Mycorrhizal fungi enhance plant nutrient acquisition and modulate nitrogen loss with variable water regimes.

Climate change will alter both the amount and pattern of precipitation and soil water availability, which will directly affect plant growth and nutrient acquisition, and potentially, ecosystem functions like nutrient cycling and losses as well. Given their role in facilitating plant nutrient acquisition and water stress resistance, arbuscular mycorrhizal (AM) fungi may modulate the effects of changing water availability on plants and ecosystem functions. The well-characterized mycorrhizal tomato (Solanum lycopersicum L.) genotype 76R (referred to as MYC+) and the mutant mycorrhiza-defective tomato genotype rmc were grown in microcosms in a glasshouse experiment manipulating both the pattern and amount of water supply in unsterilized field soil. Following 4 weeks of differing water regimes, we tested how AM fungi affected plant productivity and nutrient acquisition, short-term interception of a 15NH4+ pulse, and inorganic nitrogen (N) leaching from microcosms. AM fungi enhanced plant nutrient acquisition with both lower and more variable water availability, for instance increasing plant P uptake more with a pulsed water supply compared to a regular supply and increasing shoot N concentration more when lower water amounts were applied. Although uptake of the short-term 15NH4+ pulse was higher in rmc plants, possibly due to higher N demand, AM fungi subtly modulated NO3- leaching, decreasing losses by 54% at low and high water levels in the regular water regime, with small absolute amounts of NO3- leached (<1 kg N/ha). Since this study shows that AM fungi will likely be an important moderator of plant and ecosystem responses to adverse effects of more variable precipitation, management strategies that bolster AM fungal communities may in turn create systems that are more resilient to these changes.

Effects of arbuscular mycorrhizae on tomato yield, nutrient uptake, water relations, and soil carbon dynamics under deficit irrigation in field conditions.

Plant strategies to cope with future droughts may be enhanced by associations between roots and soil microorganisms, including arbuscular mycorrhizal (AM) fungi. But how AM fungi affect crop growth and yield, together with plant physiology and soil carbon (C) dynamics, under water stress in actual field conditions is not well understood. The well-characterized mycorrhizal tomato (Solanum lycopersicum L.) genotype 76R (referred to as MYC+) and the mutant nonmycorrhizal tomato genotype rmc were grown in an organic farm with a deficit irrigation regime and control regime that replaced evapotranspiration. AM increased marketable tomato yields by ~25% in both irrigation regimes but did not affect shoot biomass. In both irrigation regimes, MYC+ plants had higher plant nitrogen (N) and phosphorus (P) concentrations (e.g. 5 and 24% higher N and P concentrations in leaves at fruit set, respectively), 8% higher stomatal conductance (gs), 7% higher photosynthetic rates (Pn), and greater fruit set. Stem water potential and leaf relative water content were similar in both genotypes within each irrigation regime. Three-fold higher rates of root sap exudation in detopped MYC+ plants suggest greater capacity for water uptake through osmotic driven flow, especially in the deficit irrigation regime in which root sap exudation in rmc was nearly absent. Soil with MYC+ plants also had slightly higher soil extractable organic C and microbial biomass C at anthesis but no changes in soil CO2 emissions, although the latter were 23% lower under deficit irrigation. This study provides novel, field-based evidence for how indigenous AM fungi increase crop yield and crop water use efficiency during a season-long deficit irrigation and thus play an important role in coping with increasingly limited water availability in the future.

Tightly-Coupled Plant-Soil Nitrogen Cycling: Comparison of Organic Farms across an Agricultural Landscape.

