Diversity, recombination and misclassification in the family Geminiviridae: Insight from bioinformatics analysis
Moshood Olamide Lateef, Dauda Nathaniel, Bolaji Osundahunsi, Neil Arvin Bretana, Islam Hamim, Islam Hamim, Shunmugiah Ramesh, Shunmugiah Ramesh
TL;DR
This study uses bioinformatics to analyze the diversity and evolution of geminiviruses, revealing misclassifications, recombination patterns, and potential new virus species.
Contribution
The study provides the first global geographic map of all Geminiviridae genera and identifies misclassified viruses and potential new taxa.
Findings
Begomovirus and Mastrevirus are the only genera found on all continents, with Asia showing the highest diversity.
Phylogenetic analysis revealed misclassified viral species and potential new taxa, including reclassification of French bean severe leaf curl virus.
High-frequency recombination events involving Begomovirus suggest its key role in geminivirus evolution.
Abstract
The family Geminiviridae comprises 15 genera and over 500 species of diverse plant-infecting viruses. Previous studies on this virus’s diversity primarily focused on the members’ selection without considering the entire genomic divergence. This study presents comprehensive comparative genomic analyses and a global distribution map using 17,718 complete genomes and 28,185 geminivirus-associated metadata records. Intergeneric pairwise identity among monopartite and Begomovirus DNA-A is ≥ 40%, while interspecies identity among Begomovirus DNA-B is ≥ 41%, corresponding to genetic variations of ≤60% and ≤59%, respectively. Begomovirus and Mastrevirus are the only genera detected across all continents, with Asia exhibiting the highest genus diversity (11 genera). However, in Africa, geminiviruses from six genera are more broadly distributed across individual countries. To our knowledge, this…
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Taxonomy
TopicsPlant Virus Research Studies · Polyomavirus and related diseases · Animal Virus Infections Studies
Introduction
Geminiviridae is a cosmopolitan virus family that causes several plant diseases and is transmitted by insect vectors [1,2]. It exists as monopartite or bipartite twinned virions that encapsulate the circular single-stranded deoxyribonucleic acid (DNA) [3,4]. Economically, these viruses cause huge losses to various plant hosts, such as vegetables, fiber, and root crops, mainly in the subtropical and tropical regions of the globe [5,6]. Several studies have reported severe crop losses caused by specific geminivirus species. Notably, cotton leaf curl disease (CLCuD), primarily caused by Begomovirus gossypimultanense and Begomovirus gossypikokranense in Pakistan and India [7], has hindered cotton production in these countries, while African cassava mosaic virus (ACMV, Begomovirus manihotis) is responsible for cassava mosaic disease across Africa [9]. In the United States, tomato yellow leaf curl virus (TYLCV, Begomovirus coheni) has significantly affected tomato crops [5]. The cotton industry in Pakistan alone suffers estimated annual losses of 140 million in annual losses to tomato production in the USA. Hema et al. [8] reported over 2 billion in annual losses across Africa [9]. Currently, fifteen genera and over five hundred species have been identified as members of the Geminiviridae [10], making it the largest family of plant viruses. The genera include Capulavirus, Citlodavirus, Curtovirus, Eragrovirus, Grablovirus, Maldovirus, Mastrevirus, Mulcrilevirus, Opunvirus, Topilevirus, Topocuvirus, Turncurtovirus, Welwivirus, Becurtovirus, and Begomovirus. Among these genera, Begomovirus contains over four hundred species and remains the most studied. New genera and species are continually being detected due to advances in sequencing technology with the use of next-generation sequencing to detect new and unclassified viruses [11–13].
Insect vectors are the major mode of spread of these viruses, with a single vector capable of transmitting viruses to multiple species or genera of susceptible hosts. This remains a potential source for the intra- or inter-genus recombinant virus. However, mutation, recombination, and pseudo-recombination are the driving forces of geminivirus evolution [14]. The emergence of new virus species and genera with modified virulence can overcome host resistance genes and challenge surveillance due to the virus’s increased adaptation to environmental factors and susceptible host plants [15–17]. This menace potentially challenges food security across the world.
