Unity in diversity Field, Katie J.; Pressel, Silvia
The New phytologist,
12/2018, Letnik:
220, Številka:
4
Journal Article
Recenzirano
Odprti dostop
Mycorrhizal symbiosis is an ancient and widespread mutualism between plants and fungi that facilitated plant terrestrialisation > 500 million years ago, with key roles in ecosystem functioning at ...multiple scales. Central to the symbiosis is the bidirectional exchange of plant-fixed carbon for fungal-acquired nutrients. Within this unifying role of mycorrhizas, considerable diversity in structure and function reflects the diversity of the partners involved. Early diverging plants form mutualisms not only with arbuscular mycorrhizal Glomeromycotina fungi, but also with poorly characterised Mucoromycotina, which may also colonise the roots of ‘higher’ plants as fine root endophytes. Functional diversity in these symbioses depends on both fungal and plant life histories and is influenced by the environment. Recent studies have highlighted the roles of lipids/fatty acids in plant-to-fungus carbon transport and potential contributions of Glomeromycotina fungi to plant nitrogen nutrition. Together with emerging appreciation of mycorrhizal networks as multi-species resource-sharing systems, these insights are broadening our views on mycorrhizas and their roles in nutrient cycling. It is crucial that the diverse array of biotic and abiotic factors that together shape the dynamics of carbon-for-nutrient exchange between plants and fungi are integrated, in addition to embracing the unfolding and potentially key role of Mucoromycotina fungi in these processes.
Arbuscular mycorrhizal fungi (AMF) form symbioses with most crops, potentially improving their nutrient assimilation and growth. The effects of cultivar and atmospheric CO2 concentration (CO2) on ...wheat–AMF carbon‐for‐nutrient exchange remain critical knowledge gaps in the exploitation of AMF for future sustainable agricultural practices within the context of global climate change. We used stable and radioisotope tracers (15N, 33P, 14C) to quantify AMF‐mediated nutrient uptake and fungal acquisition of plant carbon in three wheat (Triticum aestivum L.) cultivars. We grew plants under current ambient (440 ppm) and projected future atmospheric CO2 concentrations (800 ppm). We found significant 15N transfer from fungus to plant in all cultivars, and cultivar‐specific differences in total N content. There was a trend for reduced N uptake under elevated atmospheric CO2. Similarly, 33P uptake via AMF was affected by cultivar and atmospheric CO2. Total P uptake varied significantly among wheat cultivars and was greater at the future than current atmospheric CO2. We found limited evidence of cultivar or atmospheric CO2 effects on plant‐fixed carbon transfer to the mycorrhizal fungi. Our results suggest that AMF will continue to provide a route for nutrient uptake by wheat in the future, despite predicted rises in atmospheric CO2. Consideration should therefore be paid to cultivar‐specific AMF receptivity and function in the development of climate smart germplasm for the future.
Arbuscular mycorrhizal fungi (AMF) form symbioses with most crops, potentially improving their nutrient assimilation with possible applications in future sustainable agriculture. However, the effects of cultivar and increasing CO2 on wheat mycorrhizal function remain unknown. Using isotope tracers, we tracked mycorrhizal function in three wheat cultivars across two CO2 scenarios. Our results suggest AMF could provide a route of nutrient uptake to wheat in the future, despite predicted rises in atmospheric CO2. Consideration should be paid to cultivar‐specific AMF receptivity and function in the development of climate smart future crops.
Soil is a crucial component of the biosphere and is a major sink for organic carbon. Plant roots are known to release a wide range of carbon-based compounds into soils, including polysaccharides, but ...the functions of these are not known in detail.
Using a monoclonal antibody to plant cell wall xyloglucan, we show that this polysaccharide is secreted by a wide range of angiosperm roots, and relatively abundantly by grasses. It is also released from the rhizoids of liverworts, the earliest diverging lineage of land plants. Using analysis of water-stable aggregate size, dry dispersion particle analysis and scanning electron microscopy, we show that xyloglucan is effective in increasing soil particle aggregation, a key factor in the formation and function of healthy soils.
To study the possible roles of xyloglucan in the formation of soils, we analysed the xyloglucan contents of mineral soils of known age exposed upon the retreat of glaciers. These glacial forefield soils had significantly higher xyloglucan contents than detected in a UK grassland soil.
We propose that xyloglucan released from plant rhizoids/roots is an effective soil particle aggregator and may, in this role, have been important in the initial colonization of land.
