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Bioinformatic evidence for a stem-loop structure 5'-adjacent to the IGR-IRES and for an overlapping gene… Firth, Andrew E; Wang, Qing S; Jan, Eric; Atkins, John F Nov 6, 2009

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ralssBioMed CentVirology JournalOpen AcceShort reportBioinformatic evidence for a stem-loop structure 5'-adjacent to the IGR-IRES and for an overlapping gene in the bee paralysis dicistrovirusesAndrew E Firth*1, Qing S Wang2, Eric Jan2 and John F Atkins*1,3Address: 1BioSciences Institute, University College Cork, Cork, Ireland, 2Department of Biochemistry and Molecular Biology, University of British Columbia, 2350 Health Sciences Mall, Vancouver, BC, Canada and 3Department of Human Genetics, University of Utah, Salt Lake City, UT 84112-5330, USAEmail: Andrew E Firth* -; Qing S Wang -; Eric Jan -; John F Atkins* -* Corresponding authors    AbstractThe family Dicistroviridae (order Picornavirales) includes species that infect insects and otherarthropods. These viruses have a linear positive-sense ssRNA genome of ~8-10 kb, which containstwo long ORFs. The 5' ORF encodes the nonstructural polyprotein while the 3' ORF encodes thestructural polyprotein. The dicistroviruses are noteworthy for the intergenic Internal RibosomeEntry Site (IGR-IRES) that mediates efficient translation initation on the 3' ORF without therequirement for initiator Met-tRNA. Acute bee paralysis virus, Israel acute paralysis virus of beesand Kashmir bee virus form a distinct subgroup within the Dicistroviridae family. In this brief report,we describe the bioinformatic discovery of a new, apparently coding, ORF in these viruses. TheORF overlaps the 5' end of the structural polyprotein coding sequence in the +1 reading frame.We also identify a potential 14-18 bp RNA stem-loop structure 5'-adjacent to the IGR-IRES. Wediscuss potential translation initiation mechanisms for the novel ORF in the context of the IGR-IRES and 5'-adjacent stem-loop.FindingsThe family Dicistroviridae includes a number of insect- andarthropod-infecting species such as Cricket paralysis virus,Black queen cell virus, Plautia stali intestine virus andTaura syndrome virus. The species Acute bee paralysisvirus (ABPV), Israel acute paralysis virus of bees (IAPV)and Kashmir bee virus (KBV) - which have been associatedwith Colony Collapse Disorder of honeybees - form atight subclade within the family (Figure 1; [1-5]). Thedicistroviruses have a linear positive-sense ssRNA genome(hereafter CDS2) encodes the structural polyprotein. Theintergenic region (IGR) contains an internal ribosomeentry site (IRES), comprising a complex and compact tri-ple-pseudoknotted RNA structure that binds ribosomesand mediates efficient translation initation on CDS2. TheIGR-IRES essentially mimics the E- and P-site tRNAs(including the P-site codon:anticodon duplex), allowingA-site initiation at a non-AUG codon, without anyrequirement for initiator Met-tRNA (Met-tRNAi) or any ofthe usual initiation factors (see Refs. [6-12] for recentPublished: 6 November 2009Virology Journal 2009, 6:193 doi:10.1186/1743-422X-6-193Received: 23 September 2009Accepted: 6 November 2009This article is available from:© 2009 Firth et al; licensee BioMed Central Ltd. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (, which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.Page 1 of 8(page number not for citation purposes)containing two long ORFs. The 5' ORF (hereafter CDS1)encodes the nonstructural polyprotein while the 3' ORFreviews).Virology Journal 2009, 6:193 genes are common in RNA viruses wherethey serve as a mechanism to optimize the coding poten-tial of compact genomes. However, annotation of over-lapping genes can be difficult using conventional gene-finding software [13]. Recently we have been using anumber of complementary approaches to systematicallyidentify new overlapping genes in virus genomes [13-17].When we applied these methods to the dicistroviruses, wefound strong evidence for a new coding sequence - hereaf-ter ORFX - in the bee paralysis viruses (i.e. ABPV, IAPV andKBV), overlapping the 5'-terminal region of CDS2 in the+1 reading frame (Figure 2). Here we describe the bioin-formatic analyses.Dicistrovirus sequences were extracted from GenBank, thepolyprotein coding sequences were extracted, translated,aligned with CLUSTALW [18], back-translated to nucle-otide sequence alignments, and clustered into