Recombination has been the driving force behind the evolution and emergence of new viruses within the Geminiviridae family through possible adaptation to changing environmental conditions and susceptible host plants [15]. Several studies have reported intra- and interspecies recombination leading to the emergence of new viruses within Geminiviridae [18–22]. These studies mainly focused on begomoviruses and a few other genera. Therefore, all 15 genera of Geminiviridae need to be considered for recombination analysis to provide a comprehensive view of recombination across the entire family. This study’s sampling approach considered every virus genome with either high or low sequence diversity to represent the full sequence diversity of this highly diverse virus family.
The distribution of all geminiviruses is reported to be global [23–25]; however, these studies depicted the global distribution through a geographical map with data points on a few genera, whitefly vector distribution, or geminivirus-based satellites. A comprehensive map showing the global distribution of all genera is still lacking. The construction of such a map will provide substantial information at a glance for prompt decision-making. Understanding the diversity and evolution of both new and previously reported species is essential to support surveillance efforts against emerging diseases threatening food security. This study therefore focuses on the patterns of diversity and recombination within and among all 15 genera and a geographical distribution map for the entire genera*.*
Materials and methods
Sampling procedure and techniques
The complete genomes of all available monopartite and bipartite viruses of the family Geminiviridae available until May 10, 2024, were retrieved from the GenBank [26]. This included 14,778 genomes of monopartite viruses and DNA-A components of bipartite viruses and 2,940 genomes of DNA-B of bipartite viruses. A chart showing the number of retrieved and sampled sequences across each genus is included in the supplementary materials (S1 and S2 Figs). The downloaded sequences were exported to the sequence demarcation tool (SDT) version 1.3, a tool that classifies sequences based on their percentage pairwise identity [27]. The sequences with the same percentage identities were grouped together and served as a pool to select representative samples. The genetic diversity among these genera varies. Conventionally, geminivirus sequences with ≤ 95% pairwise identity were chosen for the study performed by Padidam et al. [21]. In this study, ≥ 95% pairwise similarity in viral sequences within each of the Topocuvirus, Topilevirus, Maldovirus, and Eragrovirus was partitioned, and sequence(s) were sampled from each partition using SDT. Similarly, ≥ 92% pairwise similarity was used for Capulavirus, Citlodavirus, Curtovirus, Becurtovirus, Grablovirus, Mulcrilevirus, Opunvirus, Turncurtovirus, and Welwivirus.
Sequences for Mastrevirus and Begomovirus, which had a large number of available sequences, were grouped into batches for parallel computation, and sampling was performed using ≥80% pairwise similarity. Similarly, Bandoo et al. [28] adopted 80% pairwise identity when selecting members of Begomovirus. The detailed procedures for virus genome sampling and geographical map construction are available at https://doi.org/10.17504/protocols.io.j8nlkybjdg5r/v1. The selected sequences from each genus partition were gathered and used as representatives for the respective genus. In addition, the corresponding amino acid sequences of the coat protein (CP) and replication-associated protein (Rep) for all the sampled nucleotide sequences across all genera were retrieved from the GenBank. Details of these sampled geminiviruses are provided in the supplementary materials (S1 Table).
Intra-geminivirus sequence alignment
The sampled virus sequences for each genus were imported into individual FASTA files and aligned with multiple alignments using Fast Fourier Transform (MAFFT) algorithm version 7.526 [29]. The options L-INS-I and --ep were selected to efficiently align the sequences. The alignment was performed with and without outgroup sequences for the diversity and recombination analysis, respectively. The chicken anemia virus with accession number M55918.1 was used as the outgroup for the nucleotide-based phylogenies, consistent with previous studies [3,30]. BioEdit software version 7.2.5 [31] was used to view and monitor the alignments manually. A few sequences with incorrect orientation were corrected, and the sequences were realigned.
