Facultative symbiosis with a saprotrophic soil fungus promotes potassium uptake in American sweetgum trees.

Several species of soil free-living saprotrophs can sometimes establish biotrophic symbiosis with plants, but the basic biology of this association remains largely unknown. Here, we investigate the symbiotic interaction between a common soil saprotroph, Clitopilus hobsonii (Agaricomycetes), and the American sweetgum (Liquidambar styraciflua). The colonized root cortical cells were found to contain numerous microsclerotia-like structures. Fungal colonization led to increased plant growth and facilitated potassium uptake, particularly under potassium limitation (0.05 mM K+ ). The expression of plant genes related to potassium uptake was not altered by the symbiosis, but colonized roots contained the transcripts of three fungal genes with homology to K+ transporters (ACU and HAK) and channel (SKC). Heterologously expressed ChACU and ChSKC restored the growth of a yeast K+ -uptake-defective mutant. Upregulation of ChACU transcript under low K+ conditions (0 and 0.05 mM K+ ) compared to control (5 mM K+ ) was demonstrated in planta and in vitro. Colonized plants displayed a larger accumulation of soluble sugars under 0.05 mM K+ than non-colonized plants. The present study suggests reciprocal benefits of this novel tree-fungus symbiosis under potassium limitation mainly through an exchange of additional carbon and potassium between both partners.

Decomposing litter and associated microbial activity responses to nitrogen deposition in two subtropical forests containing nitrogen-fixing or non-nitrogen-fixing tree species.

Atmospheric nitrogen (N) deposition has caused concern due to its effects on litter decomposition in subtropical regions where N-fixing tree species are widespread. However, the effect of N deposition on litter decomposition in N-fixing plantations remains unclear. We investigated the effects of a 2-year N deposition treatment on litter decomposition, microbial activity, and nutrient release in two subtropical forests containing Alnus cremastogyne (AC, N-fixing) and Liquidambar formosana (LF, non-N-fixing). The decomposition rate in AC was faster than in LF when there was no experimental N deposition. In AC, the initial decomposition rate was faster when additional N was applied and was strongly linked to higher cellulose-degrading enzyme activities during the early decomposition stage. However, N deposition reduced litter decomposition and inhibited lignin-degrading enzyme activities during the later decomposition stage. Nitrogen deposition enhanced carbohydrate and alcohol utilization, but suppressed amino acid and carboxylic acid uptake in the AC plantation. However, it did not significantly affect litter decomposition and microbial activity in the LF plantation. In conclusion, N deposition could inhibit litter decomposition by changing microbial enzyme and metabolic activities during the decomposition process and would increase carbon accumulation and nitrogen retention in subtropical forests with N-fixing tree species.

Effects of artificial defoliation on growth and biomass accumulation in short-rotation sweetgum (Liquidambar styraciflua) in North Carolina.

Sweetgum, Liquidambar styraciflua L. (Hamamelidales: Hamamelidaceae), is a species of interest for short-rotation plantation forestry in the southeastern United States. Despite its high levels of resistance to many native insects and pathogens, the species is susceptible to generalist defoliators during outbreak epidemics. The objective of this field study was to evaluate the potential impact of defoliation on sweetgum growth and productivity within the context of an operational plantation. Over three growing seasons, trees were subjected to artificial defoliation treatments of various intensity (control = 0% defoliation; low intensity = 33% defoliation; moderate intensity = 67% defoliation; high intensity = 99% defoliation) and frequency (not defoliated; defoliated once in April of the first growing season; defoliated twice, once in April of the first growing season and again in April of the second growing season). The responses of stem height, stem diameter, stem volume, crown volume, total biomass accumulation, and branch growth were measured in November of each growing season. At the end of the first growing season, when trees had received single defoliations, significant reductions in all growth traits followed the most severe (99%) defoliation treatment only. After the second and third growing seasons, when trees had received one or two defoliations of varying intensity, stem diameter and volume and total tree biomass were reduced significantly by 67 and 99% defoliation, while reductions in stem height and crown volume followed the 99% treatment only. All growth traits other than crown volume were reduced significantly by two defoliations but not one defoliation. Results indicate that sweetgum is highly resilient to single defoliations of low, moderate, and high intensity. However, during the three-year period of the study, repeated high-intensity defoliation caused significant reductions in growth and productivity that could have lasting impacts on yield throughout a harvest rotation.

