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Identification and Detection of a Virus Associated with Strawberry Pallidosis Disease

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Identification and Detection of a Virus Associated with Strawberry Pallidosis Disease Identification and Detection of a Virus Associated with Strawberry Pallidosis Disease Ioannis E. Tzanetakis and Anne B. Halgren, Department of Botany and Plant Pathology, Oregon State University, Corvallis 97331; Karen E. Keller, Horticulture Crops Research Lab, USDA-ARS, Corvallis 97330; Stanley C. Hokanson, Department of Horticultural Science, University of Minnesota, St. Paul 55108; John L. Maas, USDA- ARS Fruit Lab, Beltsville 20705; Paul L. McCarthy and Robert R. Martin, Horticulture Crops Research Lab, USDA-ARS, Corvallis 97330 from commercial fields in Maryland (M1 ABSTRACT to M29), two from California (C1 and C2) Tzanetakis, I. E., Halgren, A. B., Keller, K. E., Hokanson, S. C., Maas, J. L., McCarthy, P. L., that indexed positive for pallidosis by and Martin, R. R. 2004. Identification and detection of a virus associated with strawberry pal- grafting at USDA-ARS, Corvallis, OR, lidosis disease. Plant Dis. 88:383-390. seven pallidosis isolates from the National Clonal Germplasm Repository (NCGR) in The etiology of pallidosis, a disease of strawberry identified more than 45 years ago, remains Corvallis (CFRA no. 9006, 9037, 9038, unknown. We report a putative agent of the disease, a virus belonging to the Crinivirus genus of 9064, 9065, 9067, 9087), and 12 certified the Closterovirideae family. A sensitive reverse transcription–polymerase chain reaction (RT- virus-free plants from USDA-ARS, Cor- PCR) test has been developed. Polyclonal antibodies that can be used to detect the virus in peti- ole tissue blots were developed using a recombinant virus coat protein. The nucleotide se- vallis, were used. quences of regions of the viral genome that encode the heat shock protein 70 homolog and the Mechanical transmission. Plants be- major coat protein were obtained. Alignments of the major coat protein show that the virus iso- longing to 24 species and eight families lated from strawberry plants positive for pallidosis is most closely related to Cucumber yellows (Table 1) were mechanically inoculated virus (syn. Beet pseudo-yellows virus) and Cucurbit yellow stunt disorder virus, members of the with a mix of leaf tissue of the seven Crinivirus genus. NCGR pallidosis isolates. Four plants of each species were inoculated twice. The wt/vol ratio was 1:10 to 1:20 in phosphate buffered saline (PBS), pH 7.4, with the Pallidosis is a disease of strawberry first a graft transmissible agent(s) that causes addition of 2% nicotine. Carborundum reported in California and Australia in distortion, chlorosis of leaves, and dwarf- (600 mesh) was added on the leaf surface 1957 (6). Since then it has been reported in ing of grafted Fragaria virginiana, ‘UC- to facilitate delivery of the pallidosis Eastern Canada (4), Arkansas (8), and 10’ or ‘UC-11’ plants, while F. vesca indi- agent(s) into the indicator plants. Maryland (10). Pallidosis disease is an cator plants and commercial strawberry Purification of virus and dsRNA. Vi- unrecognized or under-recognized problem cultivars remain symptomless. It is impor- rus was purified as described previously in the strawberry industry, but there are tant to note that because of the latent infec- (14) with the initial wt/vol ratio changed to recent studies showing that the disease is tion in most cultivars, the detection of the 1:6 or 1:10 due to the viscosity of the very widespread in the Mid-Atlantic states disease has only been possible by grafting strawberry tissue. Double-stranded RNA (10). In greenhouse-grown plants of onto both F. virginiana and F. vesca indica- ‘Northwest’ strawberry, the disease re- tor plants (7). duces runner production and root growth We report a putative causal agent of pal- Table 1. Indicator plants used for mechanical by 15 to 20% (3). However, its major im- lidosis disease, a virus in the Crinivirus transmission of Strawberry pallidosis associated pact in yield loss is believed to result when genus of the Closterovirideae family, and virus it occurs in mixed infections with other tentatively designate it as Strawberry pal- Plant name Family strawberry viruses (16). lidosis associated virus (SPaV). In addi- The pallidosis agent is graft-transmitted, tion, the complete nucleotide sequences of Antirrhinum majus Scrophulariaceae Beta vulgaris Chenopodiaceae and high-molecular-weight dsRNA species the heat shock protein 70 homolog Chenopodium giganteum Chenopodiaceae have been purified previously from in- (HSP70h) and major coat protein (CP) Chenopodium quinoa Chenopodiaceae fected plants (21). Inclusion bodies similar genes of the virus are presented, and mo- Cucumis sativus Cucurbitaceae to those of Beet yellows virus (BYV), the lecular and immunological assays devel- Datura stramonium Solanaceae type member of the Closterovirideae fam- oped for detection of SPaV are described. Glycine max Fabaceae ily of plant viruses, have been observed in Gomphrena