ABSTRACT
Arbuscular mycorrhizal (AM) fungi engage in symbiosis with more than 80% of terrestrial plants, enlarging root phosphorus (P) absorption volume by producing extensive extraradical hyphae (ERH) in the soil. In addition, AM fungi recruit and cooperate with soil bacteria to enhance soil organic P mobilization and improve fungal and plant fitness through hyphal exudates. However, the role of the dominant compounds in the hyphal exudates in enhancing organic P mobilization in the mycorrhizal pathway is still not well understood. In this study, we added sugars, i.e., glucose, fructose, and trehalose, which are detected in the hyphal exudates, to the hyphal compartments (HCs) that allowed the ERH of the AM fungus to grow or not. The results showed that in AM fungus-inoculated pots, adding three sugars at a concentration of 2 mmol C kg-1 soil significantly increased the phosphatase activity and facilitated the mobilization of organic P in the HCs. The addition of fructose at a concentration of 2 mmol C kg-1 soil was the most efficient in increasing the phosphatase activity and enhancing organic P mobilization. The released inorganic P was then absorbed by the ERH of the AM fungus. The enhanced mobilization of organic P was correlated with the increase in phoD gene number and the changing bacterial community in the presence of fungal hyphae. The sugar addition enriched the relative abundance of some bacterial taxa, e.g., Betaproteobacteriales. Our study suggested that the addition of the sugars by mycorrhizae could be a pivotal strategy in managing P uptake in agricultural production, potentially directing future practices to optimize plant-fungi-bacteria interactions for improved P use efficiency.
ABSTRACT
KEY MESSAGE: Characterisation and genetic mapping of a key gene defining root morphology in bread wheat. Root morphology is central to plants for the efficient uptake up of soil water and mineral nutrients. Here we describe a conditional mutant of hexaploid wheat (Triticum aestivum L.) that when grown in soil with high Ca2+ develops a larger rhizosheath accompanied with shorter roots than the wild type. In wheat, rhizosheath size is a reliable surrogate for root hair length and this was verified in the mutant which possessed longer root hairs than the wild type when grown in high Ca2+ soil. We named the mutant Stumpy and showed it to be due to a single semi-dominant mutation. The short root phenotype at high Ca2+ was due to reduced cellular elongation which might also explain the long root hair phenotype. Analysis of root cell walls showed that the polysaccharide composition of Stumpy roots is remodelled when grown at non-permissive (high) Ca2+ concentrations. The mutation mapped to chromosome 7B and sequencing of the 7B chromosomes in both wild type and Stumpy identified a candidate gene underlying the Stumpy mutation. As part of the process to determine whether the candidate gene was causative, we identified wheat lines in a Cadenza TILLING population with large rhizosheaths but accompanied with normal root length. This finding illustrates the potential of manipulating the gene to disconnect root length from root hair length as a means of developing wheat lines with improved efficiency of nutrient and water uptake. The Stumpy mutant will be valuable for understanding the mechanisms that regulate root morphology in wheat.
Subject(s)
Soil , Triticum , Triticum/metabolism , Mutation , Chromosome Mapping , Water/metabolism , Plant Roots/geneticsABSTRACT
Efficient micronutrient acquisition is a critical factor in selecting micronutrient dense crops for human consumption. Enhanced exudation and re-uptake of metal chelators, so-called phytosiderophores, by roots of graminaceous plants has been implicated in efficient micronutrient acquisition. We compared PS biosynthesis and exudation as a response mechanism to either Fe, Zn or Cu starvation. Two barley (Hordeum vulgare L.) lines with contrasting micronutrient grain yields were grown hydroponically and PS exudation (LC-MS) and root gene expression (RNAseq) were determined after either Fe, Zn, or Cu starvation. The response strength of the PS pathway was micronutrient dependent and decreased in the order Fe > Zn > Cu deficiency. We observed a stronger expression of PS pathway genes and greater PS exudation in the barley line with large micronutrient grain yield suggesting that a highly expressed PS pathway might be an important trait involved in high micronutrient accumulation. In addition to several metal specific transporters, we also found that the expression of IRO2 and bHLH156 transcription factors was not only induced under Fe but also under Zn and Cu deficiency. Our study delivers important insights into the role of the PS pathway in the acquisition of different micronutrients.
