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Elvira Fiallo-Olivé, F. Murilo Zerbini, Rob W Briddon, Darren P Martin, Jesús Navas-Castillo, Philippe Roumagnac and Arvind Varsani
Corresponding author: Elvira Fiallo-Olivé (email@example.com)Edited by: Hélène Sanfaçon and Andrew J. DavisonPosted: March 2017, updated September 2018 & August 2020
The geminiviruses are a family of small, non-enveloped viruses with genomes comprising one or two single-stranded, circular DNAs of 2.5–5.2 kb. Geminiviruses infect a wide range of plant species are transmitted by various insects in four families of homopterans (whiteflies, leafhoppers, aphids and treehoppers). Geminiviruses are important plant pathogens causing economically important diseases in most tropical and subtropical regions of the world.
Table 1.Geminiviridae. Characteristics of members of the family Geminiviridae.
bean golden yellow mosaic virus-[Dominican Republic:1987] (DNA-A L01635; DNA-B L01636), species Bean golden yellow mosaic virus, genus Begomovirus
Twinned (geminate) incomplete icosahedra, T=1, 22×38 nm with a single coat protein
2.5–5.2 kb of single-stranded, circular DNA, mono- or bipartite
Complementary strand synthesized in the nucleus by host replication factors; double-stranded circular molecules serve as templates for both transcription and replication; replication employs a rolling-circle mechanism and also a recombination-dependent mechanism
From transcribed mRNAs
Plants (monocots and dicots)
Realm Monodnaviria, kingdom Shotokuvirae, phylum Cressdnaviricota, class Repensiviricetes, order Geplafuvirales; nine genera collectively including 483 species and two further species unassigned to a genus
Viruses classified into the nine genera show distinct host ranges, insect vectors and genome organizations:
Becurtovirus. This genus includes three species, Beet curly top Iran virus, Exomis microphylla latent virus (Claverie et al., 2018) and Spinach curly top Arizona virus (Varsani et al., 2014). Becurtoviruses are monopartite viruses infecting dicot plants and members of at least two species are transmitted by leafhoppers. Members are unusual in that instead of the 5′-TAATATTAC-3′ nonanucleotide found at the origin of virion strand replication (v-ori) in almost all other geminiviruses, they have a 5′-TAAGATTCC-3′ nonanucleotide.
Begomovirus. This genus includes of 424 species, members of which infect dicot plants and are transmitted by whiteflies of the Bemisia tabaci cryptic species complex (Brown et al., 2015). The genome can be either bipartite (two circular ssDNA molecules, each about 2.6 kb) or monopartite (a single approximately 2.7 kb circular ssDNA molecule) (Rojas et al., 2005). Begomoviruses usually induce severe symptoms in their hosts, including yellow mosaic, golden mosaic and leaf curl. Devastating pathogens include members of the species African cassava mosaic virus, Bean golden mosaic virus, Cotton leaf curl Multan virus and Tomato yellow leaf curl virus. Three classes of circular DNA satellites have been described associated with begomoviruses: betasatellites, alphasatellites and deltasastellites (Zhou 2013, Lozano et al., 2016).
Capulavirus. This genus includes four species of viruses, members of which have monopartite genomes (Varsani et al., 2017). Members of the species Alfalfa leaf curl virus and Plantago lanceolata latent virus are transmitted by aphids (Roumagnac et al., 2015, Susi et al., 2019). A unique feature of capulavirus genomes is the complex arrangement of possible movement protein-encoding ORFs located in a 5′-direction from the coat protein gene. All known capulaviruses have a 5′-TAATATTAC-3′ nonanucleotide at the v-ori.
Curtovirus. This genus includes three recognised species, including Beet curly top virus, whose members are economically important pathogens in North America and Iran (Chen and Gilbertson 2009) and have the widest host range of any geminivirus. Members infect dicot plants and are transmitted by leafhoppers.
Eragrovirus. This genus includes the single species, Eragrostis curvula streak virus, members of which have monopartite genomes (Varsani et al., 2014). All known isolates have been found infecting the monocot plant Eragrostis curvula (weeping love grass) in the Kwa-Zulu Natal region of South Africa (Varsani et al., 2009). Like the becurtoviruses, eragroviruses have a 5′-TAAGATTCC-3′ nonanucleotide sequence at the v-ori.
Grablovirus. This genus includes three species, Grapevine red blotch virus (Varsani et al., 2017), Prunus latent virus (Al Rwahnih et al., 2018) and Wild Vitis latent virus (Perry et al., 2018). Members have a 5′-TAATATTAC-3′ nonanucleotide at the v-ori and infect dicot plants.
Mastrevirus. Mastreviruses have monopartite genomes, infect mostly monocots and some dicots, and are transmitted by different species of leafhoppers (Muhire et al., 2013). Of the 41 species included in this genus, the best studied are Maize streak virus, members of which cause a severe disease of maize in Africa (Shepherd et al., 2010), and Wheat dwarf virus, members of which cause a disease of wheat across northern Europe, the Middle East and Asia (Kvarnheden et al., 2002). Recently a member of the species Wheat dwarf India virus has been shown to associate with alphasatellites and betasatellites (Kumar et al., 2014).
