The family Geminiviridae is one of the largest and most important families of plant viruses. The small, single-stranded DNA genomes of geminiviruses encode 5–7 proteins that redirect host machineries and processes to establish a productive infection. These interactions reprogramme plant cell cycle and transcriptional controls, inhibit cell death pathways, interfere with cell signalling and protein turnover, and suppress defence pathways. This Review describes our current knowledge of how geminiviruses interact with their plant hosts and the functional consequences of these interactions.
At a glance
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- Functional analysis of a novel motif conserved across geminivirus Rep proteins. J. Virol. 85, 1182–1192 (2011). et al.
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- Subviral agents associated with plant single-stranded DNA viruses. Virology 344, 198–210 (2006). &
- RNA-primed complementary-sense DNA synthesis of the geminivirus African cassava mosaic virus. Nucleic Acids Res. 20, 6311–6315 (1992). , &
- A putative primer for second-strand DNA synthesis of Maize streak virus is virion-associated. EMBO J. 3, 3069–3073 (1984). , , , &
- DNA forms indicate rolling circle and recombination-dependent replication of Abutilion mosaic virus. EMBO J. 20, 6158–6167 (2001). , &
- Two proteins of a plant DNA virus coordinate nuclear and plasmodesmal transport. Cell 76, 925–932 (1994). , &
- Cooperation in viral movement: the geminivirus BL1 movement protein interacts with BR1 and redirects it from the nucleus to the cell periphery. Plant Cell 7, 1185–1194 (1995). &
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- Global analysis of Arabidopsis gene expression uncovers a complex array of changes impacting pathogen response and cell cycle during geminivirus infection. Plant Physiol. 148, 436–454 (2008). et al.
- Assessing global transcriptome changes in response to South African cassava mosaic virus [ZA-99] infection in susceptible Arabidopsis thaliana. PLoS ONE 8, e67534 (2013).
References 26 and 27 describe the global impact of geminivirus infection on the host transcriptome and highlight the diversity of plant pathways that are altered during the infection process.
- MicroRNA profiling of Tomato leaf curl New Delhi virus (ToLCNDV) infected tomato leaves indicates that deregulation of mir159/319 and mir172 might be linked with leaf curl disease. Virol. J. 7, 281 (2010). , &
- A common set of developmental miRNAs are upregulated in Nicotiana benthamiana by diverse begomoviruses. Virol. J. 8, 143 (2011). , , , &
- In vitro cleavage and joining at the viral origin of replication by the replication initiator protein of tomato yellow leaf curl virus. Proc. Natl Acad. Sci. USA 92, 3879–3883 (1995). et al.
- Reprogramming plant gene expression: a prerequisite to geminivirus DNA replication. Mol. Plant Pathol. 5, 149–156 (2004). , &
- Geminivirus C3 protein: replication enhancement and protein interactions. J. Virol. 79, 9885–9895 (2005). , &
- Dual interaction of plant PCNA with geminivirus replication accessory protein (Ren) and viral replication protein (Rep). Virology 312, 381–394 (2003). , , , &
- PCNA interacts with Indian mung bean yellow mosaic virus rep and downregulates Rep activity. J. Virol. 78, 11890–11903 (2004). , , , &
- Interaction of geminivirus Rep protein with replication factor C and its potential role during geminivirus DNA replication. Virology 302, 83–94 (2002). , , , &
- The 32 kDa subunit of replication protein A (RPA) participates in the DNA replication of mung bean yellow mosaic India virus (MYMIV) by interacting with the viral Rep protein. Nucleic Acids Res. 35, 755–770 (2007). , , , &
- A novel role for RAD54: this host protein modulates geminiviral DNA replication. FASEB J. 26, 1142–1160 (2012). , , &
- Abutilon mosaic geminivirus double-stranded DNA is packed into minichromosomes. Virology 189, 800–802 (1992). &
- A geminivirus replication protein interacts with a protein kinase and a motor protein that display different expression patterns during plant development and infection. Plant Cell 14, 1817–1832 (2002). &
- Viral genome methylation as an epigenetic defense against geminiviruses. J. Virol. 82, 8997–9007 (2008). , , &
- Arabidopsis thaliana MCM2 plays role(s) in mungbean yellow mosaic India virus (MYMIV) DNA replication. Arch. Virol. 158, 981–992 (2013). , &
- A geminivirus induces expression of a host DNA synthesis protein in terminally differentiated plant cells. Plant Cell 7, 705–719 (1995). , , , &
- Proliferating cell nuclear antigen transcription is repressed through an E2F consensus element and activated by geminivirus infection in mature leaves. Plant Cell 13, 1437–1452 (2001).
