Most cited article - PubMed ID 27549438
Monitoring CO2 emissions to gain a dynamic view of carbon allocation to arbuscular mycorrhizal fungi
Plant-plant interactions and coexistence can be directly mediated by symbiotic arbuscular mycorrhizal (AM) fungi through asymmetric resource exchange between the plant and fungal partners. However, little is known about the effects of AM fungal presence on resource allocation in mixed plant stands. Here, we examined how phosphorus (P), nitrogen (N) and carbon (C) resources were distributed between coexisting con- and heterospecific plant individuals in the presence or absence of AM fungus, using radio- and stable isotopes. Congeneric plant species, Panicum bisulcatum and P. maximum, inoculated or not with Rhizophagus irregularis, were grown in two different culture systems, mono- and mixed-species stands. Pots were subjected to different shading regimes to manipulate C sink-source strengths. In monocultures, P. maximum gained more mycorrhizal phosphorus uptake benefits than P.bisulcatum. However, in the mixed culture, the AM fungus appeared to preferentially transfer nutrients (33P and 15N) to P.bisulcatum compared to P. maximum. Further, we observed higher 13C allocation to mycorrhiza by P.bisulcatum in mixed- compared to the mono-systems, which likely contributed to improved competitiveness in the mixed cultures of P.bisulcatum vs. P. maximum regardless of the shading regime. Our results suggest that the presence of mycorrhiza influenced competitiveness of the two Panicum species in mixed stands in favor of those with high quality partner, P. bisulcatum, which provided more C to the mycorrhizal networks. However, in mono-species systems where the AM fungus had no partner choice, even the lower quality partner (i.e., P.maximum) could also have benefitted from the symbiosis. Future research should separate the various contributors (roots vs. common mycorrhizal network) and mechanisms of resource exchange in such a multifaceted interaction.
Arbuscular mycorrhizal (AM) fungi establish symbiotic associations with many plant species, transferring significant amounts of soil nutrients such as phosphorus to plants and receiving photosynthetically fixed carbon in return. Functioning of AM symbiosis is thus based on interaction between two living partners. The importance of dead AM fungal biomass (necromass) in ecosystem processes remains unclear. Here, we applied either living biomass or necromass (0.0004 potting substrate weight percent) of monoxenically produced AM fungus (Rhizophagus irregularis) into previously sterilized potting substrate planted with Andropogon gerardii. Plant biomass production significantly improved in both treatments as compared to non-amended controls. Living AM fungus, in contrast to the necromass, specifically improved plant acquisition of nutrients normally supplied to the plants by AM fungal networks, such as phosphorus and zinc. There was, however, no difference between the two amendment treatments with respect to plant uptake of other nutrients such as nitrogen and/or magnesium, indicating that the effect on plants of the AM fungal necromass was not primarily nutritional. Plant growth stimulation by the necromass could thus be either due to AM fungal metabolites directly affecting the plants, indirectly due to changes in soil/root microbiomes or due to physicochemical modifications of the potting substrate. In the necromass, we identified several potentially bioactive molecules. We also provide experimental evidence for significant differences in underground microbiomes depending on the amendment with living or dead AM fungal biomass. This research thus provides the first glimpse into possible mechanisms responsible for observed plant growth stimulation by the AM fungal necromass.
