The discovery of the first non-cellular infectious agent, later determined to be tobacco mosaic virus, paved the way for the field of virology. In the ensuing decades, research focused on discovering and eliminating viral threats to plant and animal health. However, recent conceptual and methodological revolutions have made it clear that viruses are not merely agents of destruction but essential components of global ecosystems. As plants make up over 80% of the biomass on Earth, plant viruses likely have a larger impact on ecosystem stability and function than viruses of other kingdoms. Besides preventing overgrowth of genetically homogeneous plant populations such as crop plants, some plant viruses might also promote the adaptation of their hosts to changing environments. However, estimates of the extent and frequencies of such mutualistic interactions remain controversial. In this Review, we focus on the origins of plant viruses and the evolution of interactions between these viruses and both their hosts and transmission vectors. We also identify currently unknown aspects of plant virus ecology and evolution that are of practical importance and that should be resolvable in the near future through viral metagenomics.
This is a preview of subscription content
Subscribe to Nature+
Get immediate online access to the entire Nature family of 50+ journals
Subscribe to Journal
Get full journal access for 1 year
only $8.25 per issue
All prices are NET prices.
VAT will be added later in the checkout.
Tax calculation will be finalised during checkout.
Get time limited or full article access on ReadCube.
All prices are NET prices.
Edwards, R. A. & Rohwer, F. Viral metagenomics. Nat. Rev. Microbiol. 3, 504–510 (2005).
Greninger, A. L. A decade of RNA virus metagenomics is (not) enough. Virus Res. 244, 218–229 (2018).
Koonin, E. V. & Dolja, V. V. Metaviromics: a tectonic shift in understanding virus evolution. Virus Res. 246, A1–A3 (2018). This review highlights how our understanding of virology is changing as a consequence of advances in metagenomics.
Suttle, C. A. Viruses: unlocking the greatest biodiversity on Earth. Genome 56, 542–544 (2013).
Gregory, A. C. et al. Marine DNA viral macro- and microdiversity from pole to pole. Cell 177, 1109–1123 (2019). This study provides the most comprehensive inventory of marine viral diversity to date.
Morris, J. L. et al. The timescale of early land plant evolution. Proc. Natl Acad. Sci. USA 115, E2274–E2283 (2018).
Mushegian, A., Shipunov, A. & Elena, S. F. Changes in the composition of the RNA virome mark evolutionary transitions in green plants. BMC Biol. 14, 68 (2016).
Bernardo, P. et al. Geometagenomics illuminates the impact of agriculture on the distribution and prevalence of plant viruses at the ecosystem scale. ISME J. 12, 173–184 (2018). This article is a viromics study of agro-ecological interfaces that demonstrates the impacts of agriculture on the diversity and prevalence of plant-associated viruses.
Muthukumar, V. et al. Non-cultivated plants of the Tallgrass Prairie Preserve of northeastern Oklahoma frequently contain virus-like sequences in particulate fractions. Virus Res. 141, 169–173 (2009).
Koonin, E. V., Dolja, V. V. & Krupovic, M. Origins and evolution of viruses of eukaryotes: the ultimate modularity. Virology 479–480, 2–25 (2015).
Nasir, A. & Caetano-Anolles, G. A phylogenomic data-driven exploration of viral origins and evolution. Sci. Adv. 1, e1500527 (2015).
Dolja, V. V. & Koonin, E. V. Common origins and host-dependent diversity of plant and animal viromes. Curr. Opin. Virol. 1, 322–331 (2011).
Wolf, Y. I. et al. Origins and evolution of the global RNA virome. mBio 9, e02329–18 (2018). This study yields new insights relating to the evolution of RNA viruses in light of novel RNA viruses that have recently been discovered using metagenomics techniques.
Volk, M., Gibbs, A. J. & Suttle, C. A. Metagenomes of a freshwater charavirus from British Columbia provide a window into ancient lineages of viruses. Viruses 11, 299 (2019).
Krupovic, M. & Koonin, E. V. Multiple origins of viral capsid proteins from cellular ancestors. Proc. Natl Acad. Sci. USA 114, E2401–E2410 (2017).
Dolja, V. V. & Koonin, E. V. Metagenomics reshapes the concepts of RNA virus evolution by revealing extensive horizontal virus transfer. Virus Res. 244, 36–52 (2018).
Roossinck, M. J. Evolutionary and ecological links between plant and fungal viruses. New Phytol. 221, 86–92 (2019). This review describes our current knowledge of mycoviruses and their evolutionary relationships with plant viruses.
Vieira, P. & Nemchinov, L. G. A novel species of RNA virus associated with root lesion nematode Pratylenchus penetrans. J. Gen. Virol. 100, 704–708 (2019).
