Specificity of Resistance and Tolerance to Cucumber Vein Yellowing Virus in Melon Accessions and Resistance Breaking with a Single Mutation in VPg

Abstract

Cucumber vein yellowing virus (CVYV) is an emerging virus on cucurbits in the Mediterranean Basin, against which few resistance sources are available, particularly in melon. The melon accession PI 164323 displays complete resistance to isolate CVYV-Esp, and accession HSD 2458 presents a tolerance, i.e. very mild symptoms in spite of virus accumulation in inoculated plants. The resistance is controlled by a dominant allele Cvy-11, while the tolerance is controlled by a recessive allele cvy-2, independent from Cvy-11. Before introducing the resistance or tolerance in commercial cultivars through a long breeding process, it is important to estimate their specificity and durability. Upon inoculation with eight molecularly diverse CVYV isolates, the resistance was found to be isolate-specific since many CVYV isolates induced necrosis on PI 164323, whereas the tolerance presented a broader range. A resistance-breaking isolate inducing severe mosaic on PI 164323 was obtained. This isolate differed from the parental strain by a single amino acid change in the VPg coding region. An infectious CVYV cDNA clone was obtained, and the effect of the mutation in the VPg cistron on resistance to PI 164323 was confirmed by reverse genetics. This represents the first determinant for resistance-breaking in an ipomovirus. Our results indicate that the use of the Cvy-11 allele alone will not provide durable resistance to CVYV and that, if used in the field, it should be combined with other control methods such as cultural practices and pyramiding of resistance genes to achieve long-lasting resistance against CVYV.

Determinants of Virus Variation, Evolution, and Host Adaptation

“…Plant viruses rely on host factors to replicate, move cell to cell, and travel systemically, but there is natural variation in those host factors [20,32]. Accordingly, plant viruses co-evolve with their host [33,34] and establish a balance between genomic functionality and the bottlenecks imposed by host genetic diversity, host compatibility, antiviral defense, and the fitness cost to the virus associated with host-range expansion or host specialization [10,30,35,36].…”

“…Interestingly, not all areas of the virus genome accumulate mutations at the same rate. Instead, mutations preferentially accumulate in parts of the genome that are determinants of host adaptation [20,[39][40][41].…”

“…Dominant and recessive R genes have been identified in wild relatives and introduced through plant breeding into commercial cultivars of important crops such as tomato, soybean, and potato [16][17][18]. However, new virus variants and species can quickly break host resistance, especially when virus resistance is dependent on a single gene [19,20]. This phenomenon occurs when in key areas of the virus genome, mutations accumulate that provide a selective advantage [19][20][21].…”

“…However, new virus variants and species can quickly break host resistance, especially when virus resistance is dependent on a single gene [19,20]. This phenomenon occurs when in key areas of the virus genome, mutations accumulate that provide a selective advantage [19][20][21].…”

“…During replication, viruses may recombine, generate mutations, and, for RNA viruses, exist as a cloud of genetic variants (quasispecies) [22][23][24][25]. There is natural genetic diversity in host plants and vectors and variation in environmental conditions [20,26]. Accordingly, viruses are forced to interact with and adapt to genetically diverse host and vector factors in diverse environments.…”