Mycorrhizal associations between fungi and plant roots have globally significant impacts on nutrient cycling. Mucoromycotina ‘fine root endophytes’ (MFRE) are a distinct and recently characterised ...group of mycorrhiza‐forming fungi that associate with the roots of a range of host plant species. Given their previous misidentification and assignment as arbuscular mycorrhizal fungi (AMF) of the Glomeromycotina, it is now important to untangle the specific form and function of MFRE symbioses. In particular, relatively little is known about the nature of MFRE colonisation and its role in N uptake and transfer to host plants. Even less is known about the mechanisms by which MFRE access and assimilate N, and how this N is processed and subsequently exchanged with host plants for photosynthates. Here, we summarise and contrast the structures formed by MFRE and arbuscular mycorrhizal fungi in host plants as well as compare the N source preference of each mycorrhizal fungal group with what is currently known for MFRE N uptake. We compare the mechanisms of N assimilation and transfer to host plants utilised by the main groups of mycorrhizal fungi and hypothesise potential mechanisms for MFRE N assimilation and transfer, outlining directions for future research.
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.
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 mycorrhizal fungi colonize the roots of most plants, forming a near-ubiquitous symbiosis1 that is typically characterized by the bi-directional exchange of fungal-acquired nutrients for ...plant-fixed carbon.2 Mycorrhizal fungi can form below-ground networks3,4,5,6 with potential to facilitate the movement of carbon, nutrients, and defense signals across plant communities.7,8,9 The importance of neighbors in mediating carbon-for-nutrient exchange between mycorrhizal fungi and their plant hosts remains equivocal, particularly when other competing pressures for plant resources are present. We manipulated carbon source and sink strengths of neighboring pairs of host plants through exposure to aphids and tracked the movement of carbon and nutrients through mycorrhizal fungal networks with isotope tracers. When carbon sink strengths of both neighboring plants were increased by aphid herbivory, plant carbon supply to extraradical mycorrhizal fungal hyphae was reduced, but mycorrhizal phosphorus supply to both plants was maintained, albeit variably, across treatments. However, when the sink strength of only one plant in a pair was increased, carbon supply to mycorrhizal fungi was restored. Our results show that loss of carbon inputs into mycorrhizal fungal hyphae from one plant may be ameliorated through inputs of a neighbor, demonstrating the responsiveness and resilience of mycorrhizal plant communities to biological stressors. Furthermore, our results indicate that mycorrhizal nutrient exchange dynamics are better understood as community-wide interactions between multiple players rather than as strict exchanges between individual plants and their symbionts, suggesting that mycorrhizal C-for-nutrient exchange is likely based more on unequal terms of trade than the “fair trade” model for symbiosis.
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•We assessed neighbors’ impact on mycorrhizal function in plant-aphid interactions•When both plants were aphid infested, carbon supply to mycorrhizal fungi decreased•If only one plant was infested, carbon supply was partially restored•Mycorrhizal nutrient exchanges are better understood as community-wide interactions
Durant et al. show that mycorrhizal nutrient exchange involves community-wide interactions between multiple players. Loss of carbon inputs into mycorrhizal fungi caused by aphid herbivory of one plant can be compensated for by aphid-free neighbors, demonstrating the responsiveness and resilience of mycorrhizal plant communities to biological stressors.
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.