Hollings, M. Viruses associated with a die-back disease of cultivated mushroom. Nature 196, 962–965 (1962).
Pearson, M. N., Beever, R. E., Boine, B. & Arthur, K. Mycoviruses of filamentous fungi and their relevance to plant pathology. Mol. Plant Pathol. 10, 115–128 (2009).
Mu, F. et al. Virome characterization of a collection of S. sclerotiorum from Australia. Front. Microbiol. 8, 2540 (2017).
Marzano, S. L. & Domier, L. L. Novel mycoviruses discovered from metatranscriptomics survey of soybean phyllosphere phytobiomes. Virus Res. 213, 332–342 (2016).
Gilbert, K., Holcomb, E. E., Allscheid, R. L. & Carrington, J. Discovery of new mycoviral genomes within publicly available fungal transcriptomic datasets. Preprint at bioRxiv https://www.biorxiv.org/content/10.1101/510404v1 (2019).
Marzano, S. L. et al. Identification of diverse mycoviruses through metatranscriptomics characterization of the viromes of five major fungal plant pathogens. J. Virol. 90, 6846–6863 (2016).
Frank, A. C. & Wolfe, K. H. Evolutionary capture of viral and plasmid DNA by yeast nuclear chromosomes. Eukaryot. Cell 8, 1521–1531 (2009).
Taylor, D. J. & Bruenn, J. The evolution of novel fungal genes from non-retroviral RNA viruses. BMC Biol. 7, 88 (2009).
Hillman, B. I. & Cai, G. The family Narnaviridae: simplest of RNA viruses. Adv. Virus Res. 86, 149–176 (2013).
Nerva, L. et al. Biological and molecular characterization of Chenopodium quinoa mitovirus 1 reveals a distinct small RNA response compared to those of cytoplasmic RNA viruses. J. Virol. 93, e01998–18 (2019).
Rastgou, M. et al. Molecular characterization of the plant virus genus Ourmiavirus and evidence of inter-kingdom reassortment of viral genome segments as its possible route of origin. J. Gen. Virol. 90, 2525–2535 (2009).
Nerva, L., Varese, G. C., Falk, B. W. & Turina, M. Mycoviruses of an endophytic fungus can replicate in plant cells: evolutionary implications. Sci. Rep. 7, 1908 (2017).
Andika, I. B. et al. Phytopathogenic fungus hosts a plant virus: a naturally occurring cross-kingdom viral infection. Proc. Natl Acad. Sci. USA 114, 12267–12272 (2017).
Mascia, T. et al. Infection of Colletotrichum acutatum and Phytophthora infestans by taxonomically different plant viruses. Eur. J. Plant Pathol. 153, 1001–1017 (2018).
Malloch, D. W., Pirozynski, K. A. & Raven, P. H. Ecological and evolutionary significance of mycorrhizal symbioses in vascular plants (a review). Proc. Natl Acad. Sci. USA 77, 2113–2118 (1980).
Bonfante, P. & Genre, A. Mechanisms underlying beneficial plant–fungus interactions in mycorrhizal symbiosis. Nat. Commun. 1, 48 (2010).
Redman, R. S., Sheehan, K. B., Stout, R. G., Rodriguez, R. J. & Henson, J. M. Thermotolerance generated by plant/fungal symbiosis. Science 298, 1581 (2002).
Rodriguez, R. & Redman, R. More than 400 million years of evolution and some plants still can’t make it on their own: plant stress tolerance via fungal symbiosis. J. Exp. Bot. 59, 1109–1114 (2008).
Li, C. X. et al. Unprecedented genomic diversity of RNA viruses in arthropods reveals the ancestry of negative-sense RNA viruses. eLife 4, e05378 (2015).
Shi, M. et al. Redefining the invertebrate RNA virosphere. Nature 540, 539–543 (2016). This study identified ~1,400 RNA viruses using metatranscriptomics, which tremendously expands our current knowledge of RNA virus diversity.
Dasgupta, R., Garcia, B. H. 2nd & Goodman, R. M. Systemic spread of an RNA insect virus in plants expressing plant viral movement protein genes. Proc. Natl Acad. Sci. USA 98, 4910–4915 (2001).
Gibbs, A. J., Wood, J., Garcia-Arenal, F., Ohshima, K. & Armstrong, J. S. Tobamoviruses have probably co-diverged with their eudicotyledonous hosts for at least 110 million years. Virus Evol. 1, vev019 (2015).
Stobbe, A. H., Melcher, U., Palmer, M. W., Roossinck, M. J. & Shen, G. Co-divergence and host-switching in the evolution of tobamoviruses. J. Gen. Virol. 93, 408–418 (2012).