separatealignments for each GenBank dicistrovirus RefSeq (using65% nucleotide identity to the RefSeq as a cut-off thresh-old). Beginning with pairwise sequence comparisons,conservation at synonymous sites (only) was evaluated bycomparing the observed number of base substitutionsymous site codons are 1-, 2-, 3-, 4- or 6-fold degenerateand the differing probabilities of transitions and transver-sions (see [17] for details). Statistics were then summedover a phylogenetic tree as described in [14], and averagedover a sliding window.When this procedure was applied to the bee paralysisviruses (see Figure 3 caption for GenBank accession num-bers), a striking and extended peak in synonymous siteconservation (p ~ 10-14 for the total conservation withinORFX) was apparent at the 5' end of CDS2 (Figure 2B,panels 5-7). Such conservation peaks are indicative ofoverlapping functional elements, though such elementsmay be either coding or non-coding. However, in thiscase, coinciding with the conserved region there was anunusually extended and conserved absence of stop codonsin the +1 reading frame (Figure 2B; panel 3), thus suggest-ing an overlapping coding sequence in the +1 frame as apossible explanation for the enhanced conservation.Inspection of an additional 74 sequences with only partialcoverage of CDS2, but nearly complete coverage of theORFX region, again revealed the complete absence of +1frame stop codons in this region. If this region does notPhylogenetic tree for representative dicistrovirusesFigure 1Phylogenetic tree for representative dicistroviruses. A simple neighbour-joining phylogenetic tree, for representative dicistroviruses based on the CDS2 (structural polyprotein) amino acid sequences. The tree was produced with CLUSTALX [18]. Columns with alignment gaps were excluded. Numbers indicate bootstrap support (out of 1000), while the scale bar rep-resents the number of substitutions per site.0.05 substitutions per siteSolenopsis invicta virus 1Israel acute paralysis virus of beesKashmir bee virusAcute bee paralysis virusTaura syndrome virusHomalodisca coagulata virus 1Black queen cell virusTriatoma virusHimetobi P virusPlautia stali intestine virusAphid lethal paralysis virusRhopalosiphum padi virusCricket paralysis virusDrosophila C virus1000100010001000736958100061410001000973Page 2 of 8(page number not for citation purposes)with the number expected under a neutral evolutionmodel. The procedure takes into account whether synon-harbour an overlapping coding sequence, then the unusu-ally high synonymous site conservation in this regionVirology Journal 2009, 6:193 2 (see legend on next page)(A)CDS1 CDS2(non−structural polyprotein) (structural polyprotein)5′ 3′ORFX6630 9296609(B)CDS2 (0 frame)ORFX (+1 frame)(1)positions of stopcodons (       ) andalignment gaps (  ) (2) Frame= +0(3) Frame= +1(4) Frame= +2synonymous site conservation25−codonsliding window15−codonsliding window0.41.01.6(5) Σwindow obsΣwindow exp102104106108(6)1p−value102104106108(7)1p−valueMLOGD log likelihood ratios30 codonsliding window7 codonwindow−300+30(8) Frame= +0−300+30(9) Frame= +1−300+30(10) Frame= +20 500 1000 1500 2000 250000.25(11)ORFXonlyCDS2 alignment nucleotide indexPage 3 of 8(page number not for citation purposes)Virology Journal 2009, 6:193 certainly reflects some other functional element -perhaps playing some role in normal IGR-IRES initiationin the bee paralysis viruses. One possibility is simple selec-tion against certain nucleotides in order to avoid forma-tion of alternative RNA structures that disrupt the IGR-IRES [19]. However, the extent and degree of conservationappears unusually high (e.g. as compared with other dicis-troviruses) if this is indeed the only explanation.Next, the bee paralysis virus CDS2 alignment was ana-lysed with MLOGD - a gene-finding program which wasdesigned specifically for identifying overlapping codingsequences, and which includes explicit models forsequence evolution in multiply-coding regions [13,14](Figure 2B, panels 8-11). Due to the overall high conser-vation, the absolute MLOGD scores tend to be low withinthe ORFX region (since there are fewer substitutions withwhich to discrimate the null or non-coding model fromthe alternative or coding model). Nonetheless, MLOGDpredicts that ORFX is indeed a coding sequence, with con-secutive positively-scoring windows in the ORFX region(Figure 2B, panels 9 and 11).Given the location of ORFX and the unusual translationmechanism of CDS2, the