1. The 20th century saw dramatic increases in agricultural productivity, largely through the development and application of pesticides, fertilisers rich in nitrogen and phosphorus, and advances in ...plant breeding and genetic technologies. In the last 15 years, however, many key crop yields have plateaued. Climate change, an ever-increasing human population, depletion of global rock-phosphorus and growing energy prices make current fertiliser production unsustainable and represent sizeable challenges to global food security. 2. Many important crops form symbioses with arbuscular mycorrhizal fungi (AMF), and this has motivated the development of novel approaches in crop breeding and agricultural practices to support and promote AMF in agroecosystems. 3. Arbuscular mycorrhizal fungal symbiosis can be high beneficial in crops and wider agroecosystems in many ways, including improved soil structure and resistance to pests. However, AMF colonisation does not necessarily translate directly into enhanced plant performance or crop yield, while land management practices that would encourage mycorrhiza-crop associations, such as lowtill or minimal chemical input often incur yield-reducing trade-offs. 4. Synthesis. We draw on ecological knowledge of AMF to inform their role in agroecosystems, providing a balanced look at mycorrhiza-crop symbioses in terms of plant ecophysiology and the wider role of AMF in agroecosystems and ask the question: are AMF our sustainable saviours?
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 (Amsterdam),
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.
Abstract Arbuscular mycorrhizal (AM) fungi frequently colonise plant roots and can affect plant morphology and physiology through their contribution to plant nutrition. However, the functional role ...of AM fungi in the presence of other microbial symbionts, including widespread Mucoromycotina ‘fine root endophytes’ (MFRE) fungi, remains largely unknown. While both AM fungi and MFRE transfer nutrients, including nitrogen, from inorganic and organic sources to host plants, their combined effects on co‐colonised plants have only been investigated in liverworts. Here, we compare the morphology and physiology of the grass Holcus lanatus grown with an AM fungal community versus a more diverse symbiotic fungal community containing both AM fungi and MFRE. Holcus lanatus plants were grown in the presence of either a diverse MFRE+AM fungi soil inoculum or a multi‐species AM fungal inoculum. Plant traits associated with growth were quantified, along with fungal transfer of 15 N tracer to plants from a variety of sources (ammonium chloride, alanine, glycine and algal necromass). Holcus lanatus grown with the AM fungal community had greater root and shoot growth during early development and prior to the addition of 15 N‐labelled sources, compared with plants grown with the more diverse symbiotic fungal community. When nitrogen sources were made available to the fungal symbionts in the pot microcosms, plants growing with the MFRE+AM fungi soil inoculum had a faster growth rate than plants growing with the AM fungal community. At harvest, H. lanatus grown with the AM fungal community had a larger biomass, and there were no differences in 15 N tracer assimilation in plants across the two fungal community treatments. Our results demonstrate that the diversity of fungal inocula in conjunction with soil nutrient availability determine the benefits derived by plants from diverse fungal symbionts. Our research contributes to understanding host plant outcomes in diverse multi‐symbiont scenarios. Read the free Plain Language Summary for this article on the Journal blog.
Abstrakt Kërpudhat mikorizale arbuskulare (AM) shpesh gjënden në rrënjët e bimëve, dhe mund të ndikojnë në morfologjinë dhe fiziologjinë e bimëve nëpërmjet kontributit ushqimor ndaj tyre. Funksioni i kërpudhave AM në prani të simbioneve të tjera mikrobiale, duke përfshirë kërpudhat e përhapura endofite të klasifikimit Mucoromycotina (MFRE), mbetet kryesisht i panjohur. Kërpudhat AM dhe MFRE lëvizin lëndë ushqyese, duke përfshirë azotin, nga burimet inorganike dhe organike tek bimët pritëse, mirëpo efektet e tyre sinergjike tek bimët janë studiuar vetëm në bimët jo‐vaskulare: mëlçitë me gjethe (Anglisht: ‘ liverworts ’). Këtu, ne krahasojmë morfologjinë dhe fiziologjinë e barit Holcus lanatus të rritur me një komunitet kërpudhash AM kundrejt një komuniteti kërpudhash simbiotike më të larmishëm që përmban si kërpudhat AM, ashtu edhe MFRE. Bimët Holcus lanatus u rritën në prani të një inokulimi të larmishëm të kërpudhave MFRE+AM, ose në prani të një inokulimi kërpudhash AM e përbërë nga disa specie. Tipare bimore që kanë lidhje me rritjen e bimës u matën, së bashku me lëvizjen e izotopit të azotit ( 15 N) përmes kërpudhave nga një shumëllojshmëri burimesh (klorur amoni, alanina, glicina, algat e thata) deri tek bimët. Holcus lanatus i rritur me komunitetin e kërpudhave AM pësoj rritje më të madhe herët në zhvillim dhe para shtimit të burimeve me 15 N, në krahasim me bimët e rritura me komunitetin kërpudhor më të larmishëm. Kur burimet e azotit iu shtuan eksperimentit dhe u vunë në dispozicion të kërpudhave, bimët që po rriteshin me kërpudhat MFRE+AM pësuan rritje më të shpejtë në krahasim me bimët që po rriteshin me kërpudhat AM. Në fund të eksperimentit, H. lanatus i rritur me komunitetin e kërpudhave AM kishte një biomasë më të madhe, dhe nuk u gjëndën dallime në asimilimin e 15 N midis bimëve të rritura në dy trajtimet e kërpudhave. Rezultatet tona tregojnë se ndërveprimi i shumëllojshmërisë së kërpudhave me sasinë e lëndëve ushqyese në tokë, përcakton përfitimet që marrin bimët nga simbionet e ndryshme kërpudhore. Puna jonë kërkimore na ndihmon të kuptojmë më mire ç'farë efektesh mbi bimën pritëse ka lidhja me disa kërpudha simbiotike njëkohësisht.
