Direct nocturnal water transfer from oaks to their mycorrhizal symbionts during severe soil drying

Mycorrhiza, 2011

Ectomycorrhizal (ECM) communities of mature trees and regenerating seedlings of a non-native tree species Pinus mugo grown in a harsh environment of the coastal region of the Curonian Spit National Park in Lithuania were assessed. We established three study sites (S1, S2, and S3) that were separated from each other by 15 km. The ECM species richness was rather low in particular for mature, 100-year-old trees: 12 ectomycorrhizal taxa were identified by molecular analysis from 11 distinguished morphotypes. All 12 taxa were present on seedlings and on mature trees, with between 8-11 and 9-11 taxa present on seedlings and mature trees, respectively. Cenococcum geophilum dominated all ECM communities, but the relative abundance of C. geophilum mycorrhizas was nearly two times higher on seedlings than on mature trees. Mycorrhizal associations formed by Wilcoxina sp., Lactarius rufus, and Russula paludosa were also abundant. Several fungal taxa were only occasionally detected, including Cortinarius sp., Cortinarius obtusus, Cortinarius croceus, and Meliniomyces sp. Shannon's diversity indices for the ECM assemblages of P. mugo ranged from 0.98 to 1.09 for seedling and from 1.05 to 1.31 for mature trees. According to analysis of similarity, the mycorrhizal communities were similar between the sites (R = 0.085; P = 0.06) and only slightly separated between seedlings and mature trees (R = 0.24; P < 0.0001). An incidental fruiting body survey that was conducted weakly reflected the below-ground assessment of the ECM fungal community and once again showed that ECM and fruiting body studies commonly supply different partial accounts of the true ECM fungal diversity. Our results show that P. mugo has moved into quite distinct habitats and is able to adapt a suite of ECM symbionts that sufficiently support growth and development of this tree and allow for natural seedling regeneration.

Ecohydrology, 2014

Hydraulic lift, water movement from deep to upper soil layers by roots, is a widespread process in temperate and semi-arid environments. It can contribute 17-81% of total water transpired and favour the uptake of nutrients available mainly from soil organic matter decomposition (e.g. N). Downward siphoning, water movement from upper to deep soil layers, can represent 10-60% of total transpired water, favouring the uptake of nutrients supplied mainly from the leaching of bedrock minerals (e.g. P and K). These vertical water movements also can affect the N : P ratio of runoff waters when, in the case of hydraulic lift, they open the possibility for a given pulse of water to circulate multiple times across the N-rich upper soil layers. Plants, thus, affect the stoichiometry of nutrients in soils and groundwater not only through the physical protection of the soil and through the water uptake but also through water redistribution. Soil water redistribution can also play an outstanding role in the ecosystem responses to global change drivers. The increase in soil patchiness in current and future arid lands modifies runoff fluxes, hydraulic lift and downward siphoning, allowing plants to dispose of higher water and nutrient availabilities. The higher use of hydraulic lift and/or downward siphoning by alien species is a possible cause of alien plant success. Further mechanistic and quantitative research is thus warranted to discern the plant role in water and nutrient cycling and in the responses to global change.

Functional Ecology, 2003

We report hydraulic lift in the savanna vegetation of central Brazil ( Cerrado ). Both heat-pulse measurements and isotopic (deuterium) labelling were used to determine whether hydraulic lift occurred in two common species, and whether neighbouring small shrubs and trees were utilizing this water. 2. Both techniques showed water uptake by tap-roots and reverse flow of water in lateral roots. Roots transferred hydraulically lifted water to the soil, and small shrubs and trees neighbouring the labelled individuals were labelled by deuterated water. 3. Isotopic mass-balance equations and sap-flow measurements showed that water taken up by the central tap-root in each individual constituted only a small percentage of total flux of water through the treated plants. Mass-balance equations also indicated that small shrubs and trees neighbouring the treated plants utilized only a few thousandths of a per cent of the label. 4 . The small proportion of water uptake by the tap-root of these two species may be limiting hydraulic lift in this system, unless sinker roots descending from lateral roots contribute to hydraulic lift.

Plant and Soil, 2013

There is growing evidence of the importance of extramatrical mycelium (EMM) of mycorrhizal fungi in carbon (C) cycling in ecosystems. However, our understanding has until recently been mainly based on laboratory experiments, and knowledge of such basic parameters as variations in mycelial production, standing biomass and turnover as well as the regulatory mechanisms behind such variations in forest soils is limited. Presently, the production of EMM by ectomycorrhizal (EM) fungi has been Plant Soil

Plant and Soil, 2013

Background and aims Knowledge of plant water fluxes is critical for assessing mechanistic processes linked to biogeochemical cycles, yet resolving root water transport dynamics has been a particularly daunting task. Our objectives were to demonstrate the ability to non-invasively monitor individual root functionality and water fluxes within Zea mays L. (maize) and Panicum virgatum L. (switchgrass) seedlings using neutron imaging.