References 42 and 43 demonstrate that geminiviruses induce the expression of the host DNA replication machinery in infected cells and that viral Rep is sufficient for this induction.
- The nanovirus-encoded Clink protein affects plant cell cycle regulation through interaction with the retinoblastoma-related protein. J. Virol. 81, 4177–4185 (2007). et al.
- Emerging roles of RETINOBLASTOMA-RELATED proteins in evolution and plant development. Trends Plant Sci. 17, 139–148 (2012). , &
- A geminivirus replication protein interacts with the retinoblastoma protein through a novel domain to determine symptoms and tissue specificity of infection in plants. EMBO J. 19, 3485–3495 (2000). et al.
- Cell type-specific role of the retinoblastoma/E2F pathway during Arabidopsis leaf development. Plant Physiol. 140, 67–80 (2006). , , , &
- Bean yellow dwarf virus RepA, but not Rep, binds to maize retinoblastoma protein, and the virus tolerates mutations in the consensus binding motif. Virology 256, 270–279 (1999). , , , &
- A novel motif in geminivirus replication proteins interacts with the plant retinoblastoma-related protein. J. Virol. 78, 4817–4826 (2004). et al.
- An intact RBR-binding motif is not required for infectivity of maize streak virus in cereals, but is required for invasion of mesophyll cells. J. Gen. Virol. 86, 797–801 (2005).
References 46 and 50 show that geminiviruses impaired for Rep–RBR interactions cause fewer symptoms and display a restricted tissue tropism.
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- Dual interaction of a geminivirus replication accessory factor with a viral replication protein and a plant cell cycle regulator. Virology 279, 570–576 (2001). , , &
- Influence of retinoblastoma-related gene silencing on the initiation of DNA replication by African cassava mosaic virus Rep in cells of mature leaves in Nicotiana benthamiana plants. Virol. J. 8, 561 (2011). , , , &
- A NAC domain protein interacts with tomato leaf curl virus replication accessory protein and enhances viral replication. Plant Cell 17, 311–325 (2005). et al.
- Host DNA replication is induced by geminivirus infection of differentiated plant cells. Plant Cell 14, 2995–3007 (2002). , &
- Chromosome condensation induced by geminivirus infection of mature plant cells. J. Cell Sci. 113, 1149–1160 (2000). , , &
- Cotton leaf curl disease, a multicomponent begomovirus complex. Mol. Plant Pathol. 4, 427–434 (2003).
- Altered cell shapes, hyperplasia, and secondary growth in Arabidopsis caused by beet curly top geminivirus infection. Mol. Cells 17, 117–124 (2004). et al.
- RKP, a RING finger E3 ligase induced by BSCTV C4 protein, affects geminivirus infection by regulation of the plant cell cycle. Plant J. 57, 905–917 (2009).
This paper shows that a viral C4 protein can cause plant cell proliferation by inducing the synthesis of a host RING finger protein that targets host cyclin kinase inhibitors for degradation. These results establish that geminiviruses use multiple mechanisms to alter plant cell cycle controls.
- βC1, the pathogenicity factor of TYLCCNV, interacts with AS1 to alter leaf development and suppress selective jasmonic acid responses. Genes Dev. 22, 2564–2577 (2008). et al.
- The geminivirus nuclear shuttle protein is a virulence factor that suppresses transmembrane receptor kinase activity. Genes Dev. 18, 2545–2556 (2004).
This paper shows that a geminivirus NSP interacts with and inhibits a small family of plant receptor kinases to suppress the host defence response.
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- Conserved threonine residues within the A-loop of the receptor NIK differentially regulate the kinase function required for antiviral signaling. PLoS ONE 4, e5781 (2009). , , , &
- The ribosomal protein L10/QM-like protein is a component of the NIK-mediated antiviral signaling. Virology 380, 165–169 (2008). , , &
- Regulated nuclear trafficking of rpL10A mediated by NIK1 represents a defense strategy of plant cells against virus. PLoS Pathog. 4, e1000247 (2008). et al.
- NSP-interacting kinase, NIK: a transducer of plant defence signalling. J. Exp. Bot. 61, 3839–3845 (2010). , , &
- Geminivirus infection up-regulates the expression of two Arabidopsis protein kinases related to yeast SNF1- and mammalian AMPK-activating kinases. Plant Physiol. 142, 1642–1655 (2006). &
- Arabidopsis protein kinases GRIK1 and GRIK2 specifically activate SnRK1 by phosphorylating its activation loop. Plant Physiol. 150, 996–1005 (2009). , &
- Geminivirus AL2 and L2 proteins interact with and inactivate SNF1 kinase. Plant Cell 15, 1034–1048 (2003). , , &
- Tomato SlSnRK1 protein interacts with and phosphorylates betaC1, a pathogenesis protein encoded by a geminivirus beta-satellite. Plant Physiol. 157, 1394–1406 (2011). et al.
