The discovery that Mucoromycotina, an ancient and partially saprotrophic fungal lineage, associates with the basal liverwort lineage Haplomitriopsida casts doubt on the widely held view that ...Glomeromycota formed the sole ancestral plant–fungus symbiosis. Whether this association is mutualistic, and how its functioning was affected by the fall in atmospheric CO₂concentration that followed plant terrestrialization in the Palaeozoic, remains unknown. We measured carbon‐for‐nutrient exchanges between Haplomitriopsida liverworts and Mucoromycotina fungi under simulated mid‐Palaeozoic (1500 ppm) and near‐contemporary (440 ppm) CO₂concentrations using isotope tracers, and analysed cytological differences in plant–fungal interactions. Concomitantly, we cultured both partners axenically, resynthesized the associations in vitro, and characterized their cytology. We demonstrate that liverwort–Mucoromycotina symbiosis is mutualistic and mycorrhiza‐like, but differs from liverwort–Glomeromycota symbiosis in maintaining functional efficiency of carbon‐for‐nutrient exchange between partners across CO₂concentrations. Inoculation of axenic plants with Mucoromycotina caused major cytological changes affecting the anatomy of plant tissues, similar to that observed in wild‐collected plants colonized by Mucoromycotina fungi. By demonstrating reciprocal exchange of carbon for nutrients between partners, our results provide support for Mucoromycotina establishing the earliest mutualistic symbiosis with land plants. As symbiotic functional efficiency was not compromised by reduced CO₂, we suggest that other factors led to the modern predominance of the Glomeromycota symbiosis.
Symbiotic options for the conquest of land Field, Katie J.; Pressel, Silvia; Duckett, Jeffrey G. ...
Trends in ecology & evolution,
08/2015, Letnik:
30, Številka:
8
Journal Article
Recenzirano
Odprti dostop
•Plant terrestrialization involved establishing mutualisms with fungi over 450 Mya.•The discovery of an ancient symbiosis challenges a decades-old paradigm.•Function, signaling, and regulation of ...plant–microbe symbioses are being unraveled.•Conquering land relied on a variety of symbiotic strategies still at work today.
The domination of the landmasses of Earth by plants starting during the Ordovician Period drastically altered the development of the biosphere and the composition of the atmosphere, with far-reaching consequences for all life ever since. It is widely thought that symbiotic soil fungi facilitated the colonization of the terrestrial environment by plants. However, recent discoveries in molecular ecology, physiology, cytology, and paleontology have brought into question the hitherto-assumed identity and biology of the fungi engaged in symbiosis with the earliest-diverging lineages of extant land plants. Here, we reconsider the existing paradigm and show that the symbiotic options available to the first plants emerging onto the land were more varied than previously thought.
• Liverworts, which are amongst the earliest divergent plant lineages and important ecosystem pioneers, often form nutritional mutualisms with arbuscular mycorrhiza-forming Glomeromycotina and ...fine-root endophytic Mucoromycotina fungi, both of which coevolved with early land plants. Some liverworts, in common with many later divergent plants, harbour both fungal groups, suggesting these fungi may complementarily improve plant access to different soil nutrients.
• We tested this hypothesis by growing liverworts in single and dual fungal partnerships under a modern atmosphere and under 1500 ppm CO₂, as experienced by early land plants. Access to soil nutrients via fungal partners was investigated with 15N-labelled algal necromass and 33P orthophosphate. Photosynthate allocation to fungi was traced using 14CO₂.
• Only Mucoromycotina fungal partners provided liverworts with substantial access to algal 15N, irrespective of atmospheric CO₂ concentration. Both symbionts increased 33P uptake, but Glomeromycotina were often more effective. Dual partnerships showed complementarity of nutrient pool use and greatest photosynthate allocation to symbiotic fungi.
• We show there are important functional differences between the plant–fungal symbioses tested, providing new insights into the functional biology of Glomeromycotina and Mucoromycotina fungal groups that form symbioses with plants. This may explain the persistence of the two fungal lineages in symbioses across the evolution of land plants.
An accurate understanding of the diversity and distribution of fungal symbioses in land plants is essential for mycorrhizal research. Here we update the seminal work of Wang and Qiu (Mycorrhiza ...16:299-363,
2006
) with a long-overdue focus on early-diverging land plant lineages, which were considerably under-represented in their survey, by examining the published literature to compile data on the status of fungal symbioses in liverworts, hornworts and lycophytes. Our survey combines data from 84 publications, including recent, post-2006, reports of Mucoromycotina associations in these lineages, to produce a list of at least 591 species with known fungal symbiosis status, 180 of which were included in Wang and Qiu (Mycorrhiza 16:299-363,
2006
). Using this up-to-date compilation, we estimate that fewer than 30% of liverwort species engage in symbiosis with fungi belonging to all three mycorrhizal phyla, Mucoromycota, Basidiomycota and Ascomycota, with the last being the most widespread (17%). Fungal symbioses in hornworts (78%) and lycophytes (up to 100%) appear to be more common but involve only members of the two Mucoromycota subphyla Mucoromycotina and Glomeromycotina, with Glomeromycotina prevailing in both plant groups. Our fungal symbiosis occurrence estimates are considerably more conservative than those published previously, but they too may represent overestimates due to currently unavoidable assumptions.
