Insights into root growth, function, and mycorrhizal abundance from chemical and isotopic data across root orders

Background and aims: Detailed analyses of root chemistry by branching order may provide insights into root function, root lifespan and the abundance of root-associated mycorrhizal fungi in forest ecosystems. Methods: We examined the nitrogen and carbon stable isotopes (δ15N and δ13C) and concentration (%N and %C) in the fine roots of an arbuscular mycorrhizal tree, Fraxinus mandshurica, and an ectomycorrhizal tree, Larix gmelinii, over depth, time, and across five root branching orders. Results and conclusions: Larix δ15N increased by 2.3 ‰ from 4th order to 1st order roots, reflecting the increased presence of 15N-enriched ECM fungi on the lower root orders. In contrast, arbuscular mycorrhizal Fraxinus only increased by 0.7 ‰ from 4th order to 1st order roots, reflecting the smaller 15N enrichment and lower fungal mass on arbuscular mycorrhizal fine roots. Isotopic and anatomical mass balance calculations indicate that first, second, and third order roots in ectomycorrhizal Larix averaged 36 %, 23 %, and 8 % fungal tissue by mass, respectively. Using literature values of root production by root branching order, we estimate that about 25 % of fine root production in ECM species like Larix is actually of fungal sheaths. In contrast to %N, %C, and δ15N, δ13C changed minimally across depth, time, and branching order. The homogeneity of δ13C suggests root tissues are constructed from a large well-mixed reservoir of carbon, although compound specific δ13C data is needed to fully interpret these patterns. The measurements developed here are an important step towards explicitly including mycorrhizal production in forest ecosystem carbon budgets

Linkage of root morphology to anatomy with increasing nitrogen availability in six temperate tree species

Aims Fine root morphological traits are generally changed under soil nitrogen (N) enrichment, however, the underlying mechanism and functional significance are still not well understood. Our aims were to investigate the linkage of root morphology to anatomy, and its implication for root function at elevated soil N availability. Methods Ingrowth cores were used to sample root tips (0-20 cm soil depth) from six temperate tree species growing in monoculture plantations at a common site in northeastern China. Root morphological and anatomical traits were concurrently measured, and their relationships were determined within and among species in both control and N fertilization (10 g N m(-2)y(-1)) plots. Results Root diameter generally increased in all six species (non-significant for Phellodendron amurense) following N fertilization, which was caused by the increased root stele radius rather than cortical thickness. Congruently, N fertilization significantly decreased the ratio of cortical thickness to stele radius, but increased the ratio of total cross-sectional area of conduits to stele area in root tips across all species. Conclusions The observed anatomical changes of root tips contributed to the alternations of morphological root traits following N fertilization, with potentially important impacts on root physiological functions, like increased water and nutrient transport

Changes in soil phosphorus fractions after 9 years of continuous nitrogen addition in a Larix gmelinii plantation

International audienceThe key message N addition decreased soil inorganic P availability, microbial biomass P, and acid phosphatase activity in the larch plantation. Soil inorganic P availability decreased after N addition due to the changes in both microbial properties and plant uptake.• Context Soil phosphorus (P) availability is considered an important factor in influencing the biomass production of plants. Sustained inputs of nitrogen (N) through atmospheric deposition or N fertilizers, particularly in temperate forests, may change the composition and availability of P and thus affect long-term forest productivity.• Aims The objective of this study was to assess soil P availability, P fractions, and microbial properties including microbial biomass P and acid phosphatase activity after 9 consecutive years of N addition in a larch (Larix gmelinii) plantation, northeastern China.• Methods From 2003 to 2011, NH4NO3 was added to replicate plots (three 20 m × 30 m plots) in the larch plantation each year at a rate of 100 kg N ha−1 year−1. Soil samples from 0–10-cm and 10–20-cm depths were collected in N addition plots and control (no N addition) plots.• Results N addition significantly decreased soil NaHCO3-Pi (Pi is inorganic P), microbial biomass P, and acid phosphatase activity but increased the NaOH-Pi concentration. N addition appeared to induce a decrease in soil inorganic P availability by changing pH and P uptake by trees. In addition, N addition significantly decreased the NaOH-Po (Po is organic P) concentration, possibly because of increased P mineralization. However, the total P and other P fractions were unaffected by N fertilization.• Conclusion Our results suggested that N addition enhanced P uptake by trees, whereas it reduced soil inorganic P availability as well as microbial biomass and activity related to soil P cycling in the larch plantation

