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Genome Organization and Phylogenetic Relationship of Pineapple Mealybug Wilt Associated Virus-3 with Family Closteroviridae Members

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Genome Organization and Phylogenetic Relationship of Pineapple Mealybug Wilt Associated Virus-3 with Family Closteroviridae Members Virus Genes (2009) 38:414–420 DOI 10.1007/s11262-009-0334-5 Genome organization and phylogenetic relationship of Pineapple mealybug wilt associated virus-3 with family Closteroviridae members Diane M. Sether Æ Michael J. Melzer Æ Wayne B. Borth Æ John S. Hu Received: 28 August 2008 / Accepted: 2 February 2009 / Published online: 19 February 2009 Ó Springer Science+Business Media, LLC 2009 Abstract The nucleotide sequence of Pineapple mealy- growing regions of the world [1–8]. PMWaV-1, PMWaV-2, bug wilt associated virus-3 (PMWaV-3) (Closteroviridae: and PMWaV-3 are mealybug transmitted viruses [7, 9]in Ampelovirus), spanning seven open reading frames (ORFs) the genus Ampelovirus of the family Closteroviridae. The and the untranslatable region of the 30 end was determined. presence of PMWaV-2 in conjunction with the feeding of Based on the amino acid identities with orthologous ORFs mealybugs has been shown to result in mealybug wilt of of PMWaV-1 (54%–73%) and PMWaV-2 (13%–35%), we pineapple (MWP), a devastating disease of pineapple propose PMWaV-3 is a new species in the PMWaV com- worldwide [10]. Pink and grey pineapple mealybugs, plex. PMWaV-3 lacks an intergenic region between Dysmicoccus brevipes (Cockerell) and D. neobrevipes ORF1b and ORF2, encodes a relatively small, 28.8 kDa, Beardsley, respectively, can transmit PMWaV-2 and induce coat protein, and lacks a coat protein duplicate. Phyloge- MWP [10]. These mealybug species can also transmit netic analyses were used to analyze seven different PMWaV-1 and PMWaV-3, but these viruses in conjunction domains and ORFs from members of the family Closte- with mealybug feeding do not result in MWP [7, 10]. Also, roviridae. Two distinct clades within the recognized genus mealybug feeding on PMWaV-free plants does not induce Ampelovirus were observed; one that includes PMWaV-3 MWP [10, 11]. and PMWaV-1 and several GLRaVs and another that The family Closteroviridae is currently composed of includes PMWaV-2 and GLRaV-3, the type member of the three recognized genera, Ampelovirus, Closterovirus, and genus Ampelovirus. Crinivirus. Virus species within these genera are charac- teristically mealybug, aphid, or whitefly transmitted, Keywords Virus genome Á Pineapple Á Mealybug wilt Á respectively, although vector species have not been deter- Ananas comosus Á Virus transmission mined for some of the virus species in each group. The partial genome sequence of PMWaV-2 and, more recently, the complete genome sequence of PMWaV-1 have been Introduction determined [12, 13]. Sequence comparisons of the RNA- dependent RNA polymerase (RdRp), heat shock protein 70 A complex of pineapple mealybug wilt associated viruses homolog (Hsp70h), and coat protein (CP) regions suggested (PMWaVs), have been identified in the Ananas (pineapple) that PMWaV-1, Plum bark necrotic stem-pitting-associated and Pseudoananus genera throughout the pineapple virus (PBNSPaV), Grapevine leafroll-associated virus-4 (GLRaV-4), GLRaV-5, GLRaV-6, and GLRaV-9 form a distinct branch from PMWaV-2, GLRaV-1, and GLRaV-3, Electronic supplementary material The online version