globosa Amaranthaceae plants that indexed positive for pallidosis MATERIALS AND METHODS Lathyrus odoratus Fabaceae Plant source. Fra- Lactuca sativa Asteraceae (9). Several lines of evidence suggest that Strawberry plants ( Lycopersicon esculentum Solanaceae the pallidosis disease is of viral etiology. garia × ananassa) from commercial fields Medicago sativa Fabaceae Pallidosis is defined as a disease caused by in Maryland were tested at the USDA- Nicotiana benthamiana Solanaceae ARS Fruit Laboratory in Beltsville, MD, Nicotiana glutinosa Solanaceae for virus infection by grafting onto indica- Nicotiana rustica Solanaceae Corresponding author: Robert R. Martin tor plants F. vesca (‘UC-4’ or ‘UC-5’) and Nicotiana tabacum Solanaceae E-mail: [email protected] F. virginiana (‘UC-10’ or ‘UC-11’) as (cv. Samsun NN) described previously (5). Source plants Petunia × hybrida Solanaceae Accepted for publication 12 December 2003. Phaseolus vulgaris Fabaceae that resulted in symptoms when grafted Phlox drummondii Polemoniaceae onto F. virginiana plants (yellowing, dis- Pisum sativum Fabaceae Publication no. D-2004-0203-01R tortion of leaves, cachexia) but failed to Spinacia oleracea Chenopodiaceae This article is in the public domain and not copy- F. vesca Tagetes patula Asteraceae rightable. It may be freely reprinted with custom- cause any visible symptoms on ary crediting of the source. The American Phyto- plants were considered to have pallidosis. Trifolium pratense Fabaceae pathological Society, 2004. Twenty-nine individual strawberry plants Vigna unguiculata Fabaceae Plant Disease / April 2004 383 (dsRNA) was purified as described previ- Laboratory at Oregon State University the primers mentioned above as well as the ously (21) from 22 of the available pallido- using an ABI 377 DNA sequencer. The M13 forward and reverse primers. All sis isolates in addition to four certified BLAST databases (blastn and blastp) at the consensus sequences were assembled us- virus-free strawberry cultivar plants. At National Center for Biotechnology Infor- ing the Clustal W program (European Bio- least 100 dsRNA extractions were carried mation (NCBI, published online) were informatics Institute, published online). out in this study and subjected to gel elec- used to compare the unknown sequences to Detection by RT-PCR. RNA was ex- trophoresis. After extraction, the dsRNA the GenBank’s nucleotide and protein tracted from 100 mg of strawberry leaf was aliquoted and precipitated by centrifu- databases, respectively. tissue as described previously (11) and was gation at 16,000 × g for 30 min at room Three clones (SP 21, SP 37, and SP 44) resuspended in 40 µl of water. Reverse temperature in 70% ethanol and 0.1 M corresponding to the HSP70h gene and transcription was performed using Super- sodium acetate. The dsRNA was resus- two clones (SP 60 and SP 63) correspond- script II reverse transcriptase (Invitrogen) pended in 10 µl of Tris-borate-EDTA ing to the CP gene of the virus were identi- according to the manufacturer’s instruc- (TBE), pH 8.0, and was resolved by elec- fied after using BLAST by comparison tions using RNA as 1/10 of the volume of trophoresis through a 1% agarose gel con- with related sequences in the database. the reaction and using 0.3 µg of random taining ethidium bromide at 100 ng/ml. Oligonucleotide primers HSP 5′, HSP 3′, nucleotide hexamers (Invitrogen). The Cloning and analysis. An amount of CP 5′, and CP 3′ (Table 2) were developed, reaction was terminated by heating at 75°C dsRNA equivalent to that extracted from 4 which allowed the amplification of the for 20 min followed by incubation with g of fresh strawberry leaf tissue of Mary- complete HSP70h (HSP 5′/HSP 3′) and CP one unit of RNase H (Invitrogen) for 30 land field isolate M1 was incubated with (CP 5′/CP 3′) genes by RT-PCR. The first- min at 37°C. For PCR, we used primers SP 20 mM methyl mercuric hydroxide and strand cDNA was prepared using reverse 44F and SP 44R that amplify a 517 base random nucleotide hexamer primers (0.5 transcriptase as described above from pair (bp) fragment of the HSP70h gene and µg) (Invitrogen, Carlsbad, CA) for 20 min dsRNA, and 5 µl of the RT reaction was CP 5′ and CP n731R (Table 2) that amplify at room temperature in water. The cDNA used as template in a 50-µl PCR reaction a 752 bp fragment containing the largest synthesis was performed according to the that consisted of 50 mM KCl, 10 mM Tris- part of the CP gene. We developed primers manufacturer’s instructions using Thermo- HCl (pH 9.0), 0.1% Triton X-100, 2 mM SPL F and SPL R (Table 2) that amplify a script reverse transcriptase (RT) (Invitro- MgCl2, 0.2 mM dNTPs, 400 nM each of 5′ 301 bp fragment of the strawberry pectate gen) in a final volume of 50 µl. The cDNA and 3′ primers, and 1 unit Taq Polymerase lyase B gene, which we used as an internal was ethanol precipitated, air-dried, and (Invitrogen). control in our PCR reactions. The program second-strand synthesis carried out as The PCR program we used consisted of consisted of initial denaturation for 5 min described previously (12).
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