Impact of Cultivated Hosts on the Recombination of Cucumber Mosaic Virus

Abstract

Cucumber mosaic virus (CMV) is one of the most successful viruses known, infecting over 1,200 species of plants. Like other single-stranded RNA viruses, CMV is known to have a high potential for population diversity due to error-prone replication and short generation times. Recombination is also a mechanism that allows viruses to adapt to new hosts. Host genes have been identified that impact the recombination of RNA viruses by using single-cell yeast systems. To determine the impact that the natural plant host has on virus recombination, we used a highrecombination-frequency strain of CMV, LS-CMV, which belongs to subgroup II, in three different cultivated hosts: Capsicum annuum cv. Marengo (pepper), Nicotiana tabacum cv. Xanthi nc (tobacco), and Cucurbita pepo cv. Black Beauty (zucchini). The recombination frequency was calculated by using an RNA 3 reporter carrying restriction enzyme sites created by introducing silent mutations. Our results show that the recombination frequency of LS-CMV is correlated with the infected host. The recombination events in pepper were 1.8-fold higher than those in tobacco and 5-fold higher than those in zucchini. Furthermore, we observed the generation of defective RNAs in inoculated pepper plants, but not in tobacco or zucchini. These results indicate that the host is involved in both intra-and intermolecular recombination events and that hosts like pepper could foster more rapid evolution of the virus. In addition, we report for the first time the production of defective RNAs in a CMV subgroup II isolate. IMPORTANCE Recombination is an important mechanism used by viruses for their diversification and to adapt to diverse hosts. Understanding the host role in the mechanisms of evolution is important for virus disease management and controlling the emergence of new strains. This study shows the impact that cultivated hosts are playing in the evolution of CMV. Furthermore, our results and previous studies show how some specific hosts could be an ideal environment for the emergence of new viral strains.

Genetic Structure of Cucumber Mosaic Virus From Natural Hosts in Nigeria Reveals High Diversity and Occurrence of Putative Novel Recombinant Strains

“…Cucumber mosaic virus, like other RNA viruses, is known to have high mutation rates driven by recombination (Bonnet et al, 2005;Nouri et al, 2014;Hasiów-Jaroszewska et al, 2017;Ouedraogo et al, 2019), and our study identified a putative recombinant within the RNA1 population (isolate '29T_Ibi' from tomato in Oyo State) occurring within the Nigerian population. The high levels of genetic diversity and strain emergence identified in this study may be driven by recombination and/or reassortment of the genomes.…”

“…Strains belonging to subgroups IA and II have worldwide occurrence, while subgroup IB has Asian origins ( Roossinck, 2002 ), although it has been reported across other geographical regions ( Aramburu et al, 2007 ; Farzadfar et al, 2013 ; Kayode et al, 2014 ; Mutuku et al, 2018 ; Kidanemariam et al, 2019 ). The genetic diversity and strain differentiation in CMV is partly driven by varying degrees of recombination and reassortment ( Bonnet et al, 2005 ; Nouri et al, 2014 ; Hasiów-Jaroszewska et al, 2017 ), which is also host-driven ( Ouedraogo et al, 2019 ). This occurs within genomic segments in the same host and similar strains ( Pita et al, 2015 ), across various strains ( Chen et al, 2002 ), and with other cucumoviruses ( de Wispelaere et al, 2005 ).…”

Viruses of cucurbit crops: current status in the Mediterranean Region

“…Recombinations between subgroups of CMV has been widely reported under natural conditions. The different strains of CMV were classified into three main subgroups (IA, IB, and II) (Bonnet et al, 2005;Ouedraogo et al, 2019), notably in Spain with the prevalence of recombination events in RNA3. However, phylogenic analysis of Polish CMV isolates belonging to subgroups IA and II have revealed the prevalence of subgroup II, with detection of a new recombinant with the IA-MP/II-CP pattern (Hasiów-Jaroszewska et al, 2017).…”

High-Throughput Sequencing Discloses the Cucumber Mosaic Virus (CMV) Diversity in Slovakia and Reveals New Hosts of CMV from the Papaveraceae Family

“…It was previously noted that subgroup I isolates have greater high-temperature tolerance and are more prevalent in warmer climates and also that their symptoms are normally more severe when compared to subgroup II [13]. As an RNA virus with a divided genome, recombination and reassortment of viral strains are responsible for the genetic variation of CMV, together with mutation rates induced by a combination of short generation time and error-prone replication [6,14,15].…”

“…A mixed infection incorporating different CMV strains is important from an evolutionary point of view, as reassortment and recombination are responsible for a share of CMV populational variation. Yet these events are quite rare, and their rates are host-dependent [14]. The rarity can be to some extent caused by the reduction of individual CMV strain numbers during transmission by aphids.…”