Distribution across the world
The metadata for all geminiviruses, including both complete and partial genome sequences, were also retrieved from GenBank and served as the main data for the map illustration. Explicitly, the species of the virus and the location source were aggregated by their respective genera and source countries to construct the geographical map (S2 Table). This approach minimizes graphic clutter and facilitates data visualization. The Plotly library in Python programming was used to construct the distribution map.
Phylogenetic-based evolutionary relationship
The evolutionary relationships among all genera of the Geminiviridae were constructed with the phylogenetic tree. For all genera, as well as for the DNA-A of bipartite begomoviruses, aligned nucleotide sequences of complete genomes and amino acid sequences of Rep and CP were used to reconstruct phylogenetic trees using IQ-TREE [32]. The best-fitting substitution model was automatically selected based on Bayesian Information Criteria with 1,000 ultrafast bootstrap replicates.
In contrast to the nucleotide-based phylogeny, the amino acid-based phylogenies were constructed without an outgroup and were instead rooted at the midpoint. The reconstructed phylogenies were edited and visualized using FigTree version 1.4.4 [33].
Recombination analysis
The multiple sequence alignments without an outgroup were imported into the recombination detection program version 5 (RDP5) [34]. The following integrated methods in RDP5 were used to perform a preliminary scan for possible recombination in the aligned virus sequences: Chimaera [35], Bootscan [36–37], Geneconv [21], SisterScan [38], Maximum Chi Square [35,39], and 3Seq [40]. A Bonferroni-corrected P-value of 0.05 and default parameter settings were used for the individual method analysis. To increase the stringency and reduce false positives, recombinants that were identified by at least four methods were considered reliable.
Results
Genetic variation and pairwise identity across Geminiviridae
Analysis of pairwise identity for the sampled genomes revealed that inter-genera identity among monopartite geminiviruses and Begomovirus DNA-A is ≥ 40% (Fig 1), corresponding to a maximum genetic variation of 60%. Similarly, interspecies pairwise identity across the complete genomes of Begomovirus DNA-B is ≥ 41% (Fig 2), corresponding to a maximum genetic variation of 59%.
Pairwise identity of the sampled monopartite and DNA-A of Begomovirus genomes using SDT.
Pairwise identity of the sampled DNA-B of Begomovirus using SDT.
Mapping the global distribution of Geminiviridae: Continental spread of the viral genera
The geographical distribution map (Fig 3) constructed with the metadata of 28,185 data points (metadata for both complete and partial genomes) revealed that members of the family Geminiviridae are globally distributed across all six continents. However, only the genera Begomovirus and Mastrevirus have been isolated from every continent. Eleven out of the fifteen genera within Geminiviridae were isolated from Asia. These genera are Begomovirus, Mastrevirus, Curtovirus, Citlodavirus, Grablovirus, Topocuvirus, Turncurtovirus, Becurtovirus, Capulavirus, Maldovirus, and Mulcrilevirus. South America is the second continent with seven genera reported, namely Begomovirus, Mastrevirus, Citlodavirus, Grablovirus, Topilevirus, Capulavirus, and Welwivirus. North America and Africa have cases of six genera reported from each of the continents. Begomovirus, Mastrevirus, Grablovirus, and Becurtovirus were reported from both continents. However, Curtovirus and Opunvirus were reported from North America, while Capulavirus and Eragrovirus were the additional reported genera from Africa. Additionally, the African continent had the highest number of countries where geminivirus infections are reported. Europe has five genera of Geminiviridae reported within the continent. These are Begomovirus, Mastrevirus, Grablovirus, Capulavirus, and Maldovirus. Only three genera—Begomovirus, Mastrevirus, and Maldovirus—have been reported from Oceania.
Geographical map showing global distribution of genera within Geminiviridae.Constructed with Plotly library.