of this article (doi:10.1007/s11262-009-0334-5) contains supplementary the type member of the Ampelovirus genus. In this article, material, which is available to authorized users. we characterize the genome organization and protein fea- tures of PMWaV-3 and compare these to orthologs from & D. M. Sether Á M. J. Melzer Á W. B. Borth Á J. S. Hu ( ) other PMWaVs and members of the family Closteroviridae. Plant and Environmental Protection Sciences, University of Hawaii at Manoa, 3190 Maile Way, Honolulu, HI 96822, USA Phylogenetic analyses conducted on seven domains and e-mail: [email protected] open reading frames (ORFs) are used to further elucidate 123 Virus Genes (2009) 38:414–420 415 two distinct clades that clearly separate PMWaV-2 from the DQ399259, PMWaV-4 EU372003, PMWaV-5 EF467920, other characterized PMWaVs in the genus Ampelovirus. and Tulip severe mosaic virus (TSMV) EF203673. Closte- rovirus sequences used for phylogenetic analyses and alignment with the GAP function of SeqWeb (GCG Inc.) were as follows: Beet yellow stunt virus (BYSV) U51931, Materials and methods Beet yellows virus (BYV) X73476, Citrus tristeza virus (CTV) isolate T36 AY170468, Fig leaf mottle-associated Cloning and sequencing virus (FLMaV) AM279677, FLMaV-2 AM286422, FLMaV-3 EF654103, GLRaV-2 EF012721, Mint virus-1 PMWaV-3-infected pineapple plants were identified with (MV-1) AY792620, Olive leaf yellowing-associated virus reverse transcription (RT)-PCR and specific oligonucleo- (OLYaV) AJ440010, Raspberry mottle virus (RMoV) tide primers 264 and 263 as previously described [7]. DQ357218, and Strawberry chlorotic fleck-associated virus Double-stranded RNA (dsRNA) was purified from the leaf (SCFaV) DQ860839. Crinivirus sequences used for phylo- bases of these infected plants and used as a template for genetic analyses and GAP alignment were as follows: cDNA synthesis as previously described [3, 12]. Pineapple Abutilon yellows virus (AYV) AY422070, Bean yellow leaf bases were powdered in liquid nitrogen and RNA was disorder virus (BYDV) NC_010560/NC_010561, Beet purified from 100 mg of tissue with RNeasyTM Plant Mini Pseudo-yellows virus (BPYV) AY330919/AY330919, Kits (Qiagen, Valencia, CA) following manufacturer’s Blackberry yellow vein associated virus (BYVaV) instructions and stored at -80°C until needed. From this AY77335, Cucurbit yellow stunting disorder virus initial clone, a step-by-step walking procedure [12, 13] was (CYSDV) AJ243000, Lettuce infectious yellows virus used to obtain additional sequence information from the 50 (LIYV) NP_733943, Potato yellow vein virus (PYVV) and 30 regions of the genome with overlapping clones AJ557129, Strawberry pallidosis associated virus (SPaV) (Fig. 1a). These RT-PCR amplicons were gel purified and AY262159, Sweet potato chlorotic stunt virus (SPCSV) ligated into the plasmid pGEM-T Easy (Promega, Madison, AJ428555, and Tomato chlorosis virus (TCV) AY903448. WI). Plasmids were sequenced in both directions by auto- Sequences of unassigned members in the family Clostero- mated sequencing at the Center for Advanced Studies of viridae used for phylogenetic analyses and GAP alignment Genomics, Proteomics, and Bioinformatics at University of were as follows: LChV-1 NP_045006 and Mint vein banding Hawaii at Manoa. Nucleotide sequences were compared virus (MVBV) AY548173. with the nonredundant amino acid sequence database at the Sequences were aligned with Clustal X v1.8 [16] using National Center for Biotechnology