- Keywords
- Arbuscular mycorrhiza (AM), Mass spectrometry (MS), Metabolites, Microbiome, Necromass, Signal,
- MeSH
- Andropogon * MeSH
- Biomass MeSH
- Glomeromycota * MeSH
- Plant Roots MeSH
- Mycorrhizae * MeSH
- Symbiosis MeSH
- Publication type
- Journal Article MeSH
Research efforts directed to elucidation of mechanisms behind trading of resources between the partners in the arbuscular mycorrhizal (AM) symbiosis have seen a considerable progress in the recent years. Yet, despite of the recent developments, some key questions still remain unanswered. For example, it is well established that the strictly biotrophic AM fungus releases phosphorus to- and receives carbon molecules from the plant symbiont, but the particular genes, and their products, responsible for facilitating this exchange, are still not fully described, nor are the principles and pathways of their regulation. Here, we made a de novo quest for genes involved in carbon transfer from the plant to the fungus using genome-wide gene expression array targeting whole root and whole shoot gene expression profiles of mycorrhizal and non-mycorrhizal Medicago truncatula plants grown in a glasshouse. Using physiological intervention of heavy shading (90% incoming light removed) and the correlation of expression levels of MtPT4, the mycorrhiza-inducible phosphate transporter operating at the symbiotic interface between the root cortical cells and the AM fungus, and our candidate genes, we demonstrate that several novel genes may be involved in resource tradings in the AM symbiosis established by M. truncatula. These include glucose-6-phosphate/phosphate translocator, polyol/monosaccharide transporter, DUR3-like, nucleotide-diphospho-sugar transferase or a putative membrane transporter. Besides, we also examined the expression of other M. truncatula phosphate transporters (MtPT1-3, MtPT5-6) to gain further insights in the balance between the "direct" and the "mycorrhizal" phosphate uptake pathways upon colonization of roots by the AM fungus, as affected by short-term carbon/energy deprivation. In addition, the role of the novel candidate genes in plant cell metabolism is discussed based on available literature.
- MeSH
- Phosphorus metabolism MeSH
- Medicago truncatula genetics metabolism microbiology MeSH
- Metabolic Networks and Pathways MeSH
- Mycorrhizae genetics physiology MeSH
- Gene Expression Regulation, Plant MeSH
- Plant Proteins genetics MeSH
- Exome Sequencing MeSH
- Gene Expression Profiling MeSH
- Symbiosis MeSH
- Carbon metabolism MeSH
- Publication type
- Journal Article MeSH
- Research Support, Non-U.S. Gov't MeSH
- Names of Substances
- Phosphorus MeSH
- Plant Proteins MeSH
- Carbon MeSH
Biochar has been heralded as a multipurpose soil amendment to sustainably increase soil fertility and crop yields, affect soil hydraulic properties, reduce nutrient losses, and sequester carbon. Some of the most spectacular results of biochar (and organic nutrient) inputs are the terra preta soils in the Amazon, dark anthropogenic soils with extremely high fertility sustained over centuries. Such soil improvements have been particularly difficult to achieve on a short run, leading to speculations that biochar may need to age (weather) in soil to show its best. Further, interaction of biochar with arbuscular mycorrhizal fungi (AMF), important root symbionts of a great majority of terrestrial plants including most agricultural crops, remains little explored. To study the effect of aged biochar on highly mycotrophic Andropogon gerardii plants and their associated AMF, we made use of softwood biochar, collected from a historic charcoal burning site. This biochar (either untreated or chemically activated, the latter serving as a proxy for freshly prepared biochar) was added into two agricultural soils (acid or alkaline), and compared to soils without biochar. These treatments were further crossed with inoculation with a synthetic AMF community to address possible interactions between biochar and the AMF. Biochar application was generally detrimental for growth and mineral nutrition of our experimental plants, but had no effect on the extent of their root colonized by the AMF, nor did it affect composition of their root-borne AMF communities. In contrast, biochar affected development of two out of five AMF (Claroideoglomus and Funneliformis) in the soil. Establishment of symbiosis with AMF largely mitigated biochar-induced suppression of plant growth and mineral nutrition, mainly by improving plant acquisition of phosphorus. Both mycorrhizal and non-mycorrhizal plants grew well in the acid soil without biochar application, whereas non-mycorrhizal plants remained stunted in the alkaline soils under all situations (with or without biochar). These different and strong effects indicate that response of plants to biochar application are largely dependent on soil matrix and also on microbes such as AMF, and call for further research to enable qualified predictions of the effects of different biochar applications on field-grown crops and soil processes.
