Plant species and soil type cooperatively shape the structure and function of microbial communities in the rhizosphere

https://www.cell.com/trends/microbiology/pdf/S0966-842X(08)00192-3.pdf

Properties of bacterial endophytes and their proposed role in plant growth.

http://www.kiwiscience.com/JournalArticles/EnvironPoll2011.pdf

A review of biochars’ potential role in the remediation, revegetation and restoration of contaminated soils

Almost all land plants form symbiotic associations with mycorrhizal fungi. These below-ground fungi play a key role in terrestrial ecosystems as they regulate nutrient and carbon cycles, and influence soil structure and ecosystem multifunctionality. Up to 80% of plant N and P is provided by mycorrhizal fungi and many plant species depend on these symbionts for growth and survival. Estimates suggest that there are c. 50 000 fungal species that form mycorrhizal associations with c. 250 000 plant species. The development of high-throughput molecular tools has helped us to better understand the biology, evolution, and biodiversity of mycorrhizal associations. Nuclear genome assemblies and gene annotations of 33 mycorrhizal fungal species are now available providing fascinating opportunities to deepen our understanding of the mycorrhizal lifestyle, the metabolic capabilities of these plant symbionts, the molecular dialogue between symbionts, and evolutionary adaptations across a range of mycorrhizal associations. Large-scale molecular surveys have provided novel insights into the diversity, spatial and temporal dynamics of mycorrhizal fungal communities. At the ecological level, network theory makes it possible to analyze interactions between plant-fungal partners as complex underground multi-species networks. Our analysis suggests that nestedness, modularity and specificity of mycorrhizal networks vary and depend on mycorrhizal type. Mechanistic models explaining partner choice, resource exchange, and coevolution in mycorrhizal associations have been developed and are being tested. This review ends with major frontiers for further research.

https://nph.onlinelibrary.wiley.com/doi/epdf/10.1111/nph.13288

Mycorrhizal ecology and evolution: the past, the present, and the future

Root systems of most land plants form arbuscular mycorrhizal (AM) symbioses in the field, and these contribute to nutrient uptake. AM roots have two pathways for nutrient absorption, directly through the root epidermis and root hairs and via AM fungal hyphae into root cortical cells, where arbuscules or hyphal coils provide symbiotic interfaces. New physiological and molecular evidence shows that for phosphorus the mycorrhizal pathway (MP) is operational regardless of plant growth responses (positive or negative). Amounts delivered cannot be determined from plant nutrient contents because when responses are negative the contribution of the direct pathway (DP) is reduced. Nitrogen (N) is also delivered to roots via an MP, but the contribution to total N requirement and the costs to the plant are not clear. The functional interplay between activities of the DP and MP has important implications for consideration of AM symbioses in ecological, agronomic, and evolutionary contexts.

/pdf/roles-of-arbuscular-mycorrhizas-in-plant-nutrition-and-4crmwp9flj.pdf

Roles of Arbuscular Mycorrhizas in Plant Nutrition and Growth: New Paradigms from Cellular to Ecosystem Scales

Flavonoids are a diverse class of polyphenolic compounds that are produced as a result of plant secondary metabolism. They are known to play a multifunctional role in rhizospheric plant-microbe and plant-plant communication. Most familiar is their function as a signal in initiation of the legume-rhizobia symbiosis, but, flavonoids may also be signals in the establishment of arbuscular mycorrhizal symbiosis and are known agents in plant defence and in allelopathic interactions. Flavonoid perception by, and impact on, their microbial targets (e.g. rhizobia, plant pathogens) is relatively well characterized. However, potential impacts on 'non-target' rhizosphere inhabitants ('non-target' is used to distinguish those microorganisms not conventionally known as targets) have not been thoroughly investigated. Thus, this review first summarizes the conventional roles of flavonoids as nod gene inducers, phytoalexins and allelochemicals before exploring questions concerning 'non-target' impacts. We hypothesize that flavonoids act to shape rhizosphere microbial community structure because they represent a potential source of carbon and toxicity and that they impact on rhizosphere function, for example, by accelerating the biodegradation of xenobiotics. We also examine the reverse question, 'how do rhizosphere microbial communities impact on flavonoid signals?' The presence of microorganisms undoubtedly influences the quality and quantity of flavonoids present in the rhizosphere, both through modification of root exudation patterns and microbial catabolism of exudates. Microbial alteration and attenuation of flavonoid signals may have ecological consequences for below-ground plant-microbe and plant-plant interaction. We have a lack of knowledge concerning the composition, concentration and bioavailability of flavonoids actually experienced by microbes in an intact rhizosphere, but this may be addressed through advances in microspectroscopic and biosensor techniques. Through the use of plant mutants defective in flavonoid biosynthesis, we may also start to address the question of the significance of flavonoids in shaping rhizosphere community structure and function.

