Discovery and Characterization of Two Highly Divergent Variants of a Novel Potyvirus Species Infecting Madagascar Periwinkle (Catharanthus roseus)
- Olufemi J. Alabi1 †
- Kristian Stevens2
- John O. Oladokun1
- Cecilia Villegas1
- Min Sook Hwang2
- Maher Al Rwahnih2
- Tongyan Tian3
- Isaias Hernandez4
- Ashrafou Ouro-Djobo1
- Mamoudou Sétamou5
- John L. Jifon6
- 1Department of Plant Pathology and Microbiology, Texas A&M AgriLife Research and Extension Center, Weslaco, TX 78596
- 2Department of Plant Pathology, University of California-Davis, Davis, CA 95616
- 3California Department of Food and Agriculture, Sacramento, CA 95832
- 4School of Integrative Biological and Chemical Sciences, University of Texas Rio Grande Valley, Edinburg, TX 78539
- 5Texas A&M University-Kingsville Citrus Center, Weslaco, TX 78599
- 6Department of Horticultural Sciences, Texas A&M AgriLife Research and Extension Center, Weslaco, TX 78596
Abstract
During the summer of 2022, a cluster of Madagascar periwinkle plants with white and mauve flowers were observed with foliar mild yellow mosaic symptoms on a private property in Harlingen, Cameron County, Texas. The symptoms were reproduced on mechanically inoculated periwinkle and Nicotiana benthamiana plants. Virions of 776 to 849 nm in length and 11.7 to 14.8 nm in width were observed in transmission electron microscopy of leaf dip preparations made from symptomatic periwinkle leaves. High-throughput sequencing (HTS) analysis of total RNA extracts from symptomatic leaves revealed the occurrence of two highly divergent variants of a novel Potyvirus species as the only virus-like sequences present in the sample. The complete genomes of both variants were independently amplified via reverse transcriptase PCR, cloned, and Sanger sequenced. The 5′ and 3′ of the genomes were acquired using random amplification of cDNA ends methodology. The assembled virus genomes were 9,936 and 9,944 nucleotides (nt) long, and they shared 99.9 to 100% identities with the respective HTS-derived genomes. Each genome encoded hypothetical polyprotein of 3,171 amino acids (aa) (362.6 kilodaltons [kDa]) and 3,173 aa (362.7 kDa), respectively, and they shared 77.3/84.4% nt/aa polyprotein identities, indicating that they represent highly divergent variants of the same Potyvirus species. Both genomes also shared below-species-threshold polyprotein identity levels with the most closely phylogenetically related known potyviruses, thus indicating that they belong to a novel species. The name periwinkle mild yellow mosaic virus (PwMYMV) is given to the potyvirus with complete genomes of 9,936 nt for variant 1 (PwMYMV-1) and 9,944 nt for variant 2 (PwMYMV-2). We propose that PwMYMV be assigned into the genus Potyvirus (family Potyviridae).
