Cucumber mosaic virus populations in Tunisian pepper crops are mainly composed of virus reassortants with resistance‐breaking properties

Abstract

Cucumber mosaic virus is one of the most prevalent viruses in Tunisian pepper crops, where it has been detected in 68% of plants developing mosaic symptoms, making it essential to characterize the molecular and biological properties of local CMV populations. Two hundred and seventy-eight isolates collected in the late 1990s, 2006 and 2008-2010 were characterized genetically. Isolates belonging to the three phylogenetic subgroups of CMV (IA, IB and II) were detected, but surprisingly, 90% of the isolates were reassortants between subgroups IA and IB, with two predominant haplotypes, IB-IA-IA and IB-IA-IB (nomenclature according to the subgrouping of the three genomic RNAs). The IB-IA-IA haplotype was present in all regions surveyed, while IB-IA-IB was observed only in northern Tunisia. This situation was unexpected, because CMV reassortants were previously thought to be counterselected in nature, and this raises the questions of the origin of IB strains in Tunisia and of the widespread distribution of these two reassortant types. Phylogenetic studies revealed low diversity within haplotypes, whatever the locality or the year of sampling. However, analysis of haplotype frequencies revealed a high genetic differentiation between CMV populations, which was better explained by the localities of sampling than by years. Geographic distances affected the differentiation of CMV populations, mainly between north and central Tunisia. When tested against a polygenic resistance to CMV movement in pepper, 55 of 57 isolates tested were able to break the resistance, indicating that this resistance would not be useful for controlling CMV in Tunisian pepper fields.

Genotyping of Cucumber mosaic virus isolates in western New York State during epidemic years

“…5). A recent genetic study of CMV populations of pepper in South Korea identified geographically distinct subpopulations , a phenomenon also reported in Tunisia (Ben Tamarzizt et al, 2013). Genetic diversities in the Korean populations were highest at 0.060 in the 1a ORF and lowest at 0.029 in the MP ORF .…”

A critical evaluation of whether recombination in virus‐resistant transgenic plants will lead to the emergence of novel viral diseases

“…This suggests that it would be more biologically significant to focus on the effect of recombination on between‐host transmission. However, the rate of transmission of aphid‐transmitted plant viruses, including CMV, has been shown repeatedly to correlate with accumulation in the infected host (Escriu et al ., ; Betancourt et al ., ), establishing a link between the within‐host and between‐host components of virus fitness. The messenger/viral RNA recombinant becomes predominant in the viral population Detailed analyses of the genetic structure of field populations of CMV in different regions of the world have shown the presence of isolates generated by genetic exchange by both reassortment of genomic segments and by recombination within each segment (Bonnet et al ., ; Ben Tamarzizt et al ., ; Nouri et al ., ). However, the frequency of recombinants was always low, even under conditions in which this would not be attributed to random genetic drift (Bonnet et al ., ).…”

“…shown the presence of isolates generated by genetic exchange by both reassortment of genomic segments and by recombination within each segment (Bonnet et al, 2005;Ben Tamarzizt et al, 2013;Nouri et al, 2014). However, the frequency of recombinants was always low, even under conditions in which this would not be attributed to random genetic drift (Bonnet et al, 2005).…”

“…8. The recombinant virus is the cause of the emergence of a more aggressive viral disease Although it has been proposed that certain reassortant combinations of CMV may have a selective advantage on pepper crops (Ben Tamarzizt et al, 2013), it seems that this is not the case for recombinants. As discussed in the previous paragraph, recombinants seem to be at a disadvantage relative to their parental viruses, both under experimental conditions and in natural populations (Bonnet et al, 2005;Pierrugues et al, 2007;Nouri et al, 2014).…”

Survey of viruses infecting open‐field pepper crops in Côte d'Ivoire and diversity of Pepper veinal mottle virus and Cucumber mosaic virus

“…Polygenic resistance to CMV, combining several QTLs (quantitative trait loci) acting on different steps of plant infection, has been used to create highly resistant pepper cultivars, including F 1 hybrids (Caranta et al, 1997a(Caranta et al, , 2002Palloix & Ordon, 2011). However, a recent epidemiological survey in Tunisia showed that several CMV isolates were adapted to the resistant pepper cultivar Milord (Ben Tamarzizt et al, 2013). One common property shared by all CMV isolates virulent towards pepper resistance was the fact that they had a subgroup IB-type RNA 1.…”