Evolution and ecology of plant viruses

Abstract

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.

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Fig. 1: The many origins of plant viruses.
Fig. 2: Overlap between the plant hosts of a whitefly vector species and transmitted viruses.
Fig. 3: Co-divergence of a viral capsid protein and transmission vector sequences.
Fig. 4: Addressing important questions in the ecology and evolution of plant viruses.

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Acknowledgements

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.

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P.L., D.P.M., S.F.E., D.N.S., P.R. and A.V. wrote and edited the manuscript. P.L. and A.V. undertook the analyses for the data presented in figures 1–3.

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Correspondence to Arvind Varsani.

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Plant viruses dataset: https://lefeup.github.io/plantviruses/

Glossary

Arthropods

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.

Brassicas

Brassica is a genus in the mustard family (Brassicaceae) of plants, which includes cabbage, lettuce and cauliflower.

Angiosperms

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.

Plasmodesmata

These microscopic channels traverse plant cell walls enabling intercellular trafficking of macromolecules.

Plasmodiophorids

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.

Hemiptera

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.

Haemocoel

This is the body cavity in arthropods wherein haemolymph (plasma with haemocytes) circulates.

Aphids

These small sap-sucking insects are members of the superfamily Aphidoidea in the Hemiptera order.

Phloem

The phloem is the vascular system in plants within which soluble organic compounds that are produced during photosynthesis are transported.

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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

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