Reassortment and concerted evolution in banana bunchy top virus genomes

Abstract

The nanovirus Banana bunchy top virus (BBTV) has six standard components in its genome and occasionally contains components encoding additional Rep (replication initiation protein) genes. Phylogenetic network analysis of coding sequences of DNA 1 and 3 confirmed the two major groups of BBTV, a Pacific and an Asian group, but show evidence of web-like phylogenies for some genes. Phylogenetic analysis of 102 major common regions (CR-Ms) from all six components showed a possible concerted evolution within the Pacific group, which is likely due to recombination in this region. The CR-M of additional Rep genes is close to that of DNA 1 and 2. Comparison of tree topologies constructed with DNA 1 and DNA 3 coding sequences of 14 BBTV isolates showed distinct phylogenetic histories based on Kishino-Hasegawa and Shimodaira-Hasegawa tests. The results of principal component analysis of amino acid and codon usages indicate that DNA 1 and 3 have a codon bias different from that of all other genes of nanoviruses, including all currently known additional Rep genes of BBTV, which suggests a possible ancient genome reassortment event between distinctive nanoviruses.

FIG. 1.

Neighbor-Net trees based on 46 ORF nucleotide sequences of BBTV DNA 1 and three other nanoviruses. The Pacific group, and three Asian groups—Vietnam-N, Vietnam-S, and Asian s.s. groups—are marked accordingly. Bootstrap values over 50 are marked on the branches. The branches leading to FBNYV, MDV11, and SCSV8 sequences are shortened and marked by broken lines to save space. The inset is a phylogram based on neighbor-joining criteria, showing the relative branch length of sequences of BBTV and other nanoviruses. Accession numbers are preceded by abbreviations for the places of origin. Ina, Indonesia; Jap, Japan; Vie, Vietnam; Fij, Fiji; Haw, Hawaii; Phi, Philippines; Ton, Tonga.

FIG. 2.

Neighbor-Net trees based on 32 ORF nucleotide sequences of BBTV DNA 3 and three other nanoviruses. The Pacific group is marked on the figure, and the rest of the BBTV sequences are Asian group. Bootstrap values over 50 are marked on the branches. The branches leading to FBNYV, MDV11, and SCSV8 sequences are shortened and marked by broken lines to save space. The inset is a phylogram based on neighbor-joining criteria, showing the relative branch length of sequences of BBTV and other nanoviruses. Accession numbers are preceded by abbreviations for the places of origin. Ina, Indonesia; Jap, Japan; Vie, Vietnam; Fij, Fiji; Phi, Philippines; Bur, Burundi.

FIG. 3.

Phylogenies obtained by the BI method based on ORF nucleotide sequences of DNA 4 and DNA 5 BBTV isolates. (A) DNA 4 tree. (B) DNA 5 tree. Along the branches are the supports of posterior probabilities from BI, followed by bootstrap supports of neighbor-joining and most parsimonious methods; only values that are >50% are shown. Accession numbers are preceded by abbreviations for the places of origin. Haw, Hawaii.

FIG. 4.

(A) Unrooted phylogram of the neighbor-joining tree based on nucleotide sequences of the CR-Ms from 102 BBTV isolates under an HKY85 model. Bootstrap values for internal support of the branches are given along the branches. Two major clades are marked: the Asian and Pacific groups. The component names are given before the sequence names (i.e., DNA 1 to DNA 6 are named D1 to D6, respectively). CR-M sequences of additional Reps have full names (i.e., BBTV S1, S3, W3, and W4) before the accession numbers. (B and C) Hypothetical trees showing two scenarios of CR-M evolution: a phylogeny showing a single origin of CR-M regions, in which each component forms monophyletic groups (B) and a phylogeny showing two origins of CR-M, grouped in two major clades, accordingly (C). See text for more explanation. Accession numbers are preceded by abbreviations for the places of origin. Ina, Indonesia; Jap, Japan; Vie, Vietnam; Fij, Fiji; Haw, Hawaii; Phi, Philippines; Ton, Tonga; Bur, Burundi.

FIG. 5.

Alignment of 102 CR-Ms of BBTV and other nanoviruses. The putative concerted evolution region in the Pacific group is marked by a square. The tandem repeated sequence proposed by Burns et al. (6) is underlined. Accession numbers are preceded by abbreviations for the places of origin. Ina, Indonesia; Jap, Japan; Vie, Vietnam; Fij, Fiji; Haw, Hawaii; Phi, Philippines; Ton, Tonga; Bur, Burundi.

FIG. 6.

Phylogenies obtained by BI based on ORF nucleotide sequences of DNA 1 and DNA 3 of 14 BBTV and three other nanovirus isolates. (A) DNA 1 tree. (B) DNA 3 tree. Posterior probabilities for each branch are marked. Ina, Indonesia; Jap, Japan; Vie, Vietnam; Phi, Philippines.

FIG. 7.

Result of combined analysis of PCA on amino acid and codon usage values of 132 nanovirus genes. (A) PCA map of the two first factors realized by amino acid usage of gene products. (B) PCA map plotted by the two first factors realized by RSCU of all genes. Different components of BBTV are marked in different colors.