Abstract
Root exudates and rhizosheaths of attached soil are important features of growing roots. To elucidate factors involved in rhizosheath formation, wild-type (WT) barley (Hordeum vulgare L. cv. ...Pallas) and a root hairless mutant, bald root barley (brb), were investigated with a combination of physiological, biochemical, and immunochemical assays. When grown in soil, WT barley roots bound ∼5-fold more soil than brb per unit root length. High molecular weight (HMW) polysaccharide exudates of brb roots had less soil-binding capacity than those of WT root exudates. Carbohydrate and glycan monoclonal antibody analyses of HMW polysaccharide exudates indicated differing glycan profiles. Relative to WT plants, root exudates of brb had reduced signals for arabinogalactan-protein (AGP), extensin, and heteroxylan epitopes. In contrast, the root exudate of 2-week-old brb plants contained ∼25-fold more detectable xyloglucan epitope relative to WT. Root system immunoprints confirmed the higher levels of release of the xyloglucan epitope from brb root apices and root axes relative to WT. Epitope detection with anion-exchange chromatography indicated that the increased detection of xyloglucan in brb exudates was due to enhanced abundance of a neutral polymer. Conversely, brb root exudates contained decreased amounts of an acidic polymer, with soil-binding properties, containing the xyloglucan epitope and glycoprotein and heteroxylan epitopes relative to WT. We, therefore, propose that, in addition to physically structuring soil particles, root hairs facilitate rhizosheath formation by releasing a soil-binding polysaccharide complex.
The root exudate of a root hairless mutant of barley, relative to wild type, has an altered pattern of polysaccharide epitopes and lesser amounts of an acidic soil-binding polysaccharide complex.
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.
Fossil evidence from the Rhynie chert indicates that early land plants, which evolved in a high-CO2 atmosphere during the Palaeozoic Era, hosted diverse fungal symbionts. It is hypothesized that the ...rise of early non-vascular land plants, and the later evolution of roots and vasculature, drove the long-term shift towards a high-oxygen, low CO2 climate that eventually permitted the evolution of mammals and, ultimately, humans. However, very little is known about the productivity of the early terrestrial biosphere, which depended on the acquisition of the limiting nutrient phosphorus via fungal symbiosis. Recent laboratory experiments have shown that plant–fungal symbiotic function is specific to fungal identity, with carbon-for-phosphorus exchange being either enhanced or suppressed under superambient CO2. By incorporating these experimental findings into a biogeochemical model, we show that the differences in these symbiotic nutrient acquisition strategies could greatly alter the plant-driven changes to climate, allowing drawdown of CO2 to glacial levels, and altering the nature of the rise of oxygen. We conclude that an accurate depiction of plant–fungal symbiotic systems, informed by high-CO2 experiments, is key to resolving the question of how the first terrestrial ecosystems altered our planet.
This article is part of a discussion meeting issue ‘The Rhynie cherts: our earliest terrestrial ecosystem revisited’.
An Arabidopsis thaliana drought-tolerant mutant, altered expression of APX2 (alx8), has constitutively increased abscisic acid (ABA) content, increased expression of genes responsive to high light ...stress and is reported to be drought tolerant. We have identified alx8 as a mutation in SAL1, an enzyme that can dephosphorylate dinucleotide phosphates or inositol phosphates. Previously identified mutations in SAL1, including fiery (fry1-1), were reported as being more sensitive to drought imposed by detachment of rosettes. Here we demonstrate that alx8, fry1-1 and a T-DNA insertional knockout allele all have markedly increased resistance to drought when water is withheld from soil-grown intact plants. Microarray analysis revealed constitutively altered expression of more than 1800 genes in both alx8 and fry1-1. The up-regulated genes included some characterized stress response genes, but few are inducible by ABA. Metabolomic analysis revealed that both mutants exhibit a similar, dramatic reprogramming of metabolism, including increased levels of the polyamine putrescine implicated in stress tolerance, and the accumulation of a number of unknown, potential osmoprotectant carbohydrate derivatives. Under well-watered conditions, there was no substantial difference between alx8 and Col-0 in biomass at maturity; plant water use efficiency (WUE) as measured by carbon isotope discrimination; or stomatal index, morphology or aperture. Thus, SAL1 acts as a negative regulator of predominantly ABA-independent and also ABA-dependent stress response pathways, such that its inactivation results in altered osmoprotectants, higher leaf relative water content and maintenance of viable tissues during prolonged water stress.
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