Mucoromycotina Fine Root Endophyte Fungi Form Nutritional Mutualisms with Vascular Plants

Abstract

Fungi and plants have engaged in intimate symbioses that are globally widespread and have driven terrestrial biogeochemical processes since plant terrestrialization .500 million years ago. Recently, hitherto unknown nutritional mutualisms involving ancient lineages of fungi and nonvascular plants have been discovered, although their extent and functional significance in vascular plants remain uncertain. Here, we provide evidence of carbon-for-nitrogen exchange between an early-diverging vascular plant (Lycopodiella inundata) and Mucoromycotina (Endogonales) fine root endophyte fungi. Furthermore, we demonstrate that the same fungal symbionts colonize neighboring nonvascular and flowering plants. These findings fundamentally change our understanding of the physiology, interrelationships, and ecology of underground plant-fungal symbioses in modern terrestrial ecosystems by revealing the nutritional role of Mucoromycotina fungal symbionts in vascular plants.

Functional complementarity of ancient plant–fungal mutualisms: contrasting nitrogen, phosphorus and carbon exchanges between Mucoromycotina and Glomeromycotina fungal symbionts of liverworts

“…The latest evidence indicates that FRE fungi, which are widespread ecologically and across vascular plants, are members of the Mucoromycotina and closely related to liverwort and lycophyte Mucoromycotina symbionts (Bidartondo et al ., ; Field et al ., ; Rimington et al ., , ; Orchard et al ., ; Hoysted et al ., ). Furthermore, the same Mucoromycotina fungi can enter into symbiosis with liverworts, early vascular plants and angiosperms (Hoysted et al ., ). This finding greatly expands the potential significance of Mucoromycotina fungi in modern ecosystems (Field et al ., ; Field & Pressel, ; Hoysted et al ., , ).…”

“…These findings, together with fossil evidence of Mucoromycotina‐like and Glomeromycotina‐like fungal associations in some of the first vascular plants of the early Devonian (Strullu‐Derrien et al ., ), have led to the novel hypothesis that engagement with both fungal partners might have been a common strategy during early land plant evolution (Field et al ., ). Furthermore, new molecular evidence reveals the same Mucoromycotina fungal symbionts are shared by liverworts, early divergent vascular plants and angiosperms (Hoysted et al ., ). This is consistent with the recent finding that the globally widespread fine root endophytes (FREs), originally classified as Glomus tenue (more recently Planticonsortium tenue (Walker et al ., )) , are not members of the Glomeromycotina as hitherto assumed, but instead fall within the Mucoromycotina (Orchard et al ., ,).…”

“…This is consistent with the recent finding that the globally widespread fine root endophytes (FREs), originally classified as Glomus tenue (more recently Planticonsortium tenue (Walker et al ., )) , are not members of the Glomeromycotina as hitherto assumed, but instead fall within the Mucoromycotina (Orchard et al ., ,). In angiosperms, Mucoromycotina–FREs, when present, seem to always co‐occur with Glomeromycotina in the same host (Orchard et al ., ,; Hoysted et al ., ), while exclusive Mucoromycotina–FRE symbioses have been reported so far in only one lycophyte (Rimington et al ., , ; Pressel et al ., ; Hoysted et al ., ) and in the earliest divergent Haplomitriopsida liverworts Haplomitrium and Treubia . The majority of early divergent mycorrhizal plant clades, lycophytes, hornworts and (thalloid) liverworts (e.g.…”

“…Mycorrhizal associations (and mycorrhizal‐like associations in plants that lack roots, hereafter mycorrhizas) are near‐ubiquitous mutualisms between soil fungi and most land plant phyla (Wang & Qui, ; Wang et al ., ) with key roles in plant nutrition and health (Smith & Read, ). The earliest divergent extant branches of the land plant phylogeny supporting fungal symbionts, namely liverworts (Haplomitriopsida and thalloids), hornworts and lycophytes (Bidartondo et al ., ; Desirò et al ., ; Field et al ., ; Rimington et al ., ; Hoysted et al ., ), have recently been shown to form symbioses with members of two ancient fungal lineages, arbuscular mycorrhizal (AM) fungi falling within the Glomeromycotina, and the much less well studied, and poorly understood, symbiotic fungi of the Mucoromycotina.…”

“…The majority of early divergent mycorrhizal plant clades, lycophytes, hornworts and (thalloid) liverworts (e.g. the complex thalloid Neohodgsonia mirabilis ) engage in partnerships with both fungi, sometimes simultaneously in so‐called ‘dual’ symbiosis (Desirò et al ., ; Field et al ., , ; Rimington et al ., , ; Pressel et al ., ), paralleling the situation recently established for flowering plants (Hoysted et al ., , ). Only a few complex thalloid liverworts, such as species in the genus Marchantia , appear to associate exclusively with Glomeromycotina fungi (Field et al ., ; Rimington et al ., ).…”