Trends in seedling growth and carbon-use efficiency vary among broadleaf tree species along a latitudinal transect in eastern North America.

Factors constraining the geographic ranges of broadleaf tree species in eastern North America were examined in common gardens along a ~1500 km latitudinal transect travers in grange boundaries of four target species: trembling aspen (Populus tremuloides) and paper birch (Betula papyrifera) to the north vs. eastern cottonwood (Populus deltoides) and sweet gum (Liquidambar styraciflua) to the south. In 2006 and 2007, carbon-use efficiency (CUE), the proportion of assimilated carbon retained in biomass, was estimated for seedlings of the four species as the quotient of relative growth rate (RGR) and photosynthesis per unit tree mass (Atree ). In aspen and birch, CUE and RGR declined significantly with increasing growth temperature, which spanned 9 °C across gardens and years. The 37% (relative) CUE decrease from coolest to warmest garden correlated with increases in leaf nighttime respiration (Rleaf ) and the ratio of Rleaf to leaf photosynthesis (R%A ). For cottonwood and sweet gum, however, similar increases in Rleaf and R%A accompanied modest CUE declines, implying that processes other than Rleaf were responsible for species differences in CUE's temperature response. Our findings illustrate marked taxonomic variation, at least among young trees, in the thermal sensitivity of CUE, and point to potentially negative consequences of climate warming for the carbon balance, competitive ability, and persistence of two foundation species in northern temperate and boreal forests.

Stored carbon partly fuels fine-root respiration but is not used for production of new fine roots.

The relative use of new photosynthate compared to stored carbon (C) for the production and maintenance of fine roots, and the rate of C turnover in heterogeneous fine-root populations, are poorly understood. We followed the relaxation of a (13)C tracer in fine roots in a Liquidambar styraciflua plantation at the conclusion of a free-air CO(2) enrichment experiment. Goals included quantifying the relative fractions of new photosynthate vs stored C used in root growth and root respiration, as well as the turnover rate of fine-root C fixed during [CO(2)] fumigation. New fine-root growth was largely from recent photosynthate, while nearly one-quarter of respired C was from a storage pool. Changes in the isotopic composition of the fine-root population over two full growing seasons indicated heterogeneous C pools; < 10% of root C had a residence time < 3 months, while a majority of root C had a residence time > 2 yr. Compared to a one-pool model, a two-pool model for C turnover in fine roots (with 5 and 0.37 yr(-1) turnover times) doubles the fine-root contribution to forest NPP (9-13%) and supports the 50% root-to-soil transfer rate often used in models.

The effects of elevated CO2 and nitrogen fertilization on stomatal conductance estimated from 11 years of scaled sap flux measurements at Duke FACE.

In this study, we employ a network of thermal dissipation probes (TDPs) monitoring sap flux density to estimate leaf-specific transpiration (E(L)) and stomatal conductance (G(S)) in Pinus taeda (L.) and Liquidambar styraciflua L. exposed to +200 ppm atmospheric CO(2) levels (eCO(2)) and nitrogen fertilization. Scaling half-hourly measurements from hundreds of sensors over 11 years, we found that P. taeda in eCO(2) intermittently (49% of monthly values) decreased stomatal conductance (G(S)) relative to the control, with a mean reduction of 13% in both total E(L) and mean daytime G(S). This intermittent response was related to changes in a hydraulic allometry index (A(H)), defined as sapwood area per unit leaf area per unit canopy height, which decreased a mean of 15% with eCO(2) over the course of the study, due mostly to a mean 19% increase in leaf area (A(L)). In contrast, L. styraciflua showed a consistent (76% of monthly values) reduction in G(S) with eCO(2) with a total reduction of 32% E(L), 31% G(S) and 23% A(H) (due to increased A(L) per sapwood area). For L. styraciflua, like P. taeda, the relationship between A(H) and G(S) at reference conditions suggested a decrease in G(S) across the range of A(H). Our findings suggest an indirect structural effect of eCO(2) on G(S) in P. taeda and a direct leaf level effect in L. styraciflua. In the initial year of fertilization, P. taeda in both CO(2) treatments, as well as L. styraciflua in eCO(2), exhibited higher G(S) with N(F) than expected from shifts in A(H), suggesting a transient direct effect on G(S). Whether treatment effects on mean leaf-specific G(S) are direct or indirect, this paper highlights that long-term treatment effects on G(S) are generally reflected in A(H) as well.

