Squash vein yellowing virus from California emerged in the Middle East via intragenic and intergeneric recombination events in the hypervariable potyvirus P1 and ipomovirus P1a genes

Authors: ALVES DE MACEDO, MONICA - Instituto Federal De Educação Ciência E Tecnologia; MELGAREJO, TOMAS - Dominican University Of California; VASQUEZ-MAYORGA, MARCELA - University Of California; CESPEDES, MONICA - University Of California; ROJAS, MARIA - University Of California; TURINI, TOM - University Of California Agriculture And Natural Resources (UCANR); BATUMAN, OZGUR - University Of Florida; Wintermantel, William; GILBERTSON, ROBERT - University Of California

Submitted to: Journal of General Virology
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 9/26/2024
Publication Date: 10/17/2024
Citation: Alves de Macedo, M., Melgarejo, T., Vasquez-Mayorga, M., Cespedes, M., Rojas, M., Turini, T., Batuman, O., Wintermantel, W.M., Gilbertson, R.L. 2024. Squash vein yellowing virus from California emerged in the Middle East via intragenic and intergeneric recombination events in the hypervariable potyvirus P1 and ipomovirus P1a genes. Journal of General Virology. 105(10). Article 002033. https://doi.org/10.1099/jgv.0.002033.
DOI: https://doi.org/10.1099/jgv.0.002033

Interpretive Summary: The genome of a squash vein yellowing virus (SqVYV) isolate from California (SqVYV-CA) has been determined and found to be a natural genetic recombinant virus with the majority of the sequence related to an SqVYV isolate from Israel (SqVYV-IL), but with a portion near the beginning of the virus genome related to but distinct from papaya ringspot virus. Results of plant inoculation experiments showed that the SqVYV-CA host range and symptomatology in cucurbits is similar to those of SqVYV-FL and SqVYV-IL, revealing no impact of recombinant portion of the genome on these properties. Detection methods were developed to specifically detect SqVYV-CA and distinguish it from other SqVYV isolates. These results demonstrate that a high level of genetic diversity exists in SqVYV, recombination and mutations occur within SqVYV populations, and provides evidence that SqVYV originated in the Middle East.

Technical Abstract: The complete genome sequence of an isolate of squash vein yellowing virus from California (SqVYV-CA) has been determined and shows that it is a recombinant virus with a highly divergent 5’ untranslated region (UTR) and proximal P1a gene. The evolution of SqVYV-CA involved an intrageneric event between unknown potyviruses, related to isolates of papaya ringspot virus (PRSV) from the Old World , and an intergeneric event between this recombinant potyvirus (minor parent) and an isolate of SqVYV from Israel (SqVYV-IL) (major parent). These events occurred in the potyvirus P1 and ipomovirus P1a hotspots, and resulted in SqVYV-CA having a potyvirus 5’ UTR and chimeric P1-P1a gene/protein, and the remainder of the genome from SqVYV-IL. The SqVYV-CA chimeric P1-P1a gene is under positive selection, and the protein is intrinsically disordered and may localize to the nucleus via nuclear localization signals in the P1 portion. The C-terminal SqVYV-IL P1a portion also has diverged, but retained the conserved serine protease motif. Furthermore, substantial divergence among other isolates, especially from the Middle East, revealed genetic drift and a long evolutionary history. Results of plant inoculation experiments showed that the SqVYV-CA host range and symptomatology in cucurbits is similar to those of SqVYV-FL and -IL, revealing no impact of recombinant portion of the genome on these properties. A divergent part of the P1 sequence of the SqVYV-CA P1-P1a gene was used to develop a primer pair and RT-PCR test for specific detection of SqVYV-CA. This test was used to detect spread to a new production area of California in 2021 and 2022. Together, these results demonstrate (i) a high level of genetic diversity exists in SqVYV, (ii) involvement of intra- and intergeneric recombination and genetic drift (mutation), and (iii) evidence that SqVYV originated in the Middle East.