Characterization of two novel viruses within a complex virome from flowering ginger in Hawaii

Authors: LARREA-SARMIENTO, ANDREA - University Of Hawaii; GALANTI, RUSSELL - University Of Hawaii; OLMEDO-VELARDE, ALEJANDRO - University Of Hawaii; WANG, XUPENG - University Of Hawaii; AL RWAHNIH, MAHER - University Of California, Davis; BORTH, WAYNE - University Of Hawaii; LUTGEN, HANNAH - University Of Hawaii; FITCH, MAUREEN - Hawaii Agricultural Research Center; SUGANO, JARI - University Of Hawaii; SEWAKE, KELVIN - University Of Hawaii; Suzuki, Jon; Wall, Marisa; MELZER, MICHAEL - University Of Hawaii; HU, JOHN - University Of Hawaii

Submitted to: Plant Disease
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 3/21/2024
Publication Date: 9/26/2024
Citation: Larrea-Sarmiento, A.E., Galanti, R., Olmedo-Velarde, A., Wang, X., Al Rwahnih, M., Borth, W., Lutgen, H., Fitch, M.M, Sugano, J., Sewake, K., Suzuki, J., Wall, M.M., Melzer, M., Hu, J. 2024. Characterization of two novel viruses within a complex virome from flowering ginger in Hawaii. Plant Disease. 108(10):3001-3009. https://doi.org/10.1094/PDIS-10-23-2181-RE.
DOI: https://doi.org/10.1094/PDIS-10-23-2181-RE

Interpretive Summary: Flowering ginger is a crop of economic and cultural importance in Hawaii. It contributes to a Hawaii horticulture and nursery industry estimated at $81.6 million. The cause of decline in flowering ginger plant vigor observed among growers and researchers in recent years has been elusive. In this study, researchers applied modern sequencing methods in an effort to determine whether ginger plants were infected with plant viruses and whether any were associated with slow decline symptoms. Whole genome sequences from a total of six different viruses including two previously undescribed viruses were found among the sampled flowering ginger. Three viruses including Canna yellow mottle virus (CaYMV) and the two newly identified viruses, Alpinia vein clearing virus (ApVCV) and Alpinia vein streaking virus (ApVSV) were associated with slow decline symptoms whereas the remainder, banana bract mosaic virus (BBrMV), bean common mosaic virus (BCMV) and banana streak GF virus (BSGFV) were not. Additional experiments and data from this study suggest that CaYMV and ApVCV are carried and spread to other plants by mealybugs whereas ApVSV is spread by aphids.

Technical Abstract: Alpinia purpurata holds economic and cultural importance in Hawaii, contributing to its horticulture and nursery industry estimated at $81.6 million. Association of viral infection with slow decline symptoms observed in flowering ginger in Hawaii was investigated by using RNA-seq analyses and virus-specific PCR surveys. Viral sequences corresponding to a total of six viruses were recovered via RNA-seq data analysis from samples presenting virus-like symptoms. Three viruses including Canna yellow mottle virus (CaYMV; genus Badnavirus) and two novel viruses, Alpinia vein clearing virus (ApVCV, genus Ampelovirus) and Alpinia vein streaking virus (ApVSV; genus betanucleorhabdovirus) were concomitant with slow decline symptoms. The other three viruses comprise the two potyviruses banana bract mosaic virus (BBrMV) and bean common mosaic virus (BCMV) and the badnavirus, banana streak GF virus (BSGFV), and were not found to be associated with slow decline symptoms. Virus detection from potential vectors and transmission assays identified for the first time the mealybug Planococcus citri as vector of the semi-persistently transmitted CaYMV and ApVCV. Likewise, the aphid Pentalonia caladii was identified as vector of the novel ApVSV. Both P. citri and P. caladii are common pests in flowering ginger. Preliminary studies suggest that the host switch P. caladii had a negative influence on the transmission of ApVSV; however, ApVSV transmission was archived using aphid colonies naturally feeding on infected flowering ginger plants. Our results provide an insight into how viral infections are associated with the current decline of flowering ginger in Hawaii.