Phylogenetic patterns in Geminiviridae
The total number of sampled sequences used to construct the phylogenetic trees was 284 for the complete genome, 280 for the coat protein, and 282 for the Rep protein. After multiple sequence alignments, the orientation of all sequences was checked and confirmed. GTR + F + R9, LG + F + I + G4, and rtREV + F + G4 were the best-fit chosen models, respectively, for the nucleotides, CP, and Rep of monopartite and Begomovirus DNA-A. The reconstructed phylogeny with the virus genomes (Fig 4) revealed the members of every genus to form a cluster, subsequently forming a clade between genera. However, a few Begomovirus species, including unclassified Begomovirus, cluster outside their respective genera. Similarly, the CP of every genus forms a clade, with the exception of a few unclassified begomoviruses (Fig 5). Contrarily, the Rep of the virus species within the genus Begomovirus forms many clusters that are distributed across the Rep of other genera, including Curtovirus, Maldovirus, Turncurtovirus, and Topocuvirus (Fig 6).
Phylogenetic reconstruction with the nucleotides of monopartite and the DNA-A of the Begomovirus genome.Inferred using maximum likelihood method within IQ-tree software at 1000 ultrafast bootstrap replicates.
Phylogenetic reconstruction with the coat protein of monopartite and the DNA-A of the Begomovirus.Inferred using maximum likelihood method within IQ-tree software at 1000 ultrafast bootstrap replicates.
Phylogenetic reconstruction with the Rep protein of monopartite and the DNA-A of the Begomovirus.Inferred using maximum likelihood method within IQ-tree software at 1000 ultrafast bootstrap replicates.
Identifying and analyzing a misclassified viral accession
While analyzing the result of the phylogenetic reconstruction, French bean severe leaf curl virus (FbSLCV) with accession KC699544, classified as a member of the genus Capulavirus, formed a clade with the Begomovirus genome, CP, and Rep sequences in their respective phylogenies (Figs 4–6). However, it is possible for one or a few of all the molecular compositions (genome, CP, and Rep) of geminivirus to be more closely related to a particular different genus, but not for the entire composition. This prior knowledge prompted further analysis to complement the reconstructed phylogenies. The complete genome nucleotide and the amino acid sequences for the full CP and Rep of this virus accession were independently analyzed using BLASTN and BLASTP against the GenBank database; the result revealed several virus members of Begomovirus. Interestingly, no Capulavirus species were detected in the BLAST results.
The entire sample of representative viruses for the genus Capulavirus and some of the closest viruses from the BLAST result were subjected to the pairwise identity analysis using SDT version 1.3 [27]. ClustalW within the SDT tool was selected to align the sequences. The result showed the virus to have a close pairwise identity to the selected Begomovirus, while the disparity is too distant from the compared Capulavirus (). To explicitly visualize the pairwise identity of this misclassified virus sequence (KC699544) to each of the selected viruses, the percentage similarity scores were extracted and used to plot a multiple bar chart for the complete genome, CP, and Rep regions, as shown in Fig 10.
Pairwise identity of the misclassified virus genome.
Pairwise identity of the misclassified virus coat protein.
Pairwise identity of the misclassified virus replication-associated protein.
Comparison of Pairwise identity of the misclassified virus to Begomovirus and Capulavirus.
The virus nucleotide sequences and amino acid sequences of the coat protein have the highest percentage pairwise identity of 91.3% and 99.2% to Corchorus yellow vein mosaic virus (CoYV) accessions KX513862 and AGG18212, respectively. Similarly, the virus Rep was found to be closely related to the French bean leaf curl virus (FbLCV) with a pairwise identity of 92.3% with accession number AFM77725. All these closely related viruses belong to the genus Begomovirus. Summarily, the virus is more closely related to CoYV of the genus Begomovirus, suggesting a new isolate. Hence, the accession is proposed to be named as Corchorus yellow vein mosaic virus within the genus Begomovirus.
Proposed reassignment of unclassified viruses to the genus Maldovirus
Two unclassified begomovirus-like viruses, tentatively named “begomovirus spathoglottis 1” and “begomovirus spathoglottis 2,” were found to cluster phylogenetically with members of the genus Maldovirus (Figs 4 and 5). Notably, the clade containing these two viruses forms a sister group to the clade comprising established Begomovirus species, prompting further investigation through pairwise identity analysis (Fig 4). To assess genomic similarity, “begomovirus spathoglottis 1” and “2” were queried against the GenBank reference database using BLASTN. Genome sequences (full genome nucleotide sequences, Rep, and CP) of a few top-hit viruses were retrieved, along with representative members of the genus Maldovirus, for comparative analysis. Pairwise sequence identity was calculated using SDT with default parameters.