Information (NCBI) pairwise alignment parameters with a gap opening penalty website using the BLASTX algorithm [14, 15]. of 35, a gap extension penalty of 0.75, and the Gonet protein weight matrix. Multiple alignment parameters had Sequence comparisons and phylogenetic analyses a gap opening penalty of 15 and gap extension penalty of 0.3. Divergent sequence delay was set at 25%. Unrooted The amino acid (aa) sequences from PMWaVs and other phylogenetic trees based on 1000 replications were created family Closteroviridae members were retrieved from the with PAUP* v4.0b [17] using neighbor-joining analysis NCBI for the following domains and ORFs: ORF 1a, the with bootstrapping and parsimony analysis with jack- methyltransferase (MTR) domain belonging to pfam01660 knifing. and the helicase (HEL) domain; ORF 1b, the RNA- depen- dent RNA polymerase (RdRp); ORF 2, a small hydrophobic protein (p5); ORF 3, the heat shock 70 protein homolog Results (Hsp70h) protein; ORF 4, a 61 kDa protein (p61); and ORF5, the coat protein (CP) and the conserved clostero_coat of Genome organization of PMWaV-3 pfam01785 present in the CP open reading frame. Ampelo- virus sequences used for phylogenetic analyses and GAP The sequence composed of 11891 nucleotides of PMWaV-3, alignment in SeqWeb were as follows: Grapevine leafroll- was deposited in GenBank (accession DQ399259). The associated virus-1 (GLRaV-1) AF195822, GLRaV-3 ORF nomenclature used here follows the convention used NP_813795, GLRaV-4 AM162279, GLRaV-5 AF233934, for GLRaV-3, the type member of the genus Ampelovirus GLRaV-6 AM745345, GLRaV-9 AY297819/AY072797, [18]. The PMWaV-3 sequence spans seven ORFs including GLRaV-10 AM182328,GLRaV-11 AM494935, Little the untranslatable region at the 30 end of the virus (Fig. 1b). cherry virus-2 (LChV-2) AF416335, Plum bark necrosis The partial sequence of ORF1a contains a conserved viral stem pitting-associated virus (PBNSPaV) EF546442, methyltransferase (MTR) domain typical of pfam 01660 PMWaV-1 NC_010178, PMWaV-2 AF283103, PMWaV-3 and viral helicase (HEL) domain typical of pfam 01443 123 416 Virus Genes (2009) 38:414–420 Fig. 1 Genome organization A and phylogenetic analysis of Pineapple mealybug wilt 0 5 10 15 kb associated virus-3. a RdRp p61 p24 Approximate size and location p6 CP of clones generated to sequence MTR HEL HSP70h PMWaV-3 Pineapple mealybug wilt ? associated virus-3 (PMWaV-3), RdRp p24 b Genomic organization and p6 p61 PRO MTR HEL HSP70h CP approximate size of PMWaV-3, PMWaV-1 PMWaV-1, and PMWaV-2. Shared color indicates similar protein products. ORF1a: MTR, viral methyltransferase region; PRO MTR HEL RdRp p5 CPd p20p22 HEL, viral helicase region; ? HSP70h p46 CP p6 PMWaV-2 ORF1b: RdRp, RNA dependent B RNA polymerase; ORF2, small hydrophobic protein; ORF3 Methyltransferase domain Helicase domain Hsp70h, heat shock protein 70 BYV homolog; ORF4: p61 or p46 PMWaV-3 PMWaV-3 proteins; ORF5: CP, coat 100 MV-1 PMWaV-1 PMWaV-1 protein; ORF6, p24 or CPd, coat GLRaV-2 100 100 PMWaV-5* protein duplicate; ORF7, p20; 98 PBNSPaV 94 ORF8, p22;ORF9, p6; 90 89 100 100 PMWaV-2 CTV GLRaV-9 Phylogenetic analyses of the c 100 100 GLRaV-1 PBNSPaV 78 methyltransferase, d helicase, e 85 RMoV 100 GLRaV-3 100 ORF4, and f Closter_coat region 100 GLRaV-3 LIYV 58 LChV-1 of nonredundant sequences 100 LChV-2 MVBV SCFaV 100 98 CYSDV from members of the family LChV-1 PMWaV-2 66 LIYV 94 100 52 BYDV Closteroviridae.
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