Plant DNA harbours virus "fossils" that reflect 300 million years of evolution

Is it possible to study the history of viruses that emerged several hundred million years ago? An international team of INRAE and CIRAD researchers answered this intriguing question by exploring plant genomes to find the molecular fossils of viruses.

During infections, genome fragments from certain viruses can become embedded in their hosts' chromosomes. It is possible for these endogenous viral elements to be intergenerationally transmitted for millions of years, which means they serve as precious evolutionary records of virus infections in plants. 

The research team focused on the plant virus family Caulimoviridae, whose members are known for becoming embedded in host genomes as evolutionarily persistent endogenous elements. The researchers analysed the genomes of 93 representative species from all the major lineages of terrestrial plants, including mosses, lycophytes¹, ferns, conifers, and flowering plants. They were then able to identify more than 47,000 endogenous viral elements left by members of Caulimoviridae. The findings show that Caulimoviridae viruses have infected an extremely wide range of vascular plant hosts, from lycophytes to flowering plants. The researchers also discovered that virus diversity within this family has been greatly underestimated. Their work revealed the existence of 35 previously undescribed taxonomic clusters in Caulimoviridae, including a newly described clade found only in certain conifers. 

When the researchers compared the evolutionary history of Caulimoviridae viruses to that of their plant hosts, they found that several virus taxonomic clusters appeared to have co-evolved with vascular plants for several hundred million years. However, this extremely long relationship was not always linear. Instead, their shared history was complex: sometimes viruses switched hosts, and sometimes they went extinct. Several of these extinction events may have been tied to the mass extinction events that completely transformed life on Earth, notably the mass extinctions during the late Permian (252 million years ago) and the late Cretaceous (66 million years ago). These events completely reshaped terrestrial ecosystems, leading to the disappearance of a large number of species and the creation of new ecological niches, which could be occupied by new viruses.

This work has underscored the great value of plant genomes as natural records of virus evolution. Researchers can utilise the traces left behind by ancient infections to shine light on the enduring interactions between plants and their viruses and on the ways in which viruses mechanistically adapt to ecosystem shifts.

1. Lycophytes appeared approximately 420 million years ago and are the most ancient vascular plant taxon still in existence. In ancient times, they formed enormous forests and had highly diverse forms. There were even tree-like species that reached over 30 metres in height. These large lycophytes ended up disappearing because of mass extinction events and competition with other plant taxa. Today, only the herbaceous lycophytes remain, which are no more than a few centimetres tall. Current-day lycophytes are used as model systems for studying the evolution of terrestrial plants.