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Introduction: Phosphorus (P) deficiency in plants creates a variety of metabolic perturbations that decrease photosynthesis and growth. Phosphorus deficiency is especially challenging for the production of bioenergy feedstock plantation species, such as poplars (Populus spp.), where fertilization may not be practically or economically feasible. While the phenotypic effects of P deficiency are well known, the molecular mechanisms underlying whole-plant and tissue-specific responses to P deficiency, and in particular the responses of commercially valuable hardwoods, are less studied. Methods: We used a multi-tissue and multi-omics approach using transcriptomic, proteomic, and metabolomic analyses of the leaves and roots of black cottonwood (Populus trichocarpa) seedlings grown under P-deficient (5 µM P) and replete (100 µM P) conditions to assess this knowledge gap and to identify potential gene targets for selection for P efficiency. Results: In comparison to seedlings grown at 100 µM P, P-deficient seedlings exhibited reduced dry biomass, altered chlorophyll fluorescence, and reduced tissue P concentrations. In line with these observations, growth, C metabolism, and photosynthesis pathways were downregulated in the transcriptome of the Pdeficient plants. Additionally, we found evidence of strong lipid remodeling in the leaves. Metabolomic data showed that the roots of P-deficient plants had a greater relative abundance of phosphate ion, which may reflect extensive degradation of P-rich metabolites in plants exposed to long-term P-deficiency. With the notable exception of the KEGG pathway for Starch and Sucrose Metabolism (map00500), the responses of the transcriptome and the metabolome to P deficiency were consistent with one another. No significant changes in the proteome were detected in response to P deficiency. Discussion and conclusion: Collectively, our multi-omic and multi-tissue approach enabled the identification of important metabolic and regulatory pathways regulated across tissues at the molecular level that will be important avenues to further evaluate for P efficiency. These included stress-mediating systems associated with reactive oxygen species maintenance, lipid remodeling within tissues, and systems involved in P scavenging from the rhizosphere. [ABSTRACT FROM AUTHOR]

Changes in the nitrogen (N) status of forest ecosystems can directly and indirectly influence their carbon (C) sequestration potential by altering soil organic matter (SOM) decomposition, soil enzyme activity, and plant–soil interactions. However, model representations of linked C–N cycles and SOM decay are not well validated against experimental data. Here, we use extensive data from the Fernow Experimental Forest long-term whole-watershed N fertilization study to compare the response to N perturbations of two soil models that represent decomposition dynamics differently (first-order decay versus microbially explicit reverse Michaelis–Menten kinetics). These two soil models were coupled to a common vegetation model which provided identical input data. Key responses to N additions measured at the study site included a shift in plant allocation to favor woody biomass over belowground carbon inputs, reductions in soil respiration, accumulation of particulate organic matter (POM), and an increase in soil C:N ratios. The vegetation model did not capture the often-observed shift in plant C allocation with N additions, which resulted in poor predictions of the soil responses. We modified the parameterization of the plant C allocation scheme to favor wood production over fine-root production with N additions, which significantly improved the vegetation and soil respiration responses. Additionally, to elicit an increase in the soil C stocks and C:N ratios with N additions, as observed, we modified the decay rates of the POM in the soil models. With these modifications, both models captured negative soil respiration and positive soil C stock responses in line with observations, but only the microbially explicit model captured an increase in soil C:N. Our results highlight the need for further model development to accurately represent plant–soil interactions, such as rhizosphere priming, and their responses to environmental change. [ABSTRACT FROM AUTHOR]

Changes in the nitrogen (N) status of forest ecosystems can directly and indirectly influence their carbon (C) sequestration potential by altering soil organic matter (SOM) decomposition, soil enzyme activity, and plant-soil interactions. However, model representation of linked C-N cycles and SOM decay are not well-validated against experimental data. Here, we use extensive data from the Fernow Experimental Forest long-term, whole-watershed N fertilization study to compare the response to N perturbations of two soil models that represent decomposition dynamics differently (first-order decay versus microbially-explicit reverse Michaelis-Menten kinetics). These two soil models were coupled to a common vegetation model which provided identical input data. Key responses to N additions measured at the study site included a shift in allocation to favor woody biomass over belowground carbon inputs, reductions in soil respiration, accumulation of particulate organic matter (POM), and an increase in soil C:N ratios. The vegetation model did not capture the often-observed shift in allocation with N additions, which resulted in poor predictions of the soil responses. We modified the plant C allocation scheme to favor wood production over fine root production with N additions, which significantly improved the vegetation and soil respiration responses. To elicit an increase in the soil C stocks and C:N ratios with N additions, as observed, we also modified the decay rates of the particulate organic matter (POM) in the soil models. With all of these modifications, only the microbially explicit model captured a positive soil C stock and C:N response in line with observations. Our results highlight the importance of accurately representing plant-soil interactions, such as rhizosphere priming, and their responses to environmental change. [ABSTRACT FROM AUTHOR]