Literature Cited
- 2009. Next-generation sequencing and metagenomic analysis: A universal diagnostic tool in plant virology. Mol. Plant Pathol. 10:537-545. https://doi.org/10.1111/j.1364-3703.2009.00545.x CrossrefWeb of ScienceGoogle Scholar
- 2018. Discovery of viruses and virus-like pathogens in pistachio using high-throughput sequencing. Plant Dis. 102:1419‐1425. https://doi.org/10.1094/PDIS-12-17-1988-RE LinkWeb of ScienceGoogle Scholar
- 2012. SPAdes: A new genome assembly algorithm and its applications to single-cell sequencing. J. Comput. Biol. 19:455‐477. https://doi.org/10.1089/cmb.2012.0021 CrossrefWeb of ScienceGoogle Scholar
- 2015. Effect of insecticide-treated potato plants on aphid behavior and potato virus Y acquisition. Pest Manag. Sci. 71:1106‐1112. https://doi.org/10.1002/ps.3892 CrossrefWeb of ScienceGoogle Scholar
- 2000. Ornamental plants and thrips populations associated with tomato spotted wilt virus in Greece. Phytoparasitica 28:257‐264. https://doi.org/10.1007/bf02981804 CrossrefWeb of ScienceGoogle Scholar
- 2014. First report of Cucumber mosaic virus in Catharanthus roseus in Korea. Plant Dis. 98:1283. https://doi.org/10.1094/PDIS-03-14-0230-PDN AbstractWeb of ScienceGoogle Scholar
- 1983. A plant DNA minipreparation: Version II. Plant Mol. Biol. Rep. 1:19‐21. https://doi.org/10.1007/bf02712670 CrossrefGoogle Scholar
- 2004. MUSCLE: Multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res. 32:1792‐1797. https://doi.org/10.1093/nar/gkh340 CrossrefWeb of ScienceGoogle Scholar
- 2020. Physiology of virus-infected plants. Pages 199‐205 in: Applied Plant Virology: Advances, Detection, and Antiviral Strategies. L. P. Awasthi, ed. Academic Press, Elsevier Inc., Amsterdam, the Netherlands. Google Scholar
- 1981. Identification of potato yellow dwarf virus occurring naturally in California. Plant Dis. 65:81‐83. https://doi.org/10.1094/pd-65-81 CrossrefWeb of ScienceGoogle Scholar
- 1985. Confidence limits on phylogenies: An approach using the bootstrap. Evolution 39:783‐791. https://doi.org/10.1111/j.1558-5646.1985.tb00420.x CrossrefWeb of ScienceGoogle Scholar
- 1994. DNA primers for amplification of mitochondrial cytochrome c oxidase subunit I from diverse metazoan invertebrates. Mol. Mar. Biol. Biotechnol. 3:294‐299. Google Scholar
- 2020. The potyviruses: An evolutionary synthesis is emerging. Viruses 12:132. https://doi.org/10.3390/v12020132 CrossrefWeb of ScienceGoogle Scholar
- 1982. The effects of the repellents dodecanoic acid and polygodial on the acquisition of non-, semi- and persistent plant viruses by the aphid Myzus persicae. Ann. Appl. Biol. 100:55‐59. https://doi.org/10.1111/j.1744-7348.1982.tb07191.x CrossrefGoogle Scholar
- 2008. Design and application of two novel degenerate primer pairs for the detection and complete genomic characterization of potyviruses. Arch. Virol. 153:25‐36. https://doi.org/10.1007/s00705-007-1053-7 CrossrefWeb of ScienceGoogle Scholar
- 1999. BioEdit: A user-friendly biological sequence alignment editor and analysis program for windows 95/98/NT. Nucl. Acids Symp. Ser. 41:95‐98. Google Scholar
- 2005. Identification and molecular characterization of Zantedeschia mild mosaic virus, a new calla lily-infecting potyvirus. Arch. Virol. 150:1221‐1230. https://doi.org/10.1007/s00705-004-0488-3 CrossrefWeb of ScienceGoogle Scholar
- 2013. Complete nucleotide sequences of two begomoviruses infecting Madagascar periwinkle (Catharanthus roseus) from Pakistan. Arch. Virol. 158:505-510. https://doi.org/10.1007/s00705-012-1498-1 CrossrefWeb of ScienceGoogle Scholar
