Abstract
A virus identified as “apple green crinkle associated virus” (AGCaV) was isolated from Aurora Golden Gala apple showing severe symptoms of green crinkle disease. Evidence was obtained of a potential causal relationship to the disease. The viral genome consists of 9266 nucleotides, excluding the poly(A) tail at the 3’-terminus. It has a genome organization similar to that of members of the species Apple stem pitting virus (ASPV), the type species of the genus Foveavirus, family Betaflexiviridae. ORF1 of AGCaV encodes a replicase-complex polyprotein with a molecular mass of 247 kDa; the proteins of ORFs 2, 3, and 4 (TGB proteins) are estimated to be 25.1 kDa, 12.8 kDa, and 7.4 kDa, respectively; and ORF5 encodes the CP, with an estimated molecular mass of 43.3 kDa. Interestingly, AGCaV utilizes different stop codons for ORF1, ORF3, and ORF5 compared to the ASPV type isolate PA66, and between the two viruses, six distinct indel events were observed within ORF5. AGCaV has four non-coding regions (NCRs), including a 5’-NCR (60 nt), a 3’-NCR (134 nt), and two intergenic (IG) NCRs: IG-NCR1 (69 nt) and IG-NCR2 (91 nt). A conserved stable hairpin structure was identified in the variable 5’-NCR of members of the genus Foveavirus. AGCaV may be a variant or strain of ASPV with unique biological properties, but there is evidence that it may be a distinct putative foveavirus.
Similar content being viewed by others
References
Adams MJ, Candresse T, Hammond J, Kreuze JF, Martelli GP, Namba S, Pearson MN, Ryu KH, Saldarelli P, Yoshikawa N (2012) Betaflexiviridae. In: King AMQ, Adams MJ, Carstens EB, lefkowitz EJ (eds) Virus taxonomy: classification and nomenclature of viruses: Ninth Report of the International Committee on Taxonomy of Viruses. San Diego, Elsevier, pp 920–941
Ahmed RA, El-Shehawy MA, Lutang L (2011) The structure and competitiveness of China’s apple exports. World J Agric Sci 7:678–683
Alabi OJ, Martin RR, Naidu RA (2010) Sequence diversity, population genetics and potential recombination events in grapevine rupestris stem pitting-associated virus in Pacific North-West vineyards. J Gen Virol 91:265–276
Araujo PR, Yoon K, Ko D, Smith AD, Qiao M, Suresh U, Burns SC, Penalva LOF (2012) Before it gets started: regulating translation at the 5’UTR. Comp Funct Genomics 2012:475731. doi:10.1155/2012/475731
Atkinson JD, Robbins RE (1951) Green crinkle, a virus disease of apple. N Z J Sci Tech 33:478–482
Chen C-H, Liao B-Y, Chen F-C (2011) Exploring the selective constraint on the sizes of insertions and deletions in 5’ untranslated regions in mammals. BMC Evol Biol 11:192
Dhir A, Ram R, Hallan V, Zaidi AA (2011) Molecular characterization of an Indian variant of Apple stem pitting virus: evidence of recombination. J Plant Pathol 93:471–478
Dreher TW (1999) Functions of the 3’-untranslated regions of positive strand RNA viral genomes. Annu Rev Phytopathol 37:151174
Foissac X, Svanella-Dumas L, Gentit P, Dulucq M-J, Marais A, Candresse T (2005) Polyvalent degenerate oligonucleotides reverse transcription-polymerase chain reaction: a polyvalent detection and characterization tool for trichoviruses, capilloviruses, and foveaviruses. Phytopathology 95:617–625
Hansen AJ, Parish CL (1990) Transmissible fruit disorders In: Jones AL, Aldwinckle HS (eds) Compendium of apple and pear diseases. APS Press, APS, Minnesota, pp 77–78
James D, Upton C (1999) Single primer pair designs that facilitate simultaneous detection and differentiation of peach mosaic virus and cherry mottle leaf virus. J Virol Methods 83:103–111
James D, Varga A, Jesperson GD, Navratil M, Safarova D, Constable F, Horner M, Eastwell K, Jelkmann W (2013) Molecular analysis of a ‘new’ Foveavirus associated with a fruit deforming disease of apple. Petria (in press)