The extent to which terrestrial ecosystems slow climate change by sequestering carbon hinges in part on nutrient limitation. We used a coupled carbon--climate model that accounts for the carbon cost to plants of supporting nitrogen-acquiring microbial symbionts to explore how nitrogen limitation affects global climate. The carbon costs of supporting symbiotic nitrogen uptake reduced net primary production, with the largest absolute effects occurring at low-latitudes and the largest relative changes occurring at high-latitudes. The largest impact occurred in high-latitude ecosystems, where such costs were estimated to increase temperature by 1.0 °C and precipitation by 9 mm yr-1. Globally, our model predicted that nitrogen limitation enhances temperature and decreases precipitation; as such, our results suggest that carbon expenditures to support nitrogen-acquiring microbial symbionts have critical consequences for Earth's climate, and that carbon-climate models that omit these processes will over-predict the land carbon sink and under-predict climate change. [ABSTRACT FROM AUTHOR]

While it is well established that plants associating with arbuscular mycorrhizal ( AM) and ectomycorrhizal ( ECM) fungi cycle carbon (C) and nutrients in distinct ways, we have a limited understanding of whether varying abundance of ECM and AM plants in a stand can provide integrative proxies for key biogeochemical processes., We explored linkages between the relative abundance of AM and ECM trees and microbial functioning in three hardwood forests in southern Indiana, USA. Across each site's 'mycorrhizal gradient', we measured fungal biomass, fungal : bacterial (F : B) ratios, extracellular enzyme activities, soil carbon : nitrogen ratio, and soil pH over a growing season., We show that the percentage of AM or ECM trees in a plot promotes microbial communities that both reflect and determine the C to nutrient balance in soil. Soils dominated by ECM trees had higher F : B ratios and more standing fungal biomass than AM stands. Enzyme stoichiometry in ECM soils shifted to higher investment in extracellular enzymes needed for nitrogen and phosphorus acquisition than in C-acquisition enzymes, relative to AM soils., Our results suggest that knowledge of mycorrhizal dominance at the stand or landscape scale may provide a unifying framework for linking plant and microbial community dynamics, and predicting their effects on ecological function. [ABSTRACT FROM AUTHOR]

While multiple experiments have demonstrated that trees exposed to elevated CO2 can stimulate microbes to release nutrients from soil organic matter, the importance of root- versus mycorrhizal-induced changes in soil processes are presently unknown., We analyzed the contribution of roots and mycorrhizal activities to carbon (C) and nitrogen (N) turnover in a loblolly pine ( Pinus taeda) forest exposed to elevated CO2 by measuring extracellular enzyme activities at soil microsites accessed via root windows. Specifically, we quantified enzyme activity from soil adjacent to root tips (rhizosphere), soil adjacent to hyphal tips (hyphosphere), and bulk soil., During the peak growing season, CO2 enrichment induced a greater increase of N-releasing enzymes in the rhizosphere (215% increase) than in the hyphosphere (36% increase), but a greater increase of recalcitrant C-degrading enzymes in the hyphosphere (118%) than in the rhizosphere (19%). Nitrogen fertilization influenced the magnitude of CO2 effects on enzyme activities in the rhizosphere only. At the ecosystem scale, the rhizosphere accounted for c. 50% and 40% of the total activity of N- and C-releasing enzymes, respectively., Collectively, our results suggest that root exudates may contribute more to accelerated N cycling under elevated CO2 at this site, while mycorrhizal fungi may contribute more to soil C degradation. [ABSTRACT FROM AUTHOR]

