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Domains in Viroids Proc. Natl. Acad. Sci. USA Vol. 82, pp. 4582-4586, July 1985 Biochemistry Domains in viroids: Evidence of intermolecular RNA rearrangements and their contribution to viroid evolution (coconut cadang cadang viroid partial duplication/RNA viruses/defective Interfering RNAs/discontinuous transcription) PAUL KEESE AND ROBERT H. SYMONS* Adelaide University Centre for Gene Technology, Department of Biochemistry, University of Adelaide, Adelaide, South Australia 5000 Communicated by Paul Berg, March 7, 1985 ABSTRACT On the basis of sequence homology a model is Table 1. Viroids and their isolates whose nucleotide sequences proposed for five structural and functional domains in viroids. have been determined These domains include (i) a conserved central region capable No. of of forming two alternative structures that may regulate two Viroid residues Refs. phases of the viroid replication cycle, (ii) a region associated with pathogenicity, (iii) a domain with high sequence vari- Avocado sunblotch 247 11 ability, (iv and v) two terminal domains that are interchange- viroid (ASBV) able between viroids. That the evolution ofviroids has involved Chrysanthemum stunt 356, 354 12, 13 RNA rearrangements of domains is supported by the partial viroid (CSV) duplication of coconut cadang cadang viroid, which arises de Citrus exocortis viroid 370, 371, 13-15, 48 novo during each infection. Similar RNA rearrangements have (CEV) 372, 374, 375 been established for animal viral defective interfering RNAs, Coconut cadang cadang 246, 247 16 which arise by some form of discontinuous transcription. This viroid (CCCV)* mechanism could account for the origin of viroids and also Hop stunt viroid (HSV) 297, 303 17, 18 RNA viruses, whereby modules of genetic information may (cucumber pale fruit have undergone repeated exchange between RNA pathogens viroid) and the RNA of their hosts. Potato spindle tuber 359 10, 19, 20 viroid (PSTV) Viroids, the smallest known class of autonomously replicat- Tomato apical stunt 360 21 ing pathogens, are structurally among the best characterized viroid (TASV) RNA molecules (1, 2). Functionally, however, these single- Tomato planto macho 360 21 stranded, circular RNA molecules of 246 to 375 residues viroid (TPMV) remain an enigma. They apparently rely entirely on host We define a viroid isolate as one whose components share greater factors for their replication, which proceeds via greater than than 90%6 sequence homology with a previously published viroid unit length plus and minus RNA intermediates (3-8), since sequence. Cucumber pale fruit viroid, therefore, is an isolate ofHSV there is no evidence of any mRNA activity (9, 10). Conse- since it shares 95% sequence homology with HSV (18). all *CCCV infections produce four major RNA components, all derived quently, required enzymic functions, including the ability from an infectious monomeric small form (D-0) of 246 or 247 to amplify an RNA template, must potentially exist in the residues. These include monomers and dimers ofboth the D-0 form uninfected hosts. At present, these include only the higher and any one of a set of larger forms (D-41, D-50, or D-55) which plants, where viroids cause several economically important contains a duplication involving 41, 50, or 55 residues. diseases (9, 10). Eight viroid species and more than thirty variants have been sequenced so far (Table 1). Sequence and structural involved intermolecular rearrangements ofviroid sequences. similarities that have been previously reported include a This model can accommodate all viroids except ASBV, rod-like secondary structure with characteristic thermo- because it lacks significant sequence homology with other dynamic properties (1, 2), a conserved central region (9, 10, viroids. Subsequently in this paper the phrase "all viroids" 12-14, 16), and an oligopurine tract about 25-50 residues 5' omits ASBV. of this homologous region (10, 12, 21). Only two specific Domains ofViroids: The Model. The five structural domains regions have been associated with function. One is a region are depicted schematically in Fig. 1 and more specifically responsible for variation in pathogenicity of PSTV isolates located in Fig. 2. They are summarized together with their (19, 20, 22, 23). The second involves the in vitro, nonenzymic hypothesized functions as follows: processing of an ASBV dimeric transcript between residues C domain. This conserved central core is centered at the 55 and 56 (unpublished data). strictly conserved bulged helix To understand further how these small RNA molecules are CC CCGG able to manipulate host functions by using only sequence and structural signals, we have developed a model of viroid GGUGGCC domains in which function is correlated with five structurally It may represent an important