The multicomponent single-stranded DNA plant nanoviruses encode unique master replication initiator (Rep) proteins. We have mapped the 5′ and 3′ termini of the corresponding polyadenylated mRNAs from faba bean necrotic yellows virus (FBNYV) and subterranean clover stunt virus and found that these are terminally redundant by up to about 160 nt. Moreover, the origin of viral DNA replication is transcribed into RNA that is capable of folding into extended secondary structures. Other nanovirus genome components, such as the FBNYV DNA encoding the protein Clink or an FBNYV DNA encoding a non-essential para-Rep protein, are not transcribed in such a unique fashion. Thus, terminally redundant mRNAs and the resulting transcription of the replication origin appear to be restricted to nanovirus master Rep DNAs. We speculate that this may be a way to regulate the expression of the essential master Rep protein.
AccottoG. P.,
DonsonJ.,
MullineauxP. M.1989; Mapping of Digitaria streak virus transcripts reveals different RNA species from the same transcription unit. EMBO J 8:1033–1039
AltschulS. F.,
EricksonB. W.1985; Significance of nucleotide sequence alignments: a method for random sequence permutation that preserves dinucleotide and codon usage. Mol Biol Evol 2:526–538
BrownT.,
MackeyK.,
DuT.2004; Analysis of RNA by Northern and slot blot hybridization. In Current Protocols in Molecular Biology pp. 4.9.1–4.9.19Edited byAusubelF. M.,
BrentR.,
KingstonR. E.,
MooreD. D.,
SeidmanJ. G.,
SmithJ. A.,
StruhlK.
New York: Wiley;
Campos-OlivasR.,
LouisJ. M.,
ClerotD.,
GronenbornB.,
GronenbornA. M.2002; The structure of a replication initiator unites diverse aspects of nucleic acid metabolism. Proc Natl Acad Sci U S A 99:10310–10315[CrossRef]
CaseyJ. L.,
KoellerD. M.,
RaminV. C.,
KlausnerR. D.,
HarfordJ. B.1989; Iron regulation of transferrin receptor mRNA levels requires iron-responsive elements and a rapid turnover determinant in the 3′ untranslated region of the mRNA. EMBO J 8:3693–3699
ChuP. W.,
KeeseP.,
QiuB. S.,
WaterhouseP. M.,
GerlachW. L.1993; Putative full-length clones of the genomic DNA segments of subterranean clover stunt virus and identification of the segment coding for the viral coat protein. Virus Res 27:161–171[CrossRef]
CloteP.,
FerreF.,
KranakisE.,
KrizancD.2005; Structural RNA has lower folding energy than random RNA of the same dinucleotide frequency. RNA 11:578–591[CrossRef]
DekkerE. L.,
WoolstonC. J.,
XueY. B.,
CoxB.,
MullineauxP. M.1991; Transcript mapping reveals different expression strategies for the bicistronic RNAs of the geminivirus wheat dwarf virus. Nucleic Acids Res 19:4075–4081[CrossRef]
DongH.,
DengY.,
ChenJ.,
WangS.,
PengS.,
DaiC.,
FangY.,
ShaoJ.,
LouY.,
LiD.2007; An exploration of 3′-end processing signals and their tissue distribution in Oryza sativa . Gene 389:107–113[CrossRef]
EagleP. A.,
OrozcoB. M.,
Hanley-BowdoinL.1994; A DNA sequence required for geminivirus replication also mediates transcriptional regulation. Plant Cell 6:1157–1170[CrossRef]
GilmartinG. M.,
FlemingE. S.,
OetjenJ.1992; Activation of HIV-1 pre-mRNA 3′ processing in vitro requires both an upstream element and TAR. EMBO J 11:4419–4428
GraveleyB. R.,
GilmartinG. M.1996; A common mechanism for the enhancement of mRNA 3′ processing by U3 sequences in two distantly related lentiviruses. J Virol 70:1612–1617
Herrera-ValenciaV. A.,
DugdaleB.,
HardingR. M.,
DaleJ. L.2007; Mapping the 5′ ends of banana bunchy top virus gene transcripts. Arch Virol 152:615–620[CrossRef]
HoekemaA.,
HirschP. R.,
HooykaasP. J. J.,
SchilperoortR. A.1983; A binary plant vector strategy based on separation of vir - and T-region of the Agrobacterium tumefaciens Ti-plasmid. Nature 303:179–180[CrossRef]
HullR.,
GeeringA.,
HarperG.,
LockhartB. E.,
SchoelzJ. E.2005; Family Caulimoviridae . In Virus Taxonomy: Eighth Report of the International Committee on Taxonomy of Viruses pp 385–396Edited byFauquetC. M.,
MayoM. A.,
ManiloffJ.,
DesselbergerU.,
BallL. A.
