David Read

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Data from: Ancient plants with ancient fungi: liverworts associate with early-diverging arbuscular mycorrhizal fungi

Arbuscular mycorrhizas are widespread in land plants including liverworts, some of the closest li... more Arbuscular mycorrhizas are widespread in land plants including liverworts, some of the closest living relatives of the first plants to colonise land 500 MYA. Previous investigations reported near-exclusive colonisation 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 colonises early-diverging liverworts, with non-Glomeraceae being at least ten 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 colonised by early-diverging fungi supports the hypothesis that arbuscular mycorrhizas are an ancestral symbiosis for all land plants

Supplementary Figures S1-10 from Ancient plants with ancient fungi: liverworts associate with early-diverging arbuscular mycorrhizal fungi

Global map of collection sites, species accumulation curves, ancestral reconstruction and additio... more

Habitats: Ecological and morphological considerations from Ancient plants with ancient fungi: liverworts associate with early-diverging arbuscular mycorrhizal fungi

Further detail on the impacts of habitat on fungal colonisation of liverworts

Supplementary material from "Ancient plants with ancient fungi: liverworts associate with early-diverging arbuscular mycorrhizal fungi

Arbuscular mycorrhizas are widespread in land plants including liverworts, some of the closest li... more 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.

Genetic, cellular and molecular interactions in the establishment of arbuscular mycorrhizas

Mycorrhizal Symbiosis, 2008

Publisher Summary Development of arbuscular mycorrhizas (AM) involves a well-synchronized sequenc... more Publisher Summary Development of arbuscular mycorrhizas (AM) involves a well-synchronized sequence of events, during which morphogenetic changes to both fungus and plant take place, supporting the maintenance of a compatible, biotrophic symbiosis. This chapter discusses the genetic, cellular, and molecular interactions in the establishment of arbuscular mycorrhizas. Research in the last 10 years has revolutionized our understanding of genetic programming and control of AM colonization, although much detail remains to be revealed. The development of arbuscular mycorrhizas is under the control of plant and fungal genes, which act in a coordinated manner to produce the characteristic, biotrophic, and compatible interaction in AM plants. It is possible to describe the colonization process in precise terms and with the help of increasing numbers of mutants, identify key regulatory steps and some of the genes that control them. Signaling between the symbionts, particularly prior to contact, is now confirmed, and the identification of the molecules involved is likely to lead to much increased understanding of both the receptors with which the signals interact and of the roles of signals and receptors in facilitating integrated symbiotic development, as well as in conferring plant–fungus selectivity or specificity. Major advances have also been made in showing how gene expression is altered in both symbionts. The reasons the AM fungi, which have many similarities with damaging plant pathogens, fail to trigger major defense responses in plants have intrigued researchers for many years. In AM symbioses, some defense responses are apparently mobilized for a short period but are later suppressed.

Genetic, cellular and molecular interactions in the establishment of VA mycorrhizas

Mycorrhizal Symbiosis, 2002

Growth and carbon economy of arbuscular mycorrhizal symbionts

Mycorrhizal Symbiosis, 2008

This chapter discusses the physiological interactions between the symbionts in arbuscular mycorrh... more This chapter discusses the physiological interactions between the symbionts in arbuscular mycorrhizal (AM) plants in terms of reciprocal transfer of organic carbon (C) and soil-derived nutrients between the symbionts, the C economy of the symbioses and the growth responses of the plants to colonization by AM fungi. AM fungi are dependent on an organic C supply from a photosynthetic partner. Between 4 and 20% of net photosynthate is transferred to the fungus and used in both production of both vegetative and reproductive structures, and in respiration to support growth and maintenance, including nutrient uptake. Hexoses are absorbed by the intraradical fungal structures, rapidly converted to lipid and glycogen, and exported to the external mycelium, which itself has little or no capacity either for organic C uptake from the environment or for lipid synthesis. There appears to be considerable variation in the C expended by different AM fungi in the transfer of P to the plant. Expenditure of fixed C by the plant to maintain the fungal symbiont can be regarded as an investment, resulting in greater efficiency of nutrient acquisition when nutrient availability in the soil is low, and sometimes in luxury accumulation of nutrients for later use. The magnitude of plant responses to AM colonization responses is influenced by both environmental factors (e.g., nutrient availability and irradiance) and biotic factors (such as the identity of fungal symbionts), as well as by community interactions. Attempts to make cost-benefit analyses of the symbiosis have proved difficult, because of the complex ways in which both AM colonization and plant growth respond to and interact with mineral nutrition. It is generally accepted that plants of the same and different species may be linked into common mycelial network (CMN), which facilitates C movement between the linked plants.