How farming systems supply sufficient nitrogen (N) for high yields but with reduced N losses is a central challenge for reducing the tradeoffs often associated with N cycling in agriculture. Variability in soil organic matter and management of organic farms across an agricultural landscape may yield insights for improving N cycling and for evaluating novel indicators of N availability. We assessed yields, plant-soil N cycling, and root expression of N metabolism genes across a representative set of organic fields growing Roma-type tomatoes (Solanum lycopersicum L.) in an intensively-managed agricultural landscape in California, USA. The fields spanned a three-fold range of soil carbon (C) and N but had similar soil types, texture, and pH. Organic tomato yields ranged from 22.9 to 120.1 Mg ha-1 with a mean similar to the county average (86.1 Mg ha-1), which included mostly conventionally-grown tomatoes. Substantial variability in soil inorganic N concentrations, tomato N, and root gene expression indicated a range of possible tradeoffs between yields and potential for N losses across the fields. Fields showing evidence of tightly-coupled plant-soil N cycling, a desirable scenario in which high crop yields are supported by adequate N availability but low potential for N loss, had the highest total and labile soil C and N and received organic matter inputs with a range of N availability. In these fields, elevated expression of a key gene involved in root N assimilation, cytosolic glutamine synthetase GS1, confirmed that plant N assimilation was high even when inorganic N pools were low. Thus tightly-coupled N cycling occurred on several working organic farms. Novel combinations of N cycling indicators (i.e. inorganic N along with soil microbial activity and root gene expression for N assimilation) would support adaptive management for improved N cycling on organic as well as conventional farms, especially when plant-soil N cycling is rapid.

Use of introgression lines to determine the ecophysiological basis for changes in water use efficiency and yield in California processing tomatoes.

Field and greenhouse studies examined the effects of growth habit and chloroplast presence in leaf veins for their role in increasing agronomic water use efficiency and yields of California modern processing tomato (Solanum lycopersicum L.) cultivars. Five introgression lines (ILs), made with Solanum pennellii Cor. in the genetic background of cultivar M82, differ in genes that map to a region on Chromosome 5, including the SP5G gene (determinate vs. semideterminate (Det vs. SemiDet)) and the obv gene (presence (obscure) vs. absence (clear) of leaf vein chloroplasts (Obs vs. Clr)). The five ILs and M82 represented three of the four gene combinations (Det-Clr was unavailable). Det-Obs ILs had less leaf, stem and total aboveground biomass with earlier fruit set and ripening than SemiDet-Clr ILs. By harvest, total fruit biomass was not different among ILs. Photosynthetic rates and stomatal conductance were 4-7% and 13-26% higher, respectively, in Det-Obs ILs than SemiDet-Clr ILs. SemiDet-Obs ILs were intermediate for growth and gas exchange variables. The Det-Obs ILs had lower leaf N concentration and similar chlorophyll content per leaf area (but slightly higher per leaf mass) than SemiDet-Clr ILs. The Obs trait was associated with gains in leaf gas exchange-related traits. This study suggests that a more compact growth habit, less leaf biomass and higher C assimilation capacity per leaf area were relevant traits for the increased yields in cultivars with determinate growth. Developing new introgression libraries would contribute to understanding the multiple trait effects of desirable phenotypes.

The reduced mycorrhizal colonisation (rmc) mutation of tomato disrupts five gene sequences including the CYCLOPS/IPD3 homologue.

Arbuscular mycorrhizal (AM) symbiosis in vascular plant roots is an ancient mutualistic interaction that evolved with land plants. More recently evolved root mutualisms have recruited components of the AM signalling pathway as identified with molecular approaches in model legume research. Earlier we reported that the reduced mycorrhizal colonisation (rmc) mutation of tomato mapped to chromosome 8. Here we report additional functional characterisation of the rmc mutation using genotype grafts and proteomic and transcriptomic analyses. Our results led to identification of the precise genome location of the Rmc locus from which we identified the mutation by sequencing. The rmc phenotype results from a deletion that disrupts five predicted gene sequences, one of which has close sequence match to the CYCLOPS/IPD3 gene identified in legumes as an essential intracellular regulator of both AM and rhizobial symbioses. Identification of two other genes not located at the rmc locus but with altered expression in the rmc genotype is also described. Possible roles of the other four disrupted genes in the deleted region are discussed. Our results support the identification of CYCLOPS/IPD3 in legumes and rice as a key gene required for AM symbiosis. The extensive characterisation of rmc in comparison with its 'parent' 76R, which has a normal mycorrhizal phenotype, has validated these lines as an important comparative model for glasshouse and field studies of AM and non-mycorrhizal plants with respect to plant competition and microbial interactions with vascular plant roots.

