Genetic diversity among rose rosette virus isolates: a roadmap towards studies of gene function and pathogenicity

Authors: VERCHOT, JEANMARIE - Texas A&M University; HERATH, VENURA - University Of Peradeniya; Jordan, Ramon; Hammond, John

Submitted to: Pathogens
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 5/10/2023
Publication Date: 5/12/2023
Citation: Verchot, J., Herath, V., Jordan, R.L., Hammond, J. 2023. Genetic diversity among rose rosette virus isolates: a roadmap towards studies of gene function and pathogenicity. Pathogens. https://doi.org/10.3390/pathogens12050707.
DOI: https://doi.org/10.3390/pathogens12050707

Interpretive Summary: Roses are one of the most important cultivated ornamental plants worldwide, grown for cut flowers and attractive perennial landscape plants. Over the past several decades, Rose Rosette Disease (RRD) has caused considerable economic losses and has spread from wild roses and the invasive Rosa multiflora into cultivated roses across the US. The causal agent, rose rosette virus (RRV, Emaravirus), can be transmitted by grafting and is naturally transmitted by wind-blown eriophyid mites. Most commercial rose varieties are susceptible to RRV infection, and rose breeders are performing trials to identify new genetic sources of potential RRV resistance. Such trials depend upon recognizing common disease characteristics among RRV isolates that influence the emergence of new strains. This study was undertaken to gain insight into virus genetic diversity, population structures, and the nature of the genetic changes among the full genomes of sequenced RRV isolates. An analysis was conducted using 95 isolates of RRV for which full-length genomic sequences (with 7 RNA segments each) are available. Genetic analysis indicated differences within each genome segment among isolates and a high probability of genome segment reassortment. Only 14 of the 95 isolates were shown to be non-recombinant and were grouped into two distinct lineages. Combined, these results suggest an early series of adaptations from the wild host Rosa multiflora to cultivated roses, followed by slower further adaptation and genetic drift within the many cultivated rose genotypes. Several viral proteins appear to be evolving independently, suggesting that diversity may be important for adaptation to new host genotypes and resistance genes. Overall, these results suggest greater diversity among RRV isolates than previously recognized and suggest new avenues for research, and will aid rose breeders in selecting long-lasting resistance.

Technical Abstract: Ninety-five rose rosette virus (RRV) isolates with full-length genomic sequences were analyzed. There were 95 haplotypes for the concatenated sequences, and 74 to 91 haplotypes per genome segment, with haplotype diversity >0.97 for each segment. Recombination breakpoints were identified at four segment junctions of the concatenated sequences, indicating genome segment reassortment. Recombination breakpoints were identified within RNA2 and RNA6, with isolates from Arkansas and Texas as potential parents. Fourteen non-recombinant isolates belong to major lineages I and II. Lineage I has two subclades, with some genome segments switched between subclades, further indicating reassortment. Informative amino acid variations among each of the viral proteins were mainly among the basal branches of the respective phylogenetic trees, including a minimum of three non-recombinant isolates. This suggests early adaptations from Rosa multiflora to cultivated roses, followed by adaptation and genetic drift within cultivated roses. Restriction site and amino acid variations between isolates may aid in classifying virus subtypes, mutation hotspots, and genetic variations influencing biological properties. Protein P6a was typically 61 residues, with three isolates truncated to 29 residues, and four extending 76-94 residues. Homologous P5 and P7 proteins appear to be evolving independently. These results suggest greater diversity among RRV isolates than previously recognized.