Perception and modification of plant flavonoid signals by rhizosphere microorganisms

Alnus glutinosa is an important pioneer species that forms effective symbioses with Frankia and ecto and arbuscular mycorrhizal fungi (AMF). There is evidence that Frankia and AMF interact and the focus of this study was to investigate how interactions affected root system and root hair development. A. glutinosa seedlings were grown in pots in soil pre-inoculated with the AMF Gigaspora rosea. Seedlings were inoculated with Frankia either immediately on transfer to AMF-inoculated pots (day 0) on day 15 or on day 30 following AMF inoculation so the effect of timing of inoculation on interactions could be determined. Seedlings were harvested in batches at intervals of 10, 15, 20, 25 and 30 days after the commencement of each treatment. Both G. rosea and Frankia increased root branching and effects were greater when both were present. By contrast, both G. rosea and Frankia decreased root hair numbers markedly. Effects on root hair development were not a consequence of phosphorous, as P levels were not changed significantly in seedlings colonised by G. rosea or nodulated by Frankia. Effects are not due to differences in root system size but conceivably could offset some of the carbon costs incurred by the symbioses.

Both the arbuscular mycorrhizal fungus Gigaspora rosea and Frankia increase root system branching and reduce root hair frequency in Alnus glutinosa.

Plants colonised with the arbuscular mycorrhizal fungi (AMF) Glomus E3 and Glomus tenue were grown in microcosms that permitted separation into root:hyphae and hyphae compartments. Hydrolysed polysaccharides from the hyphae and water-soluble sugars released into the hyphosphere were assayed using chromatography. Total sugars and most monosaccharides were elevated in the hyphosphere of Glomus E3 but not in the hyphosphere of G. tenue. Differences in the levels of sugars did not depend on hyphal surface area. It is suggested the diversity in sugars produced in the hyphosphere of AMF may drive some of the spatial and temporal variation in microbial diversity and function in soils.

Polysaccharides and monosaccharides in the hyphosphere of the arbuscular mycorrhizal fungi Glomus E3 and Glomus tenue

The flavonoid class of plant secondary metabolites play a multifunctional role in below-ground plant–microbe interactions with their best known function as signals in the nitrogen fixing legume–rhizobia symbiosis. Flavonoids enter rhizosphere soil as a result of root exudation and senescence but little is known about their subsequent fate or impacts on microbial activity. Therefore, the present study examined the sorptive behaviour, biodegradation and impact on dehydrogenase activity (as determined by iodonitrotetrazolium chloride reduction) of the flavonoids naringenin and formononetin in soil. Organic carbon normalised partition coefficients, log Koc, of 3.12 (formononetin) and 3.19 (naringenin) were estimated from sorption isotherms and, after comparison with literature log Koc values for compounds whose soil behaviour is better characterised, the test flavonoids were deemed to be moderately sorbed. Naringenin (spiked at 50 μg g−1) was biodegraded without a detectable lag phase with concentrations reduced to 0.13±0.01 μg g−1 at the end of the 96 h time course. Biodegradation of formononetin proceeded after a lag phase of ∼24 h with concentrations reduced to 4.5±1% of the sterile control after 72 h. Most probable number (MPN) analysis revealed that prior to the addition of flavonoids, the soil contained 5.4×106 MPN g−1 (naringenin) and 7.9×105 MPN g−1 (formononetin) catabolic microbes. Formononetin concentration had no significant (p>0.05) effect on soil dehydrogenase activity, whereas naringenin concentration had an overall but non-systematic impact (p=0.045). These results are discussed with reference to likely total and bioavailable concentrations of flavonoids experienced by microbes in the rhizosphere.

The fate and toxicity of the flavonoids naringenin and formononetin in soil

Impacts of divergent arbuscular mycorrhizal (AM) fungi, Glomus intraradices and Gigaspora margarita, on denitrifying and diazotrophic bacterial communities of Plantago lanceolata in nutrient-limited dune soil were assessed. We hypothesized AM species-related modifications that were confirmed in respective bacterial nirK and nifH sequence polymorphism -based community clustering and community variance allocation. The denitrifying community appeared more responsive to AM fungi than the nitrogen-fixing community. Nevertheless, the main explanatory variable, in both cases, was plant age. We conclude that AM fungi can modify N-cycling microbial rhizosphere communities and future work should aim to verify the functional significance and mechanistic basis.

John E. Hooker

Papers

Perception and modification of plant flavonoid signals by rhizosphere microorganisms

Both the arbuscular mycorrhizal fungus Gigaspora rosea and Frankia increase root system branching and reduce root hair frequency in Alnus glutinosa.

Polysaccharides and monosaccharides in the hyphosphere of the arbuscular mycorrhizal fungi Glomus E3 and Glomus tenue

The fate and toxicity of the flavonoids naringenin and formononetin in soil

Arbuscular mycorrhizal modulation of diazotrophic and denitrifying microbial communities in the (mycor)rhizosphere of Plantago lanceolata