Jelkmann W (1994) Nucleotide sequence of apple stem pitting virus and of the coat protein gene of a similar virus from pear associated with vein yellows disease and their relationship with potex- and carlaviruses. J Gen Virol 75:1535–1542
Komorowska B, Siedlecki P, Kaczanowski S, Hasiów-Jaroszewska B, Malinowski T (2011) Sequence diversity and potential recombination events in the coat protein gene of Apple stem pitting virus. Virus Res 158:263–267
Liu N, Niu J, Zhao Y (2012) Complete genomic sequence analyses of Apple stem pitting virus isolates from China. Virus Genes 44:124–130
Martelli GP, Adams MJ, Kreuze JF, Dolja VV (2007) Family Flexiviridae: a case study in virion and genome plasticity. Annu Rev Phytopathol 45:73–100
Morris TJ, Dodds JA (1979) Isolation and analysis of double-stranded RNA from virus-infected plant and fungal tissue. Phytopathology 69:854–858
Myrta A, Varga A, James D (2006) The complete genome sequence of an El Amar isolate of plum pox virus (PPV) and its phylogenetic relationship to other PPV strains. Arch Virol 151:1189–1198
Nemeth M (1986) Apple green crinkle, pp 160–161. In: Virus, mycoplasma and Rickettsia diseases of fruit trees. Akademiai Kiado, Budapest, p 841
Sawamura K (1965) Studies on apple virus diseases: on mosaic, kikei-ka, and sabi-ka diseases. Bull Fruit Tree Res Stn 3C:25–33
Somogyi LP, Barrett DM, Hui YH (1996) Processing fruits: science and technology: major processed products. Technomic Publishing Co Inc, Pennsylvania, vol 2, p 545
Stebbins RL, Aldwinckle HS (1990) Introduction. In: Jones AL, Aldwinckle HS (eds) Compendium of apple and pear diseases. APS Press, APS, Minnesota, pp 1–5
Stouffer RF, Fridlund PR (1989) Indexing using woody indicators. In: Fridlund PR (ed) Virus and viruslike diseases of pome fruits and simulating noninfectious disorders. Washington State University Cooperative Extension Service, Pullman, pp 255–265
Thompson JD, Gibson TJ, Plewniak F, Jeanmougin F, Higgins DG (1997) The Clustal X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res 24:4876–4882
Thomsen A (1989) Green crinkle. In: Fridlund PR (ed) Virus and viruslike diseases of pome fruits and simulating noninfectious disorders. Washington State University Cooperative Extension Service, Pullman, pp 55–57
USITC (United States International Trade Commission) (2010) Apples: industry and trade summary. USITC Publication ITS-04, Washington, p 55
Youssef F, Marais A, Faure C, barone M, Gentit P, Candresse T (2011) Characterization of prunus-infecting apricot latent virus-like foveaviruses: evolutionary and taxonomic implications. Virus Res 155:440–450
Zhang Y-P, Uyemoto JK, Golino DA, Rowhani A (1998) Nucleotide sequence and RT-PCR detection of a virus associated with grape-vine rupestris stem pitting disease. Phytopathology 88:1231–1237
Zuker M (2003) Mfold webserver for nucleic acid folding and hybridization prediction. Nucleic Acids Res 31:3406–3415
Acknowledgments
We are grateful to the staff of the Diagnostic Section, Sidney Laboratory, Canadian Food Inspection Agency, for generously providing the sample material from the Sidney Virus Repository and information on the disease status and comprehensive results of bioassays and molecular tests conducted over several years.
Author information
Authors and Affiliations
Corresponding author
Electronic supplementary material
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
James, D., Varga, A., Jesperson, G.D. et al. Identification and complete genome analysis of a virus variant or putative new foveavirus associated with apple green crinkle disease. Arch Virol 158, 1877–1887 (2013). https://doi.org/10.1007/s00705-013-1678-7
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00705-013-1678-7