Chapter 13 : Genome Diversity and Evolution of Rotaviruses

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Rotaviruses (RVs) are a major cause of acute gastroenteritis (AGE) in infants and young children worldwide, and in the young of a large variety of animals (mammals and birds). This chapter describes the basic facts of genome diversity of RVs and discusses several mechanisms driving their evolution. An attempt is made to judge how the diversity of cocirculating wild-type (wt) RVs may be influenced by the ongoing vaccination programs. RVs are subdivided into different groups based on differences in antigenic properties of VP6, of which groups A through E are well distinguished. For the evolution of human RVs, the following genetic mechanisms have been found to be operative: accumulation of point mutations, genome reassortment, genome rearrangements (recombination), zoonotic transmission, and combinations of the above factors. Genome rearrangements have been found in combination with point mutations, and reassortment is frequently combined with zoonotic transmission. The conditions of genome diversity of RVs are very reminiscent of those of influenza viruses. Whole-genome sequencing, resulting in the assignment of genotypes to all 11 individual RV RNA segments, has allowed further insights into RV evolution. Since 2006, two RV vaccines have been licensed in various countries, and millions of doses have been distributed in universal mass vaccination (UMV) programs.

Citation: Matthijnssens J, Desselberger U. 2012. Genome Diversity and Evolution of Rotaviruses, p 214-241. In Hacker J, Dobrindt U, Kurth R (ed), Genome Plasticity and Infectious Diseases. ASM Press, Washington, DC. doi: 10.1128/9781555817213.ch13
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Image of FIGURE 1

Structural organization of RVs. (a) RNA gel showing RV RNA segments and encoded products. (b) Surface representation of the RV structure: besides the VP4 spikes (red) and the VP7 outer layer (yellow), three types of channels are indicated (I, II, and III). (c) Cutaway diagram of the RV structure showing the middle VP6 (blue) and internal VP2 (green) layers. The flower-shaped VP1-VP3 complex on the inside of VP2 is shown in red. (d) Structural organization of the VP2 layer. Some of the 60 dimers forming this layer are shown in red and purple. (e) Genomic RNA in the RV structure. The VP6 and VP2 layers are half cut away to show the genomic organization. (f) Structure of the actively transcribing DLPs, with exit pathway for the single-stranded positive-sense RNAs through the class I channels at the fivefold vertex. (g) Close-up cutaway view depicting the exit pathway in one of the channels. The transcripts are shown as gray strands in panels f and g. From with kind permission from B. V. V. Prasad, Baylor College of Medicine, Houston, TX.

Citation: Matthijnssens J, Desselberger U. 2012. Genome Diversity and Evolution of Rotaviruses, p 214-241. In Hacker J, Dobrindt U, Kurth R (ed), Genome Plasticity and Infectious Diseases. ASM Press, Washington, DC. doi: 10.1128/9781555817213.ch13
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Image of FIGURE 2

Point mutations in RV genes. Alignment of fragments of the VP4 gene (VP8⋆ portion) and the reverse complementary sequence of the original primer 1T-1 and the degenerate primer 1T-1D is shown. Divisions are as follows: I, sequences from strains which were not typed by RT-PCR with the primer 1T-1; II, sequences from strains typed as P[8] with the 1T-1 primer; III, sequences from strains typed as P[8] with the new degenerate primer 1T-1D; and IV, sequences of P[8] strains obtained from GenBank or EMBL. Strains in division I could also be successfully typed as P[8] by the degenerate primer 1T-1D. Strains from the same geographical region are marked with an asterisk. Residues that match primer 1T-1 are denoted by dots. Substitutions in the P[8] primer-binding site that are conserved in all sequences are boldface. The reverse complement sequences of primers 1T-1 and 1T-1D are shown with the changes in boldface. Adapted from with permission of the publisher.

Citation: Matthijnssens J, Desselberger U. 2012. Genome Diversity and Evolution of Rotaviruses, p 214-241. In Hacker J, Dobrindt U, Kurth R (ed), Genome Plasticity and Infectious Diseases. ASM Press, Washington, DC. doi: 10.1128/9781555817213.ch13
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Image of FIGURE 3

Gene reassortment of RVs. Phylogenetic analyses of the VP7 (A) and VP4 (B) gene segments of RV strains DRC88 (G8P[8]) and DRC86 (G8P[6]), isolated in the Democratic Republic of the Congo, are shown, indicating reassortment of the VP4 gene segment. RV strains DRC88 and DRC86 are indicated by arrows. Bootstrap values above 70 are shown.