Identity scores between apple geminivirus 1 (a member of Maldovirus) and the selected viruses were plotted (Fig 11). The genome-wide nucleotide identity across all viruses analyzed ranged from 62% to 65%. The CP was identified as the primary genomic region distinguishing Begomovirus species from both Maldovirus members and “begomovirus spathoglottis 1” and “2” (Fig 11). The CP of Maldovirus members and “begomovirus spathoglottis 1” and “2” shared 45–48% pairwise identity compared to 18–22% with the selected begomoviruses. These results support the phylogenetic analyses (Figs 4 and 5), which indicate a close relationship between Maldovirus and these two unclassified viruses. Based on these findings, we propose that “begomovirus spathoglottis 1” and “begomovirus spathoglottis 2” be reclassified within the genus Maldovirus, under the tentative names “maldovirus spathoglottis 1” and “maldovirus spathoglottis 2.” It is important to note that these proposed virus names remain provisional and are subject to formal approval by the International Committee on Taxonomy of Viruses (ICTV).
Comparison of the pairwise identity of the newly proposed species of Maldovirus to Begomovirus and Maldovirus.
Recombination-driven evolution in Geminiviridae
Interspecies recombination was more frequent in Begomovirus, with many species containing recombinant sequences derived from other species. Additionally, interspecies recombination was also detected in various species of Begomovirus DNA-B. Tables detailing the recombinant viruses are included (S3–S5 Tables). Additionally, inter-genera recombination was detected in Opunvirus, Curtovirus, and Topocuvirus.
Discussion
The sampling approach adopted in this study considers the entire diversity in all the complete genome sequences in the family Geminiviridae. To the best of our knowledge, this is the first constructed geographical map using the entire genera of the family Geminiviridae. Previous studies used a few genera, such as Begomovirus [23], whitefly-infecting Begomovirus [25], and weed-infecting geminivirus [24], to depict the global distribution of geminivirus.
Notably, Begomovirus and Mastrevirus were the only genera found across all continents, a pattern consistent with previous studies highlighting their broad host range and efficient transmission by insect vectors such as whiteflies (Bemisia tabaci) and leafhoppers (Cicadellidae) [41,42]. The highest diversity of geminivirus genera exhibited by Asia may be attributed to the region’s rich agroecological zones, dense cultivation of susceptible crops, and favorable climates that support vector populations.
South America ranked second in diversity, with seven genera reported. While the region showed lower genera diversity than Asia, the presence of less commonly detected genera such as Topilevirus [43] may suggest localized evolution or limited dispersal beyond the region. Africa stood out for having the highest number of countries affected, emphasizing its significance as both a center of geminivirus diversity and vulnerability [44]. This finding may be driven by widespread vector presence, the predominance of smallholder farming systems, and limited phytosanitary infrastructure. The lower genera diversity in Europe and Oceania could be a true reflection of limited viral presence or could result from lower sampling intensity and fewer molecular diagnostics being performed. Nevertheless, the presence of Begomovirus and Mastrevirus across all regions supports their dominant role in global geminivirus spread and evolution.
Summarily, while Geminiviridae members are globally distributed, their occurrence varies by region. This uneven distribution is likely influenced by multiple factors, including vector distribution, agricultural practices, plant host range, and environmental conditions, as well as the intensity of viral surveillance and reporting systems [45]. These findings underscore the need for enhanced global and regional surveillance, particularly in regions with high reported diversity, such as Africa, Asia, and South America. Understanding the evolutionary dynamics and ecological niches of these viruses remains crucial for developing effective management strategies.
The ≥ 40% inter-genera identity across the family supports the idea of a shared evolutionary origin, despite the extensive diversification driven by recombination, host adaptation, and vector specificity [19,46]. Moreover, the DNA-B segment with ≥41% interspecies identity exhibits less recombination-driven divergence due to its limited gene content and essential movement functions [47]. These pairwise identity calculations affirm the robustness of current molecular criteria used for virus classification in the family Geminiviridae.