translation of ORFX - if it isindeed expressed - is clearly of interest and may providenew insights into the mechanics of IGR-IRES mediatedinitiation. Possible ORFX translation mechanisms include(i) a portion of ribosomes initiate at more-or-less the nor-mal IGR-IRES mediated non-Met-tRNAi initiation site butin the +1 frame; (ii) a portion of ribosomes, or rather 40Sribosome subunits, binding to the IGR-IRES somehowstart scanning, and normal AUG-initiation takes place at aconserved tandem pair of +1 frame AUG codons ~35codons downstream (Figure 3A) or, in some sequences, atAUG codons further 5'; or (iii) normal IGR-IRES mediatedCDS2 initiation occurs but is followed by a programmedThe synonymous site conservation plot peaks around thetandem +1 frame AUG codons (Figure 2B, panel 7; Figure3A), falling off rapidly upstream and more slowly down-stream. However, it is unclear whether or not this favoursscanning and AUG initiation. There is still significant syn-onymous site conservation upstream of the AUG codons(Figure 3A). The peak in synonymous site conservationmay just represent the region of the putative protein thatis subject to the strongest amino acid constraints. TheMLOGD statistics, on the other hand, indicate that thepositive coding signature in the +1 frame extends right upto the 5' end of CDS2 (Figure 2B, panel 11), thus favour-ing the model in which a portion of ribosomes initiate ator near the usual IGR-IRES initiation site but in the +1reading frame.If ORFX initiation occurs at the normal IGR-IRES initia-tion site but in the +1 frame then translation of ORFXwould result in an 11.2 kDa, 93 amino acid product inKBV, and 92 and 94 amino acid products in ABPV andIAPV respectively. If, however, initiation takes place at thedownstream tandem AUG codons, then translation ofORFX would result in a 7.1 kDa, 60 amino acid product inall three species. Within the longer (i.e. 92-94 amino acid)potential ORFX product, there are 61 residues that arecompletely conserved between the KBV, ABPV and IAPVGenBank RefSeqs. In the region of the structural polypro-tein that is encoded by the portion of the CDS2 sequencethat ORFX overlaps, there are 66 completely conservedresidues. Thus the putative ORFX product is apparentlysubject to slightly weaker functional constraints than the'corresponding' portion of the structural polyprotein.The IGR-IRESes of the bee paralysis viruses differ from theIGR-IRESes of most other sequenced dicistroviruses inone notable aspect - namely they have an extra hairpinstructure within domain 3 (see Refs. [11,20] for details).Coding potential statistics for bee paralysis dicistrovirus CDS2 and the overlapping ORFXFigure 2 (see previou  page)Coding potential statistics for bee paralysis dicistrovirus CDS2 and the overlapping ORFX. (A) Genome map for KBV [GenBank:NC_004807]. (B2-B11) Coding potential statistics based on an alignment of 16 bee paralysis virus CDS2 sequences (see Figure 3 caption for accession numbers). (B2-B4) Positions of stop codons in each of the three forward read-ing frames. Note the conserved absence of stop codons in the +1 frame within ORFX. (B5-B7) Conservation at synonymous sites within CDS2 (see [17]). (B6-B7) depict the probability that the degree of conservation within a given window could be obtained under a null model of neutral evolution at synonymous sites, while (B5) depicts the ratio of the observed number of substitutions within a given window to the number expected under the null model. (B8-B10) MLOGD sliding-window plots (see [14]). In (B8) the null model, in each window, is that the sequence is non-coding, while the alternative model is that the sequence is coding in the +0/CDS2 frame. Positive scores favour the alternative model and, as expected, there is a strong cod-ing signature throughout CDS2 except where CDS2 is overlapped by ORFX. In (B9-B10) the null model is that only the CDS2 frame is coding, while the alternative model is that both the CDS2 frame and the window frame are coding. The ORFX region has consecutive positively scoring windows, albeit only just (see text; B9). (B11) MLOGD statistics restricted to ORFX. Here, for increased sensitivity, the null and alternative models were fitted specifically for the ORFX region.