- Geminivirus pathogenicity protein C4 interacts with Arabidopsis thaliana shaggy-related protein kinase AtSKη, a component of the brassinosteroid signalling pathway. Virology 362, 428–440 (2007). , , &
- A novel shaggy-like kinase interacts with the tomato leaf curl virus pathogenicity determinant C4 protein. Plant Mol. Biol. 71, 25–38 (2009). , , &
- Identification of host genes involved in geminivirus infection using a reverse genetics approach. PLoS ONE 6, e22383 (2011). , , &
- Geminivirus C4 protein alters Arabidopsis development. Protoplasma 239, 95–110 (2010). &
- Up-regulation of LSB1/GDU3 affects geminivirus infection by activating the salicylic acid pathway. Plant J. 62, 12–23 (2010). et al.
- Characterization of geminivirus resistance in an accession of Capsicum chinense Jacq. Mol. Plant Microbe Interact. 24, 172–182 (2011). &
- Geminiviruses subvert ubiquitination by altering CSN-mediated derubylation of SCF E3 ligase complexes and inhibit jasmonate signaling in Arabidopsis thaliana. Plant Cell 23, 1014–1032 (2011).
The paper describes the interaction of a geminivirus C2 protein with a host hub protein, leading to changes in several plant hormone signalling pathways.
- Expression of geminiviral AC2 RNA silencing suppressor changes sugar and jasmonate responsive gene expression in transgenic tobacco plants. BMC Plant Biol. 12, 204 (2012). , &
- The interaction between geminivirus pathogenicity proteins and adenosine kinase leads to increased expression of primary cytokinin-responsive genes. Virology 402, 238–247 (2010). , &
- Adenosine kinase is inactivated by geminivirus AL2 and L2 proteins. Plant Cell 15, 3020–3032 (2003). , , , &
- The nuclear shuttle protein of tomato leaf curl New Delhi virus is a pathogenicity determinant. J. Virol. 79, 4434–4439 (2005). , , , &
- Comparison of phenotypes produced in response to transient expression of genes encoded by four distinct begomoviruses in Nicotiana benthamiana and their correlation with the levels of developmental miRNAs. Virol. J. 8, 238 (2011). , , , &
- Functional analysis of gene-silencing suppressors from Tomato yellow leaf curl disease viruses. Mol. Plant Microbe Interact. 25, 1294–1306 (2012). , , &
- Geminivirus-induced gene silencing of the tobacco retinoblastoma-related gene results in cell death and altered development. Plant Mol. Biol. 65, 163–175 (2007). , , &
- The hypersensitive response induced by the V2 protein of a monopartite begomovirus is countered by the C2 protein. Mol. Plant Pathol. 11, 245–254 (2010). , , , &
- Suppression of RNA silencing by a geminivirus nuclear protein, AC2, correlates with transactivation of host genes. J. Virol. 79, 2517–2527 (2005). et al.
- Ubiquitination during plant immune signaling. Plant Physiol. 160, 15–27 (2012). , &
- SUMO, a heavyweight player in plant abiotic stress responses. Cell. Mol. Life Sci. 69, 3269–3283 (2012). , , &
- Ubiquitin and plant viruses, let's play together! Plant Physiol. 160, 72–82 (2012). &
- BSCTV C2 attenuates the degradation of SAMDC1 to suppress DNA methylation-mediated gene silencing in Arabidopsis. Plant Cell 23, 273–288 (2011). et al.
- Interaction with a host ubiquitin-conjugating enzyme is required for the pathogenicity of a geminiviral DNA β satellite. Mol. Plant Microbe Interact. 22, 737–746 (2009). et al.
- Perturbation of the ubiquitin system causes leaf curling, vascular tissue alterations and necrotic lesions in a higher plant. EMBO J. 9, 4543–4549 (1990). , , &
- Clink, a nanovirus-encoded protein, binds both pRB and SKP1. J. Virol. 74, 2967–2972 (2000). et al.
- Interaction between a geminivirus replication protein and the plant sumoylation system. J. Virol. 78, 2758–2769 (2004). , , &
- Interaction between geminivirus replication protein and the SUMO-conjugating enzyme is required for viral infection. J. Virol. 85, 9789–9800 (2011). et al.