Subject(s)
Hordeum , Iron , Humans , Iron/metabolism , Zinc/metabolism , Hordeum/genetics , Hordeum/metabolism , Copper/metabolism , Micronutrients/metabolism , Plant Roots/metabolismABSTRACT
Arbuscular mycorrhizal (AM) fungi-associated hyphosphere microbiomes can be considered as the second genome of the mycorrhizal phosphorus uptake pathway. Their composition can be thought of as a stably recurring component of a holobiont, defined by the hyphosphere core microbiome, which is thought to benefit AM fungal fitness. Here, we review evidence indicating the existence of the hyphosphere core microbiome, highlight its functions linked to those functions lacking in AM fungi, and further explore the mechanisms by which different core members ensure their stable coexistence. We conclude that deciphering and utilizing the hyphosphere core microbiome provides an entry point for understanding the complex interactions among plants, AM fungi, and bacteria.
ABSTRACT
Future crops need to be sustainable in the face of climate change. Modern barley varieties have been bred for high productivity and quality; however, they have suffered considerable genetic erosion, losing crucial genetic diversity. This renders modern cultivars vulnerable to climate change and stressful environments. We highlight the potential to tailor crops to a specific environment by utilising diversity inherent in an adapted landrace population. Tapping into natural biodiversity, while incorporating information about local environmental and climatic conditions, allows targeting of key traits and genotypes, enabling crop production in marginal soils. We outline future directions for the utilisation of genetic resources maintained in landrace collections to support sustainable agriculture through germplasm development via the use of genomics technologies and big data.
Subject(s)
Hordeum , Soil , Hordeum/genetics , Plant Breeding , Agriculture , Adaptation, Physiological/genetics , Crops, Agricultural/geneticsABSTRACT
The extraradical hyphae of arbuscular mycorrhizal (AM) fungi are colonized by different bacteria in natural and agricultural systems, but the mechanisms by which AM fungi interact with the hyphosphere soil microbiome and influence soil organic phosphorus (P) mobilization remain unclear. We grew Medicago in two-compartment microcosms, inoculated with Rhizophagus irregularis, or not, in the root compartment and set up P treatments (without P, with P addition as KH2 PO4 or nonsoluble phytate) in the hyphal compartment. We studied the processes of soil P turnover and characterized the microbiome functional profiles for P turnover in the hyphosphere soil by metagenomic sequencing. Compared with the bulk soil, the hyphosphere soil of R. irregularis was inhabited by a specific bacterial community and their functional profiles for P turnover was stimulated. At the species level, the shift in hyphosphere soil microbiome was characterized by the recruitment of the genome bin2.39 harbouring both gcd and phoD genes and genome bin2.97 harbouring the phoD gene, which synergistically drove nonsoluble phytate mobilization in the hyphosphere soil. Our results suggest that AM fungi recruits a specific hyphosphere soil microbiome and stimulated their functional profiles for P turnover to enhance utilization of phytate.
Subject(s)
Microbiota , Mycorrhizae , Mycorrhizae/metabolism , Phosphorus/metabolism , Soil , Phytic Acid/metabolism , Fungi/metabolism , Bacteria/metabolism , Plant Roots/metabolism , Soil MicrobiologyABSTRACT
The mycorrhizal pathway is an important phosphorus (P) uptake pathway for more than two-thirds of land plants. The arbuscular mycorrhizal (AM) fungi-associated hyphosphere microbiome has been considered as the second genome of mycorrhizal P uptake pathway and functionality in mobilizing soil organic P (Po). However, whether there is a core microbiome in the hyphosphere and how this is implicated in mining soil Po are less understood. We established on-site field trials located in humid, semiarid, and arid zones and a microcosm experiment in a glasshouse with specific AM fungi and varying soil types to answer the above questions. The hyphosphere microbiome of AM fungi enhanced soil phosphatase activity and promoted Po mineralization in all sites. Although the assemblage of hyphosphere microbiomes identified in three climate zones was mediated by environmental factors, we detected a core set in three sites and the subsequent microcosm experiment. The core members were co-enriched in the hyphosphere and dominated by Alphaproteobacteria, Actinobacteria, and Gammaproteobacteria. Moreover, these core bacterial members aggregate into stable guilds that contributed to phosphatase activity. The core hyphosphere microbiome is taxonomically conserved and provides functions, with respect to the mineralization of Po, that AM fungi lack.