+1 frameshift into ORFX. We investigated the possibility that the presence of thePage 4 of 8(page number not for citation purposes)extra hairpin structure might be correlated with the pres-Virology Journal 2009, 6:193 3 (see legend on next page)    																																																																																																																																																																																																																																																																							    																																																																																																																														 	 !									"#$%%%%%%&&&&&&%%%%%%''''''((((((''''''														#$ 										 )!#%%%%&&&&&%%%%%'''''(((((''''Page 5 of 8(page number not for citation purposes)Virology Journal 2009, 6:193 of ORFX. Two other sequenced dicistroviruses havethe extra hairpin structure - (i) the ant-infecting Solenop-sis invicta virus 1 or SINV-1 ([GenBank:NC_006559];[21,22]), and (ii) the shrimp-infecting Taura syndromevirus or TSV ([GenBank:NC_003005]; [23]).SINV-1 clusters with the bee paralysis viruses in the phyl-ogenetic tree (Figure 1), and an analysis of its sequenceshows that it does indeed contain a potential ORFX. Infact ORFX in SINV-1 is substantially longer than in the beeparalysis viruses - 125 codons if initiated in the +1 frameat the IGR-IRES normal initiation site; 83 codons if initi-ated at the tandem AUG codons (which are present inSINV-1 and align with the tandem AUG codons in the beeparalysis viruses); or 121 codons if initiated at anunstream intervening AUG codon (Figure 3A). (An addi-tional SINV-1 sequence - [GenBank:FJ229495] - with par-tial coverage of the ORFX region contained an ORFX-frame premature termination codon [PTC] that truncatesORFX by 33 codons. However, apart from the potentialfor sequencing errors, PTCs in a small number of isolatesare not unusual for short overlapping genes, which tendto have non-essential 'secondary' functions, and we donot believe that this ORFX-defective partial sequence nec-essarily precludes the presence of a functional ORFX inSINV-1.)On the other hand, ORFX was not present in TSV. The first+1 frame AUG codon 3' of the IGR-IRES initiation site ispreceded by a CDS2-frame AUG codon, and is closely fol-lowed by a +1 frame stop codon, while non-AUG +1frame initiation at the usual IGR-IRES initiation sitewould only give a 16 amino acid product. Thus the pres-ence of ORFX does not seem to correlate with the presenceof the extra hairpin structure within domain 3 of the IGR-However, we did identify a novel (so far as we are aware)potential RNA hairpin structure immediately 5'-adjacentto, but not overlapping, the IGR-IRES in the bee paralysisviruses (Figure 3C). In the KBV and IAPV RefSeqs, thehairpin comprises 18 consecutive base pairs (with a 4 ntterminal loop containing the CDS1 termination codon)and is supported by many compensatory substitutions(i.e. paired substitutions that maintain the base pairings)between KBV and IAPV. Inspection of 77 additionalsequences with coverage of this region revealed six(mostly identical) sequences with single mismatches inthe stem, one sequence with two mismatches, and onesequence with a 4-nt deletion at the apical end of thestem. Nonetheless, the majority of sequences retained aperfect 18 bp hairpin, and a total of 14 different substitu-tions that preserved the base pairings were observed. Asimilar, though shorter (14 bp), hairpin stucture wasidentified in ABPV (Figure 3C). Again, inspection of tenadditional sequences revealed five different substitutionsin the stem, all of which preserved the predicted base pair-ings. Whether the hairpin is in any way relevant to trans-lation of the putative ORFX remains to be seen. However,preliminary experimental results indicate that presence ofthe predicted hairpin does have a strong effect on IGR-IRES activity (unpublished data, QS Wang and E Jan).Recent results suggest that under certain circumstances(namely the presence of an initiator tRNA species that rec-ognizes the P-site codon) the IGR-IRES can, at some level,mediate initiation at the P-site (presumably in competi-tion with A-site initiation) [24]. The codon:anticodonduplex mimicking part of the IGR-IRES (a.k.a. PKI) hasbeen shown to be dynamic and flexible [25-27], and Ref.