Effective monitoring of agriculture: a response.

The development of effective agricultural monitoring networks is essential to track, anticipate and manage changes in the social, economic and environmental aspects of agriculture. We welcome the perspective of Lindenmayer and Likens (J. Environ. Monit., 2011, 13, 1559) as published in the Journal of Environmental Monitoring on our earlier paper, "Monitoring the World's Agriculture" (Sachs et al., Nature, 2010, 466, 558-560). In this response, we address their three main critiques labeled as 'the passive approach', 'the problem with uniform metrics' and 'the problem with composite metrics'. We expand on specific research questions at the core of the network design, on the distinction between key universal and site-specific metrics to detect change over time and across scales, and on the need for composite metrics in decision-making. We believe that simultaneously measuring indicators of the three pillars of sustainability (environmentally sound, social responsible and economically viable) in an effectively integrated monitoring system will ultimately allow scientists and land managers alike to find solutions to the most pressing problems facing global food security.

Global and local concerns: what attitudes and beliefs motivate farmers to mitigate and adapt to climate change?

In response to agriculture's vulnerability and contribution to climate change, many governments are developing initiatives that promote the adoption of mitigation and adaptation practices among farmers. Since most climate policies affecting agriculture rely on voluntary efforts by individual farmers, success requires a sound understanding of the factors that motivate farmers to change practices. Recent evidence suggests that past experience with the effects of climate change and the psychological distance associated with people's concern for global and local impacts can influence environmental behavior. Here we surveyed farmers in a representative rural county in California's Central Valley to examine how their intention to adopt mitigation and adaptation practices is influenced by previous climate experiences and their global and local concerns about climate change. Perceived changes in water availability had significant effects on farmers' intention to adopt mitigation and adaptation strategies, which were mediated through global and local concerns respectively. This suggests that mitigation is largely motivated by psychologically distant concerns and beliefs about climate change, while adaptation is driven by psychologically proximate concerns for local impacts. This match between attitudes and behaviors according to the psychological distance at which they are cognitively construed indicates that policy and outreach initiatives may benefit by framing climate impacts and behavioral goals concordantly; either in a global context for mitigation or a local context for adaptation.

Biodiversity and ecosystem services science for a sustainable planet: the DIVERSITAS vision for 2012-20.

DIVERSITAS, the international programme on biodiversity science, is releasing a strategic vision presenting scientific challenges for the next decade of research on biodiversity and ecosystem services: "Biodiversity and Ecosystem Services Science for a Sustainable Planet". This new vision is a response of the biodiversity and ecosystem services scientific community to the accelerating loss of the components of biodiversity, as well as to changes in the biodiversity science-policy landscape (establishment of a Biodiversity Observing Network - GEO BON, of an Intergovernmental science-policy Platform on Biodiversity and Ecosystem Services - IPBES, of the new Future Earth initiative; and release of the Strategic Plan for Biodiversity 2011-2020). This article presents the vision and its core scientific challenges.

Assessment of carbon in woody plants and soil across a vineyard-woodland landscape.