control region in viroid distinguishable regions (Fig. 1). This model not only provides replication and signal functional changes through structural a more rational basis for mutagenic studies of infectious alterations. viroid cDNA recombinant clones (refs. 24-26; unpublished P domain. This region is associated with pathogenicity (19, data) but also indicates that the evolution of viroids has Abbreviations: See Table 1 for abbreviations of viroids; SCMoV, The publication costs of this article were defrayed in part by page charge subterranean clover mottle virus; DI RNA, defective interfering payment. This article must therefore be hereby marked "advertisement" RNA. in accordance with 18 U.S.C. §1734 solely to indicate this fact. *To whom reprint requests should be addressed. 4582 Downloaded by guest on September 25, 2021 Biochemistry: Keese and Symons Proc. Natl. Acad. Sci. USA 82 (1985) 4583 Tl p c V T2 pathogenicity. More interestingly, it may be involved in RNA rearrangements such as that found for the partial duplication in CCCV (16). T domains. The terminal regions are considered to have I tI iJ undergone intermolecular RNA exchange between viroids. Although the functional role ofthese domains is unclear, the evidence for these exchanges suggests a role for RNA Left hand Pathogenic Conserved Vatriable Right hand rearrangements in the origin and evolution of viroids. terminal region central rejgion terminal Control Function of the Conserved Central Domain C. In domain core domain addition to the conserved bulged helix (Fig. 1), an alternative FIG. 1. Model of five viroid domains (TI, P, C, V, and T2) structure is possible (Fig. 3). This stem-loop (1, 2) is deduced determined from sequence homologies between vixroids. The arrows from temperature-jump experiments to monitor the thermal depict an inverted repeat, which can potentially formnanine-base-pair denaturation ofPSTV, CEV, CSV, and CCCV (1, 2). By such stem (Fig. 3). a and b are segments of the TI do] that flank a region of RNA exchange (dashed box). R and Ymain a scheme, the highly conserved CCCCGGGG sequence oligopurine oligopyrimidine helix. would form part of the loop atop a nine-base-pair stem (Fig. 3), preventing the conserved bulged helix from forming. 20, 22, 23) and is characterized by an (A)54 se:quence present Despite many sequence differences, the same nine-base-pair in all viroids. stem can be formed for all viroids, except for a single V domain. This region shows the greattest variability non-base-paired C residue in HSV. between closely related viroids and may be aassociated with It is proposed that both mutually exclusive structures are Ti p c v T2 ,a ~~~~~~~~~~~~b4 ~~120 ~ 1 49 ~~~~~~~~~~~~~~ALAA:GACUAGAC AC 12A AC AGGAU CCAGCGG CCG G A C6G6 CAUGACA UGGC RA GGGGA CC AC.AGAGU AGGAUU IGCAACUAAAC CAsSAUUCGACUC ACICABACCUCCUGAAGLAAAAGA AAGAAGC6G ....... ........... .... ..... UU ... ......... .. ..... UCCCBCtCAAA ......... C........... I. ......... ... w..... ... ....... GGCCCA ....... LUCC ...... GCUCCAUC ....... .. COtUG;X UUGA tCGCAAG;lCCtCGAUVUG*GGA CtGGtUifUUCAUUAu C;;CUAUGACAAiAL CUCC AALUCA AAAGA CGGCUUCGCU GUCGCA CCCGCUCCCCACCAGGACGBCCC u GGCUUUUAC UACCCAC IC G0cLAAUCLCACLA 369 31 206 PSTV 241 212 46 T6 122 146 I""ttU Uttt~AAAAA/AG^tstU~~l;tUAUttCtss~t;G~s A \ /tAALG~tUtt tl CGAGA GGBAAC AUAUUC BAAUCC fG&UAL C~A CCGA :AG AL ABAGA ALAGALU GCGA' CAGGBAG.CGAUCABG ALCC CCGAGG CCUG6AGCGAACUGGCG AA GAGACCG6GCAGAGLGAGCAUCC CJ ACABBABA tAUCCCCCGCAGAAA C AAGGBU . .......... ...... ...... .A.. ... ..... ..... ..... ..... .. U ACCCAGGGAAAAGC CCCAABAI CCAAAGUIGA UCGGGCCAAUCA AuISCA UUUUU CACCGAC CCCUB ABACAA ALGGGCCCA ABACLAC6CU BUACACUALACAcAC CCACUCCCACAACAUBBCB CBC AGGACAtCALtUUL Au L GA6C CL / A uu c CCCL)t;CU 360 312 284 237 209 1 46 T6 122 161 / u CA / C IA GAUCG A ACUAUBA GU.AAACAGAABCUC' ACCA\CAGAC CCU LAG AGALLALALAALLGAG AGBCABGCGBBAGG GAAGACCAUCAG LLCC CCAGAG ALLCGCCAGAGGLAALGUAGB A AGG AGAACGCLACACAGLCGCC CBC UUGCCS6CAC A AA C GA C C t ................................. ... ..._. ...... .. cssccAAcucuAlc^ucssCCA.AUGAGBC.LC LCAACU. ^CAAACCC CCCC CUC'UUC GLBCA'A LAUACCUCA AGCUCACLCA GCU UJ jCCCAAAAAAuAl CIazC~~ iAZuii /iii~ABAOC;~c~;,~A CCA '6,CA AAA'GG 'GCC UCLAU AGUCCUGA AClCC/GC LCCCCL~CCCC6GAUGUCUCACLCCACAAAACCLC LGAGCACACUc C~~CACUCCCUACCACAB C 371 326 203 CEV-A 244 214 _____ 46 77 123 160 UC AA CGGAUtUUtAGACCA LGACCU 6CAC UrCC ..... .... .. ..... LCCCt ..AALL .. AU ..... .... ......e. , .. ... .. ... ... .. ..... ..... ..... J ... ..... ........ ..... I....... -U -@@ --*@ CCCUG UAAG C $JiU CBL;AAGIPGA CUBA cc ACAUAAAAAUG CAAA CUCAUUACACCCAU*AAAGUAA AAGLGUBCCCA AUG UCUCUCCUUAGAGGC CCCAUCCUGLUUlUGGAAGG CC GCAtGCCUAUut; CCUtA C 360 316 284 TASV 235 211 44 73 119 156 AL ALA ABG CCCLACBC ' GBA UCCLLLA G AA AG A ICUAGAC U UACUUAGuACCAUGCACICUCCCUCAGCU
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