[24] suggest that P-site initation takes place only upon dis-sociation of the duplex. However, this duplex is critical forNucleotide and amino acid sequence alignments and predicted RNA structuresFigure 3 (see previous page)Nucleotide and amino acid sequence alignments and predicted RNA structures. (A1) Nucleotide alignment of ORFX and flanking regions for the sequences [GenBank:NC_009025] (IAPV), [GenBank:NC_004807] KBV, and [Gen-Bank:NC_002548] (ABPV). Spaces separate +0/CDS2-frame codons. Colour coding is as follows: light blue - CDS2 IGR-IRES-mediated initiation site; red - ORFX termination codon; green - potential +1/ORFX-frame AUG initiation codons if ORFX is AUG-initiated (there are no intervening +0 or +2 frame AUG codons). Black arrows indicate the approximate expected initia-tion site if ORFX is IGR-IRES initiated (see text). Symbols '*' and 'x' represent completely conserved columns (based on a larger alignment comprising GenBank accession numbers NC_009025, EU436455, EU436456, EU436423, NC_004807, AY053375, AY053374, AY053372, AF486072, AY053367, AY053370, AY053366, AY053368, AF486073, AY053371 and NC_002548). (A2) The corresponding region in [GenBank:NC_006559] (SINV-1). (B) Amino acid alignment of the translated ORFX assuming initiation at the normal IGR-IRES initiation site but in the +1 reading frame. Methionine residues are high-lighted in green. (C) Representative sequences showing a potential RNA hairpin structure directly upstream of the predicted IGR-IRES in the bee paralysis dicistroviruses. The CDS1 termination codons are underlined and in bold. The 5' end of the IGR-IRESs (as summarized in Ref. [11]) are underlined. Predicted base pairings are indicated by paired parentheses and coloured background shading. Substitutions that maintain the predicted base pairings are highlighted in blue (for single substitutions involving G:U pairings) or pink (for compensatory paired substitutions).IRES. selection of the CDS2 reading frame [25] so, upon disso-Page 6 of 8(page number not for citation purposes)ciation of the duplex, there may be flexibility in the selec-Virology Journal 2009, 6:193 of reading frame, thus perhaps allowing +1 frame P-site initiation. In fact, all available bee paralysis virussequences have a CUG codon at this location, which isknown to be recognizable by native Met-tRNAi [28].Other dicistroviruses lack a long overlapping ORF at thisgenomic location and lack the corresponding extendedregion of synonymous site conservation (data notshown). At least some other dicistroviruses do exhibitsome degree of heightened synonymous site conservationat the very 5' end of CDS2, but the 3' extent of theseregions appears to be much more limited than in the beeparalysis viruses (perhaps it simply reflects selectionagainst certain nucleotides in order to avoid forming alter-native RNA secondary structures that may disrupt IGR-IRES activity [19]). In fact the sequence data is rather lim-ited for most dicistroviruses in the sense that it is difficultto make alignments with sufficiently large phylogeneti-cally-summed diversity but sufficiently small pairwisedivergences for the above analyses to produce useful sta-tistics. Thus, there may be features in the other dicistrovi-ruses that will remain hidden until more sequence databecomes available.Overlapping genes are difficult to identify and are oftenoverlooked. However, it is important to be aware of suchgenes as early as possible in order to avoid confusion (oth-erwise functions of the overlapping gene may be wronglyascribed to the gene they overlap), and also so that thefunctions of the overlapping gene may be investigated intheir own right. Although overlapping the structural poly-protein, there is no reason to suspect that ORFX encodesa structural protein - indeed the limited phylogenetic dis-tribution of ORFX suggests that it does not. We are cur-rently investigating the translation mechanism for theputative ORFX and how it relates to the IGR-IRES and thepotential upstream hairpin structure.Note: during the preparation of this manuscript, the pos-itive coding potential of ORFX was also predicted by Ref.[29] (who name the ORF 'pog'), albeit using different bio-informatic approaches.Competing interestsThe authors declare that they have no competing interests.Authors' contributionsAEF carried out the bioinformatic analysis and wrote themanuscript. All authors edited and approved the finalmanuscript.AcknowledgementsThis work was supported by National Institutes of Health Grant R01 References1. Govan VA, Leat N, Allsopp M, Davison S: Analysis of the completegenome sequence of acute bee paralysis virus shows that itbelongs to the novel group of insect-infecting RNA viruses.Virology 2000, 277:457-463.2. 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