BACKGROUND: Quantification of ecosystem services, such as carbon (C) storage, can demonstrate the benefits of managing for both production and habitat conservation in agricultural landscapes. In this study, we evaluated C stocks and woody plant diversity across vineyard blocks and adjoining woodland ecosystems (wildlands) for an organic vineyard in northern California. Carbon was measured in soil from 44 one m deep pits, and in aboveground woody biomass from 93 vegetation plots. These data were combined with physical landscape variables to model C stocks using a geographic information system and multivariate linear regression. RESULTS: Field data showed wildlands to be heterogeneous in both C stocks and woody tree diversity, reflecting the mosaic of several different vegetation types, and storing on average 36.8 Mg C/ha in aboveground woody biomass and 89.3 Mg C/ha in soil. Not surprisingly, vineyard blocks showed less variation in above- and belowground C, with an average of 3.0 and 84.1 Mg C/ha, respectively. CONCLUSIONS: This research demonstrates that vineyards managed with practices that conserve some fraction of adjoining wildlands yield benefits for increasing overall C stocks and species and habitat diversity in integrated agricultural landscapes. For such complex landscapes, high resolution spatial modeling is challenging and requires accurate characterization of the landscape by vegetation type, physical structure, sufficient sampling, and allometric equations that relate tree species to each landscape. Geographic information systems and remote sensing techniques are useful for integrating the above variables into an analysis platform to estimate C stocks in these working landscapes, thereby helping land managers qualify for greenhouse gas mitigation credits. Carbon policy in California, however, shows a lack of focus on C stocks compared to emissions, and on agriculture compared to other sectors. Correcting these policy shortcomings could create incentives for ecosystem service provision, including C storage, as well as encourage better farm stewardship and habitat conservation.

Monitoring the world's agriculture.

To feed the world without further damaging the planet, Jeffrey Sachs and 24 foodsystem experts call for a global data collection and dissemination network to track the myriad impacts of different farming practices.

Tomato root transcriptome response to a nitrogen-enriched soil patch.

BACKGROUND: Nitrogen (N), the primary limiting factor for plant growth and yield in agriculture, has a patchy distribution in soils due to fertilizer application or decomposing organic matter. Studies in solution culture over-simplify the complex soil environment where microbial competition and spatial and temporal heterogeneity challenge roots' ability to acquire adequate amounts of nutrients required for plant growth. In this study, various ammonium treatments (as 15N) were applied to a discrete volume of soil containing tomato (Solanum lycopersicum) roots to simulate encounters with a localized enriched patch of soil. Transcriptome analysis was used to identify genes differentially expressed in roots 53 hrs after treatment. RESULTS: The ammonium treatments resulted in significantly higher concentrations of both ammonium and nitrate in the patch soil. The plant roots and shoots exhibited increased levels of 15N over time, indicating a sustained response to the enriched environment. Root transcriptome analysis identified 585 genes differentially regulated 53 hrs after the treatments. Nitrogen metabolism and cell growth genes were induced by the high ammonium (65 mug NH4+-N g-1 soil), while stress response genes were repressed. The complex regulation of specific transporters following the ammonium pulse reflects a simultaneous and synergistic response to rapidly changing concentrations of both forms of inorganic N in the soil patch. Transcriptional analysis of the phosphate transporters demonstrates cross-talk between N and phosphate uptake pathways and suggests that roots increase phosphate uptake via the arbuscular mycorrhizal symbiosis in response to N. CONCLUSION: This work enhances our understanding of root function by providing a snapshot of the response of the tomato root transcriptome to a pulse of ammonium in a complex soil environment. This response includes an important role for the mycorrhizal symbiosis in the utilization of an N patch.

Land use and climatic factors structure regional patterns in soil microbial communities.

AIM: Although patterns are emerging for macroorganisms, we have limited understanding of the factors determining soil microbial community composition and productivity at large spatial extents. The overall objective of this study was to discern the drivers of microbial community composition at the extent of biogeographical provinces and regions. We hypothesized that factors associated with land use and climate would drive soil microbial community composition and biomass. LOCATION: Great Basin Province, Desert Province and California Floristic Province, California, USA. METHODS: Using phospholipid fatty acid analysis, we compared microbial communities across eight land-use types sampled throughout the State of California, USA (n = 1117). RESULTS: The main factor driving composition and microbial biomass was land-use type, especially as related to water availability and disturbance. Dry soils were more enriched in Gram-negative bacteria and fungi, and wetter soils were more enriched in Gram-positive, anaerobic and sulphate-reducing bacteria. Microbial biomass was lowest in ecosystems with the wettest and driest soils. Disturbed soils had less fungal and more Gram-positive bacterial biomass than wildland soils. However, some factors known to influence microbial communities, such as soil pH and specific plant taxa, were not important here. MAIN CONCLUSIONS: Distinct microbial communities were associated with land-use types and disturbance at the regional extent. Overall, soil water availability was an important determinant of soil microbial community composition. However, because of the inclusion of managed and irrigated agricultural ecosystems, the effect of precipitation was not significant. Effects of environmental and management factors, such as flooding, tillage and irrigation, suggest that agricultural management can have larger effects on soil microbial communities than elevation and precipitation gradients.