[Soil heterotrophic respiration and its sensitivity to soil temperature and moisture in Liquidambar formosana and Pinus massoniana forests in hilly areas of southeast Hubei Province, China].

Field monitoring was conducted to study the annual dynamics of soil heterotrophic respiration and soil temperature and moisture in Liquidambar formosana and Pinus massoniana forests in hilly areas of southeast Hubei Province, China. At the same time, laboratory experiment was performed to study the heterotrophic respiration rate along soil profile, and the sensitivity of surface soil (0-5 cm) heterotrophic respiration to soil temperature and moisture. Then, a model was established to valuate the potential effects of warming change on the soil heterotrophic respiration in study area. In L. formosana and P. massoniana forests, the soil heterotrophic respiration rate in 0-5 cm layer was 2.39 and 2.62 times, and 2.01 and 2.94 times of that in 5-10 cm and 10-20 cm layers, respectively, illustrating that soil heterotrophic respiration mainly occurred in 0-5 cm surface layer. The temperature sensitivity factor (Q10) of soil heterotrophic respiration in 0-5 cm, 5-10 cm, and 10-20 cm layers was 2.10, 1.86, and 1.78 in L. formosana forest, and 1.86, 1.77, and 1.44 in P. massoniana forest, respectively. The relationship between surface soil heterotrophic respiration and temperature (T) well fitted exponential function R = alphaexp (beta3T), and that between surface soil heterotrophic respiration and moisture (W) well fitted quadratic function R = a+bW+cW2. Therefore, the relationship of surface soil heterotrophic respiration with soil temperature and moisture could be described by the model lnR = a+bW+cW2 +dT+eT2, which suggested that the response of soil heterotrophic respiration to soil moisture was depended on soil temperature, i.e., the sensitivity decreased with decreasing soil temperature. The calculation of the annual soil heterotrophic respiration rate in the two forests with the established model showed that the calculated respiration rate was a slightly higher in L. formosana forest but close to the measured one in P. massoniana forest, illustrating the applied importance of the model. Our results suggested that the soil heterotrophic respiration in the L. formosana and P. massoniana forests in hilly areas of southeast Hubei Province would have an obvious increase under the background of global warming.

Litterfall 15N abundance indicates declining soil nitrogen availability in a free-air CO2 enrichment experiment.

Forest productivity increases in response to carbon dioxide (CO2) enrichment of the atmosphere. However, in nitrogen-limited ecosystems, increased productivity may cause a decline in soil nitrogen (N) availability and induce a negative feedback on further enhancement of forest production. In a free-air CO2 enrichment (FACE) experiment, the response of sweetgum (Liquidambar styraciflua L.) productivity to elevated CO2 concentrations [CO2] has declined over time, but documenting an associated change in soil N availability has been difficult. Here we assess the time history of soil N availability through analysis of natural 15N abundance in archived samples of freshly fallen leaf litterfall. Litterfall delta15N declined from 1998 to 2005, and the rate of decline was significantly faster in elevated [CO2]. Declining leaf litterfall delta15N is indicative of a tighter ecosystem N cycle and more limited soil N availability. By integrating N availability over time and throughout the soil profile, temporal dynamics in leaf litterfall delta15N provide a powerful tool for documenting changes in N availability and the critical feedbacks between C and N cycles that will control forest response to elevated atmospheric CO2 concentrations.