ICTV Report Consortium . 2022. ICTV virus Taxonomy profile: Potyviridae 2022. J. Gen. Virol. 103:001738. https://doi.org/10.1099/jgv.0.001738 CrossrefWeb of ScienceGoogle Scholar , and- 2019. Global dimensions of plant virus diseases: Current status and future perspectives. Annu. Rev. Virol. 6:387‐409. https://doi.org/10.1146/annurev-virology-092818-015606 CrossrefWeb of ScienceGoogle Scholar
- 2015. Catharanthus mosaic virus: A potyvirus from a gymnosperm, Welwitschia mirabilis. Virus Res. 203:41‐46. https://doi.org/10.1016/j.virusres.2015.03.007 CrossrefWeb of ScienceGoogle Scholar
- 2018. MEGA X: Molecular evolutionary genetics analysis across computing platforms. Mol. Biol. Evol. 35:1547‐1549. https://doi.org/10.1093/molbev/msy096 CrossrefWeb of ScienceGoogle Scholar
- 2008. An improved general amino acid replacement matrix. Mol. Biol. Evol. 25:1307-1320. https://doi.org/10.1093/molbev/msn067 CrossrefWeb of ScienceGoogle Scholar
- 2011. Characterization of a new potyvirus causing mosaic and flower variegation in Catharanthus roseus in Brazil. Sci. Agric. 68:687‐690. https://doi.org/10.1590/s0103-90162011000600013 CrossrefWeb of ScienceGoogle Scholar
- 1981. Sorghum stunt mosaic. Plant Dis. 65:84‐86. https://doi.org/10.1094/pd-65-84 CrossrefWeb of ScienceGoogle Scholar
- 2015. First report of Catharanthus mosaic virus in Mandevilla in the United States. Plant Dis. 99:165. https://doi.org/10.1094/PDIS-09-14-0913-PDN LinkWeb of ScienceGoogle Scholar
- 2014. SDT: A virus classification tool based on pairwise sequence alignment and identity calculation. PLoS One 9:e108277. https://doi.org/10.1371/journal.pone.0108277 CrossrefWeb of ScienceGoogle Scholar
- 2015. Molecular biology of potyviruses. Adv. Virus Res. 92:101‐199. https://doi.org/10.1016/bs.aivir.2014.11.006 CrossrefWeb of ScienceGoogle Scholar
- 2000. Potato yellow vein virus: Its host range, distribution in South America and identification as a crinivirus transmitted by Trialeurodes vaporariorum. Ann. Appl. Biol. 137:7‐19. https://doi.org/10.1111/j.1744-7348.2000.tb00052.x CrossrefWeb of ScienceGoogle Scholar
SAS Institute . 2014. SAS Software V9.4 (TS1M2). SAS Institute Inc, Cary, NC, U.S.A. Google Scholar- 1994. Evolution, weighting, and phylogenetic utility of mitochondrial gene sequences and a compilation of conserved polymerase chain reaction primers. Ann. Entomol. Soc. Am. 87:651‐701. https://doi.org/10.1093/aesa/87.6.651 CrossrefWeb of ScienceGoogle Scholar
- 2005. Characterization of an Indian isolate of Carnation mottle virus infecting carnations. Curr. Sci. 88:594‐601. https://www.jstor.org/stable/24110259 Web of ScienceGoogle Scholar
- 2014. Adaptation of Lettuce mosaic virus to Catharanthus roseus involves mutations in the central domain of the VPg. Mol. Plant-Microbe Interact. 27:491‐497. https://doi.org/10.1094/MPMI-10-13-0320-R LinkWeb of ScienceGoogle Scholar
- 2011. Next generation sequence assembly with AMOS. Curr. Protoc. Bioinform. 33:11.8.1‐11.8.18. https://doi.org/10.1002/0471250953.bi1108s33 CrossrefGoogle Scholar
USDA-NASS . 2023. 2022 Floriculture Crops. NASS Highlights. https://www.nass.usda.gov/Publications/Highlights/2023/Floriculture_Highlights.pdf (accessed 31 January 2024). Google Scholar- 2019. Molecular characterization and analysis of conserved potyviral motifs in bean common mosaic virus (BCMV) for RNAi-mediated protection. Arch. Virol. 164:181‐194. https://doi.org/10.1007/s00705-018-4065-6 CrossrefWeb of ScienceGoogle Scholar
- 2019. A virome from ornamental flowers in an Australian rural town. Arch. Virol. 164:2255‐2263. https://doi.org/10.1007/s00705-019-04317-7 CrossrefWeb of ScienceGoogle Scholar
- 2010. A novel pair of universal primers for the detection of potyviruses. Plant Pathol. 59:211‐220. https://doi.org/10.1111/j.1365-3059.2009.02201.x CrossrefWeb of ScienceGoogle Scholar