Experimental evolution of cowpea mild mottle virus reveals recombination-driven reduction in virulence accompanied by increases in diversity and viral fitness

• Published in: Virus research Vol. 303; p. 198389
• Main Authors: Zanardo, Larissa G., Trindade, Tiago A., Mar, Talita B., Barbosa, Tarsiane M.C., Milanesi, Diogo F., Alves, Murilo S., Lima, Roberta R.P.N., Zerbini, F. Murilo, Janssen, Arne, Mizubuti, Eduardo S.G., Elliot, Simon L., Carvalho, Claudine M.
• Format: Journal Article
• Language: English
• Published: Netherlands Elsevier B.V 02.10.2021
• Subjects: Animals; Bemisia tabaci; Carlavirus; Carlavirus - genetics; DNA Viruses - genetics; Evolution of virulence; Hemiptera - genetics; Recombination; Recombination, Genetic; RNA; RNA virus; RNA Viruses - genetics; Vigna; Virulence - genetics; Virus evolution; Carlavirus; Evolution of virulence; Virus evolution; Recombination; RNA virus; Bemisia tabaci
• ISSN: 0168-1702; 1872-7492
• DOI: 10.1016/j.virusres.2021.198389

•The Cowpea mild mottle virus (CPMMV) lost the capacity to cause necrosis after serial passages through the host plant.•The change to milder symptoms had fitness benefits for the virus and for its vector, the whitefly Bemisia tabaci.•Reduction in virulence was a consequence of the emergence of new variants, driven by recombination.•Recombination-driven switch in virulence allows the pathogen to rapidly adapt to a new host and, potentially, switch back. Major themes in pathogen evolution are emergence, evolution of virulence, host adaptation and the processes that underlie them. RNA viruses are of particular interest due to their rapid evolution. The in vivo molecular evolution of an RNA plant virus was demonstrated here using a necrotic isolate of cowpea mild mottle virus (CPMMV) and a susceptible soybean genotype submitted to serial inoculations. We show that the virus lost the capacity to cause necrosis after six passages through the host plant. When a severe bottleneck was imposed, virulence reduction occurred in the second passage. The change to milder symptoms had fitness benefits for the virus (higher RNA accumulation) and for its vector, the whitefly Bemisia tabaci. Genetic polymorphisms were highest in ORF1 (viral replicase) and were independent of the symptom pattern. Recombination was a major contributor to this diversity – even with the strong genetic bottleneck, recombination events and hot spots were detected within ORF1. Virulence reduction was associated with different sites in ORF1 associated to recombination events in both experiments. Overall, the results demonstrate that the reduction in virulence was a consequence of the emergence of new variants, driven by recombination. Besides providing details of the evolutionary mechanisms behind a reduction in virulence and its effect under viral and vector fitness, we propose that this recombination-driven switch in virulence allows the pathogen to rapidly adapt to a new host and, potentially, switch back.