Subject(s)
Microbiota , Mycorrhizae , Mycorrhizae/metabolism , Phosphorus/metabolism , Fungi/metabolism , Bacteria/metabolism , Soil , Soil Microbiology , Phosphoric Monoester Hydrolases/metabolism , Plant Roots/metabolismABSTRACT
Microbial immobilization of fertilizer nitrogen (N) can effectively reduce N losses in soil. However, the effects of crop residue on microbial assimilation of fertilizer-N and the underlying microbial mechanisms in upland soils are unclear. We evaluated the influence of maize residue (13C) addition on the microbial assimilation of ammonium-N (15N) in DNA from fertilizer, and quantified the bacterial 13C or 15N assimilation by quantitative stable isotope probing (DNA-qSIP). We found that the straw addition did increase total microbial assimilation of ammonium from fertilizer during the 2-week incubation. However, bacterial taxa varied in their responses to straw addition: Bacteriodetes and Proteobacteria accounted for large fractions of ammonium assimilation and their N assimilations were increased, while N assimilations of Acidobacteria were decreased. We revealed that highly 13C-labeled taxa were the main contributors of N assimilation under straw addition. The straw primarily enhanced the contributions of bacterial taxa to ammonium assimilation through increasing the extent of N assimilation, or enhancing the abundance of the N-assimilating bacterial taxa. Overall, our study elucidated an interaction between microbial assimilation of fertilizer-N and straw-C, showing a close element coupling of the keystone functional microbial taxa in N immobilization driven by organic carbon.
Subject(s)
Ammonium Compounds , Fertilizers , Bacteria , Carbon , DNA , Fertilizers/analysis , Nitrogen/analysis , Soil/chemistry , Soil MicrobiologyABSTRACT
Ongoing climate change is resulting in increasing areas of salinity affected soils, rising saline groundwater and droughts resulting in irrigation with brackish water. This leads to increased salinity stress in crops that are already grown on marginal agricultural lands, such as barley. Tolerance to salinity stress is limited in the elite barley cultivar pools, but landraces of barley hold potential sources of tolerance due to their continuous selection on marginal lands. This study analyzed 140 heritage cultivars and landrace lines of barley, including 37 Scottish Bere lines that were selected from coastal regions, to screen for tolerance to salinity stress. Tolerance to salinity stress was screened by looking at the germination speed and the early root growth during germination, and the pre-maturity biomass accumulation during early growth stages. Results showed that most lines increased germination time, and decreased shoot biomass and early root growth with greater salinity stress. Elite cultivars showed increased response to the salinity, compared to the landrace lines. Individual Bere and landrace lines showed little to no effect of increased salinity in one or more experiments, one line showed high salinity tolerance in all experiments-Bere 49 A 27 Shetland. A Genome Wide Association Screening identified a number of genomic regions associated with increased tolerance to salinity stress. Two chromosomal regions were found, one associated with shoot biomass on 5HL, and another associated with early root growth, in each of the salinities, on 3HS. Within these regions a number of promising candidate genes were identified. Further analysis of these new regions and candidate genes should be undertaken, along with field trials, to identify targets for future breeding for salinity tolerance.
ABSTRACT
Better understanding of the mechanistic basis of plant plasticity will enhance efforts to breed crops resilient to predicted climate change. However, complexity in plasticity's conceptualisation and measurement may hinder fruitful crossover of concepts between disciplines that would enable such advances. We argue active adaptive plasticity is particularly important in shaping the fitness of wild plants, representing the first line of a plant's defence to environmental change. Here, we define how this concept may be applied to crop breeding, suggest appropriate approaches to measure it in crops, and propose a refocussing on active adaptive plasticity to enhance crop resilience. We also discuss how the same concept may have wider utility, such as in ex situ plant conservation and reintroductions.