- Keywords
- arbuscular mycorrhizal fungi, community, historic biochar, mycorrhizal response, nitrogen, phosphorus,
- Publication type
- Journal Article MeSH
Establishment of nonmycorrhizal controls is a "classic and recurrent theme" in mycorrhizal research. For decades, authors reported mycorrhizal plant growth/nutrition as compared to various nonmycorrhizal controls. In such studies, uncertainties remain about which nonmycorrhizal controls are most appropriate and, in particular, what effects the control inoculations have on substrate and root microbiomes. Here, different types of control and mycorrhizal inoculations were compared with respect to plant growth and nutrition, as well as the structure of root and substrate microbiomes, assessed by next-generation sequencing. We compared uninoculated ("absolute") control to inoculation with blank pot culture lacking arbuscular mycorrhizal fungi, filtrate of that blank inoculum, and filtrate of complex pot-produced mycorrhizal inoculum. Those treatments were compared to a standard mycorrhizal treatment, where the previously sterilized substrate was inoculated with complex pot-produced inoculum containing Rhizophagus irregularis SYM5. Besides this, monoxenically produced inoculum of the same fungus was applied either alone or in combination with blank inoculum. The results indicate that the presence of mycorrhizal fungus always resulted in stimulation of Andropogon gerardii plant biomass as well as in elevated phosphorus content of the plants. The microbial (bacterial and fungal) communities developing in the differently inoculated treatments, however, differed substantially from each other and no control could be obtained comparable with the treatment inoculated with complex mycorrhizal inoculum. Soil microorganisms with significant biological competences that could potentially contribute to the effects of the various inoculants on the plants were detected in roots and in plant cultivation substrate in some of the treatments.
- Keywords
- Andropogon gerardii, Appropriate nonmycorrhizal control, Arthrobotrys, Microbiome, Pot experiment, Rhizophagus irregularis,
- MeSH
- Andropogon microbiology MeSH
- Bacteria metabolism MeSH
- Biomass MeSH
- Phosphorus analysis MeSH
- Plant Roots microbiology MeSH
- Microbiota * MeSH
- Mycorrhizae physiology MeSH
- Soil Microbiology * MeSH
- Symbiosis MeSH
- High-Throughput Nucleotide Sequencing MeSH
- Publication type
- Journal Article MeSH
- Names of Substances
- Phosphorus MeSH
Common mycorrhizal networks (CMNs) formed by arbuscular mycorrhizal fungi (AMF) interconnect plants of the same and/or different species, redistributing nutrients and draining carbon (C) from the different plant partners at different rates. Here, we conducted a plant co-existence (intercropping) experiment testing the role of AMF in resource sharing and exploitation by simplified plant communities composed of two congeneric grass species (Panicum spp.) with different photosynthetic metabolism types (C3 or C4). The grasses had spatially separated rooting zones, conjoined through a root-free (but AMF-accessible) zone added with 15N-labeled plant (clover) residues. The plants were grown under two different temperature regimes: high temperature (36/32°C day/night) or ambient temperature (25/21°C day/night) applied over 49 days after an initial period of 26 days at ambient temperature. We made use of the distinct C-isotopic composition of the two plant species sharing the same CMN (composed of a synthetic AMF community of five fungal genera) to estimate if the CMN was or was not fed preferentially under the specific environmental conditions by one or the other plant species. Using the C-isotopic composition of AMF-specific fatty acid (C16:1ω5) in roots and in the potting substrate harboring the extraradical AMF hyphae, we found that the C3-Panicum continued feeding the CMN at both temperatures with a significant and invariable share of C resources. This was surprising because the growth of the C3 plants was more susceptible to high temperature than that of the C4 plants and the C3-Panicum alone suppressed abundance of the AMF (particularly Funneliformis sp.) in its roots due to the elevated temperature. Moreover, elevated temperature induced a shift in competition for nitrogen between the two plant species in favor of the C4-Panicum, as demonstrated by significantly lower 15N yields of the C3-Panicum but higher 15N yields of the C4-Panicum at elevated as compared to ambient temperature. Although the development of CMN (particularly of the dominant Rhizophagus and Funneliformis spp.) was somewhat reduced under high temperature, plant P uptake benefits due to AMF inoculation remained well visible under both temperature regimes, though without imminent impact on plant biomass production that actually decreased due to inoculation with AMF.