Topocuvirus. Members of the single species in this genus, Tomato pseudo-curly top virus, are transmitted by a treehopper (Briddon et al., 1996). The virus genome is similar to those of curtoviruses.
Turncurtovirus. There are currently three species in this genus, Turnip curly top virus (Varsani et al., 2014, Razavinejad et al., 2013), Turnip leaf roll virus (Kamali et al., 2016) and Sesame curly top virus (Hasanvand et al., 2018). Members are monopartite. Isolates of turnip curly top virus (TCTV) and turnip leaf roll virus (TLRV) have only been found so far in Iran and are transmitted by the leafhopper Circulifer haematoceps. Isolates of sesame curly top virus (SeCTV) have been identified from sesame (Sesamum indicum) in Pakistan and Iran and from the leafhopper Circulifer haematoceps collected from sesame plants also in Iran.
Virions are typically twinned ("geminate"). For maize streak virus (MSV, genus Mastrevirus), cryo-electron microscopy has shown that virions are about 22×38 nm in size, consisting of two incomplete icosahedra (T=1) containing a total of 110 coat protein subunits organized as 22 pentameric capsomers (Zhang et al., 2001) (Figure 1.Geminiviridae).
Figure 1.Geminiviridae. (Left) Cryo-electron microscopic reconstruction of maize streak virus (MSV) viewed along a two-fold axis of symmetry. The bar represents 10 nm. (Right) Purified particles of MSV stained with uranyl acetate showing typical twinned quasi-isometric subunits. The bar represents 50 nm. (From (Zhang et al., 2001); courtesy of R. McKenna).
The virion S20,w is approximately 70S (Goodman et al., 1980).
Twinned virions contain a single copy of circular ssDNA, ranging from 2.5 to 3.2 kb. Hence, for viruses with bipartite genomes, two virions containing different genomic components are required for infection, the total genome being about 5.2 kb (Von Arnim et al., 1993, Hamilton et al., 1983). Half-size defective components and ssDNA satellites are also encapsidated (Zhou 2013).
Virions contain a single structural protein (CP; Mr about 28–34×103). No other proteins have been found associated with virions (Zhang et al., 2001, Goodman et al., 1980).
Viruses in the genera Becurtovirus, Capulavirus, Curtovirus, Eragrovirus, Grablovirus, Mastrevirus, Topocuvirus and Turncurtovirus have a single genomic component, whereas those in the genus Begomovirus have either one or two components (Figure 2.Geminiviridae).
Figure 2.Geminiviridae. Genomic organization of geminiviruses. ORFs are denoted as being encoded on the virion-sense (V) or complementary-sense (C) strand, and corresponding protein products are coded by colour. The position of the stem-loop containing the conserved 5′-TAAGATTCC-3′ sequence located in the long intergenic region (LIR) is shown. For begomoviruses, V2/AV2 is not present in New World viruses. For becurtoviruses, an intron is predicted to occur at between ORFs C1 and C2. CRA and CRB, common regions A and B; CP, coat protein; IR, intergenic region; MP, movement protein; NSP, nuclear shuttle protein; REn, replication enhancer protein; Rep, replication-associated protein; SIR, short intergenic region; TrAP, transcriptional activator protein.
Replication occurs through double-stranded replicative intermediates by both recombination-dependent and rolling circle mechanisms (Stenger et al., 1991, Preiss and Jeske 2003). Complementary-sense DNA synthesis on the virion-sense (encapsidated) strand to produce dsDNA depends solely on host factors (Saunders et al., 1992). Virus ssDNA synthesis is initiated by cleavage of the virion-sense strand by the virus-encoded replication-associated protein (Rep) immediately downstream of the 3′-thymidine residue in a conserved 5′-TARTATT↓AC-3′ sequence located in the loop of a potential stem-loop structure within the intergenic region (IR) (Laufs et al., 1995, Fontes et al., 1994). Large amounts of heterogenous sub- and extra-genome length geminivirus DNA (hDNA) are generated during rolling circle replication, and most of the viral DNA that accumulates within infected cells is likely produced from this hDNA by recombination-dependent mechanisms that rely on host DNA double-stranded break repair complexes (Preiss and Jeske 2003). Geminiviruses do not encode a DNA polymerase, and consequently rely entirely on host factors that must be recruited during the early stages of replication.
In all cases, coding regions in both virion-sense and complementary-sense strands diverge from an intergenic region, and transcription is bi-directional, with independently controlled transcripts initiating within the intergenic region (IR) (Sunter and Bisaro 1989). Geminiviruses use multiple overlapping transcripts to control gene expression; those in the genus Mastrevirus and, probably, also in the genera Becurtovirus, Capulavirus and Grablovirus additionally use transcript splicing (Schalk et al., 1989).