Associations formed between plants and arbuscular mycorrhizal (AM) fungi are characterized by the bi-directional exchange of fungal-acquired soil nutrients for plant-fixed organic carbon compounds. ...Mycorrhizal-acquired nutrient assimilation by plants may be symmetrically linked to carbon (C) transfer from plant to fungus or governed by sink-source dynamics. Abiotic factors, including atmospheric CO2 concentration (CO2), can affect the relative cost of resources traded between mutualists, thereby influencing symbiotic function. Whether biotic factors, such as insect herbivores that represent external sinks for plant C, impact mycorrhizal function remains unstudied. By supplying 33P to an AM fungus (Rhizophagus irregularis) and 14CO2 to wheat, we tested the impact of increasing C sink strength (i.e., aphid herbivory) and increasing C source strength (i.e., elevated CO2) on resource exchange between mycorrhizal symbionts. Allocation of plant C to the AM fungus decreased dramatically following exposure to the bird cherry-oat aphid (Rhopalosiphum padi), with high CO2 failing to alleviate the aphid-induced decline in plant C allocated to the AM fungus. Mycorrhizal-mediated uptake of 33P by plants was maintained regardless of aphid presence or elevated CO2, meaning insect herbivory drove asymmetry in carbon for nutrient exchange between symbionts. Here, we provide direct evidence that external biotic C sinks can limit plant C allocation to an AM fungus without hindering mycorrhizal-acquired nutrient uptake. Our findings highlight the context dependency of resource exchange between plants and AM fungi and suggest biotic factors—individually and in combination with abiotic factors—should be considered as powerful regulators of symbiotic function.
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•We tested how aphid herbivory and increasing CO2 affects wheat mycorrhizal function•Aphids reduced wheat C supply to mycorrhizal fungi. High CO2 had no effect.•Transfer of fungal 33P to plant was maintained regardless of aphids or high CO2•Mycorrhizal function is context dependent, affected by biotic and abiotic factors
Little is known about how mycorrhizal function is affected by insect herbivory and environment. Charters et al. show aphids reduce plant C allocation to mycorrhizas, although fungal P transfer to plants is maintained, suggesting high context dependency where resource exchange between symbionts is influenced by interacting biotic and abiotic factors.
Summary
Plants simultaneously interact with a range of biotrophic symbionts, ranging from mutualists such as arbuscular mycorrhizal fungi (AMF), to parasites such as the potato cyst nematode (PCN). ...The exchange of mycorrhizal‐acquired nutrients for plant‐fixed carbon (C) is well studied; however, the impact of competing symbionts remains underexplored.
In this study, we examined mycorrhizal nutrient and host resource allocation in potato with and without AMF and PCN using radioisotope tracing, whilst determining the consequences of such allocation.
The presence of PCN disrupted C for nutrient exchange between plants and AMF, with plant C overwhelmingly obtained by the nematodes. Despite this, AMF maintained transfer of nutrients on PCN‐infected potato, ultimately losing out in their C for nutrient exchange with the host. Whilst PCN exploited the greater nutrient reserves to drive population growth on AMF–potato, the fungus imparted tolerance to allow the host to bear the parasitic burden.
Our findings provide important insights into the belowground dynamics of plant–AMF symbioses, where simultaneous nutritional and nonnutritional benefits conferred by AMF to hosts and their parasites are seldom considered in plant community dynamics. Our findings suggest this may be a critical oversight, particularly in the consideration of C and nutrient flows in plant and soil communities.
Long computation times in vegetation and climate models hamper our ability to evaluate the potentially powerful role of plants on weathering and carbon sequestration over the Phanerozoic Eon. ...Simulated vegetation over deep time is often homogenous, and disregards the spatial distribution of plants and the impact of local climatic variables on plant function. Here we couple a fast vegetation model (FLORA) to a spatially-resolved long-term climate-biogeochemical model (SCION), to assess links between plant geographical range, the long-term carbon cycle and climate. Model results show lower rates of carbon fixation and up to double the previously predicted atmospheric CO
concentration due to a limited plant geographical range over the arid Pangea supercontinent. The Mesozoic dispersion of the continents increases modelled plant geographical range from 65% to > 90%, amplifying global CO
removal, consistent with geological data. We demonstrate that plant geographical range likely exerted a major, under-explored control on long-term climate change.
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