Arbuscular mycorrhizal (AM) fungi can significantly contribute to plant nitrogen (N) uptake from complex organic sources, most likely in concert with activity of soil saprotrophs and other microbes releasing and transforming the N bound in organic forms. Here, we tested whether AM fungus (Rhizophagus irregularis) extraradical hyphal networks showed any preferences towards certain forms of organic N (chitin of fungal or crustacean origin, DNA, clover biomass, or albumin) administered in spatially discrete patches, and how the presence of AM fungal hyphae affected other microbes. By direct 15N labeling, we also quantified the flux of N to the plants (Andropogon gerardii) through the AM fungal hyphae from fungal chitin and from clover biomass. The AM fungal hyphae colonized patches supplemented with organic N sources significantly more than those receiving only mineral nutrients, organic carbon in form of cellulose, or nothing. Mycorrhizal plants grew 6.4-fold larger and accumulated, on average, 20.3-fold more 15N originating from the labeled organic sources than their nonmycorrhizal counterparts. Whereas the abundance of microbes (bacteria, fungi, or Acanthamoeba sp.) in the different patches was primarily driven by patch quality, we noted a consistent suppression of the microbial abundances by the presence of AM fungal hyphae. This suppression was particularly strong for ammonia oxidizing bacteria. Our results indicate that AM fungi successfully competed with the other microbes for free ammonium ions and suggest an important role for the notoriously understudied soil protists to play in recycling organic N from soil to plants via AM fungal hyphae.
- Keywords
- 15N–labeling, Metatranscriptomics, Organic nitrogen (N), Quantitative real-time PCR (qPCR), Root-free compartments, Soil microbial loop,
- MeSH
- Acanthamoeba metabolism MeSH
- Ammonia metabolism MeSH
- Andropogon growth & development metabolism microbiology MeSH
- Bacteria metabolism MeSH
- Nitrogen metabolism MeSH
- Hyphae metabolism MeSH
- Mycorrhizae metabolism MeSH
- Organic Chemicals metabolism MeSH
- Oxidation-Reduction MeSH
- Publication type
- Journal Article MeSH
- Names of Substances
- Ammonia MeSH
- Nitrogen MeSH
- Organic Chemicals MeSH
Legumes establish root symbioses with rhizobia that provide plants with nitrogen (N) through biological N fixation (BNF), as well as with arbuscular mycorrhizal (AM) fungi that mediate improved plant phosphorus (P) uptake. Such complex relationships complicate our understanding of nutrient acquisition by legumes and how they reward their symbiotic partners with carbon along gradients of environmental conditions. In order to disentangle the interplay between BNF and AM symbioses in two Medicago species (Medicago truncatula and M. sativa) along a P-fertilization gradient, we conducted a pot experiment where the rhizobia-treated plants were either inoculated or not inoculated with AM fungus Rhizophagus irregularis 'PH5' and grown in two nutrient-poor substrates subjected to one of three different P-supply levels. Throughout the experiment, all plants were fertilized with 15N-enriched liquid N-fertilizer to allow for assessment of BNF efficiency in terms of the fraction of N in the plants derived from the BNF (%NBNF). We hypothesized (1) higher %NBNF coinciding with higher P supply, and (2) higher %NBNF in mycorrhizal as compared to non-mycorrhizal plants under P deficiency due to mycorrhiza-mediated improvement in P nutrition. We found a strongly positive correlation between total plant P content and %NBNF, clearly documenting the importance of plant P nutrition for BNF efficiency. The AM symbiosis generally improved P uptake by plants and considerably stimulated the efficiency of BNF under low P availability (below 10 mg kg-1 water extractable P). Under high P availability (above 10 mg kg-1 water extractable P), the AM symbiosis brought no further benefits to the plants with respect to P nutrition even as the effects of P availability on N acquisition via BNF were further modulated by the environmental context (plant and substrate combinations). As a response to elevated P availability in the substrate, the extent of root length colonization by AM fungi was reduced, the turning points occurring at about 8 and 10 mg kg-1 water extractable P for M. sativa and M. truncatula, respectively. Our results indicated competition for limited C resource between the two kinds of microsymbionts and thus degradation of AM symbiotic functioning under ample P supply.
- Keywords
- arbuscular mycorrhiza, competition, legumes, nitrogen acquisition, phosphorus uptake, rhizobia, root symbioses, synergies,
- Publication type
- Journal Article MeSH