Gibbs, A. How ancient are the tobamoviruses? Intervirology 14, 101–108 (1980).
Varsani, A., Lefeuvre, P., Roumagnac, P. & Martin, D. Notes on recombination and reassortment in multipartite/segmented viruses. Curr. Opin. Virol. 33, 156–166 (2018).
Briddon, R. W. et al. Alphasatellitidae: a new family with two subfamilies for the classification of geminivirus- and nanovirus-associated alphasatellites. Arch. Virol. 163, 2587–2600 (2018).
Gnanasekaran, P. & Chakraborty, S. Biology of viral satellites and their role in pathogenesis. Curr. Opin. Virol. 33, 96–105 (2018).
Lucia-Sanz, A. & Manrubia, S. Multipartite viruses: adaptive trick or evolutionary treat? NPJ Syst. Biol. Appl. 3, 34 (2017).
Escriu, F., Fraile, A. & Garcia-Arenal, F. Constraints to genetic exchange support gene coadaptation in a tripartite RNA virus. PLOS Pathog. 3, e8 (2007).
Sicard, A. et al. Gene copy number is differentially regulated in a multipartite virus. Nat. Commun. 4, 2248 (2013).
Wu, B., Zwart, M. P., Sanchez-Navarro, J. A. & Elena, S. F. Within-host evolution of segments ratio for the tripartite genome of alfalfa mosaic virus. Sci. Rep. 7, 5004 (2017).
Benitez-Alfonso, Y., Faulkner, C., Ritzenthaler, C. & Maule, A. J. Plasmodesmata: gateways to local and systemic virus infection. Mol. Plant Microbe Interact. 23, 1403–1412 (2010).
Lucas, W. J. Plant viral movement proteins: agents for cell-to-cell trafficking of viral genomes. Virology 344, 169–184 (2006).
Sicard, A., Michalakis, Y., Gutierrez, S. & Blanc, S. The strange lifestyle of multipartite viruses. PLOS Pathog. 12, e1005819 (2016). This article reviews the ‘lifestyles’ of multipartite viruses, their peculiarities and the gaps in our understanding of their biology.
Gilmer, D., Ratti, C. & Michel, F. Long-distance movement of helical multipartite phytoviruses: keep connected or die? Curr. Opin. Virol. 33, 120–128 (2018).
Fauquet, C. M., Mayo, M. A., Maniloff, J., Desselberger, U. & Ball, L. A. Virus Taxonomy: VIII th Report of the International Committee on Taxonomy of Viruses (Academic Press, 2005).
Liu, S. et al. Fungal DNA virus infects a mycophagous insect and utilizes it as a transmission vector. Proc. Natl Acad. Sci. USA 113, 12803–12808 (2016).
Sacristan, S., Diaz, M., Fraile, A. & Garcia-Arenal, F. Contact transmission of tobacco mosaic virus: a quantitative analysis of parameters relevant for virus evolution. J. Virol. 85, 4974–4981 (2011).
Jones, R. A. C. Plant and insect viruses in managed and natural environments: novel and neglected transmission pathways. Adv. Virus Res. 101, 149–187 (2018).
Hamelin, F. M., Allen, L. J., Prendeville, H. R., Hajimorad, M. R. & Jeger, M. J. The evolution of plant virus transmission pathways. J. Theor. Biol. 396, 75–89 (2016).
Hamelin, F. M. et al. The evolution of parasitic and mutualistic plant–virus symbioses through transmission–virulence trade-offs. Virus Res. 241, 77–87 (2017).
Nault, L. R. Arthropod transmission of plant viruses: a new synthesis. Ann. Entomol. Soc. Am. 90, 521–541 (1997).
Tamada, T. & Kondo, H. Biological and genetic diversity of plasmodiophorid-transmitted viruses and their vectors. J. Gen. Plant Pathol. 79, 307–320 (2013).
Hogenhout, S. A., Ammar el, D., Whitfield, A. E. & Redinbaugh, M. G. Insect vector interactions with persistently transmitted viruses. Annu. Rev. Phytopathol. 46, 327–359 (2008).
Dader, B. et al. Insect transmission of plant viruses: multilayered interactions optimize viral propagation. Insect Sci. 24, 929–946 (2017).
Uzest, M. et al. A protein key to plant virus transmission at the tip of the insect vector stylet. Proc. Natl Acad. Sci. USA 104, 17959–17964 (2007).
Ammar, E.-D., Tsai, C. W., Whitfield, A. E., Redinbaugh, M. G. & Hogenhout, S. A. Cellular and molecular aspects of rhabdovirus interactions with insect and plant hosts. Annu. Rev. Entomol. 54, 447–468 (2009).
