Contemporaneous radiations of fungi and plants linked to symbiosis - PubMed (original) (raw)

doi: 10.1038/s41467-018-07849-9.

Michael D Nowak 2, Michael E Alfaro 3, Valérie Reeb 4, Jolanta Miadlikowska 1, Michael Krug 5, A Elizabeth Arnold 6 7, Louise A Lewis 8, David L Swofford 1 9, David Hibbett 10, Khidir Hilu 11, Timothy Y James 12, Dietmar Quandt 5, Susana Magallón 13

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Contemporaneous radiations of fungi and plants linked to symbiosis

François Lutzoni et al. Nat Commun. 2018.

Abstract

Interactions between fungi and plants, including parasitism, mutualism, and saprotrophy, have been invoked as key to their respective macroevolutionary success. Here we evaluate the origins of plant-fungal symbioses and saprotrophy using a time-calibrated phylogenetic framework that reveals linked and drastic shifts in diversification rates of each kingdom. Fungal colonization of land was associated with at least two origins of terrestrial green algae and preceded embryophytes (as evidenced by losses of fungal flagellum, ca. 720 Ma), likely facilitating terrestriality through endomycorrhizal and possibly endophytic symbioses. The largest radiation of fungi (Leotiomyceta), the origin of arbuscular mycorrhizae, and the diversification of extant embryophytes occurred ca. 480 Ma. This was followed by the origin of extant lichens. Saprotrophic mushrooms diversified in the Late Paleozoic as forests of seed plants started to dominate the landscape. The subsequent diversification and explosive radiation of Agaricomycetes, and eventually of ectomycorrhizal mushrooms, were associated with the evolution of Pinaceae in the Mesozoic, and establishment of angiosperm-dominated biomes in the Cretaceous.

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Conflict of interest statement

The authors declare no competing interests.

Figures

Fig. 1

Fig. 1

Contemporaneous changes revealed from independent estimates of divergence times for plants (top) and fungi (bottom) aligned using a single time scale. For clarity, only the most relevant error bars are shown for each divergence time estimate (see Supplementary Figs. 2, 3 for error bars). Exceptional shifts in diversification rates, highlighted by a change in color on the branches, are numbered on each tree (within yellow circles) and placed before the node where a shift was detected. The yellow circles numbered “1” indicate the basal rate relative to which the first major accelerations or decelerations were detected. Numbers at the tips of the trees refer to monophyletic groups listed to the left of each tree. Each taxon name listed on the left side is followed by its known species richness in parentheses. The asterisk after prasinophyceans indicates that this is a paraphyletic group of nine lineages of green algae currently classified at the rank of class or order, or as clades without formal taxonomic description. Three wide beige vertical bars spanning both trees highlight major events in the evolutionary history of fungi and plants that were defined by the origin of fungal key innovations, including traits that enabled mutualistic symbioses with plants. Two light green vertical bars delimit time periods when plant key innovations, such as seeds, enabled plants to form inland forests, and angiosperm diversification rates drastically accelerated, profoundly affecting the evolution of fungi. The light red vertical bar spanning both trees highlights a period when the most important diversification of plants (during the early evolution of tracheophytes) and the largest radiation of fungi (the Leotiomyceta radiation; yellow circle number 5) took place, starting around 450 Ma. Each arc represents an important event in the biology of plants (green arcs) and fungi (black arcs), including putative origins of major plant–fungal symbioses (arbuscular mycorrhizal [AM], endophytic and endolichenic [endophytes], ascolichenic [ascolichens], and ectomycorrhizal [ECM]). Horizontal dashed lines with arrows indicate major transitions from aquatic to terrestrial environments or from terrestrial wet to terrestrial dry (inland) forests, or the expansion of fungal lignin-degrading peroxidases

Fig. 2

Fig. 2

Pairwise comparison of selected land plant and fungal divergence times (node ages) posterior densities and their differences. a–l Positive age differences indicate that the fungal evolutionary event preceded the plant evolutionary event; negative age differences indicate that the plant evolutionary event preceded the fungal event

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