London: Elsevier/Academic Press;
KatulL.,
MaissE.,
MorozovS. Y.,
VettenH. J.1997; Analysis of six DNA components of the faba bean necrotic yellows virus genome and their structural affinity to related plant virus genomes. Virology 233:247–259[CrossRef]
KhromykhA. A.,
MekaH.,
GuyattK. J.,
WestawayE. G.2001; Essential role of cyclization sequences in flavivirus RNA replication. J Virol 75:6719–6728[CrossRef]
LaufsJ.,
JupinI.,
DavidC.,
SchumacherS.,
Heyraud-NitschkeF.,
GronenbornB.1995; Geminivirus replication: genetic and biochemical characterization of Rep protein function, a review. Biochimie 77:765–773[CrossRef]
LoebD. D.,
MackA. A.,
TianR.2002; A secondary structure that contains the 5′ and 3′ splice sites suppresses splicing of duck hepatitis B virus pregenomic RNA. J Virol 76:10195–10202[CrossRef]
LokeJ. C.,
StahlbergE. A.,
StrenskiD. G.,
HaasB. J.,
WoodP. C.,
LiQ. Q.2005; Compilation of mRNA polyadenylation signals in Arabidopsis revealed a new signal element and potential secondary structures. Plant Physiol 138:1457–1468[CrossRef]
MasonW. S.,
BurrellC. J.,
CaseyJ.,
GerlichW. H.,
HowardC. R.,
KannM.,
LanfordR.,
NewboldJ.,
SchaeferS.other authors2005; Family Hepadnaviridae . In Virus Taxonomy: Eighth Report of the International Committee on Taxonomy of Viruses pp 373–384Edited byFauquetC. M.,
MayoM. A.,
ManiloffJ.,
DesselbergerU.,
BallL. A.
London: Elsevier/Academic Press;
PfeifferP.,
HohnT.1983; Involvement of reverse transcription in the replication of cauliflower mosaic virus: a detailed model and test of some aspects. Cell 33:781–789[CrossRef]
RothnieH. M.,
ChapdelaineY.,
HohnT.1994; Pararetroviruses and retroviruses: a comparative review of viral structure and gene expression strategies. Adv Virus Res 44:1–67
SanfaconH.,
WieczorekA.1992; Analysis of cauliflower mosaic virus RNAs in Brassica species showing a range of susceptibility to infection. Virology 190:30–39[CrossRef]
SanoY.,
WadaM.,
HashimotoY.,
MatsumotoT.,
KojimaM.1998; Sequences of ten circular ssDNA components associated with the milk vetch dwarf virus genome. J Gen Virol 79:3111–3118
Shirasawa-SeoN.,
SanoY.,
NakamuraS.,
MurakamiT.,
SeoS.,
OhashiY.,
HashimotoY.,
MatsumotoT.2005; Characteristics of the promoters derived from the single-stranded DNA components of Milk vetch dwarf virus in transgenic tobacco. J Gen Virol 86:1851–1860[CrossRef]
TimchenkoT.,
de KouchkovskyF.,
KatulL.,
DavidC.,
VettenH. J.,
GronenbornB.1999; A single Rep protein initiates replication of multiple genome components of faba bean necrotic yellows virus, a single-stranded DNA virus of plants. J Virol 73:10173–10182
TimchenkoT.,
KatulL.,
SanoY.,
de KouchkovskyF.,
VettenH. J.,
GronenbornB.2000; The master Rep concept in nanovirus replication: identification of missing genome components and potential for natural genetic reassortment. Virology 274:189–195[CrossRef]
Vega-RochaS.,
ByeonI. J.,
GronenbornB.,
GronenbornA. M.,
Campos-OlivasR.2007a; Solution structure, divalent metal and DNA binding of the endonuclease domain from the replication initiation protein from porcine circovirus 2. J Mol Biol 367:473–487[CrossRef]
Vega-RochaS.,
GronenbornB.,
GronenbornA. M.,
Campos-OlivasR.2007b; Solution structure of the endonuclease domain from the master replication initiator protein of the nanovirus faba bean necrotic yellows virus and comparison with the corresponding geminivirus and circovirus structures. Biochemistry 46:6201–6212[CrossRef]
VettenH. J.,
ChuP. W. G.,
DaleJ. L.,
HardingR.,
HuJ.,
KatulL.,
KojimaM.,
RandlesJ. W.,
SanoY.,
ThomasJ. E.2005; Family Nanoviridae . In Virus Taxonomy: Eighth Report of the International Committee on Taxonomy of Viruses pp 343–352Edited byFauquetC. M.,
MayoM. A.,
ManiloffJ.,
DesselbergerU.,
BallL. A.
London: Elsevier/Academic Press;
WanitchakornR.,
HafnerG. J.,
HardingR. M.,
DaleJ. L.2000; Functional analysis of proteins encoded by banana bunchy top virus DNA-4 to -6. J Gen Virol 81:299–306
WuR.-Y.,
YouL.-R.,
SoongT.-S.1994; Nucleotide sequences of two circular single-stranded DNAs associated with banana bunchy top virus. Phytopathology 84:952–958[CrossRef]