Citation: Matthijnssens J, Desselberger U. 2012. Genome Diversity and Evolution of Rotaviruses, p 214-241. In Hacker J, Dobrindt U, Kurth R (ed), Genome Plasticity and Infectious Diseases. ASM Press, Washington, DC. doi: 10.1128/9781555817213.ch13
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Image of FIGURE 4

Intra-and intersegmental recombination. (A) Intrasegmental recombination (gene rearrangement). Diagram of the structures of normal and rearranged NSP4 gene of a human RV. Adapted from , with permission of the publisher. (B) Intersegmental recombination. Diagram of the structures of normal and recombined NSP2 and NSP5 genes of a human RV. Adapted from with permission of the publisher.

Citation: Matthijnssens J, Desselberger U. 2012. Genome Diversity and Evolution of Rotaviruses, p 214-241. In Hacker J, Dobrindt U, Kurth R (ed), Genome Plasticity and Infectious Diseases. ASM Press, Washington, DC. doi: 10.1128/9781555817213.ch13
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Image of FIGURE 5

NSP1 gene diversity. (A) Phylogenetic tree of the NSP1 nucleotide sequence (entire ORF) of mammalian group A RVs. Bootstrap values (500 replicates) above 70 are shown. Designation of species of origin: Bo, bovine; Hu, human; Rh, rhesus monkey; Eq, equine; Po, porcine; Ov, ovine; La, lapine; Si, simian; Fe, feline; Ca, canine; Mu, murine; Gu, guanaco; An, antelope; Bu, buffalo. Some clusters of nearly identical human RVs in the A1 genotype were replaced by triangles and designated DC followed by the year of isolation for the sake of clarity. The closing braces on the right side of the dendrograms depict the 15 A-genotypes. Genotype A4 is found in avian group A RV isolates and is not included as being too diverse. (B) Pairwise identity frequency diagram.

Citation: Matthijnssens J, Desselberger U. 2012. Genome Diversity and Evolution of Rotaviruses, p 214-241. In Hacker J, Dobrindt U, Kurth R (ed), Genome Plasticity and Infectious Diseases. ASM Press, Washington, DC. doi: 10.1128/9781555817213.ch13
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Image of FIGURE 6

G-P genotype combinations of group A RVs. A summary of the different G-P genotype combinations for the 25 G and 34 P genotypes (as of October 2010) is shown. Different color codes are used to differentiate the origin of RVs of a particular G-P combination. ★ indicates that only the partial VP4 gene sequence of the new G22 strains have been determined, and this sequence was considered to be distantly related to P[17] strains. ★★ indicates that the P genotype of the new G23 strain has not yet been determined. To the right of every row and under every column, the number of different combinations found is indicated.

Citation: Matthijnssens J, Desselberger U. 2012. Genome Diversity and Evolution of Rotaviruses, p 214-241. In Hacker J, Dobrindt U, Kurth R (ed), Genome Plasticity and Infectious Diseases. ASM Press, Washington, DC. doi: 10.1128/9781555817213.ch13
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Image of FIGURE 7

Application of whole-genome analysis to the structural and nonstructural protein-encoding genes for known human, bovine, porcine, and avian group A RV strains. Green and red indicate Wa-like and DS-1-gene segments, respectively. Yellow, blue, and purple represent the avian PO-13-like RV gene segments, some typical porcine VP4, VP7, and VP6 genotypes, and some typical bovine VP4 and VP7 genotypes, respectively. Updated from .

Citation: Matthijnssens J, Desselberger U. 2012. Genome Diversity and Evolution of Rotaviruses, p 214-241. In Hacker J, Dobrindt U, Kurth R (ed), Genome Plasticity and Infectious Diseases. ASM Press, Washington, DC. doi: 10.1128/9781555817213.ch13
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5′- and 3′-terminal nucleotide sequences of the RNAs of group A-D rotaviruses

Citation: Matthijnssens J, Desselberger U. 2012. Genome Diversity and Evolution of Rotaviruses, p 214-241. In Hacker J, Dobrindt U, Kurth R (ed), Genome Plasticity and Infectious Diseases. ASM Press, Washington, DC. doi: 10.1128/9781555817213.ch13
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Gene-protein assignments and protein functions of group A RVs

Citation: Matthijnssens J, Desselberger U. 2012. Genome Diversity and Evolution of Rotaviruses, p 214-241. In Hacker J, Dobrindt U, Kurth R (ed), Genome Plasticity and Infectious Diseases. ASM Press, Washington, DC. doi: 10.1128/9781555817213.ch13
Generic image for table

Nucleotide percentage similarity cutoff values defining genotypes of the 11 RV genome segments

Citation: Matthijnssens J, Desselberger U. 2012. Genome Diversity and Evolution of Rotaviruses, p 214-241. In Hacker J, Dobrindt U, Kurth R (ed), Genome Plasticity and Infectious Diseases. ASM Press, Washington, DC. doi: 10.1128/9781555817213.ch13

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