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. 2008 Apr;82(7):3204-19.
doi: 10.1128/JVI.02257-07. Epub 2008 Jan 23.

Full genome-based classification of rotaviruses reveals a common origin between human Wa-Like and porcine rotavirus strains and human DS-1-like and bovine rotavirus strains

Affiliations

Full genome-based classification of rotaviruses reveals a common origin between human Wa-Like and porcine rotavirus strains and human DS-1-like and bovine rotavirus strains

Jelle Matthijnssens et al. J Virol. 2008 Apr.

Abstract

Group A rotavirus classification is currently based on the molecular properties of the two outer layer proteins, VP7 and VP4, and the middle layer protein, VP6. As reassortment of all the 11 rotavirus gene segments plays a key role in generating rotavirus diversity in nature, a classification system that is based on all the rotavirus gene segments is desirable for determining which genes influence rotavirus host range restriction, replication, and virulence, as well as for studying rotavirus epidemiology and evolution. Toward establishing such a classification system, gene sequences encoding VP1 to VP3, VP6, and NSP1 to NSP5 were determined for human and animal rotavirus strains belonging to different G and P genotypes in addition to those available in databases, and they were used to define phylogenetic relationships among all rotavirus genes. Based on these phylogenetic analyses, appropriate identity cutoff values were determined for each gene. For the VP4 gene, a nucleotide identity cutoff value of 80% completely correlated with the 27 established P genotypes. For the VP7 gene, a nucleotide identity cutoff value of 80% largely coincided with the established G genotypes but identified four additional distinct genotypes comprised of murine or avian rotavirus strains. Phylogenetic analyses of the VP1 to VP3, VP6, and NSP1 to NSP5 genes showed the existence of 4, 5, 6, 11, 14, 5, 7, 11, and 6 genotypes, respectively, based on nucleotide identity cutoff values of 83%, 84%, 81%, 85%, 79%, 85%, 85%, 85%, and 91%, respectively. In accordance with these data, a revised nomenclature of rotavirus strains is proposed. The novel classification system allows the identification of (i) distinct genotypes, which probably followed separate evolutionary paths; (ii) interspecies transmissions and a plethora of reassortment events; and (iii) certain gene constellations that revealed (a) a common origin between human Wa-like rotavirus strains and porcine rotavirus strains and (b) a common origin between human DS-1-like rotavirus strains and bovine rotaviruses. These close evolutionary links between human and animal rotaviruses emphasize the need for close simultaneous monitoring of rotaviruses in animals and humans.