Brault, V., Herrbach, E. & Reinbold, C. Electron microscopy studies on luteovirid transmission by aphids. Micron 38, 302–312 (2007).
Blanc, S. & Michalakis, Y. Manipulation of hosts and vectors by plant viruses and impact of the environment. Curr. Opin. Insect Sci. 16, 36–43 (2016).
Safari, M., Ferrari, M. J. & Roossinck, M. J. Manipulation of aphid behavior by a persistent plant virus. J. Virol. 93, e01781–18 (2019).
Mauck, K., Bosque-Perez, N. A., Eigenbrode, S. D., De Moraes, C. M. & Mescher, M. C. Transmission mechanisms shape pathogen effects on host–vector interactions: evidence from plant viruses. Funct. Ecol. 26, 1162–1175 (2012).
Gallitelli, D. The ecology of Cucumber mosaic virus and sustainable agriculture. Virus Res. 71, 9–21 (2000).
Power, A. G. & Flecker, A. S. in Infectious Disease Ecology: The Effects of Ecosystems on Disease and of Disease on Ecosystems Ch. 2 (eds Ostfeld, R. S., Keesing, F. & Eviner, V. T.) (Princeton Univ. Press, 2010).
Anderson, P. K. et al. Emerging infectious diseases of plants: pathogen pollution, climate change and agrotechnology drivers. Trends Ecol. Evol. 19, 535–544 (2004).
Gilbertson, R. L., Batuman, O., Webster, C. G. & Adkins, S. Role of the insect supervectors Bemisia tabaci and Frankliniella occidentalis in the emergence and global spread of plant viruses. Annu. Rev. Virol. 2, 67–93 (2015).
Fereres, A. Insect vectors as drivers of plant virus emergence. Curr. Opin. Virol. 10, 42–46 (2015).
Simmonds, P., Aiewsakun, P. & Katzourakis, A. Prisoners of war — host adaptation and its constraints on virus evolution. Nat. Rev. Microbiol. 17, 321–328 (2019). This study provides both a summary of viral evolutionary rates and a tentative framework to accommodate potentially conflicting long-term and short-term evolutionary rate inferences.
Stroud, J. T. & Losos, J. B. Ecological opportunity and adaptive radiation. Annu. Rev. Ecol. Evol. Syst. 47, 507–532 (2016).
Scholthof, K. B. et al. Top 10 plant viruses in molecular plant pathology. Mol. Plant Pathol. 12, 938–954 (2011).
Jacquemond, M. Cucumber mosaic virus. Adv. Virus Res. 84, 439–504 (2012).
Dietzgen, R. G., Mann, K. S. & Johnson, K. N. Plant virus–insect vector interactions: current and potential future research directions. Viruses 8, E303 (2016).
Bragard, C. et al. Status and prospects of plant virus control through interference with vector transmission. Annu. Rev. Phytopathol. 51, 177–201 (2013).
Eastop, V. F. in Aphids As Virus Vectors (eds Harris, K. F. & Maramorosch, K.) 3–62 (Academic Press, 1977).
Li, C., Cox-Foster, D., Gray, S. M. & Gildow, F. Vector specificity of barley yellow dwarf virus (BYDV) transmission: identification of potential cellular receptors binding BYDV-MAV in the aphid, Sitobion avenae. Virology 286, 125–133 (2001).
Bedhomme, S., Hillung, J. & Elena, S. F. Emerging viruses: why they are not jacks of all trades? Curr. Opin. Virol. 10, 1–6 (2015).
Elena, S. F. Local adaptation of plant viruses: lessons from experimental evolution. Mol. Ecol. 26, 1711–1719 (2017).
Remold, S. Understanding specialism when the Jack of all trades can be the master of all. Proc. Biol. Sci. 279, 4861–4869 (2012).
Kawecki, T. J. Accumulation of deleterious mutations and the evolutionary cost of being a generalist. Am. Nat. 144, 833–838 (1994).
Cooper, I. & Jones, R. A. Wild plants and viruses: under-investigated ecosystems. Adv. Virus Res. 67, 1–47 (2006).
Rodriguez-Nevado, C., Montes, N. & Pagan, I. Ecological factors affecting infection risk and population genetic diversity of a novel potyvirus in its native wild ecosystem. Front. Plant Sci. 8, 1958 (2017).
Susi, H., Filloux, D., Frilander, M. J., Roumagnac, P. & Laine, A. L. Diverse and variable virus communities in wild plant populations revealed by metagenomic tools. PeerJ 7, e6140 (2019).
Elena, S. F., Fraile, A. & García-Arenal, F. Evolution and emergence of plant viruses. Adv. Virus Res. 88, 161–191 (2014).