Nitrogen mobilization and nutrition in ectomycorrhizal plants

Mycorrhizal Symbiosis, 2008

Constraints upon plant growth imposed by low availability of N are a characteristic feature of ma... more Constraints upon plant growth imposed by low availability of N are a characteristic feature of many ecosystems dominated by ectomycorrhizal (ECM) plants. The potential importance of organic N sources for the nutrition of mycorrhizal plants came from studies first of ericoid mycorrhiza (ERM) and then of ECM symbioses. The ease with which many ECM fungi can be grown in axenic culture has enabled screening of their abilities to use different forms of N. Most species readily use ammonium, nitrate, and some simple organic N compounds, although there are differences at both the inter- and intraspecific levels. Much new information has been gained concerning the biochemistry of N assimilation, in particular in relation to the enzymes involved in assimilation of ammonium, which in many ECM fungi, appears to be the preferred source of inorganic N. Progress has been made towards characterization of the processes of nitrate and ammonium uptake and transport at the molecular levels. This has enabled a better understanding of the mechanisms and pathways whereby uptake of mineral N sources takes place in ECM symbioses. It has been recognized that much of the N contained in the superficial layer of soil occupied by ECM roots is in organic form and that some ECM fungi have access to these more complex N sources. The molecular studies, mostly using Amanita muscaria, by revealing N dependent expression profiles of N importer genes, have enabled us to envisage how N uptake by the fungi and transfer to the plant may occur in nature. The pathways and processes involved in the import and transfer of N across the ECM interfaces are intrinsically linked to those by which carbon is transferred in the reverse direction.

Vesicular-arbuscular mycorrhizas in agriculture and horticulture

Mycorrhizal Symbiosis, 2002

This chapter explores vesicular arbuscular (VA) mycorrhizas. The mycorrhizal type is used in agri... more This chapter explores vesicular arbuscular (VA) mycorrhizas. The mycorrhizal type is used in agriculture and horticulture. There are many instances where crop productivity is influenced by the VA mycorrhizal symbiosis, but as yet, there are few examples where inoculation or management is carried out in normal commercial production. These attempts have received most publicity in developed and highly mechanized agricultural, horticultural, or forestry systems. In these systems, the application of large amounts of fertilizers and pesticides is normal and accepted practice, and the potential of making money from the sale of inoculum has attracted interest from biotechnology companies. Relatively less attention is paid to the establishment or maintenance of production systems that are sustainable by preserving (or improving) soil resources, as well as economic productivity. The possible economic benefits of managing mycorrhizal populations in agriculture and horticulture need to be critically assessed in the context of the ecology of the systems, not simply the growth of crops. In most cases, experiments have been carried out with annual crops grown in monoculture. However, tree crops are also important and, particularly in developing countries, are sometimes cultivated in plantations or gardens with considerable diversity of species.

Mycorrhizas in ecological interactions

Mycorrhizal Symbiosis, 2008

Mycorrhizal symbioses are prevalent in all major terrestrial biomes. The researchers are now acti... more Mycorrhizal symbioses are prevalent in all major terrestrial biomes. The researchers are now actively addressing the questions that relate to the biology of mycorrhizal plants in natural environments, such as whether there are impacts of mycorrhizal colonization on the fitness of individual plants. Do mycorrhizal fungi influence the outcome of competitive interactions? Investigations have explored the contributions of mycorrhizas to fitness of individuals and species, to outcomes of competitive interactions between species, and to the possibility that mycorrhizal status may change both the ability of plants to coexist and the diversity of plant assemblages. With the wider recognition of structural and functional diversity among different mycorrhizal partnerships, has come the appreciation that the interdependence of plant and fungal partners may lead to changes in fungal, as well as plant communities. This chapter discusses the current research and understanding on the ecological interactions of mycorrhizas. The recognition of stimulatory effects of some classes of bacteria on the processes of ectomycorrhiza (ECM) colonization of roots has heightened awareness of the complexities of microbial interactions in soil. There are many reports of the interactions between mycorrhizal colonization of plants and the incidence and severity of diseases caused by plant pathogens. The effects are variable and influenced by plant nutrition, relative density of the inoculum of the pathogen and mycorrhizal fungus, and whether or not the plants were mycorrhizal before being challenged with propagules of the pathogen. It has long been recognized that hyphae of arbuscular mycorrhizal (AM) fungi are important binding agents in soil. Exudates from hyphae of quite specialized types have been suggested to be important contributors to stabilization of soil structure by AM fungi. The outcomes of multitrophic interactions are variable and mechanisms even less well understood. They are, however, likely to play significant roles in nature.