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Figures

FIG. 1.
FIG. 1.
Phylogenetic dendrograms of VP4 at the nucleotide (nt) level (A) and the amino acid (aa) level (B) Bootstrap values (1,000 replicates) are shown. Certain clusters are replaced by triangles, in which the height of the triangle represents the number of sequences, and the width represents the genetic diversity inside that cluster. The dashed lines indicate the current division into P genotypes. Panels C and D show the respective identity frequency graphs. Panels E, F and G show details of the boxed regions of panel C, and panels H, I, and J show details of the boxed regions of panel D. In panels F and I, the identities between rotavirus strains belonging to the P[4] and P[8] genotypes are shown. In panels G and J, the identities between rotavirus strains belonging to the P[4] and P[8] genotypes are omitted to show that the 80% nucleotide and 89% amino acid cutoff values are the most suited cutoff values.
FIG. 2.
FIG. 2.
Phylogenetic dendrograms of VP7 at the nucleotide (nt) level (A) and the amino acid (aa) level (B). Bootstrap values (1,000 replicates) are shown. Certain clusters are replaced by triangles, in which the height of the triangle represents the number of sequences, and the width represents the genetic diversity inside that cluster. The dashed lines indicate the current division into G genotypes. Panels C and D show the respective identity frequency graphs. Panels E, F, G, and H show details of the boxed regions of panel C, and panels I, J, K, and L show details of the boxed regions of panel D. In panels F and J, identities between rotavirus strains belonging to the murine G3 strains and the remaining G3 strains (dark green), between rotavirus strains belonging to the G5 and G11 strains (red), and among rotavirus strains belonging to the G7 genotype (dark blue) are shown. In panels G and K identities among rotavirus strains belonging to the G3 genotype (light green) and between rotavirus strains belonging to the G3 and G14 genotypes (turquoise) are shown.
FIG. 3.
FIG. 3.
Phylogenetic dendrogram of VP6 at the nucleotide (nt) level (A). Bootstrap values (2,000 replicates) are shown. Designations of species of origin are as follows: Bo, bovine; Hu, human; Rh, rhesus; Eq, equine; Po, porcine; Ov, ovine; La, lapine; Si, simian; Mu, murine; Av, avian. The dashed line indicates the best option to divide the dendrogram into appropriate genotypes. The closing braces on the right side of the dendrograms depict the genotypes as they are proposed in this study. Panel B shows the identity frequency graph. Panels C, D, and E show details of the boxed region of panel B. In panel D, the identities among rotavirus strains belonging to the I2 genotype are shown. VP6 nucleotide accession numbers collected from GenBank are as follows for the indicated strains: BRV033, AF317126; B223, AF317128; WC3, AF411322; NCDV, AF317127; RRV, EF583009; OH4, D82975; PA169, EF554130; RF, K02254; Po, DQ119822; 111/05-27, EF554141; UKtc, X53667; R-22, D82977; OVR762, EF554152; B10925-97, EF554119; HP113, DQ003294; HP140, DQ003295; I321, X94618; 22R, AB040055; US6259, EF426123; US8720, EF426124; US8922, EF426132; US8635, EF426133; N26-02, DQ146686; US1205, AF079357; DRC86, DQ005121; DRC88, DQ005110; IS2, X94617; B1711, EF554086; US5139, EF426130; US8908, EF426140; TK126, AY456528; RV176-00, DQ490555; RV161-00, DQ490549; NR1, AF309652; TK119, AY456527; MG6, EF554097; AY456527; B4106, AY740737; 30/96, DQ205226; SA11-tsG, L15384; SA11-H96, DQ838650; SA11-30/19, DQ838648; SA11-5N, DQ838646; SA11-30/1A, DQ838649; SA11, AY187029; SA11-5S, DQ838647; 1076, D00325; Hun5, EF554108; FI-23, D82971; H-2, D00324; L26, DQ146695; TB-Chen, AY787645; S2, Y00437; Lp14, L11595; TUCH, AY594670; CMH222, ABC41660; T152, DQ146702; CMH134/04, DQ923800; CMH120/04, DQ923796; EO, AY947543; EMcN, AY267007; EDIM, U65988; EW, U36474; RMC321, AF531913; RMC/G60, AAT99008; RMC/G7, AY601551; RU172, DQ204741; 4F, L29184; 4S, L29186; CMP034, DQ534018; CRW-8, U82971; CN86, U10031; A411, AF317125; YM, X69487; A253, AF317122; A131, AF317124; H-1, AF242394; OSU, AF317123; HO-5, D82973; R-13, D82976; FI-14, D00323; HI-23, D82972; R-3, D82978; L338, D82974; Gottfried, D00326; CJN, AF461757; US6253, EF426131; KU, AB022768; 116E, U85998; Hu, X57943; Wa, K02086; E210, U36240; 97B53, AF260931; RMC61, AY601549; B4633-03, DQ146642; RV3, U04741; US9810, EF426127; US0408, EF426119; Dhaka12-03, DQ146664; Matlab13-03, DQ146675; Dhaka16-03, DQ492673; Dhaka25-02, DQ146653; RMC437, AY601554; US0468, EF426120; RMC/G66, AY601553; RMC100, AF531912; RMC83, AY601550; US8673, EF426135; US6097, EF426134; US9828, EF426139; US6153, EF426121; US8616, EF426138; US9951, EF426129; US9825, EF426128; US9875, EF426137; US9874, EF426136; US8960, EF426125; US8979, EF426126; US6161, EF426122; Ch-1, D82970; Ch-1, X98870; 02V0002G3, DQ096805; PO-13, D16329; 993-83, L13765; RK3, BAA22523; Ty-1, D82980; Ty-3, D82981; Ty-3, X98872.
FIG. 4.
FIG. 4.
Phylogenetic dendrogram of NSP4 at the nucleotide (nt) level (A). Bootstrap values (2,000 replicates) above 50 are shown. Designations of species of origin are as follows: Bo, bovine; Hu, human; Po, porcine; Ca, canine; Av, avian. The dashed line indicates the best option to divide the dendrogram into appropriate genotypes. Certain clusters are replaced by triangles, in which the height of the triangle represents the number of sequences, and the width represents the genetic diversity inside that cluster. The full NSP4 phylogenetic dendrogram is provided in Data S6 in the supplemental material as well as the accession numbers used to construct the dendrogram. The closing braces on the right side of the dendrograms depict the 11 E genotypes as they are proposed in this study (C). Panel B depicts the genotypes as they were previously used. Panel D shows the identity frequency graph. Panels E, F, and G show details of the boxed region of panel D. In panel F, the identities among rotavirus strains belonging to the E3, E1, and E2 genotypes are shown. In panel G, the above-mentioned bars are omitted.

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