Roots, nitrogen transformations, and ecosystem services.

This review considers some of the mechanistic processes that involve roots in the soil nitrogen (N) cycle, and their implications for the ecological functions that retain N within ecosystems: 1) root signaling pathways for N transport systems, and feedback inhibition, especially for NO(3)(-) uptake; 2) dependence on the mycorrhizal and Rhizobium/legume symbioses and their tradeoffs for N acquisition; 3) soil factors that influence the supply of NH(4)(+) and NO(3)(-) to roots and soil microbes; and 4) rhizosphere processes that increase N cycling and retention, such as priming effects and interactions with the soil food web. By integrating information on these plant-microbe-soil N processes across scales and disciplinary boundaries, we propose ideas for better manipulating ecological functions and processes by which the environment provides for human needs, i.e., ecosystem services. Emphasis is placed on agricultural systems, effects of N deposition in natural ecosystems, and ecosystem responses to elevated CO(2) concentrations. This shows the need for multiscale approaches to increase human dependence on a biologically based N supply.

Growth, nutrition, and soil respiration of a mycorrhiza-defective tomato mutant and its mycorrhizal wild-type progenitor.

The effects of colonisation of roots by arbuscular mycorrhizal fungi (AMF) on soil respiration, plant growth, nutrition, and soil microbial communities were assessed using a mycorrhiza-defective tomato (Solanum lycopersicum L.) mutant and its mycorrhizal wild-type progenitor. Plants were grown in rhizocosms in an automated respiration monitoring system over the course of the experiment (79 days). Soil respiration was similar in the two tomato genotypes, and between P treatments with plants. Mycorrhizal colonisation increased P and Zn content and decreased root biomass, but did not affect aboveground plant biomass. Soil microbial biomass C and soil microbial communities based on phospholipid fatty acid (PLFA) analysis were similar across all treatments, suggesting that the two genotypes differed little in their effect on soil activity. Although approximately similar amounts of C may have been expended belowground in both genotypes, they may have differed in the relative C allocation to root construction v. respiration. Further, net soil respiration did not differ between the two tomato genotypes, but root dry weight was lower in mycorrhizal roots, and respiration of mycorrhizal roots per unit dry weight was higher than nonmycorrhizal roots. This indicates that the AM contribution to soil respiration may indeed be significant, and nutrient uptake per unit C expenditure belowground in this experiment appeared to be higher in mycorrhizal plants.

Mycorrhizal effects on growth and nutrition of tomato under elevated atmospheric carbon dioxide.

Arbuscular mycorrhizas are predicted to be important in defining plant responses to elevated atmospheric CO2 concentrations. A mycorrhiza-defective tomato (Solanum lycopersicum L.) mutant with reduced mycorrhizal colonisation (rmc) and its mycorrhizal wild-type progenitor (76R MYC+) were grown under ambient and elevated atmospheric CO2 concentrations (eCO2) in a controlled environment chamber-based pot study. Plant growth, nutrient contents and mycorrhizal colonisation were measured four times over a 72-day period. The 76R MYC+ plants generally had higher concentrations of P, N and Zn than their rmc counterparts. Consistent with earlier studies, mycorrhizal colonisation was not affected by eCO2. Growth of the two genotypes was very similar under ambient CO2 conditions. Under eCO2 the mycorrhizal plants initially had higher biomass, but after 72 days, biomass was lower than for rmc plants, suggesting that in this pot study the costs of maintaining carbon inputs to the fungal symbiont outweighed the benefits with time.

Application of real-time PCR to study effects of ammonium on population size of ammonia-oxidizing bacteria in soil.