McLeish, M. J., Fraile, A. & Garcia-Arenal, F. Ecological complexity in plant virus host range evolution. Adv. Virus Res. 101, 293–339 (2018). This article presents a comprehensive review of plant virus ecology.
Cuevas, J. M., Willemsen, A., Hillung, J., Zwart, M. P. & Elena, S. F. Temporal dynamics of intrahost molecular evolution for a plant RNA virus. Mol. Biol. Evol. 32, 1132–1147 (2015).
Minicka, J., Rymelska, N., Elena, S. F., Czerwoniec, A. & Hasiów-Jaroszewska, B. Molecular evolution of Pepino mosaic virus during long-term passaging in different hosts and its impact on virus virulence. Ann. Appl. Biol. 166, 389–401 (2015).
Ciota, A. T. et al. Experimental passage of St. Louis encephalitis virus in vivo in mosquitoes and chickens reveals evolutionarily significant virus characteristics. PLOS ONE 4, e7876 (2009).
Greene, I. P. et al. Effect of alternating passage on adaptation of sindbis virus to vertebrate and invertebrate cells. J. Virol. 79, 14253–14260 (2005).
Turner, P. E. & Elena, S. F. Cost of host radiation in an RNA virus. Genetics 156, 1465–1470 (2000).
Bedhomme, S., Lafforgue, G. & Elena, S. F. Multihost experimental evolution of a plant RNA virus reveals local adaptation and host-specific mutations. Mol. Biol. Evol. 29, 1481–1492 (2012). This study provides experimental evidence for the possible existence of no-cost generalists in plant viruses.
Hillung, J., Cuevas, J. M., Valverde, S. & Elena, S. F. Experimental evolution of an emerging plant virus in host genotypes that differ in their susceptibility to infection. Evolution 68, 2467–2480 (2014).
Lalic, J., Agudelo-Romero, P., Carrasco, P. & Elena, S. F. Adaptation of tobacco etch potyvirus to a susceptible ecotype of Arabidopsis thaliana capacitates it for systemic infection of resistant ecotypes. Phil. Trans. R. Soc. B 365, 1997–2007 (2010).
Charron, C. et al. Natural variation and functional analyses provide evidence for co-evolution between plant eIF4E and potyviral VPg. Plant J. 54, 56–68 (2008).
Jenner, C. E., Wang, X., Ponz, F. & Walsh, J. A. A fitness cost for Turnip mosaic virus to overcome host resistance. Virus Res. 86, 1–6 (2002).
Hillung, J., Garcia-Garcia, F., Dopazo, J., Cuevas, J. M. & Elena, S. F. The transcriptomics of an experimentally evolved plant–virus interaction. Sci. Rep. 6, 24901 (2016).
McCallum, E. J., Anjanappa, R. B. & Gruissem, W. Tackling agriculturally relevant diseases in the staple crop cassava (Manihot esculenta). Curr. Opin. Plant Biol. 38, 50–58 (2017).
Almeida, R. P. et al. Ecology and management of grapevine leafroll disease. Front. Microbiol. 4, 94 (2013).
Walls, J., Rajotte, E. & Rosa, C. The past, present, and future of barley yellow dwarf management. Agriculture 9, 23 (2019).
Pinel-Galzi, A., Traore, O., Sere, Y., Hebrard, E. & Fargette, D. The biogeography of viral emergence: rice yellow mottle virus as a case study. Curr. Opin. Virol. 10, 7–13 (2015).
Fargette, D. et al. Molecular ecology and emergence of tropical plant viruses. Annu. Rev. Phytopathol. 44, 235–260 (2006).
Jones, R. A. Plant virus emergence and evolution: origins, new encounter scenarios, factors driving emergence, effects of changing world conditions, and prospects for control. Virus Res. 141, 113–130 (2009). This article reviews various anthropogenic factors associated with the emergence of plant viruses and the ongoing challenges in mitigating emerging disease threats.
Pagan, I. et al. Effect of biodiversity changes in disease risk: exploring disease emergence in a plant–virus system. PLOS Pathog. 8, e1002796 (2012).
Roossinck, M. J. & Garcia-Arenal, F. Ecosystem simplification, biodiversity loss and plant virus emergence. Curr. Opin. Virol. 10, 56–62 (2015).
Rodelo-Urrego, M. et al. Landscape heterogeneity shapes host–parasite interactions and results in apparent plant–virus codivergence. Mol. Ecol. 22, 2325–2340 (2013).
Rocha, C. S. et al. Brazilian begomovirus populations are highly recombinant, rapidly evolving, and segregated based on geographical location. J. Virol. 87, 5784–5799 (2013).