- Four plant Dicers mediate viral small RNA biogenesis and DNA virus induced silencing. Nucleic Acids Res. 34, 6233–6246 (2006). et al.
- Arabidopsis RNA-dependent RNA polymerases and dicer-like proteins in antiviral defense and small interfering RNA biogenesis during Turnip mosaic virus infection. Plant Cell 22, 481–496 (2010). et al.
- The 21-nucleotide, but not 22-nucleotide, viral secondary small interfering RNAs direct potent antiviral defense by two cooperative Argonautes in Arabidopsis thaliana. Plant Cell 23, 1625–1638 (2011). et al.
- Molecular characterization of geminivirus-derived small RNAs in different plant species. Nucleic Acids Res. 34, 462–471 (2006). et al.
- RNA silencing against geminivirus: complementary action of posttranscriptional gene silencing and transcriptional gene silencing in host recovery. J. Virol. 83, 1332–1340 (2009). , &
- Characterization of small interfering RNAs derived from the geminivirus/βsatellite complex using deep sequencing. PLoS ONE 6, e16928 (2011). et al.
- Primary and secondary siRNAs in geminivirus-induced gene silencing. PLoS Pathog. 8, e1002941 (2012). et al.
- DNA methylation inhibits propagation of tomato golden mosaic virus DNA in transfected protoplasts. Plant Mol. Biol. 18, 703–712 (1992). et al.
- Conformation-selective methylation of geminivirus DNA. J. Virol. 85, 12001–12012 (2011).
This paper uses two-dimensional electrophoresis to assess viral DNA methylation, showing that most methylation occurs on non-productive, linear products. Circular viral DNA, which is the propagated form, has minimal methylation, suggesting that geminviruses escape TGS by replication.
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- Adenosine kinase inhibition and suppression of RNA silencing by geminivirus AL2 and L2 proteins. J. Virol. 79, 7410–7418 (2005). , , , &
- Suppression of methylation-mediated transcriptional gene silencing by βC1–SAHH protein interaction during geminivirus-betasatellite infection. PLoS Pathog. 7, e1002329 (2011). et al.
- Geminivirus Rep protein interferes with the plant DNA methylation machinery and suppresses transcriptional gene silencing. New Phytol. 199, 464–475 (2013). et al.
- Recovery from Cucurbit leaf crumple virus (family Geminiviridae, genus Begomovirus) infection is an adaptive antiviral response associated with changes in viral small RNAs. Phytopath. 98, 1029–1037 (2008). , , &
- Geminivirus VIGS of endogenous genes requires SGS2/SDE1 and SGS3 and defines a new branch in the genetic pathway for silencing in plants. Plant J. 38, 1004–1014 (2004).
References 94 and 107 show that an RDR participates in host defence against geminiviruses and that PTGS affects the levels of wild-type viral DNA.
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- Structural and genetic requirements for the biogenesis of tobacco rattle virus-derived small interfering RNAs. J. Virol. 82, 5167–5177 (2008). et al.
- Gene silencing in Arabidopsis spreads from the root to the shoot, through a gating barrier, by template-dependent, nonvascular, cell-to-cell movement. Plant Physiol. 159, 984–1000. , &
- Cell-to-cell and long-distance siRNA movement in plants: mechanisms and biological implications. Curr. Opin. Plant Biol. 14, 580–587 (2011). &
- dsRNA with 5′ overhangs contributes to endogenous and antiviral RNA silencing pathways in plants. EMBO J. 28, 545–555 (2009). &
- Interaction with host SGS3 is required for suppression of RNA silencing by tomato yellow leaf curl virus V2 protein. Proc. Natl Acad. Sci. USA 105, 157–161 (2008). et al.
- Suppressors of RNA silencing encoded by the components of the cotton leaf curl begomovirus-betasatellite complex. Mol. Plant Microbe Interact. 24, 973–983 (2011).
References 40, 112 and 113 show that geminivirus VSRs target both TGS and PTGS pathways and that as many as four different viral proteins in a geminivirus complex can show VSR activity.
- V2 protein encoded by tomato yellow leaf curl China virus is an RNA silencing suppressor. Virus Res. 163, 51–58 (2012). , , &
- The tomato yellow leaf curl virus resistance genes Ty-1 and Ty-3 are allelic and code for DFDGD-class RNA-dependent RNA polymerases. PLoS Genet. 9, e1003399 (2013).
This study shows that TY1, the first geminivirus resistance gene to be identified, has homology to an uncharacterized RDR class.