[Effects of eutrophic nitrogen nutrition on carbon balance capacity of Liquidambar formosana seedlings under low light].

To investigate the effects of atmospheric nitrogen deposition on the seedlings regeneration of Liquidambar formosana, a greenhouse experiment was conducted, in which, the low light- and nitrogen supplies were controlled similar to those in typical L. formosana secondary forests, with the effects of different light- and nitrogen supply on the L. formosana seedlings survival, leaf functional traits, biomass allocation, and gas exchange studied. The whole plant light compensation point (LCP(whoIe-plant)) of the seedlings was estimated with a whole plant carbon balance model, and then compared with the understory photosynthetic active radiance (PAR) of the typical secondary forests. Under 3.0% and 6.0% of full sunlight, eutrophic nitrogen supply led to a decrease of seedlings survival (shade tolerance) and specific leaf area (SLA), but had no obvious effects on the seedlings biomass allocation. At eutrophic nitrogen supply, light intensity had significant effects on the leaf area based maximum assimilation rate, whereas increasing nitrogen supply under low light induced the increase of leaf mass based dark respiration rate. Both light intensity and nitrogen supply had significant effects on the mass based leaf respiration rate, and the interaction of light and nitrogen had significant effects on the mass based stem respiration rate. Increasing nitrogen supply increased the LCP(wholeplant), under 3.0%, 6.0%, and 12.0% of full sunlight, but decreased the LCP(whoIe-plant) under 25.0% of full sunlight. The decrease of the seedlings shade tolerance induced by the increasing nitrogen supply under low light was correlated with the variations of the seedlings carbon balance capacity. Under the background of elevated atmospheric nitrogen deposition, the maintenance of L. formosana populations in China would more depend on disturbances and gap regeneration, and the population dynamics would be deeply affected.

[Effects of phosphorus stress on the growth and nitrogen and phosphorus absorption of different Formosan sweet gum provenances].

Aiming at the ecological value of Formosan sweet gum (Liquidambar formosana) as a pioneer species and the status of red soil phosphorus (P) deficiency, a sand culture experiment of split design was conducted to study the responses of three-leaf stage seedlings of seven Formosan sweet gum provenances from Yixing of Jiangsu, Jingxian of Anhui, Yongkang of Zhejiang, Nanchang of Jiangxi, Shaowu of Fujian, Yanping of Fujian, and Nandan of Guangxi to four levels of P (P0, P1/2, P1, P2). With increasing P stress, the biomass and the N and P absorption of test provenances decreased, whereas the utilization efficiency increased. In higher P treatments, the provenances from Nanchang and Yixing had higher biomass and higher N and P absorption but lower utilization efficiency, while the provenance from Nandan had lower N and P absorption but higher utilization efficiency. In lower P treatments, the biomass and the P absorption and utilization efficiency of the provenances from Nanchang and Nandan were all higher. All the results illustrated that the provenances with high biomass had high P absorption at high P level, and had both high P absorption and high utilization efficiency at low P level. The provenance from Nanchang could be considered to be an excellent P stress-resistant provenance, followed by that from Nandan. Phosphorus was not a limiting nutritional factor of Formosan sweet gum, biomass, leaf delta (N/P) ratio and P efficiency could be used as the indicators of P stress-tolerance of Formosan sweet gum provenances.

CO2 enrichment increases carbon and nitrogen input from fine roots in a deciduous forest.

