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Distinct evolutionary histories of the DNA-A and DNA-B components of bipartite begomoviruses.

ABSTRACT: BACKGROUND: Viruses of the genus Begomovirus (family Geminiviridae) have genomes consisting of either one or two genomic components. The component of bipartite begomoviruses known as DNA-A is homologous to the genomes of all geminiviruses and encodes proteins required for replication, control of gene expression, overcoming host defenses, encapsidation and insect transmission. The second component, referred to as DNA-B, encodes two proteins with functions in intra- and intercellular movement in host plants. The origin of the DNA-B component remains unclear. The study described here was initiated to investigate the relationship between the DNA-A and DNA-B components of bipartite begomoviruses with a view to unraveling their evolutionary histories and providing information on the possible origin of the DNA-B component. RESULTS: Comparative phylogenetic and exhaustive pairwise sequence comparison of all DNA-A and DNA-B components of begomoviruses demonstrates that the two molecules have very distinct molecular evolutionary histories and likely are under very different evolutionary pressures. The analysis highlights that component exchange has played a far greater role in diversification of begomoviruses than previously suspected, although there are distinct differences in the apparent ability of different groups of viruses to utilize this "sexual" mechanism of genetic exchange. Additionally we explore the hypothesis that DNA-B originated as a satellite that was captured by the monopartite progenitor of all extant bipartite begomoviruses and subsequently evolved to become the integral (essential) genome component that we recognize today. The situation with present-day satellites associated with begomoviruses provides some clues to the processes and selection pressures that may have led to the "domestication" of a wild progenitor of the DNA-B component. CONCLUSIONS: The analysis has highlighted the greater genetic variation of DNA-B components, in comparison to the DNA-A components, and that component exchange is more widespread than previously demonstrated and confined to viruses from the Old World. Although the vast majority of New World and some Old World begomoviruses show near perfect co-evolution of the DNA-A and DNA-B components, this is not the case for the majority of Old World viruses. Genetic differences between Old and New World begomoviruses and the cultivation of exotic crops in the Old World are likely factors that have led to this dichotomy.

SUBMITTER: Briddon RW

PROVIDER: S-EPMC2858149 | biostudies-literature | 2010

REPOSITORIES: biostudies-literature

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Distinct evolutionary histories of the DNA-A and DNA-B components of bipartite begomoviruses.

Briddon Rob W RW Patil Basavaprabhu L BL Bagewadi Basavaraj B Nawaz-ul-Rehman Muhammad Shah MS Fauquet Claude M CM

BMC evolutionary biology 20100408

<h4>Background</h4>Viruses of the genus Begomovirus (family Geminiviridae) have genomes consisting of either one or two genomic components. The component of bipartite begomoviruses known as DNA-A is homologous to the genomes of all geminiviruses and encodes proteins required for replication, control of gene expression, overcoming host defenses, encapsidation and insect transmission. The second component, referred to as DNA-B, encodes two proteins with functions in intra- and intercellular moveme ...[more]

PMID: 20377896

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Project description:The complete sequences of the RhsB and RhsC elements of Escherichia coli K-12 have been determined. These sequence data reveal a new repeated sequence, called H-rpt (Hinc repeat), which is distinct from the Rhs core repetition that is found in all five Rhs elements. H-rpt is found in RhsB, RhsC, and RhsE. Characterization of H-rpt supports the view that the Rhs elements are composite structures assembled from components with very different evolutionary histories and that their incorporation into the E. coli genome is relatively recent. In each case, H-rpt is found downstream from the Rhs core and is separated from the core by a segment of DNA that is unique to the individual element. The H-rpt's of RhsB and RhsE are very similar, diverging by only 2.1%. They are 1,291 bp in length, and each contains an 1,134-bp open reading frame (ORF). RhsC has three tandem copies of H-rpt, all of which appear defective in that they are large deletions and/or have the reading frame interrupted. Features of H-rpt are analogous to features typical of insertion sequences; however, no associated transposition activity has been detected. A 291-bp fragment of H-rpt is found near min 5 of the E. coli K-12 map and is not associated with any Rhs core homology. The complete core sequences of RhsB and RhsC have been compared with that of RhsA. As anticipated, the three core sequences are closely related, all having identical lengths of 3,714 bp each. Like RhsA, the RhsB and RhsC cores constitute single ORFs that begin with the first core base. In each case, the core ORF extends beyond the core into the unique sequence. Of the three cores, RhsB and RhsA are the most similar, showing only 0.9% sequence divergence, while RhsB and RhsC are the least similar, diverging by 2.9%. All three cores conserve the 28 repetitions of a peptide motif noted originally for RhsA. A secondary structure is proposed for this motif, and the possibility of its having an extracellular binding function is discussed. RhsB contains one additional unique ORF, and RhsC contains two additional unique ORFs. One of these ORFs includes a signal peptide that is functional when fused to TnphoA.

Project description:The genus Begomovirus represents a group of multipartite viruses that significantly damage many agricultural crops, including papaya, and influence overall production. Papaya leaf curl disease (PaLCD) caused by the complex begomovirus species has several important implications and substantial losses in papaya production in many developing countries, including India. The increase in the number of begomovirus species poses a continuous threat to the overall production of papaya. Here, we attempted to map the genomic variation, mutation, evolution rate, and recombination to know the disease complexity and successful adaptation of PaLCD in India. For this, we retrieved 44 DNA-A and 26 betasatellite sequences from GenBank reported from India. An uneven distribution of evolutionary divergence has been observed using the maximum-likelihood algorithm across the branch length. Although there were phylogenetic differences, we found high rates of nucleotide substitution mutation in both viral and sub-viral genome datasets. We demonstrated frequent recombination of begomovirus species, with a maximum in intra-species recombinants. Furthermore, our results showed a high degree of genetic variability, demographic selection, and mean substitution rate acting on the population, supporting the emergence of a diverse and purifying selection of viruses and associated betasatellites. Moreover, variation in the genetic composition of all begomovirus datasets revealed a predominance of nucleotide diversity principally driven by mutation, which might further accelerate the advent of new strains and species and their adaption to various hosts with unique pathogenicity. Therefore, the finding of genetic variation and selection emphases on factors that contribute to the universal spread and evolution of Begomovirus and this unanticipated diversity may also provide guidelines toward future evolutionary trend analyses and the development of wide-ranging disease control strategies for begomoviruses associated with PaLCD.

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Distinct evolutionary histories of the DNA-A and DNA-B components of bipartite begomoviruses.

Publications

Distinct evolutionary histories of the DNA-A and DNA-B components of bipartite begomoviruses.

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