- Enhanced viral intergenic region-specific short interfering RNA accumulation and DNA methylation correlates with resistance against a geminivirus. Mol. Plant Microbe Interact. 24, 1189–1197 (2011). &
- Unique functionality of 22-nt miRNAs in triggering RDR6-dependent siRNA biogenesis from target transcripts in Arabidopsis. Nature Struct. Mol. Biol. 17, 997–1003 (2010). et al.
- Cytoplasmic Arabidopsis AGO7 accumulates in membrane-associated siRNA bodies and is required for ta-siRNA biogenesis. EMBO J. 31, 1704–1713 (2012). et al.
- NERD, a plant-specific GW protein, defines an additional RNAi-dependent chromatin-based pathway in Arabidopsis. Mol. Cell 48, 121–132 (2012). et al.
- Genome-wide identification of viral and host transcripts targeted by viral siRNAs in Vitis vinifera. Mol. Plant Pathol. 14, 30–43 (2013). , , &
- Geminiviruses: models for plant DNA replication, transcription, and cell cycle regulation. Crit. Rev. Biochem. Mol. Biol. 35, 105–140 (2000). , , , &
- Functional characterization of coat protein and V2 involved in cell to cell movement of cotton leaf curl Kokhran virus-Dabawali. PLoS ONE 6, e26929 (2011). , , &
- Splicing features in maize streak virus virion- and complementary-sense gene expression. Plant J. 12, 1285–1297 (1997). , , , &
- Transactivation of geminivirus AR1 and BR1 gene expression by the viral AL2 gene product occurs at the level of transcription. Plant Cell 4, 1321–1331 (1992). &
- Post-transcriptional gene silencing suppressor activity of two non-pathogenic alphasatellites associated with a begomovirus. Virology 405, 300–308 (2010). , , , &
- The induction of stromule formation by a plant DNA-virus in epidermal leaf tissues suggests a novel intra- and intercellular macromolecular trafficking route. Front. Plant Sci. 3, 291 (2012). , &
- Functional analysis of proteins involved in movement of the monopartite begomovirus, tomato yellow leaf curl virus. Virology 291, 110–125 (2001). et al.
- Histone H3 interacts and colocalizes with the nuclear shuttle protein and the movement protein of a geminivirus. J. Virol. 85, 11821–11832 (2011). et al.
- Interaction of the movement protein NSP and the Arabidopsis acetyltransferase AtNSI is necessary for cabbage leaf curl geminivirus infection and pathogenicity. J. Virol. 78, 11161–11171 (2004). &
- The geminivirus nuclear shuttle protein NSP inhibits the activity of AtNSI, a vascular-expressed Arabidopsis acetyltransferase regulated with the sink-to-source transition. Plant Physiol. 140, 1317–1330 (2006). , &
- The geminivirus BL1 movement protein is associated with endoplasmic reticulum-derived tubules in developing phloem cells. J. Virol. 71, 3726–3733 (1997). , , &
- A novel nucleocytoplasmic traffic GTPase identified as a functional target of the bipartite geminivirus nuclear shuttle protein. Plant J. 55, 869–880 (2008). et al.
- NSP-interacting GTPase: a cytosolic protein as cofactor for nuclear shuttle proteins. Plant Signal Behav. 3, 752–754 (2008). , , &
- A plastid-targeted heat shock cognate 70kDa protein interacts with the Abutilon mosaic virus movement protein. Virology 401, 6–17 (2010). , , , &
- Arabidopsis synaptotagmin SYTA regulates endocytosis and virus movement protein cell-to-cell transport. Proc. Natl Acad. Sci. USA 107, 2491–2496 (2010). &
- Rate of tomato yellow leaf curl virus translocation in the circulative transmission pathway of its vector, the whitefly Bemisia tabaci. Phytopathology 91, 188–196 (2001). , &
- Arsenophonus GroEL interacts with CLCuV and is localized in midgut and salivary gland of whitefly B. tabaci. PLoS ONE 7, e42168 (2012). , , , &
- Begomovirus coat protein interacts with a small heat-shock protein of its transmission vector (Bemisia tabaci). Insect Mol. Biol. 18, 693–703 (2009). &
- The transmission efficiency of tomato yellow leaf curl virus by the whitefly Bemisia tabaci is correlated with the presence of a specific symbiotic bacterium species. J. Virol. 84, 9310–9317 (2010).
This paper demonstrates that the interactions of geminivirus proteins with proteins produced by endosymbiotic bacteria play a part in vector transmission.
- Global analysis of the transcriptional response of whitefly to tomato yellow leaf curl China virus reveals the relationship of coevolved adaptations. J. Virol. 85, 3330–3340 (2011). et al.
- Supplementary information S1 (table) (387 KB)