* Greater fine-root production under elevated [CO2] may increase the input of carbon (C) and nitrogen (N) to the soil profile because fine root populations turn over quickly in forested ecosystems. * Here, the effect of elevated [CO)] was assessed on root biomass and N inputs at several soil depths by combining a long-term minirhizotron dataset with continuous, root-specific measurements of root mass and [N]. The experiment was conducted in a CO(2)-enriched sweetgum (Liquidambar styraciflua) plantation. * CO2) enrichment had no effect on root tissue density or [N] within a given diameter class. Root biomass production and standing crop were doubled under elevated [CO2]. Though fine-root turnover declined under elevated [CO2], fine-root mortality was also nearly doubled under CO2 enrichment. Over 9 yr, root mortality resulted in 681 g m(-2) of extra C and 9 g m(-2) of extra N input to the soil system under elevated [CO2]. At least half of these inputs were below 30 cm soil depth. * Increased C and N input to the soil under CO2 enrichment, especially below 30 cm depth, might alter soil C storage and N mineralization. Future research should focus on quantifying root decomposition dynamics and C and N mineralization deeper in the soil.

Nitrogen uptake, distribution, turnover, and efficiency of use in a CO2-enriched sweetgum forest.

The Progressive Nitrogen Limitation (PNL) hypothesis suggests that ecosystems in a CO2-enriched atmosphere will sequester C and N in long-lived biomass and soil organic pools, thereby limiting available N and constraining the continued response of net primary productivity to elevated [CO2]. Here, we present a six-year record of N dynamics of a sweetgum (Liquidambar styraciflua) stand exposed to elevated [CO2] in the free-air CO2 enrichment (FACE) experiment at Oak Ridge, Tennessee, USA. We also evaluate the concept of PNL for this ecosystem from the perspective of N uptake, content, distribution, and turnover, and N-use efficiency. Leaf N content was 11% lower on a leaf mass basis (NM) and 7% lower on a leaf area basis (NA) in CO2-enriched trees. However, there was no effect of [CO2] on total canopy N content. Resorption of N during senescence was not altered by [CO2], so NM of litter, but not total N content, was reduced. The NM of fine roots was not affected, but the total amount of N required for fine-root production increased significantly, reflecting the large stimulation of fine-root production in this stand. Hence, total N requirement of the trees was higher in elevated [CO2], and the increased requirement was met through an increase in N uptake rather than increased retranslocation of stored reserves. Increased N uptake was correlated with increased net primary productivity (NPP). N-use efficiency, however, did not change with CO2 enrichment because increased N productivity was offset by lower mean residence time of N in the trees. None of the measured responses of plant N dynamics in this ecosystem indicated the occurrence of PNL, and the stimulation of NPP by elevated [CO2] was sustained for the first six years of the experiment. Although there are some indications of developing changes in the N economy, the N supply in the soil at this site may be sufficient to meet an increasing demand for available N, especially as the roots of CO2-enriched trees explore deeper in the soil profile.

Fine-root production dominates response of a deciduous forest to atmospheric CO2 enrichment.

Fine-root production and turnover are important regulators of the biogeochemical cycles of ecosystems and key components of their response to global change. We present a nearly continuous 6-year record of fine-root production and mortality from minirhizotron analysis of a closed-canopy, deciduous sweetgum forest in a free-air CO(2) enrichment experiment. Annual production of fine roots was more than doubled in plots with 550 ppm CO(2) compared with plots in ambient air. This response was the primary component of the sustained 22% increase in net primary productivity. Annual fine-root mortality matched annual production, and the mean residence time of roots was not altered by elevated CO(2), but peak fine-root standing crop in midsummer was significantly higher in CO(2)-enriched plots, especially deeper in the soil profile. The preferential allocation of additional carbon to fine roots, which have a fast turnover rate in this species, rather than to stemwood reduces the possibility of long-term enhancement by elevated CO(2) of carbon sequestration in biomass. However, sequestration of some of the fine-root carbon in soil pools is not precluded, and there may be other benefits to the tree from a seasonally larger and deeper fine-root system. Root-system dynamics can explain differences among ecosystems in their response to elevated atmospheric CO(2); hence, accurate assessments of carbon flux and storage in forests in a globally changing atmosphere must account for this unseen and difficult-to-measure component.

Impacts of fine root turnover on forest NPP and soil C sequestration potential.