Plant and Soil, 2012

Background and aims We conducted a mesocosm study to investigate the extent to which the process of hydraulic redistribution of soil water by plant roots is affected by mycorrhizosphere disturbance. Methods We used deuterium-labeled water to track the transfer of hydraulically lifted water (HLW) from well-hydrated donor oaks (Quercus agrifolia Nee.) to drought-stressed receiver seedlings growing together in mycorrhizal or fungicide-treated mesocosms. We hypothesized that the transfer of HLW from donor to receiver plants would be enhanced in undisturbed (non-fungicide-treated) mesocosms where an intact mycorrhizal hyphal network was present.

Advances in Citrus Nutrition, 2012

Rhizosphere, the soil region nearest to plant root system, inhabits various microorganisms varying in their community structure and diversity, still remains largely unexploited despite so much of breakthroughs in isolation and characterization, but lacks in addressing citrus speci fi c rhizosphere properties. Exploiting microbial synergisms is one of the popular methods of substrate dynamics and associated changes in nutrient environment of rhizosphere. Soil microbial biomass dominates fungal mycelium accumulates and retains mineral nutrients, immobilizing as much as ~20% of the total soil N and P. The extraradical mycorrhizal mycelial (attains as much as 3% of root weight) networks are recognized as the hidden nutrient/ water-absorbing interfaces (glomalin, a soil-based glycoprotein secreted by AMF as a major seat of activity) in addition to safeguarding citrus against a number of other biotic and abiotic stresses. The microbial diversity existing within top 0-20-cm citrus rhizosphere soil was characterized and isolated by the promising microbes, namely, Bacillus polymyxa , Azoto bacter chroococcum , Bacillus mycoides , Pseudomonas fl uorescens , and Trichoderma harzianum . Pure culture of these microbes in value-added form ( Bacillus polymyxa 33-44 × 10 6 -10 7 cfu mL −1 , Azotobacter chroococcum as 10-38 × 10 6 -10 7 cfu mL −1 , Bacillus mycoides 7-22 × 10 5 -10 6 cfu mL −1 ), Pseudomonas fl uorescens 14-28 × 10 6 -10 7 cfu mL −1 , and Trichoderma harzianum 30-32 × 10 6 -10 7 cfu mL −1 was developed and prepared a mixture called microbial consortium (MC). MC so developed displayed an excellent response under both nursery as well as grown-up plants in integrated nutrient management (INM) module. These results suggested two cardinal points, namely, (1) the developed microbial consortium holds a good promise as an independent use as well as use in format of integrated nutrient management and (2) deserves an application in providing resilience to rhizosphere against any possible depletion in either available supply of nutrients or loss of native soil microbial biomass as an indicator of rhizosphere health.

Archives of Agronomy and Soil Science, 2013

Glomalin-related soil protein (GRSP), a glycoprotein of arbuscular mycorrhizal fungi (AMF) secreted into soil, governs the aggregate stability, but the role of GRSP in soil and plant water is sparsely studied. The 24-week-old red tangerine (Citrus tangerina) inoculated with Glomus etunicatum and G. mosseae were subjected to a soil drying for 12 days as soil water deficit (SWD). Length of SWD significantly reduced mycorrhizal colonization, soil hyphal length, and leaf and soil water potential (Ψ), but increased total GRSP (T-GRSP), easily extractable GRSP (EE-GRSP), and proportion of waterstable aggregates (WSAs) in >0.25 mm size, irrespective of AMF source. The AMFinoculated seedlings showed significantly higher T-GRSP, EE-GRSP, and leaf/soil Ψ than non-AMF seedlings during SWD. A significantly positive correlation was observed for mycorrhizal colonization versus leaf or soil Ψ, and hyphal length versus leaf Ψ, suggesting that root intra-and extra-radical hyphae participated in water transport. Interestingly, in GRSP fractions, only T-GRSP was significantly positively correlated with 0.25-1 and >0.25 mm WSA and negatively with leaf and soil Ψ. These results revealed a strong glue function of T-GRSP (not EE-GRSP and hyphae) to alter the proportional distribution of WSA size, thereby aiding toward prevention of soil water loss for improving soil-plant water relations.