The symbionts forming arbuscular mycorrhizas

Mycorrhizal Symbiosis, 2008

This chapter focuses on fungi symbionts that form arbuscular mycorrhizas (AM). AM are the most co... more This chapter focuses on fungi symbionts that form arbuscular mycorrhizas (AM). AM are the most common mycorrhizal type. They are formed in an enormously wide variety of host plants by obligately symbiotic fungi, which have recently been reclassified on the basis of DNA sequences into a separate fungal phylum, the Glomeromycota. The plants include angiosperms, gymnosperms, and the sporophytes of pteridophytes, all of have roots, as well as the gametophytes of some hepatics and pteridophytes, which do not. Through their roles in nutrient uptake, AM fungi were probably important in the colonization of land by plants and they remain major determinants of plant interactions in ecosystems to the present day. The name “arbuscular” is derived from characteristic structures, the arbuscules, which occur within the cortical cells of many plant roots, and also some mycothalli colonized by AM fungi. An arbuscular mycorrhiza has three important components: the root itself, the fungal structures within and between the cells of the root, and an extraradical mycelium in the soil. AM fungi have been recognized as obligate symbionts of a very wide range of plant species. The symbioses are biotrophic and normally mutualistic, the long-term compatible interactions being based largely on bidirectional nutrient transfer between the symbionts, sometimes supplemented by other benefits such as drought and disease tolerance. There is increasing evidence for specificity or selectivity of some plant species for particular fungal symbionts. Non-mycorrhizal plants and plants which form more than one type of mycorrhiza are found in a number of families, supporting the idea that loss of AM status or gain of another type of mycorrhiza has evolved many times, probably as a result of different selection pressures and based on different mechanisms.

Ectendomycorrhizas

Mycorrhizal Symbiosis, 2002

Nitrogen nutrition of ectomycorrhizal plants

Mycorrhizal Symbiosis, 2002

This chapter examines low availability of nitrogen and its impact on many ecosystems dominated by... more This chapter examines low availability of nitrogen and its impact on many ecosystems dominated by ectomycorrhizal plants. Thus, in the extensive boreal and temperate forests of the northern hemisphere, nitrogen (N) is the most important determinant of productivity. Therefore, it is essential to establish the mechanisms and processes whereby the element is mobilized, assimilated, and transported. The quest to artificially introduce nitrogen in the soil has led to scientific research and experimentation with ammonium and ectomycorrhizal fungi. The ease with which many ectomycorrhizal fungi can be grown in axenic culture has enabled extensive screening of their abilities to use different forms of nitrogen. Most species readily use NH 4 , NO 3, and some simple organic N compounds, although there are differences at both the inter and intraspecific levels. Several new information is gained concerning the biochemistry of N assimilation—in particular in relation to the enzymes involved in the assimilation of NH 4 —that in many ectomycorrhizal fungi appears to be the preferred source of inorganic nitrogen. These studies have been extended to allow analysis of N assimilation by the fungi when grown in the mycorrhizal condition and, importantly, to investigate the influence of the plant upon the pattern of events.

European and African maize cultivars differ in their physiological and molecular responses to mycorrhizal infection

New Phytologist, 2005

Physiological and molecular responses to phosphorus (P) supply and mycorrhizal infection by Glomu... more Physiological and molecular responses to phosphorus (P) supply and mycorrhizal infection by Glomus intraradices were compared in European (River) and African (H511) maize (Zea mays) cultivars to examine the extent to which these responses differed between plants developed for use in high- and low-nutrient-input agricultural systems. Biomass, photosynthetic rates, nutrient and carbohydrate contents, mycorrhizal colonization and nutrient-responsive phosphate transporter gene expression were measured in nonmycorrhizal and mycorrhizal plants grown at different inorganic phosphorus (P(i)) supply rates. Nonmycorrhizal River plants grew poorly at low P(i) but were highly responsive to mycorrhizal infection; there were large increases in biomass, tissue P content and the rate of photosynthesis and a decline in the expression of phosphate transporter genes. Nonmycorrhizal H511 plants grew better than River plants at low P(i), and had a higher root : shoot ratio. However, the responses of H511 plants to higher P(i) supplies and mycorrhizal infection were much more limited than those of River plants. The adaptations that allowed nonmycorrhizal H511 plants to perform well in low-P soils limited their ability to respond to higher nutrient supply rates and mycorrhizal infection. The European variety had not lost the ability to respond to mycorrhizas and may have traits useful for low-nutrient agriculture where mycorrhizal symbioses are established.

The dawn of symbiosis between plants and fungi

Biology Letters, 2011

The colonization of land by plants relied on fundamental biological innovations, among which was ... more 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 member...

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Ancient plants with ancient fungi: liverworts associate with early-diverging arbuscular mycorrhizal fungi

Proceedings of the Royal Society B: Biological Sciences, 2018

Arbuscular mycorrhizas are widespread in land plants including liverworts, some of the closest li... more 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...