Keesing, F. et al. Impacts of biodiversity on the emergence and transmission of infectious diseases. Nature 468, 647–652 (2010). This article addresses the impacts of reduced biodiversity on disease transmission.
Lima, A. T. et al. Synonymous site variation due to recombination explains higher genetic variability in begomovirus populations infecting non-cultivated hosts. J. Gen. Virol. 94, 418–431 (2013).
Thingstad, T. F. & Lignell, R. Theoretical models for the control of bacterial growth rate, abundance, diversity and carbon demand. Aquat. Microb. Ecol. 13, 19–27 (1997).
Coutinho, F. H. et al. Marine viruses discovered via metagenomics shed light on viral strategies throughout the oceans. Nat. Commun. 8, 15955 (2017).
Coutinho, F. H., Gregoracci, G. B., Walter, J. M., Thompson, C. C. & Thompson, F. L. Metagenomics sheds light on the ecology of marine microbes and their viruses. Trends Microbiol. 26, 955–965 (2018).
Mitchell, C. E. & Power, A. G. Release of invasive plants from fungal and viral pathogens. Nature 421, 625–627 (2003).
Borer, E. T., Hosseini, P. R., Seabloom, E. W. & Dobson, A. P. Pathogen-induced reversal of native dominance in a grassland community. Proc. Natl Acad. Sci. USA 104, 5473–5478 (2007).
Malmstrom, C. M., McCullough, A. J., Johnson, H. A., Newton, L. A. & Borer, E. T. Invasive annual grasses indirectly increase virus incidence in California native perennial bunchgrasses. Oecologia 145, 153–164 (2005). This article addresses the impacts of an invasive plant species on viral dynamics in native plants.
Faillace, C. A., Lorusso, N. S. & Duffy, S. Overlooking the smallest matter: viruses impact biological invasions. Ecol. Lett. 20, 524–538 (2017). This article reviews the impacts of rapidly evolving plant viruses on plant community structure within a biological invasion framework.
Cervera, H., Ambros, S., Bernet, G. P., Rodrigo, G. & Elena, S. F. Viral fitness correlates with the magnitude and direction of the perturbation induced in the host’s transcriptome: the Tobacco Etch Potyvirus-Tobacco Case Study. Mol. Biol. Evol. 35, 1599–1615 (2018).
Alizon, S., Hurford, A., Mideo, N. & Van Baalen, M. Virulence evolution and the trade-off hypothesis: history, current state of affairs and the future. J. Evol. Biol. 22, 245–259 (2009).
Anderson, R. M. & May, R. M. Coevolution of hosts and parasites. Parasitology 85, 411–426 (1982).
Doumayrou, J., Avellan, A., Froissart, R. & Michalakis, Y. An experimental test of the transmission–virulence trade-off hypothesis in a plant virus. Evolution 67, 477–486 (2013).
Froissart, R., Doumayrou, J., Vuillaume, F., Alizon, S. & Michalakis, Y. The virulence–transmission trade-off in vector-borne plant viruses: a review of (non-)existing studies. Phil. Trans. R. Soc. B 365, 1907–1918 (2010). This article reviews our current understanding of the transmission–virulence trade-off hypothesis in the context of plant viruses.
Leggett, H. C., Buckling, A., Long, G. H. & Boots, M. Generalism and the evolution of parasite virulence. Trends Ecol. Evol. 28, 592–596 (2013).
Roossinck, M. J. A new look at plant viruses and their potential beneficial roles in crops. Mol. Plant Pathol. 16, 331–333 (2015).
Roossinck, M. J. Plants, viruses and the environment: ecology and mutualism. Virology 479–480, 271–277 (2015). This review addresses the paradigm shift away from viewing viruses as antagonistic pathogens towards viewing them as possible mutualists.
Shates, T. M., Sun, P., Malmstrom, C. M., Dominguez, C. & Mauck, K. E. Addressing research needs in the field of plant virus ecology by defining knowledge gaps and developing wild dicot study systems. Front. Microbiol. 9, 3305 (2018).
Fraile, A. & Garcia-Arenal, F. The coevolution of plants and viruses: resistance and pathogenicity. Adv. Virus Res. 76, 1–32 (2010).
Calil, I. P. & Fontes, E. P. B. Plant immunity against viruses: antiviral immune receptors in focus. Ann. Bot. 119, 711–723 (2017).
Malmstrom, C. M. & Alexander, H. M. Effects of crop viruses on wild plants. Curr. Opin. Virol. 19, 30–36 (2016).
Prendeville, H. R., Ye, X., Morris, T. J. & Pilson, D. Virus infections in wild plant populations are both frequent and often unapparent. Am. J. Bot. 99, 1033–1042 (2012).