Shift from Acquisitive to Conservative Root Resource Acquisition Strategy Associated with Increasing Tree Age: A Case Study of <i>Fraxinus mandshurica</i>

Tree age has an important effect on the form and function of fine roots. Previous studies have focused on the variations in root morphological and chemical traits among tree ages, while less attention has been given to the physiological traits, impeding a full understanding of the relationship between root resource acquisition strategy and tree age. Here, we measured root morphological (diameter, specific root length, specific root area and tissue density), chemical (nitrogen concentration) and physiological (respiration and exudation rate) traits of young, middle-aged and mature trees of Fraxinus mandshurica in a temperate secondary forest in northeastern China. Our overall aim was to determine how root traits and related resource acquisition strategy change with tree age. The results showed that from young to mature trees, root diameter gradually increased, but specific root length, specific root area, root nitrogen concentration, respiration and exudation rates all decreased, and the significant differences were mainly found between young and mature trees. Pearson’s correlation analysis revealed that the relationships of root respiration and exudation rates to root morphological and chemical traits depended on tree age and the specific traits examined, but these correlations were all significant except for root tissue density when the data were pooled across all tree age classes. Principal component analysis (PCA) showed that the conservative traits represented by root diameter, and the acquisitive traits such as root respiration and exudation rates and related morphological and chemical traits, occupied two ends of the first axis, respectively, while root tissue density occupied one end of the second axis, partially confirming the conceptual framework of “root economics space”. Standardized major axis (SMA) analysis of root exudation and respiration rates showed that young trees allocated more root carbon flux to the formation of root exudation, compared to middle-aged and mature trees. Our findings suggest that root resource acquisition strategy in F. mandshurica appears to shift from an absorptive to conservative strategy associated with increasing tree age, which may have substantial consequences for individual growth and interspecific competition, as well as belowground carbon allocation in ecosystems

Temporal dynamics of fine root production, mortality and turnover deviate across branch orders in a larch stand.

Fine roots play a key role in carbon, nutrient, and water biogeochemical cycles in forest ecosystems. However, inter-annual dynamics of fine root production, mortality, and turnover on the basis of long-term measurement have been less studied. Here, field scanning rhizotrons were employed for tracking fine root by branch order over a 6&nbsp;years period in a larch plantation. For total fine roots, from the first- to the fifth-order roots, annual root length production, length mortality, standing crops, and turnover rate varied up to 3.4, 2.3, 1.5, and 2.3-folds during the study period, respectively. The inter-annual variability of those roots indices in the first-order and the second-order roots were greater than that of the higher order (third- to fifth-order) roots. The turnover rate was markedly larger for the first-order roots than for the higher order roots, showing the greatest variability up to 20&nbsp;times. Seasonal dynamics of root length production followed a general concentrated pattern with peak typically occurring in June or July, whereas root length mortality followed a general bimodal mortality pattern with the dominant peak in May and the secondary peak in August or October. Furthermore, the seasonal patterns of root length production and mortality were similar across years, especially for the first-order and the second-order roots. These results from long-term observation were beneficial for reducing uncertainty of characterizing fine root demography in consideration of large variation among years. Our findings highlight it is important for better understanding of fine root dynamics and determining root demography through distinguishing observation years and root branch orders

Variations in Arbuscular Mycorrhizal Colonization Associated with Root Diameter and Hypodermis Passages Cells across Temperate and Tropical Woody Species