Ammonium oxidation by autotrophic ammonia-oxidizing bacteria (AOB) is a key process in agricultural and natural ecosystems and has a large global impact. In the past, the ecology and physiology of AOB were not well understood because these organisms are notoriously difficult to culture. Recent applications of molecular techniques have advanced our knowledge of AOB, but the necessity of using PCR-based techniques has made quantitative measurements difficult. A quantitative real-time PCR assay targeting part of the ammonia-monooxygenase gene (amoA) was developed to estimate AOB population size in soil. This assay has a detection limit of 1.3 x 10(5) cells/g of dry soil. The effect of the ammonium concentration on AOB population density was measured in soil microcosms by applying 0, 1.5, or 7.5 mM ammonium sulfate. AOB population size and ammonium and nitrate concentrations were monitored for 28 days after (NH4)2SO4 application. AOB populations in amended treatments increased from an initial density of approximately 4 x 10(6) cells/g of dry soil to peak values (day 7) of 35 x 10(6) and 66 x 10(6) cells/g of dry soil in the 1.5 and 7.5 mM treatments, respectively. The population size of total bacteria (quantified by real-time PCR with a universal bacterial probe) remained between 0.7 x 10(9) and 2.2 x 10(9) cells/g of soil, regardless of the ammonia concentration. A fertilization experiment was conducted in a tomato field plot to test whether the changes in AOB density observed in microcosms could also be detected in the field. AOB population size increased from 8.9 x 10(6) to 38.0 x 10(6) cells/g of soil by day 39. Generation times were 28 and 52 h in the 1.5 and 7.5 mM treatments, respectively, in the microcosm experiment and 373 h in the ammonium treatment in the field study. Estimated oxidation rates per cell ranged initially from 0.5 to 25.0 fmol of NH4+ h(-1) cell(-1) and decreased with time in both microcosms and the field. Growth yields were 5.6 x 10(6), 17.5 x 10(6), and 1.7 x 10(6) cells/mol of NH4+ in the 1.5 and 7.5 mM microcosm treatments and the field study, respectively. In a second field experiment, AOB population size was significantly greater in annually fertilized versus unfertilized soil, even though the last ammonium application occurred 8 months prior to measurement, suggesting a long-term effect of ammonium fertilization on AOB population size.

Rototillage, disking, and subsequent irrigation: effects on soil nitrogen dynamics, microbial biomass, and carbon dioxide efflux.

Spring and summer tillage are usually followed by irrigation before planting crops in California's summer-dry Mediterranean-type climate. Tillage treatments such as rototillage or disking are known to disturb the soil structure to different extents, but little is known about how the intensity of a tillage event and subsequent irrigation affect the microbial biomass, respiration, CO2 efflux, and mineral N of agricultural soils. We carried out an experiment with a Yolo silt loam (fine-silty, mixed, superactive, nonacid, thermic Mollic Xerofluvent) with two tilled treatments (rototillage and disked and rolled) and a nontilled control. The soil was subsequently sampled throughout a 17-d period. Nine days after tillage, all treatments were lightly sprinkler-irrigated to bring the soil water potential above -10 kPa. After tillage, the soil ammonium and nitrate content increased rapidly relative to the control with highest increases in the disked soil. Mineral N remained higher in the tilled treatments after irrigation. Rototillage and disking increased the CO2 efflux of the soil within 24 h of the disturbance. The increase was higher in the disked soil, which was more than three times the CO2 efflux of the control soil at 0.25 h after tillage. This effect may be due to degassing of dissolved CO2 since microbial respiration did not increase in tilled soils. Irrigation increased the CO2 efflux of all treatments but this was most pronounced in the control soil, which had an order of magnitude increase in CO2 efflux after irrigation. An ancillary experiment carried out under similar conditions but with more frequent sampling showed that increases in CO2 efflux after irrigation were accompanied by increases in soil respiration. This study shows that different tillage implements affect CO2 efflux, nitrate accumulation, and microbial activity, and thus have different effects on soil and atmospheric environmental quality.