Remold, S. K. Unapparent virus infection and host fitness in three weedy grass species. J. Ecol. 90, 967–977 (2002).
Fraile, A. et al. Environmental heterogeneity and the evolution of plant-virus interactions: viruses in wild pepper populations. Virus Res. 241, 68–76 (2017).
Faure, D., Simon, J. C. & Heulin, T. Holobiont: a conceptual framework to explore the eco-evolutionary and functional implications of host–microbiota interactions in all ecosystems. New Phytol. 218, 1321–1324 (2018).
Grasis, J. A. The intra-dependence of viruses and the holobiont. Front. Immunol. 8, 1501 (2017).
Harth, J. E., Ferrari, M. J., Tooker, J. F. & Stephenson, A. G. Zucchini yellow mosaic virus infection limits establishment and severity of powdery mildew in wild populations of Cucurbita pepo. Front. Plant Sci. 9, 792 (2018).
Gibbs, A. A plant virus that partially protects its wild legume host against herbivores. Intervirology 13, 42–47 (1980).
Davis, T. S., Bosque-Perez, N. A., Foote, N. E., Magney, T. & Eigenbrode, S. D. Environmentally dependent host–pathogen and vector–pathogen interactions in the Barley yellow dwarf virus pathosystem. J. Appl. Ecol. 52, 1392–1401 (2015).
Hily, J. M., Poulicard, N., Mora, M. A., Pagan, I. & Garcia-Arenal, F. Environment and host genotype determine the outcome of a plant–virus interaction: from antagonism to mutualism. New Phytol. 209, 812–822 (2016). This study provides compelling evidence that conditional interactions of plant viruses, plant genotypes and the environment modulate the outcome of symbiosis.
Westwood, J. H. et al. A viral RNA silencing suppressor interferes with abscisic acid-mediated signalling and induces drought tolerance in Arabidopsis thaliana. Mol. Plant Pathol. 14, 158–170 (2013).
Xu, P. et al. Virus infection improves drought tolerance. New Phytol. 180, 911–921 (2008).
Prasch, C. M. & Sonnewald, U. Simultaneous application of heat, drought, and virus to Arabidopsis plants reveals significant shifts in signaling networks. Plant Physiol. 162, 1849–1866 (2013).
Berges, S. E. et al. Interactions between drought and plant genotype change epidemiological traits of cauliflower mosaic virus. Front. Plant Sci. 9, 703 (2018).
Bera, S., Fraile, A. & Garcia-Arenal, F. Analysis of fitness trade-offs in the host range expansion of an RNA virus, tobacco mild green mosaic virus. J. Virol. 92, e01268–18 (2018).
Zhang, Y. Z., Shi, M. & Holmes, E. C. Using metagenomics to characterize an expanding virosphere. Cell 172, 1168–1172 (2018).
Saunders, K., Bedford, I. D., Yahara, T. & Stanley, J. Aetiology: the earliest recorded plant virus disease. Nature 422, 831 (2003).
Lesnaw, J. A. & Ghabrial, S. A. Tulip breaking: past, present, and future. Plant Dis. 84, 1052–1060 (2000).
Ivanowski, D. Ueber die Mosaikkrankheit der Tabakspflanze. Bull. Acad. Imp. Sci. 35, 67–70 (1892).
Beijerinck, W. M. Ueber ein contagium vivum fluidum als Ursache der Fleckenkrankheit der Tabaksblatter. Verh. Kon. Akad. Wetensch. 5, 3–21 (1898).
Stanley, W. M. Isolation of a crystalline protein possessing the properties of tobacco-mosaic virus. Science 81, 644–645 (1935).
Kausche, G. A., Pfankuch, E. & Ruska, H. Die Sichtbarmachung von pflanzlichem Virus im Übermikroskop. Naturwissenschaften 27, 292–299 (1939).
Bernal, J. D. & Fankuchen, I. Structure types of protein crystals from virus-infected plants. Nature 139, 923–924 (1937).
Fraenkel-Conrat, H. The genetic code of a virus. Sci. Am. 211, 47–54 (1964).
Anandalakshmi, R. et al. A viral suppressor of gene silencing in plants. Proc. Natl Acad. Sci. USA 95, 13079–13084 (1998).
Hamilton, A. J. & Baulcombe, D. C. A species of small antisense RNA in posttranscriptional gene silencing in plants. Science 286, 950–952 (1999).
Guo, Z. et al. Identification of a new host factor required for antiviral RNAi and amplification of viral siRNAs. Plant Physiol. 176, 1587–1597 (2018).
Baltimore, D. Expression of animal virus genomes. Bacteriol. Rev. 35, 235–241 (1971).