The comprehensive phylogenetic and comparative genomic analyses conducted in this study offer important insights into the evolutionary biology, host adaptation, and vector transmission strategies of members of the Geminiviridae family. This study reveals the Citlodavirus genomes and CP are closely related to Mulcrilevirus, while the Rep is similar to the Rep of virus members within Mulcrilevirus and Becurtovirus, consistent with the phylogenies inferred by Roumagnac et al. [43]. Similarly, the Curtovirus genome and CP are closely related to Becurtovirus. While the Curtovirus Rep clusters with the Turncurtovirus Rep, the Becurtovirus Rep clusters with members of Mulcrilevirus. The cluster of Curtovirus and Becurtovirus genomes and CP form a clade with the respective components of Turncurtovirus, consistent with the reported finding of Varsani et al. [48]. The close phylogenetic relationship of Curtovirus and Becurtovirus to Turncurtovirus supports the hypothesis that these genera share a common evolutionary origin [48], potentially shaped by overlapping host ranges or vector interactions. The genome sequences and the Rep amino acids of the Maldovirus are closely related to Begomovirus in this study; this is consistent with the inferred relationship by Roumagnac et al. [43].
Opunvirus (OpV1) genomes form a clade with genus Topocuvirus. However, Fontenele et al. [49] reported this genus to be close to Topocuvirus, Begomovirus, and some virus species later classified into Maldovirus. The amino acid of the OpV1 Rep is revealed to form a clade with a cluster containing Curtovirus, Topocuvirus, Turncurtovirus, Maldovirus, and Begomovirus, similar to the findings from Fontenele et al. [49]. The constructed phylogeny using amino acids of the CP shows OpV1 CP to be closely related to the genus Grablovirus CP. This is contrary to the report of OpV1 CP forming a distinct clade [49].
Topilevirus genome and amino acid sequences of the Rep have close a resemblance to Capulavirus, while amino acid sequences of the CP are closely related to Topocuvirus. These findings on members within the genus Topilevirus are consistent with the previous studies [43,50]. The CP amino acids of the members within Capulavirus form distinct clusters that distantly form a clade with clusters containing Begomovirus, Mulcrilevirus, and Citlodavirus. This is similar to the isolated cluster of Capulavirus CP in the reported phylogeny by Roumagnac et al. [43] and Vaghi Medina et al. [50].
Genus Grablovirus is related to Capulavirus, Topilevirus, and Mastrevirus, consistent with the result of Vaghi Medina et al. [50]. The amino acids of the CP-constructed phylogeny reveal this virus to be closely related to the genus Opunvirus. However, few previous studies reported geminivirus phylogeny containing Opunvirus and Grablovirus. Roumagnac et al. [43] had these two genera included in their study, but the Grablovirus was revealed to be distinctly isolated. Interestingly, this study reveals the Rep forming a sister group to the remaining genera of the family Geminiviridae. This finding is consistent with the < 45% pairwise identity of Grablovirus Rep with other geminivirus Rep [51].
The complete genomes of monopartite begomoviruses and DNA-A of bipartite are unveiled to be closely related to the maldoviruses. This is consistent with previous studies carried out by Roumagnac et al. [43] and Varsani et al. [51]. However, the amino acids of several begomoviruses CPs are closely related to CPs of citlodaviruses and mulcrileviruses. In contrast, the CP of a few viruses whose sequences are within Begomovirus in the GenBank, such as Parsley yellow leaf curl virus (PYLCV) and Sida golden yellow spot virus, are distant from the majority of the begomoviruses. PYLCV CP is closely related to Turncurtovirus, Becurtovirus, and Curtovirus, similar to the reported findings by Hasanvand et al. [52]. Nichkerdar et al. demonstrated the virus to be transmitted by leafhoppers [53]. Previous studies reported the Begomovirus CP to be closely related to the Citlodavirus and Mulcrilevirus CP [43,51]. Lastly, the Rep amino acids of the begomoviruses are distributed across various genera such as Maldovirus, Curtovirus, Turncurtovirus, and Topocuvirus, supporting potential evolutionary relationships among these genera. However, only maldoviruses and topocuviruses were shown to be closely related in previous studies [43,51]. The differences in this study in comparison with previous studies could rely majorly on the representative sampling of the entire virus members.
