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

Abstract

BackgroundViruses 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.ResultsComparative 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.ConclusionsThe 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.

Characterization of a New World Monopartite Begomovirus Causing Leaf Curl Disease of Tomato in Ecuador and Peru Reveals a New Direction in Geminivirus Evolution

“…Begomoviruses have the largest number of species in the family (and probably of any type of virus), and many have been described within the past approximately 20 years (5). This makes begomoviruses a remarkably successful group of emerging viruses (1,7), and this can be attributed to a number of factors. First, indigenous begomoviruses are widely distributed in noncultivated plants (e.g., weeds), and these serve as progenitors of crop-infecting viruses.…”

“…Second, population explosions and the expanded geographical range of the invasive polyphagous B biotype of B. tabaci have facilitated the introduction of indigenous begomoviruses into crop plants. Third, the begomovirus genome has the capacity to evolve rapidly via mutation, pseudorecombination, recombination, and acquisition of new DNA components and satellites (1,4,(7)(8)(9). Finally, the worldwide cultivation of susceptible crop plants (e.g., cassava, cotton, cucurbits, and tomato), often in monoculture and overlapping plantings, has resulted in the exposure of potential host plants to high populations of whiteflies and a diversity of begomoviruses (8,10).…”

“…he family Geminiviridae is a large and diverse group of plantpathogenic viruses that possess a small circular singlestranded DNA (ssDNA) genome encapsidated within characteristic twinned, quasi-isometric virions (1)(2)(3)(4). Four genera of geminiviruses are currently recognized, based upon genome structure, host range, and type of insect vector (5).…”

“…There are two types of begomoviruses: those with a monopartite genome (a single genomic DNA of approximately 2.9 kb) and those with a bipartite genome (two DNA components, each approximately 2.6 kb, referred to as DNA-A and DNA-B) (1,(3)(4)(5). Monopartite begomoviruses originated in the Old World (OW), and many are associated with satellite DNAs that are either required for development of typical disease symptoms (betasatellites) or have no apparent effect or modulate disease symptoms (alphasatellites) (1).…”

Emerging threats of begomoviruses to the cultivation of medicinal and aromatic crops and their management strategies

“…Both the phenomenon are responsible for the diversification in begomovirus between variants of the same virus, between different species and between different genus leading to the ability to adapt in different environment and forming new variants in new hosts. Mutations and acquiring new components like satellite molecules in the viral genome resulted in the emergence of new viruses [23,124,135]. One of a key recombinant event in ToMoV DNA-A CR with that of BDMV DNA-B component has resulted in the emergence of new virulent fitter begomovirus.…”