaptive nonsynonymous mutations. Evolutionary trajectories were well explained by the genetic drift imposed by the host. More specifically, Ne, Wi and their synergistic interaction played a major role in the fate of PVY populations. When Ne was low (i.e. strong genetic drift), the final PVY replicative fitness remained close to the initial replicative fitness, whereas when Ne was high (i.e. low genetic drift), the final PVY replicative fitness was high independently of the replicative fitness of the initially inoculated virus. We show that combining a high resistance efficiency (low Wi) and a strong genetic drift (low Ne) is the best solution to increase resistance durability, that is, to avoid virus adaptation on the long term.

Project description:The emerging and ongoing outbreak of human monkeypox (hMPX) in 2022 is a serious global threat. An understanding of the evolution of the monkeypox virus (MPXV) at the single-gene level may provide clues for exploring the unique aspects of the current outbreak: rapidly expanding and sustained human-to-human transmission. For the current investigation, alleles of 156 MPXV coding genes (which account for >95% of the genomic sequence) have been gathered from roughly 1,500 isolates, including those responsible for the previous outbreaks. Using a range of molecular evolution approaches, we demonstrated that intra-species homologous recombination has a negligible effect on MPXV evolution. Despite the fact that the majority of the MPXV genes (64.10%) were subjected to negative selection at the whole gene level, 10 MPXV coding genes (MPXVgp004, 010, 012, 014, 044, 098, 138, 178, 188, and 191) were found to have a total of 15 codons or amino acid sites that are known to evolve under positive Darwinian selection. Except for MPXVgp138, almost all of these genes encode proteins that interact with the host. Of these, five ankyrin proteins (MPXVgp004, 010, 012, 178, and 188) and one Bcl-2-like protein (MPXVgp014) are involved in poxviruses' host range determination. We discovered that the majority (80%) of positive amino acid substitutions emerged several decades ago, indicating that these sites have been under constant selection pressure and that more adaptable alleles have been circulating in the natural reservoir. This finding was also supported by the minimum spanning networks of the gene alleles. The three positive amino acid substitutions (T/A426V in MPXVgp010, A423D in MPXVgp012, and S105L in MPXVgp191) appeared in 2019 or 2022, indicating that they would be crucial for the virus' eventual adaptation to humans. Protein modeling suggests that positive amino acid substitutions may affect protein functions in a variety of ways. Further study should focus on revealing the biological effects of positive amino acid substitutions in the genes for viral adaptation to humans, virulence, transmission, and so on. Our study advances knowledge of MPXV's adaptive mechanism and provides insights for exploring factors that are responsible for the unique aspects of the current outbreak.

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Impact of genetic drift, selection and accumulation level on virus adaptation to its host plants.

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Impact of genetic drift, selection and accumulation level on virus adaptation to its host plants.

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