Subject(s)
Crops, Agricultural , Plant Breeding , Adaptation, Physiological/genetics , Climate Change , Crops, Agricultural/geneticsABSTRACT
Great potential exists to harness plant traits at the root-soil interface, mainly rhizodeposition and root hairs, to 'build' soils with better structure that can trap more carbon and resources, resist climate stresses, and promote a healthy microbiome. These traits appear to have been preserved in modern crop varieties, but scope exists to improve them further because they vary considerably between genotypes and respond to environmental conditions. From emerging evidence, rhizodeposition can act as a disperser, aggregator, and/or hydrogel in soil, and root hairs expand rhizosheath size. Future research should explore impacts of selecting these traits on plants and soils concurrently, expanding from model plants to commercial genotypes, and observing whether impacts currently limited to glasshouse studies occur in the field.
Subject(s)
Plant Roots , Soil , Genotype , Phenotype , Plant Roots/chemistry , Plant Roots/genetics , Plants , Rhizosphere , Soil/chemistry , Soil MicrobiologyABSTRACT
A culture collection of 41 bacteria isolated from the rhizosphere of cultivated barley (Hordeum vulgare subsp. vulgare) is available at the Division of Plant Sciences, University of Dundee (UK). The data include information on genes putatively implicated in nitrogen fixation, HCN channels, phosphate solubilization, and linked whole-genome sequences.
ABSTRACT
More than two-thirds of terrestrial plants acquire nutrients by forming a symbiosis with arbuscular mycorrhizal (AM) fungi. AM fungal hyphae recruit distinct microbes into their hyphosphere, the narrow region of soil influenced by hyphal exudates. They thereby shape this so-called second genome of AM fungi, which significantly contributes to nutrient mobilization and turnover. We summarize current insights into characteristics of the hyphosphere microbiome and the role of hyphal exudates on orchestrating its composition. The hyphal exudates not only contain carbon-rich compounds but also promote bacterial growth and activity and influence the microbial community structure. These effects lead to shifts in function and cause changes in organic nutrient cycling, making the hyphosphere a unique and largely overlooked functional zone in ecosystems.
Subject(s)
Microbiota , Mycorrhizae , Bacteria/metabolism , Fungi/metabolism , Mycorrhizae/metabolism , Nitrogen/metabolism , Plant Roots/metabolism , Soil/chemistry , Soil MicrobiologyABSTRACT
BACKGROUND AND AIMS: Some Caryophyllales species accumulate abnormally large shoot sodium (Na) concentrations in non-saline environments. It is not known whether this is a consequence of altered Na partitioning between roots and shoots. This paper tests the hypotheses (1) that Na concentrations in shoots ([Na]shoot) and in roots ([Na]root) are positively correlated among Caryophyllales, and (2) that shoot Na hyperaccumulation is correlated with [Na]shoot/[Na]root quotients. METHODS: Fifty two genotypes, representing 45 Caryophyllales species and 4 species from other angiosperm orders, were grown hydroponically in a non-saline, complete nutrient solution. Concentrations of Na in shoots and in roots were determined using inductively coupled plasma mass spectrometry (ICP-MS). KEY RESULTS: Sodium concentrations in shoots and roots were not correlated among Caryophyllales species with normal [Na]shoot, but were positively correlated among Caryophyllales species with abnormally large [Na]shoot. In addition, Caryophyllales species with abnormally large [Na]shoot had greater [Na]shoot/[Na]root than Caryophyllales species with normal [Na]shoot. CONCLUSIONS: Sodium hyperaccumulators in the Caryophyllales are characterized by abnormally large [Na]shoot, a positive correlation between [Na]shoot and [Na]root, and [Na]shoot/[Na]root quotients greater than unity.
Subject(s)
Caryophyllales , Magnoliopsida , Magnoliopsida/genetics , Plant Roots/chemistry , Plant Shoots/genetics , SodiumABSTRACT
Our understanding of plant-microbe interactions in soil is limited by the difficulty of observing processes at the microscopic scale throughout plants' large volume of influence. Here, we present the development of three-dimensional live microscopy for resolving plant-microbe interactions across the environment of an entire seedling growing in a transparent soil in tailor-made mesocosms, maintaining physical conditions for the culture of both plants and microorganisms. A tailor-made, dual-illumination light sheet system acquired photons scattered from the plant while fluorescence emissions were simultaneously captured from transparent soil particles and labeled microorganisms, allowing the generation of quantitative data on samples â¼3,600 mm3 in size, with as good as 5 µm resolution at a rate of up to one scan every 30 min. The system tracked the movement of Bacillus subtilis populations in the rhizosphere of lettuce plants in real time, revealing previously unseen patterns of activity. Motile bacteria favored small pore spaces over the surface of soil particles, colonizing the root in a pulsatile manner. Migrations appeared to be directed toward the root cap, the point of "first contact," before the subsequent colonization of mature epidermis cells. Our findings show that microscopes dedicated to live environmental studies present an invaluable tool to understand plant-microbe interactions.