The CP region has been demonstrated to confer vector specificity on geminivirus [54]. Additionally, the evolutionary relationships of geminivirus CPs and the cytochrome oxidase I (COI) gene of their insect vectors are closely aligned, providing strong evidence for reciprocal co-evolution between geminiviruses and their respective vectors [46]. Hence, evolutionary shifts in vector-mediated transmission of geminiviruses to new plant hosts appear to be more possible than the adaptation of known geminiviruses to novel insect vectors. This insight enhances our ability to predict potential vectors for geminivirus genera for which vector information is currently lacking. It is hypothesized that Opunvirus, Welwivirus, and Topilevirus may be transmitted by treehoppers, whereas Citlodavirus and Eragrovirus are likely transmitted by leafhoppers. The potential vector for Maldovirus, however, remains uncertain.
Comparative phylogenetic analyses based on the complete genome, CP, and Rep revealed that the CP-based phylogeny exhibited the highest degree of conservation across the family. In contrast, the Rep-based phylogeny indicated a high level of diversity, particularly among begomoviruses Reps distributed across multiple genera. Notably, recombination analysis identified the highest frequency of recombination events within the genomic region encoding the Rep.
Several previous studies had also reported interspecies recombination in Begomovirus [15,21,55]. For inter-genera recombination, Opunvirus was detected to contain 693 recombinant sequences, of which Begomovirus contributed the major parental sequences. However, Fontelele et al. reported only intra-species recombination for members of the genus Opunvirus in their recombination detection analysis [49]. Topocuvirus was also detected to contain intergeneric recombinant sequences of 1144 bases. The major parental sequence is the Begomovirus, while the minor parental sequence is the Myrica rubra citlodavirus 1 (MRV1). Padidam et al. [21] and Varsani et al. [55] reported that the tomato pseudo-curly top virus was involved in the recombination for the evolution of geminivirus. Members of the Curtovirus genus have recombinant sequences from Becurtovirus as the major parent and Juncus maritimus geminivirus 1 of Maldovirus as the minor parent. Several studies had previously detected recombination in the genus Curtovirus [21,55,56].
The extensive recombination detected across Begomovirus, Curtovirus, Topocuvirus, and Opunvirus highlights the evolutionary fluidity and plasticity within Geminiviridae. Specifically, the detection of intergeneric recombination events where Begomovirus contributed parental sequences to various genera, including Opunvirus and Topocuvirus genomes, reinforces its central role in geminivirus evolution [21]. These recombination events may facilitate cross-species transmission, adaptation to new hosts, and expansion into novel ecological niches [45].
Summarily, these results indicate that Geminiviridae evolution is driven by a combination of ancient divergence, recombination, and potential vector shifts. The phylogenetic inconsistencies between CPs and Reps further support the modular evolution of geminivirus genomes, where different genomic components may evolve independently due to differential selective pressures [19]. This modularity could also explain the potential of viruses such as those observed in Begomovirus, where CPs and Reps cluster with different genera, enabling ecological versatility and rapid evolutionary responses.
Conclusions
This study provides a comprehensive, family-wide assessment of the genetic diversity, phylogeny, and global distribution of the Geminiviridae. Inter-genus and interspecies pairwise identity analyses support the overall robustness of existing taxonomic classifications while also identifying notable exceptions that warrant taxonomic revision. The global distribution map highlights the widespread presence of Begomovirus and Mastrevirus, consistent with their broad host ranges and effective vector-mediated transmission. Phylogenetic analyses reveal the modular architecture of geminivirus genomes, with coat protein sequences exhibiting higher conservation—likely reflecting vector specificity—while replication-associated protein sequences display greater variability, driven largely by recombination. Recombination is confirmed as a major force shaping geminivirus evolution, particularly within Begomovirus, enabling rapid genetic diversification, host adaptation, and ecological expansion. These findings enhance our understanding of the evolutionary dynamics within Geminiviridae and underscore the importance of global surveillance, especially in regions with high viral diversity. The insights gained provide a critical foundation for improving the prediction of virus emergence, elucidating vector-virus relationships, and developing targeted disease management strategies essential for protecting global agricultural systems.