Temperature and substrate availability constrain the activity of the extracellular enzymes that decompose and release nutrients from soil organic matter (SOM). Proteolytic enzymes are the primary class of enzymes involved in the depolymerization of nitrogen (N) from proteinaceous components of SOM, and their activity affects the rate of N cycling in forest soils. The objectives of this study were to determine whether and how temperature and substrate availability affect the activity of proteolytic enzymes in temperate forest soils, and whether the activity of proteolytic enzymes and other enzymes involved in the acquisition of N (i.e., chitinolytic and ligninolytic enzymes) differs between trees species that form associations with either ectomycorrhizal or arbuscular mycorrhizal fungi. Temperature limitation of proteolytic enzyme activity was observed only early in the growing season when soil temperatures in the field were near 4°C. Substrate limitation to proteolytic activity persisted well into the growing season. Ligninolytic enzyme activity was higher in soils dominated by ectomycorrhizal associated tree species. In contrast, the activity of proteolytic and chitinolytic enzymes did not differ, but there were differences between mycorrhizal association in the control of roots on enzyme activity. Roots of ectomycorrhizal species but not those of arbuscular mycorrhizal species exerted significant control over proteolytic, chitinolytic, and ligninolytic enzyme activity; the absence of ectomycorrhizal fine roots reduced the activity of all three enzymes. These results suggest that climate warming in the absence of increases in substrate availability may have a modest effect on soil-N cycling, and that global changes that alter below ground carbon allocation by trees are likely to have a larger effect on nitrogen cycling in stands dominated by ectomycorrhizal fungi. [ABSTRACT FROM AUTHOR]

While multiple experiments have demonstrated that trees exposed to elevated CO2 can stimulate microbes to release nutrients from soil organic matter, the importance of root- versus mycorrhizal-induced changes in soil processes are presently unknown., We analyzed the contribution of roots and mycorrhizal activities to carbon (C) and nitrogen (N) turnover in a loblolly pine ( Pinus taeda) forest exposed to elevated CO2 by measuring extracellular enzyme activities at soil microsites accessed via root windows. Specifically, we quantified enzyme activity from soil adjacent to root tips (rhizosphere), soil adjacent to hyphal tips (hyphosphere), and bulk soil., During the peak growing season, CO2 enrichment induced a greater increase of N-releasing enzymes in the rhizosphere (215% increase) than in the hyphosphere (36% increase), but a greater increase of recalcitrant C-degrading enzymes in the hyphosphere (118%) than in the rhizosphere (19%). Nitrogen fertilization influenced the magnitude of CO2 effects on enzyme activities in the rhizosphere only. At the ecosystem scale, the rhizosphere accounted for c. 50% and 40% of the total activity of N- and C-releasing enzymes, respectively., Collectively, our results suggest that root exudates may contribute more to accelerated N cycling under elevated CO2 at this site, while mycorrhizal fungi may contribute more to soil C degradation. [ABSTRACT FROM AUTHOR]

While multiple experiments have demonstrated that trees exposed to elevated CO₂ can stimulate microbes to release nutrients from soil organic matter, the importance of root- versus mycorrhizal-induced changes in soil processes are presently unknown. We analyzed the contribution of roots and mycorrhizal activities to carbon (C) and nitrogen (N) turnover in a loblolly pine (Pinus taeda) forest exposed to elevated CO₂ by measuring extracellular enzyme activities at soil microsites accessed via root windows. Specifically, we quantified enzyme activity from soil adjacent to root tips (rhizosphere), soil adjacent to hyphal tips (hyphosphere), and bulk soil. During the peak growing season, CO₂ enrichment induced a greater increase of N-releasing enzymes in the rhizosphere (215% increase) than in the hyphosphere (36% increase), but a greater increase of recalcitrant C-degrading enzymes in the hyphosphere (118%) than in the rhizosphere (19%). Nitrogen fertilization influenced the magnitude of CO₂ effects on enzyme activities in the rhizosphere only. At the ecosystem scale, the rhizosphere accounted for c. 50% and 40% of the total activity of N- and C-releasing enzymes, respectively. Collectively, our results suggest that root exudates may contribute more to accelerated N cycling under elevated CO₂ at this site, while mycorrhizal fungi may contribute more to soil C degradation., (© 2014 The Authors. New Phytologist © 2014 New Phytologist Trust.)