Subject(s)
Bacillus subtilis/metabolism , Microscopy/methods , Plant Roots/microbiology , Rhizosphere , Seedlings/microbiology , Calibration , Environment , Equipment Design , Fluorescence , Image Processing, Computer-Assisted , Lactuca , Plant Roots/growth & development , Seedlings/growth & development , Silicon , Soil , Soil Microbiology , TemperatureABSTRACT
Arbuscular mycorrhizal (AM) fungi gain access to nutrient patches outside the rhizosphere by producing an extensive network of fine hyphae. Here, we focused on establishing the mechanism by which AM fungal hyphae reach discrete organic patches with a cohort of functional bacteria transported in a biofilm on their surface. We investigated the mechanisms and impact of the translocation of phosphate solubilising bacteria (PSB) along AM fungal hyphae in bespoke microcosms. An in vitro culture experiment was also conducted to determine the direct impact of hyphal exudates of AM fungi upon the growth of PSB. The extraradical hyphae of AM fungi can transport PSB to organic phosphorus (P) patches and enhance organic P mineralisation both under in vitro culture and soil conditions. Bacteria move in a thick water film formed around fungal hyphae. However, the bacteria cannot be transferred to the organic P patch without an energy source in the form of hyphal exudates. Our results could be harnessed to better manage plant-microbe interactions and improve the ability of biological inocula involving AM fungi and bacteria to enhance the sustainability of agricultural crops in P limited conditions.
Subject(s)
Mycorrhizae , Bacteria , Hyphae , Phosphorus , Plant Roots , Soil MicrobiologyABSTRACT
Plant roots are usually colonized by various arbuscular mycorrhizal (AM) fungal species, which vary in morphological, physiological, and genetic traits. This colonization constitutes the mycorrhizal nutrient uptake pathway (MP) and supplements the pathway through roots. Simultaneously, the extraradical hyphae of each AM fungus is associated with a community of bacteria. However, whether the community structure and function of the microbiome on the extraradical hyphae differ between AM fungal species remains unknown. In order to understand the community structure and the predicted functions of the microbiome associated with different AM fungal species, a split-root compartmented rhizobox cultivation system, which allowed us to inoculate two AM fungal species separately in two root compartments, was used. We inoculated two separate AM fungal species combinations, (i) Funneliformis mosseae and Gigaspora margarita and (ii) Rhizophagus intraradices and G. margarita, on a single root system of cotton. The hyphal exudate-fed, active microbiome was measured by combining 13C-DNA stable isotope probing with MiSeq sequencing. We found that different AM fungal species, which were simultaneously colonizing a single root system, hosted active microbiomes that were distinct from one another. Moreover, the predicted potential functions of the different microbiomes were distinct. We conclude that the arbuscular mycorrhizal fungal component of the system is responsible for the recruitment of distinct microbiomes in the hyphosphere. The potential significance of the predicted functions of the microbial ecosystem services is discussed.IMPORTANCE Arbuscular mycorrhizal (AM) fungi form tight symbiotic relationships with the majority of terrestrial plants and play critical roles in plant P acquisition, adding a further dimension of complexity. The plant-AM fungus-bacterium system is considered a continuum, with the bacteria colonizing not only the plant roots, but also the associated mycorrhizal hyphal network, known as the hyphosphere microbiome. Plant roots are usually colonized by different AM fungal species which form an independent phosphorus uptake pathway from the root pathway, i.e., the mycorrhizal pathway. The community structure and function of the hyphosphere microbiome of different AM species are completely unknown. In this novel study, we found that arbuscular mycorrhizal fungi cocolonizing on single plant roots recruit their own specific microbiomes, which should be considered in evaluating plant microbiome form and function. Our findings demonstrate the importance of understanding trophic interactions in order to gain insight into the plant-AM fungus-bacterium symbiosis.