Supporting information
S1 FigSampling approach based on pairwise identity similarity.The bar chart depicted the retrieved and sampled nucleotide sequences across each genus.(TIF)
S2 FigSampled coat and Rep proteins from each genus.(TIF)
S1 TableThe details of the selected geminiviruses.These geminiviruses were selected following the partition that was based on the pairwise identity.(XLSX)
S2 TableGeminiviridae genera and respective countries data points for map construction.(XLSX)
S3 TableInterspecies and intraspecies recombination events in the sampled monopartite and Begomovirus DNA-A.The methods with the lowest and highest P-values are superscripted with l and h respectively.(XLSX)
S4 TableInterspecies recombination events in the sampled Begomovirus DNA-B.The methods with the lowest and highest P-values are superscripted with l and h respectively.(XLSX)
S5 TableInter-genera recombination events in the sampled monopartite and Begomovirus DNA-A.The methods with the lowest and highest P-values are superscripted with l and h respectively.(XLSX)
The reference list from the paper itself. Each links out to its DOI / PubMed record.
- 1Arif M, Farooq S, Alasmari A, Alshehri MA, Hashem M, Alamri S, et al. Molecular study of geminiviruses: complex biology, host-vector interactions, and increasing diversity. J King Saud Univ Sci. 2022;34(4):102051. doi: 10.1016/j.jksus.2022.102051 · doi ↗
- 2Nadeem S, Riaz Ahmed S, Luqman T, Tan DKY, Maryum Z, Akhtar KP, et al. A comprehensive review on Gossypium hirsutum resistance against cotton leaf curl virus. Front Genet. 2024;15:1306469. doi: 10.3389/fgene.2024.1306469 38440193 PMC 10909863 · doi ↗ · pubmed ↗
- 3Brown JK. Family Geminiviridae. Virus Taxonomy, Classification and Nomenclature of Viruses: Ninth Report of the International Committee on Taxonomy of Viruses; 2012. p. 351–73. doi: 10.1016/B 978-0-12-384684-6.00035-5 · doi ↗
- 4Fiallo-OlivéE, Lett J-M, Martin DP, Roumagnac P, Varsani A, Zerbini FM, et al. ICTV virus taxonomy profile: Geminiviridae 2021. J Gen Virol. 2021;102(12):001696. doi: 10.1099/jgv.0.001696 34919512 PMC 8744271 · doi ↗ · pubmed ↗
- 5Kumar A, Khan JA. Geminivirus resistance strategies. In: Geminiviruses: impact, challenges and approaches. Springer International Publishing; 2019. p. 197–218. doi: 10.1007/978-3-030-18248-9_11 · doi ↗
- 6Navas-Castillo J, Fiallo-OlivéE, Sánchez-Campos S. Emerging virus diseases transmitted by whiteflies. Annu Rev Phytopathol. 2011;49:219–48. doi: 10.1146/annurev-phyto-072910-095235 21568700 · doi ↗ · pubmed ↗
- 7Briddon RW, Markham PG. Cotton leaf curl virus disease. Virus Res. 2000;71(1–2):151–9. doi: 10.1016/s 0168-1702(00)00195-7 11137169 · doi ↗ · pubmed ↗
- 8Hema M, Sreenivasulu P, Patil BL, Kumar PL, Reddy DVR. Tropical food legumes: virus diseases of economic importance and their control. Adv Virus Res. 2014;90:431–505. doi: 10.1016/B 978-0-12-801246-8.00009-3 25410108 · doi ↗ · pubmed ↗