New Phytologist, 2010

The role of mycorrhizal networks in forest dynamics is poorly understood because of the elusiveness of their spatial structure. We mapped the belowground distribution of the fungi Rhizopogon vesiculosus and Rhizopogon vinicolor and interior Douglas-fir trees (Pseudotsuga menziesii var. glauca) to determine the architecture of a mycorrhizal network in a multi-aged old-growth forest.

Symbiosis, 2013

Mediterranean woodlands: variation among sites and over soil depth profiles in hyphal exploration types, species richness and community composition Abstract Understanding the factors underlying the distribution of biodiversity is a challenging issue in ecology. Here, we examined the distribution patterns of ectomycorrhizal fungal diversity across the soil profile in three Quercus ilex forests. Contact exploration type strongly dominated at all sites, but was most prevalent in the upper, organic-rich soil layers. At each site, three quarters of the ectomycorrhizal tips and 59 % of taxa were restricted to the ten first centimeters of the soil profile. The relative abundance of the dominant family Russulaceae increased with increasing soil depth. Species composition varied significantly among sites, with most species being rare. Species that occurred in only one of the three sites accounted for 78.9 % of all species, and 57.3 % of species were represented by a single ECM root tip. Our results suggest that (i) rare species at both local and regional scales contribute to the highly diverse fungal assemblages in Mediterranean forests and (ii) multi-sites studies including the whole soil profile are needed to provide comprehensive overviews of the taxonomic and functional diversities of ectomycorrhizal communities.

Plant and Soil, 2011

The benefits of mycorrhizas for host plants are well known for a large number of species. However, experimental evaluations of the hyphal contribution to the total water uptake and the assessment of the bulk flow velocity in the hyphae are so far contradictory. Barley (Hordeum vulgaris L. Scarlet) with the inoculum Glomus intraradices was grown in a split plant-hyphal chamber with a 5 mm air gap. During the preparation of the chambers with a loamy-silt soil, water content sensors were inserted in each of the plant and the hyphal compartments. These sensors allow nondestructive measurements with high resolution. In total, 8 drying periods with a length of several days were applied with repeated watering following each drying period. A clear decline in water content in the hyphal compartment during each drying period supports the ability of hyphae to transfer water into the plant compartment. The difference between the decline in the hyphal compartment with and without arbuscular mycorrhyzal fungi is significant at the p< 0.000001 level. The direct and indirect hyphal contribution to the total water uptake was estimated to be about 20%. The application of capacitance sensors for water content determination with a special geometry adapted to the plant-hyphal chambers allows the evaluation of the hyphal water flow with high accuracy.

Agroforestry Systems, 2011

Chestnut plantations for fruit production in Northern Portugal have been subjected to intensive management system, including soil tillage, mineral fertilization and pruning. Some of these practices have no positive effect on productivity and soilplant-water relations. Other systems (e.g., no tillage with maintenance of grass cover) have been adopted, aiming a multifunctional land use, exploiting nuts, pasture and edible mushrooms. Thus, an experimental trial was installed to assess the effects of such systems on productivity, sustainability and annual net income, as compared with the conventional system, over a six-year period. The treatments were: conventional soil tillage (CT); no tillage with permanent spontaneous herbaceous vegetation cover (NV); no tillage with permanent rainfed seeded pasture cover (NP); and as NP but with irrigation (NIP). Production of nuts, forage and edible mushrooms were measured and sustainability was assessed by production and diversity of fungal sporocarps. Annual net income was estimated by the difference between the annual gross outputs (market values for nuts, forage and edible commercial mushrooms) and the annual input costs. The greatest nut and edible mushroom production and sporocarp biodiversity were achieved in the NIP and NV and the smallest in the CT treatment. The highest annual gross output was estimated for the NV and NIP treatments, whereas the highest annual net income was obtained for the NV. No tillage with maintenance of spontaneous grass cover showed to be the most favourable management system, as it has increased productivity and biodiversity.