Bolduc, B. et al. vConTACT: an iVirus tool to classify double-stranded DNA viruses that infect Archaea and Bacteria. PeerJ 5, e3243 (2017).
Mihara, T. et al. Linking virus genomes with host taxonomy. Viruses 8, 66 (2016).
Evans, G. A. Host Plant List of The Whiteflies (Aleyrodidae) of The World (USDA Animal Plant Health Inspection Service, 2007).
De Barro, P. J., Liu, S. S., Boykin, L. M. & Dinsdale, A. B. Bemisia tabaci: a statement of species status. Annu. Rev. Entomol. 56, 1–19 (2011).
Huang, Y., Niu, B., Gao, Y., Fu, L. & Li, W. CD-HIT Suite: a web server for clustering and comparing biological sequences. Bioinformatics 26, 680–682 (2010).
Katoh, K. & Standley, D. M. MAFFT multiple sequence alignment software version 7: improvements in performance and usability. Mol. Biol. Evol. 30, 772–780 (2013).
Guindon, S. et al. New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. Syst. Biol. 59, 307–321 (2010).
Clark, K., Karsch-Mizrachi, I., Lipman, D. J., Ostell, J. & Sayers, E. W. GenBank. Nucleic Acids Res. 44, D67–D72 (2016).
Ratnasingham, S. & Hebert, P. D. bold: the Barcode of Life Data System (http://www.barcodinglife.org). Mol. Ecol. Notes 7, 355–364 (2007).
Gerlt, J. A. et al. Enzyme Function Initiative-Enzyme Similarity Tool (EFI-EST): a web tool for generating protein sequence similarity networks. Biochim. Biophys. Acta 1854, 1019–1037 (2015).
The authors are grateful to Y. Michalakis (Centre national de la recherche scientifique, France) and A. Gibbs (Australian Nation University, Australia) for helpful comments and suggestions. P.L. was supported by the European Union: European Regional Development Fund (ERDF), by the Conseil Régional de La Réunion and by the Centre de Coopération internationale en Recherche agronomique pour le Développement (CIRAD). S.F.E. was supported by a grant (BFU2015-65037-P) from Spain Ministry of Science, Innovation and Universities–ERDF.
The authors declare no competing interests.
Peer review information
Nature Reviews Microbiology thanks M. Roossinck, A. Whitfield and the other, anonymous, reviewer(s) for their contribution to the peer review of this work.
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Plant viruses dataset: https://lefeup.github.io/plantviruses/
These invertebrate animals have exoskeletons, segmented bodies and paired jointed appendages. Arthropods belong to the phylum Euarthropoda that includes insects, arachnids, myriapods and crustaceans.
- RNA-dependent RNA polymerases
These enzymes catalyse the synthesis of RNA from an RNA template. RNA-dependent RNA polymerases are essential to the replication of viruses that have no DNA stage.
- Movement proteins
Some plant viruses encode these proteins to facilitate cell-to-cell movement of viral particles and/or uncoated viral nucleic acids. They frequently function by increasing the size exclusion limits of plasmodesmata.
Brassica is a genus in the mustard family (Brassicaceae) of plants, which includes cabbage, lettuce and cauliflower.
Angiosperms are also known as flowering plants and are the most diverse group of land plants. While both gymnosperms and angiosperms produce seeds, angiosperms are characterized by the presence of flowers, an endosperm within the seeds and the inclusion of seeds within fruits.
These microscopic channels traverse plant cell walls enabling intercellular trafficking of macromolecules.
This class of plant parasites comprises organisms in the orders Plasmodiophorida and Phagomyxida. They have long been recognized as a basal group to fungi, but recent molecular phylogenetic analysis suggests that they are more closely related to protozoa in the phylum Cercozoa.
This order of insects includes insects such as aphids, cicadas, leafhoppers and planthoppers. Most hemipterans feed on plant sap with their sucking and piercing mouthparts.
This is the body cavity in arthropods wherein haemolymph (plasma with haemocytes) circulates.
These small sap-sucking insects are members of the superfamily Aphidoidea in the Hemiptera order.
The phloem is the vascular system in plants within which soluble organic compounds that are produced during photosynthesis are transported.
About this article
Cite this article
Lefeuvre, P., Martin, D.P., Elena, S.F. et al. Evolution and ecology of plant viruses. Nat Rev Microbiol 17, 632–644 (2019). https://doi.org/10.1038/s41579-019-0232-3
Widely targeted analysis of metabolomic changes of Cucumis sativus induced by cucurbit chlorotic yellows virus
BMC Plant Biology (2022)
Archives of Virology (2022)
Nature Microbiology (2020)
Evolutionary dynamics of Tomato spotted wilt virus within and between alternate plant hosts and thrips
Scientific Reports (2020)