ABSTRACT
Plants release carbon-based exudates from their roots into the rhizosphere to increase phosphorus (P) supply to the soil solution. However, if more P than required is brought into solution, additional P could be available for leaching from riparian soils. To investigate this further, soil columns containing a riparian arable and buffer strip soil, which differed in organic matter contents, were sown with three common agricultural and riparian grass species. The P loads in leachate were measured and compared with those from unplanted columns, which were 0.17 ± 0.01 and 0.89 ± 0.04 mg kg-1 for the arable and buffer strip soil, respectively. A mixture of ryegrass and red fescue significantly (p ≤ .05) increased dissolved inorganic P loads in leachate from the arable (0.23 ± 0.01 mg kg-1 ) and buffer strip soil (1.06 ± 0.05 mg kg-1 ), whereas barley significantly reduced P leaching from the buffer strip soil (0.53 ± 0.08 mg kg-1 ). This was dependent on the dissolved organic C released under different plant species and on interactions with soil management history and biogeochemical conditions, rather than on plant uptake of P and accumulation into biomass. This suggested that the amount and forms of P present in the soil and the ability of the plants to mobilize them could be key factors in determining how plants affect leaching of soil P. Selecting grass species for different stages of buffer strip development, basing species selection on root physiological traits, and correcting soil nutrient stoichiometry in riparian soils through vegetative mining could help to lower this contribution.
Subject(s)
Phosphorus , Poaceae , Carbon , Rhizosphere , SoilABSTRACT
BACKGROUND AND AIMS: Manganese (Mn) deficiency in barley is a global problem. It is difficult to detect in the early stages of symptom development and is commonly pre-emptively corrected by Mn foliar sprays that can be costly. Landraces adapted to marginal lands around the world represent a genetic resource for potential sustainability traits including mineral use efficiency. This research aims to confirm novel Mn use efficiency traits from the Scottish landrace Bere and use an association mapping approach to identify genetic loci associated with the trait. METHODS: A hydroponic system was developed to identify and characterize the Mn deficiency tolerance traits in a collection of landraces, including a large number of Scottish Bere barleys, a group of six-rowed heritage landraces grown in the highlands and islands of Scotland. Measuring chlorophyll fluorescence, the effect of Mn deficiency was identified in the early stages of development. Genotypic data, generated using the 50k Illumina iSelect genotyping array, were coupled with the Mn phenotypic data to create a genome-wide association study (GWAS) identifying candidate loci associated with Mn use efficiency. KEY RESULTS: The Bere lines generally had good Mn use efficiency traits. Individual Bere lines showed large efficiencies, with some Bere lines recording almost double chlorophyll fluorescence readings in limited Mn conditions compared with the elite cultivar Scholar. The Mn-efficient Bere lines had increased accumulation of Mn in their shoot biomass compared with elite cultivars, which was highly correlated to the chlorophyll fluorescence. Several candidate genes were identified as being associated with Mn use efficiency in the GWAS. CONCLUSIONS: Several genomic regions for Mn use efficiency traits originating from the Bere lines were identified. Further examination and validation of these regions should be undertaken to identify candidate genes for future breeding for marginal lands.
Subject(s)
Hordeum/genetics , Manganese , Genome-Wide Association Study , Phenotype , ScotlandABSTRACT
The ionome is the elemental composition of a living organism, its tissues, cells or cell compartments. The ionomes of roots, stems and leaves of 14 native Brazilian forest species were characterised to examine the relationships between plant and organ ionomes and the phylogenetic and ecological affiliations of species. The null hypothesis that ionomes of Brazilian forest species and their organs do not differ was tested. Concentrations of mineral nutrients in roots, stems and leaves were determined for 14 Brazilian forest species, representing seven angiosperm orders, grown hydroponically in a complete nutrient solution. The 14 species could be differentiated by their ionomes and the partitioning of mineral nutrients between organs. The ionomic differences between the 14 species did not reflect their phylogenetic relationships or successional ecology. Differences between shoot ionomes and root ionomes were greater than differences in the ionome of an organ when compared among genotypes. In conclusion, differences in ionomes of species and their organs reflect a combination of ancient phylogenetic and recent environmental adaptations.