Oecologia, 2004

Hydraulic redistribution (HR), the passive movement of water via roots from moist to drier portions of the soil, occurs in many ecosystems, influencing both plant and ecosystem-water use. We examined the effects of HR on root hydraulic functioning during drought in young and old-growth Douglas-fir [Pseudotsuga menziesii (Mirb.) Franco] and ponderosa pine (Pinus ponderosa Dougl. Ex Laws) trees growing in four sites. During the 2002 growing season, in situ xylem embolism, water deficit and xylem vulnerability to embolism were measured on medium roots (2-4-mm diameter) collected at 20-30 cm depth. Soil water content and water potentials were monitored concurrently to determine the extent of HR. Additionally, the water potential and stomatal conductance (g s ) of upper canopy leaves were measured throughout the growing season. In the site with young Douglas-fir trees, root embolism increased from 20 to 55 percent loss of conductivity (PLC) as the dry season progressed. In young ponderosa pine, root embolism increased from 45 to 75 PLC. In contrast, roots of oldgrowth Douglas-fir and ponderosa pine trees never experienced more than 30 and 40 PLC, respectively. HR kept soil water potential at 20-30 cm depth above −0.5 MPa in the old-growth Douglas-fir site and −1.8 MPa in the old-growth ponderosa pine site, which significantly reduced loss of shallow root function. In the young ponderosa pine stand, where little HR occurred, the water potential in the upper soil layers fell to about −2.8 MPa, which severely impaired root functioning and limited recovery when the fall rains returned. In both species, daily maximum g s decreased linearly with increasing root PLC, suggesting that root xylem embolism acted in concert with stomata to limit water loss, thereby maintaining minimum leaf water potential above critical values. HR appears to be an important mechanism for maintaining shallow root function during drought and preventing total stomatal closure.

Plant, Cell and Environment, 2006

Hydraulic redistribution (HR) occurs in many ecosystems; however, key questions remain about its consequences at the ecosystem level. The objectives of the present study were to quantify seasonal variation in HR and its driving force, and to manipulate the soil-root system to elucidate physiological components controlling HR and utilization of redistributed water. In the upper soil layer of a young Douglas-fir forest, HR was negligible in early summer, but increased to 0.17 mm day − − − − 1 (20-60 cm layer) by late August when soil water potential was approximately − − − − 1 MPa. When maximum HR rates were observed, redistributed water replenished approximately 40% of the water depleted from the upper soil on a daily basis. Manipulations to the soil or to the soil/plant water potential driving force altered the rate of observed HR indicating that the rate of HR is controlled by a complex interplay between competing soil and plant water potential gradients and pathway resistances. Separating roots from the transpiring tree resulted in increased HR, and sap flow measurements on connected and disconnected roots showed reversal of water flow, a prerequisite for HR. Irrigating a small plot with deuterated water demonstrated that redistributed water was taken up by small understorey plants as far as 5 m from the watering source, and potentially further, but the utilization pattern was patchy. HR in the upper soil layers near the watering plot was twice that of the control HR. This increase in HR also increased the amount of water utilized by plants from the upper soil. These results indicate that the seasonal timing and magnitude of HR was strongly governed by the development of water potential differences within the soil, and the competing demand for water by the above ground portion of the tree.

Ecology, 2009

California coast live oak (Quercus agrifolia) forms tripartite symbiotic associations with arbuscular (AMF) and ectomycorrhizal (EMF) fungi. We selected oak individuals differing in topographic position and depth to groundwater (mesic valley vs. xeric hill sites) to investigate changes of tree mycorrhizal status in response to interannual rainfall variability. EMF root colonization, as well as hyphal abundance and viability in upper rhizosphere soil (0-30 cm), were negatively affected by severe multi-year drought, although not to the same extent in each topographic location. Oak trees growing in hill sites showed EMF colonization levels ,1% in upper roots during drought. By contrast, oaks in valley sites maintained much higher EMF colonization (.19%) in upper roots during drought. EMF root colonization increased sharply at both topographic positions during the ensuing wet year (78% in valley, 49% in hill), which indicates that the mycorrhizal status of roots in upper rhizosphere soil is highly responsive to interannual rainfall variability. Across sites and years, percentage EMF colonization and soil hyphal density and viability were strongly positively correlated with soil moisture potential, but percentage AMF root colonization was not. Interestingly, changes in percentage EMF root colonization and density of viable hyphae between a wet and a dry year were proportionally much greater in xeric hill sites than in mesic valley sites. The mycorrhizal status of oak trees was particularly responsive to changes in soil moisture at the hill sites, where roots in upper rhizosphere soil shifted from almost exclusively AMF during severe drought to predominantly EMF during the ensuing wet year. By contrast, the mycorrhizal status of oaks in the valley sites was less strongly coupled to current meteorological conditions, as roots in upper soil layers remained predominantly EMF during both a dry and a wet year. Canopy shading and hydraulic lift by oaks in valley sites likely contributed to maintain the integrity and viability of EMF roots and extraradical hyphae in upper rhizosphere soil during extended drought. Our results suggest that oak woodlands in water-limited ecosystems may become increasingly reliant on the AMF symbiosis under future climate change scenarios for the U.S. southwest and other world regions.