Estimates of forest net primary production (NPP) demand accurate estimates of root production and turnover. We assessed root turnover with the use of an isotope tracer in two forest free-air carbon dioxide enrichment experiments. Growth at elevated carbon dioxide did not accelerate root turnover in either the pine or the hardwood forest. Turnover of fine root carbon varied from 1.2 to 9 years, depending on root diameter and dominant tree species. These long turnover times suggest that root production and turnover in forests have been overestimated and that sequestration of anthropogenic atmospheric carbon in forest soils may be lower than currently estimated.

Leaf dynamics of a deciduous forest canopy: no response to elevated CO2.

Leaf area index (LAI) and its seasonal dynamics are key determinants of terrestrial productivity and, therefore, of the response of ecosystems to a rising atmospheric CO(2) concentration. Despite the central importance of LAI, there is very little evidence from which to assess how forest LAI will respond to increasing [CO(2)]. We assessed LAI and related leaf indices of a closed-canopy deciduous forest for 4 years in 25-m-diameter plots that were exposed to ambient or elevated CO(2) (542 ppm) in a free-air CO(2) enrichment (FACE) experiment. LAI of this Liquidambar styraciflua (sweetgum) stand was about 6 and was relatively constant year-to-year, including the 2 years prior to the onset of CO(2) treatment. LAI throughout the 1999-2002 growing seasons was assessed through a combination of data on photosynthetically active radiation (PAR) transmittance, mass of litter collected in traps, and leaf mass per unit area (LMA). There was no effect of [CO(2)] on any expression of leaf area, including peak LAI, average LAI, or leaf area duration. Canopy mass and LMA, however, were significantly increased by CO(2) enrichment. The hypothesized connection between light compensation point (LCP) and LAI was rejected because LCP was reduced by [CO(2)] enrichment only in leaves under full sun, but not in shaded leaves. Data on PAR interception also permitted calculation of absorbed PAR (APAR) and light use efficiency (LUE), which are key parameters connecting satellite assessments of terrestrial productivity with ecosystem models of future productivity. There was no effect of [CO(2)] on APAR, and the observed increase in net primary productivity in elevated [CO(2)] was ascribed to an increase in LUE, which ranged from 1.4 to 2.4 g MJ(-1). The current evidence seems convincing that LAI of non-expanding forest stands will not be different in a future CO(2)-enriched atmosphere and that increases in LUE and productivity in elevated [CO(2)] are driven primarily by functional responses rather than by structural changes. Ecosystem or regional models that incorporate feedbacks on resource use through LAI should not assume that LAI will increase with CO(2) enrichment of the atmosphere.

Genotypic effects of fertilization on seedling sweetgum biomass allocation, N uptake, and N use efficiency.

Screening and selecting tree genotypes that are responsive to N additions and that have high nutrient use efficiencies can provide better genetic material for short-rotation plantation establishment. A pot experiment was conducted to test the hypotheses that (1) sweetgum ( Liquidambar styraciflua L.) families have different patterns in biomass production and allocation, N uptake, and N use efficiency (NUE), because of their differences in growth strategies, and (2) sweetgum families that are more responsive to N additions will also have greater nutrient use efficiencies. Seedlings from two half-sib families (F10022 and F10023) that were known to have contrasting responses to fertility and other stress treatments were used for an experiment with two levels of N (0 vs. 100 kg N/ha equivalent) and two levels of P (0 vs. 50 kg P/ha equivalent) in a split-plot design. Sweetgum seedlings responded to N and P treatments rapidly, with increases in both size and biomass production, and those responses were greater with F10023 than with F10022. Growth response to N application was particularly strong. N and P application increased the proportional allocation of biomass to leaves. Under increased N supply, P application increased foliar N concentration and content, as well as total N uptake by the seedlings. However, NUE was decreased by N addition and was higher in F10023 than in F10022 when P was not limiting. A better understanding of genotype by fertility interactions is important in selecting genotypes for specific site conditions and for optimizing nutrient use in forestry production.