The dawn of symbiosis between plants and fungi

Abstract

The colonization of land by plants relied on fundamental biological innovations, among which was symbiosis with fungi to enhance nutrient uptake. Here we present evidence that several species representing the earliest groups of land plants are symbiotic with fungi of the Mucoromycotina. This finding brings up the possibility that terrestrialization was facilitated by these fungi rather than, as conventionally proposed, by members of the Glomeromycota. Since the 1970s it has been assumed, largely from the observation that vascular plant fossils of the early Devonian (400 Ma) show arbuscule-like structures, that fungi of the Glomeromycota were the earliest to form mycorrhizas, and evolutionary trees have, until now, placed Glomeromycota as the oldest known lineage of endomycorrhizal fungi. Our observation that Endogone-like fungi are widely associated with the earliest branching land plants, and give way to glomeromycotan fungi in later lineages, raises the new hypothesis that members of the Mucoromycotina rather than the Glomeromycota enabled the establishment and growth of early land colonists.

Figure 1.

Phylogenetic placement of fungi detected in basal (black filled circles), simple (grey filled circles) and complex thalloid liverworts (open circles), hornworts (squares) and ferns (right-facing triangles) within the Glomeromycota and Mucoromycotina using a full-length fungal nuclear ribosomal small subunit gene maximum-parsimony tree.

Figure 2.

Topology, relative chronology and morphology of the fungal lineages detected. (a) Maximum clade credibility topology inferred using a Bayesian relaxed clock analysis of six genes. Black dots represent support for relevant lineages (greater than or equal to 90% bootstrap and a posterior probability of 1.0). The grey dot indicates 65% bootstrap and a posterior probability of 0.99. The 95% confidence intervals of the relative age estimates for lineage origins are shown. (b) Scanning electron micrograph of a Glomeromycota-containing plant cell. (c) A Mucoromycotina-containing plant cell. See the electronic supplementary material, table S1 for all the symbioses investigated.