Arbuscular mycorrhizas are widespread in land plants including liverworts, some of the closest living relatives of the first plants to colonize land 500 million years ago (MYA). Previous ...investigations reported near-exclusive colonization of liverworts by the most recently evolved arbuscular mycorrhizal fungi, the Glomeraceae, indicating a recent acquisition from flowering plants at odds with the widely held notion that arbuscular mycorrhizal-like associations in liverworts represent the ancestral symbiotic condition in land plants. We performed an analysis of symbiotic fungi in 674 globally collected liverworts using molecular phylogenetics and electron microscopy. Here, we show every order of arbuscular mycorrhizal fungi colonizes early-diverging liverworts, with non-Glomeraceae being at least 10 times more common than in flowering plants. Arbuscular mycorrhizal fungi in liverworts and other ancient plant lineages (hornworts, lycopods, and ferns) were delimited into 58 taxa and 36 singletons, of which at least 43 are novel and specific to liverworts. The discovery that early plant lineages are colonized by early-diverging fungi supports the hypothesis that arbuscular mycorrhizas are an ancestral symbiosis for all land plants.
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 (
) 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.
A mycorrhizal revolution Hoysted, Grace A; Kowal, Jill; Jacob, Alison ...
Current opinion in plant biology,
August 2018, 2018-08-00, 20180801, Letnik:
44
Journal Article
Recenzirano
Odprti dostop
•Non-vascular and vascular plants form previously unrecognized symbioses with Mucoromycotina fungi.•Mutualisms with Glomeromycotina (i.e. arbuscular mycorrhizal fungi) and/or Mucoromycotina have ...different costs and benefits thus providing nutritional flexibility to plants.•Fine root endophytes are arbuscule-forming fungi unexpectedly placed in Mucoromycotina.
It has long been postulated that symbiotic fungi facilitated plant migrations onto land through enhancing the scavenging of mineral nutrients and exchanging these for photosynthetically fixed organic carbon. Today, land plant–fungal symbioses are both widespread and diverse. Recent discoveries show that a variety of potential fungal associates were likely available to the earliest land plants, and that these early partnerships were probably affected by changing atmospheric CO2 concentrations. Here, we evaluate current hypotheses and knowledge gaps regarding early plant–fungal partnerships in the context of newly discovered fungal mutualists of early and more recently evolved land plants and the rapidly changing views on the roles of plant–fungal symbioses in the evolution and ecology of the terrestrial biosphere.
Mycorrhizal functioning in the fern Ophioglossum is complex and poorly understood. It is unknown whether mature O. vulgatum sporophytes form mutualistic associations with fungi of the Glomeromycota ...and with what specificity. Are green sporophytes able to ‘repay’ fungal carbon (C) invested in them by mycorrhizal partners during the initially heterotrophic gametophyte and early sporophyte stages of the lifecycle? We identified fungal partners of O. vulgatum sporophytes using molecular techniques and supplied them with³³P‐orthophosphate and O. vulgatum sporophytes with¹⁴CO₂. We traced the movement of fungal‐acquired nutrients and plant‐fixed C between symbionts and analysed natural abundance¹³C and¹⁵N isotope signatures to assess nutritional interactions. We found fungal specificity of O. vulgatum sporophytes towards a mycorrhizal fungus closely related to Glomus macrocarpum. Our radioisotope tracers revealed reciprocal C‐for‐phosphorus exchange between fern sporophytes and fungal partners, despite competition from surrounding vegetation. Monocultures of O. vulgatum were enriched in¹³C and¹⁵N, providing inconclusive evidence of mycoheterotrophy when experiencing competition from the surrounding plant community. We show mutualistic and specific symbiosis between a eusporangiate fern and fungi of the Glomeromycota. Our findings suggest a ‘take now, pay later’ strategy of mycorrhizal functioning through the lifecycle O. vulgatum, from mycoheterotrophic gametophyte to mutualistic aboveground sporophyte.
Current understanding of the nature and function of fungal associations in pteridophytes is surprisingly patchy given their key evolutionary position, current research foci on other early-branching ...plant clades, and major efforts at unravelling mycorrhizal evolution and the mechanisms underlying this key interaction between plants and fungi. Here we provide a critical review of current knowledge of fungal associations across pteridophytes and consider future directions making recommendations along the way. From a comprehensive survey of the literature, a confused picture emerges： suggestions that members of the Lycopsida harbour Basidiomycota fungi contrast sharply with extensive cytological and recent molecular evidence pointing to exclusively Glomeromycota and/or Mucoromycotina associations in this group. Similarly, reports of dark septate, assumingly ascomycetous, hyphae in a range of pteridophytes, advocating a mutualistic relationship, are not backed by functional evidence and the fact that the fungus invariably occupies dead host tissue points to saprotrophy and not mutualism. The best conclusion that can be reached based on current evidence is that the fungal symbionts of pteridophytes belong to the two fungal lineages Mucoromycotina and Glomeromycota. Do symbiotic fungi and host pteridophytes engage in mutually beneficial partnerships？ To date, only two pioneering studies have addressed this key question demonstrating reciprocal exchange of nutrients between the sporophytes of Ophioglossum vulgatum and Osmunda regalis and their fungal symbionts. There is a pressing need for more functional investigations also extending to the gametophyte generation and coupled with in vitro isolation and resynthesis studies to unravel the effect of the fungi on their host.
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