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.

Enigmatic Sebacinales

“…Fungal phylogeny compiled after various authors, phylogeny of plants compiled after several authors in Ligrone et al (2012). Black lines refer to previous data (see accompanying text), red lines include new reports from Bidartondo et al (2011) Mycothalli in liverworts and Sebacinales mycobionts in jungermanniales (Fig. 7) Liverworts, Marchantiophyta, are considered as the most ancient land plants, and many of them are obligately associated with mycobionts, thus constituting mycothalli.…”

Fungal symbioses in hornworts: a chequered history

“…Glomeromycota fungi are reported to associate with five hornworts, based on electron microscope [12], in vitro [13] and molecular studies [11]. However, two hornworts are reported to harbour Endogone-like fungi [11] and two others are considered non-symbiotic [14,15]. We ignore the fungal symbioses of the vast majority of the 200-220 hornwort species, though the scanty information to date hints at some parallels with liverworts.…”

“…Glomeromycota were firmly regarded as the ancestral mycorrhizal type [9,10] until the recent discovery of Endogone-like Mucoromycotina fungi in the earliest liverwort lineage (Haplomitriopsida) and in some early simple and complex thalloid liverworts questioned that idea [11]. Glomeromycota fungi are reported to associate with five hornworts, based on electron microscope [12], in vitro [13] and molecular studies [11]. However, two hornworts are reported to harbour Endogone-like fungi [11] and two others are considered non-symbiotic [14,15].…”

“…Thus, identification of mycorrhizal fungi within plants relies routinely on Glomeromycota-specific detection. Glomeromycota were firmly regarded as the ancestral mycorrhizal type [9,10] until the recent discovery of Endogone-like Mucoromycotina fungi in the earliest liverwort lineage (Haplomitriopsida) and in some early simple and complex thalloid liverworts questioned that idea [11]. Glomeromycota fungi are reported to associate with five hornworts, based on electron microscope [12], in vitro [13] and molecular studies [11].…”

Paleomycology of the Princeton Chert II. Dark-septate fungi in the aquatic angiospermEorhiza arnoldiiindicate a diverse assemblage of root-colonizing fungi during the Eocene

“…Mutualistic relationships with fungi are thought to have been integral to the colonization of land by plants (Pirozynski and Mallock 1975, Humphreys et al 2010, Bidartondo et al 2011; in the subsequent , 450 million y, intricate associations have evolved, ranging from obligate mutualism through commensalism, parasitism and pathogenicity. A substantial number of vascular plants also are host to internal fungal biota with which they form neither typical mycorrhizal associations nor produce responses associated with infection (Saikkonen et al 1998, Jumpponen 2001.…”