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Fungal specificity bottlenecks during orchid germination and development

Molecular Ecology, 2008

Fungus‐subsidized growth through the seedling stage is the most critical feature of the life hist... more Fungus‐subsidized growth through the seedling stage is the most critical feature of the life history for the thousands of mycorrhizal plant species that propagate by means of ‘dust seeds.’ We investigated the extent of specificity towards fungi shown by orchids in the genera Cephalanthera and Epipactis at three stages of their life cycle: (i) initiation of germination, (ii) during seedling development, and (iii) in the mature photosynthetic plant. It is known that in the mature phase, plants of these genera can be mycorrhizal with a number of fungi that are simultaneously ectomycorrhizal with the roots of neighbouring forest trees. The extent to which earlier developmental stages use the same or a distinctive suite of fungi was unclear. To address this question, a total of 1500 packets containing orchid seeds were buried for up to 3 years in diverse European forest sites which either supported or lacked populations of helleborine orchids. After harvest, the fungi associated with the...

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Accumulation of pollutant nitrogen in calcareous and acidic grasslands: Evidence from N flux and 15N tracer studies

Water, Air, & Soil Pollution: Focus, 2005

Semi-natural calcareous and acidic grasslands are known to be sensitive to increased atmospheric ... more Semi-natural calcareous and acidic grasslands are known to be sensitive to increased atmospheric N deposition. However, the fate of pollutant N within these systems is unknown. This paper reports on the first studies to determine the fate of added N within a calcareous and an acidic grassland subject to long-term simulated enhanced N deposition. Intact soil/turf cores were removed from field plots treated for six years with enhanced N deposition (ambient +0, +35 and +140 kg N ha -1 year -1 ). Cores were inserted into lysimeters and output fluxes of N were monitored in detail. Complete N budgets -calculated from the N flux data -showed considerable accumulation of N within the treated grasslands, up to 76% and 38% of pollutant N in the calcareous and acidic grasslands respectively. In the second study, the short-term (21 day) fate of pollutant N was determined by tracing 15 N labelled ammonium nitrate (+35 kg N ha -1 year -1 ) though the acidic and calcareous lysimeters into plant, soil and leachate pools. Up to 91% and 59% of 15 N was recovered in soils and vegetation of the calcareous and acidic grasslands respectively, with negligible amounts recovered in soil extractable ammonium and nitrate (<0.3%) and in leachate (<0.02%). This rapid short-term immobilisation of pollutant N supports the long-term accumulation of the element calculated from the N flux study.

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Transfer of recent photosynthate into mycorrhizal mycelium of an upland grassland: short-term respiratory losses and accumulation of 14C

Soil Biology and Biochemistry, 2002

ABSTRACT The movement of carbon from plants into their natural communities of arbuscular-mycorrhi... more ABSTRACT The movement of carbon from plants into their natural communities of arbuscular-mycorrhizal (AM) fungi was investigated. Mesh-bound cores, which allowed in-growth of AM mycelium to be controlled but excluded roots, were inserted into turf monoliths removed from an upland grassland and were exposed to 14CO2. Flux of 14C-labelled carbon from plants to hyphae of AM fungi for 70h post-labelling was measured by (a) trapping CO2 released from soil cores containing AM hyphae linked to the plants compared to cores from which AM hyphal connections to the plant roots had been severed, and (b) quantification of the total amount of 14C in the cores. Release of 14CO2 from the cores colonised by active AM mycelium was highest for 0–28h from the onset of labelling and declined rapidly thereafter. The amount of 14C allocated into mycorrhizal mycelium 0–70h after labelling accounted for 3.4% of the 14C initially fixed by the plants. The results confirm the rapidity of photosynthate allocation to AM mycelium and demonstrate the importance of the short-term dynamics of C fluxes in undisturbed grasslands.

Soil Invertebrates Disrupt Carbon Flow Through Fungal Networks

Science, 2005

Annual carbon flux through soil respiration is ten times greater than fossil fuel combustion, but... more Annual carbon flux through soil respiration is ten times greater than fossil fuel combustion, but its component parts are poorly understood because they are the product of complex multitrophic interactions between soil organisms. A major component of carbon flux from plants to soil occurs through networks of symbiotic arbuscular mycorrhizal fungi. Here, using 13 CO 2 pulse labeling, we show that natural densities of the numerically dominant fungal feeding invertebrate Protaphorura armata (order Collembola) reduces 13 C enrichment of mycorrhizosphere respiration by 32%. Our findings emphasize the importance of multitrophic interactions in regulating respiration of recent plant photosynthate from soil.

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