Members of the genus Begomovirus are transmitted by whiteflies, those of the genera Mastrevirus, Curtovirus, Becurtovirus and Turncurtovirus are transmitted by leafhoppers, those of the genus Capulavirus are transmitted by aphids, and members of species in the genera Topocuvirus and Grablovirus are transmitted by treehoppers. The vectors of the only known member of the genus Eragrovirus remain unknown. Some viruses in the family Geminiviridae infect a wide range of plant species while others have a narrow host range. Members of the genera Becurtovirus, Begomovirus, Capulavirus, Curtovirus, Grablovirus, Topocuvirus and Turncurtovirus infect dicot plants. However, most members of the genus Mastrevirus and the only member of the genus Eragroviurs infect monocot plants. Geminiviruses are important plant pathogens causing economically important diseases in most tropical and subtropical regions of the world. Further information is provided on individual genus pages.
Becurto: from the type species Beet curly top Iran virus.
Begomo: from the type species Bean golden yellow mosaic virus (previously Bean golden mosaic virus).
Capula: from the type species Euphorbia caput-medusae latent virus.
Curto: from the type species Beet curly top virus.
Eragro: from the type species Eragrostis curvula streak virus.
Gemini: from Latin geminus meaning "twin", describing the characteristic twinned (geminate) particle morphology.
Grablo: from the type species Grapevine red blotch virus.
Mastre: from the type species Maize streak virus.
Topocu: from the type species Tomato pseudo-curly top virus.
Turncurto: from the type species Turnip curly top virus.
These include host range (monocots or dicots), type of vector (leafhoppers, treehoppers, whiteflies, aphids), genome organization (mono- or bipartite), and phylogenetic relationships.
Phylogenetic analysis of complete genome sequences (DNA-A sequences in the case of bipartite begomoviruses) from isolates of representative species shows that geminiviruses cluster into groups corresponding to the nine genera (Figure 3.Geminiviridae). In addition, they cluster according to geographic distribution, at least within the begomoviruses, probably reflecting their evolutionary divergence as a consequence of isolation due to the inability of their insect vectors to fly long distances (Rocha et al., 2013). Despite frequent inter-species recombination events and the increasing worldwide movement of infected plants, it is remarkable that this geographical distribution is still apparent.
Figure 3.Geminiviridae. A. Unrooted, neighbor-joining phylogenetic tree of the full genome sequences (or DNA-A sequences for bipartite geminiviruses) of representative isolates in the genera in the family Geminiviridae. This tree is presented as a guide to describe relative similarities between the geminivirus groups, as it is not possible to align all of the representative genomes from the nine genera and novel divergent geminivirus isolates, as inter-species and inter-genus recombination has played a major part in the diversification of the represented virus isolates. B. Maximum-likelihood phylogenetic tree (applying the LG+I+G amino acid substitution model) inferred from Rep sequences of representative isolates of the genera in the family Geminiviridae. Numbers associated with branches indicate percentage approximate likelihood-ratio test support for these branches. The tree is rooted with Rep sequences of members of the family Genomoviridae (not shown). (OW) and (NW) stand for Old World and New World, respectively. This phylogenetic tree and corresponding sequence alignment are available to download from the Resources page.
In addition to the nine current genera, two additional genera are likely be created in the near future to accommodate two species that are currently classified in the family but are unassigned to a genus: Citrus chlorotic dwarf virus and Mulberry mosaic dwarf virus. Viruses of these species have genome organizations which are distinct from those of the viruses in the currently existing genera.
Members of the plant virus families Geminiviridae and Nanoviridae have circular ssDNA genomes and replicate by a rolling circle mechanism. All these viruses have highly conserved sequences (5′-TARTATTAC-3′ (geminiviruses), 5′-TAGTATTAC-3′ (nanoviruses)) in the loop of a putative stem-loop structure within the IR, in which a nick is introduced during the initiation of replication. Interestingly, the majority of alphasatellites that associate with begomoviruses have the nanovirus-like sequence 5′-TAGTATTAC-3′, consistent with them having evolved from components of nanoviruses. Similar structures are found in members of the animal virus family Circoviridae as well as the genus Anellovirus, both of which also have small circular ssDNA genomes. It is speculated that geminiviruses derive from prokaryotic episomal replicons, based on conservation of motifs in proteins that function in rolling circle replication initiation.
Nine monopartite ssDNA viruses have been recently characterized from different plant hosts including, apple (Liang et al., 2015) (Liang et al., 2015), camellia (Zhang et al., 2018) (Zhang et al., 2018), grapevine (Al Rwahnih et al., 2017), Juncus maritimus (Claverie et al., 2018), Limeum africanum (Claverie et al., 2018), passion fruit (Fontenele et al., 2018), tomato, cleome (Fontenele et al., 2017), and Polygala garcinii (Claverie et al., 2018). The genome organization of these viruses resembles those of geminiviruses. Genome sequences share 62–66.8% with all other known geminiviruses. Based on genome composition and phylogenetic relationship, these viruses are clearly related to members of the nine genera and two previously unassigned species in the family Geminiviridae.
apple geminivirus 1
Camellia chlorotic dwarf-associated virus
grapevine geminivirus 1
Juncus maritimus geminivirus 1
Limeum africanum geminivirus 1
passion fruit chlorotic mottle virus
Polygala garcinii geminivirus 1
tomato apical leaf curl virus
tomato geminivirus 1
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