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What can a billion years of coexistence tell us about plants and fungi evolution and their symbiotic interactions?

A team of fourteen researchers with complementary expertise in botany, mycology, paleontology and phylogenetic methods joined forces to infer the global phylogenies and dates of major evolutionary events for the two kingdoms – plants and fungi.

Interactions between fungi and plants, including parasitism, mutualism, and saprotrophy, have been invoked as key to their respective success over one billion years of coexistence. Yet, no one has explored globally contemporaneous evolutionary events associated with phenotypic innovations and symbiotic interactions throughout the evolutionary history of plants and fungi. For this study, phylogenetic relationships, divergence times of their various lineages, and major shifts in diversification rates were inferred independently for plants (Viridiplantae) and fungi. The two resulting phylogenetic chronograms then were aligned using the same geological time scale. The origins of plant-fungal symbioses (e.g., fungal endophytes, lichens and mycorrhizae) and decomposition of plant tissues by fungi, were evaluated using this dual time-calibrated phylogenetic framework. The results revealed linked and drastic shifts in diversification rates of each kingdom, consistent with major plant-fungal interactions.

In this study, published in Nature Communications, the authors reported that fungal colonization of land was associated with at least two origins of terrestrial green algae prior to the origin of land plants. This was evidenced by losses of fungal flagellum, ca. 720 million years ago (Ma), likely facilitating terrestriality through endomycorrhizal (arbuscular mycorrhizal) and possibly endophytic symbioses. The largest radiation of fungi (Leotiomyceta), the origin of arbuscular mycorrhizae, and the differentiation of the major lineages of land plants occurred ca. 480 Ma. These evolutionary events were followed by the origin of extant lichens belonging to the Ascomycota (467-410 Ma).

The origin and initial diversification of the seed plant lineage resulted in the establishment of the first inland forests formed by lignin-rich woody trees, and with increasingly specialized reproductive strategies. The early diversification of the seed plant lineage was followed by the radiation of Agaricomycetes, the largest class of Basidiomycota. This radiation was associated with explosive diversification, and the origin of extraordinary innovations including mushrooms, ectomycorrhizae, pathogenicity on diverse plants, and the capacity to digest all components of secondary plant cell walls, including lignin, which was abundantly produced by the members of the newly established seed plant lineage.

 The origin of ectomycorrhizal fungi seems to have resulted from a series of evolutionary changes in plants including the origins of wood, seeds and roots, which enabled the formation of inland progymnospem forests with well-oxygenated soils, followed by the origin of the family Pinaceae. Contrary to arbuscular mycorrhizae, this sequence of events suggests that the origin of extant ectomycorrhizal fungi was driven by key innovations in plants.

The macroevolution of plants and fungi has been studied mostly separately, but this investigation clearly demonstrates that their respective evolutionary histories are deeply interconnected and can be understood only through a simultaneous study of their phylogenies within a robust timeframe. It is expected that the same will hold true for the evolution of the animal kingdom, another group of heterotrophic organisms highly dependent on photoautotrophic plants, as well as microorganisms in general.

Nature Communications volume 9, Article number: 5451 (2018)


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