Root hypodermis passage cells (PCs) lack suberin and lignin deposition, responsible for nutrient absorption and arbuscular mycorrhizal colonization, which are crucial for root resource acquisition. Nevertheless, their quantitative variability across diverse woody species and their relationships with root morphology and anatomy, as well as arbuscular mycorrhizal colonization, are still not well understood. Herein, the number and proportion of PCs in the root cross-section, root morphology, anatomy, and arbuscular mycorrhizal colonization rate were quantified across 10 temperate and 12 tropical woody species. The objectives of this study were to determine how PCs vary across contrasting environmental conditions and to explore their relationships with arbuscular mycorrhizal colonization rate and other root functional traits. The results showed that tropical species possessed 56% more PCs than temperate species; by contrast, they had similar proportions of PCs. In both biomes, the number of PCs had a tightly positive correlation with arbuscular mycorrhizal colonization rate (R2 = 0.35&ndash;0.87), root diameter (R2 = 0.84&ndash;0.93), and cortex thickness (R2 = 0.87&ndash;0.89), but the proportion of PCs was mostly independent of root morphological and anatomical traits. Our results suggest that variation in passage cells could well explain the tight linkage between arbuscular mycorrhizal colonization and root diameter across species and biomes, which provides insight into the collaboration gradient between plant roots and mycorrhizal fungi that dominates the root economics space

Differences in Fine Root Foraging Traits of Two Dominant Tree Species (<i>Cunninghamia lanceolata</i> and <i>Quercus acutissima</i>) in Subtropical Forests

Root biomass and length growth, functional traits, and their responses to soil nutrient availability are crucial for resource acquisition under environmental change. Previous studies have focused on the response of root morphological, architectural, and chemical traits to fertilization, while less attention has been given to root biomass and length growth, as well as mycorrhizal symbiosis, impeding a full understanding of root resource acquisition strategies. Here, using a nutrient addition experiment (control, inorganic, and organic nutrients), we explored the responses of function-based root (absorptive fine roots [AFRs] versus transport fine roots [TFRs]) growth, functional traits (morphological, architectural, and chemical traits), and mycorrhizal colonization of C. lanceolat and Q. acutissim, which are the dominant tree species in subtropical China. The results showed that the fine root biomass and total root length of AFRs for both tree species basically decreased significantly after nutrient addition, but TFRs responded less sensitively than AFRs. Nutrient addition significantly increased the mycorrhizal colonization rate in C. lanceolata but decreased it in Q. acutissima. The diameter of AFRs for C. lanceolata increased significantly, while the branch ratio and branch intensity decreased significantly in both inorganic nutrients (NPK) and organic nutrients (F); however, the opposite response pattern occurred for Q. acutissima. Fine root biomass, total root length, and root nutrient concentration exhibited the most plastic responses to changes in nutrient availability. The magnitude of the plastic response of fine root traits was slightly higher in the NPK treatment than in the F treatment. Our findings suggest that the responses of fine root traits and mycorrhizal fungi to nutrient addition were species-specific: C. lanceolata depended on mycorrhizal fungi for resource acquisition, while Q. acutissima could acquire soil nutrient resources by increasing root branching. The contrasting nutrient acquisition strategies between tree species may facilitate plant species coexistence and distribution under soil nutrient change. Fine root biomass and total root length emerged as more pivotal indicators for nutrient acquisition strategies compared to morphological traits

Whole-Tree Response of Non-Structural Carbohydrates, Carbon and Nitrogen Concentrations in Two Temperate Tree Species to 10-Year Nitrogen Fertilization

This study aimed to investigate the effects of long-term nitrogen fertilization on non-structural carbohydrates (NSC) and nitrogen (N) status and their interaction in mature trees at the whole-tree scale. Ten g N m(-2) yr(-1) of ammonium nitrate fertilizer were applied to 26-year-old Larix gmelinii Rupr. (larch) and Fraxinus mandschurica Rupr. (ash) trees in Northeastern China from 2002 to 2012. NSC, total carbon (C) and total N concentrations in different compartments were examined. For both species, concentrations of NSC and their components (soluble sugars and starch) tended to increase in aboveground organs but decrease in fine roots following N fertilization, with significant (p < 0.05) changes only observed in ash stems and larch roots. N fertilization increased N concentrations and decreased the C:N ratio in all organs, especially in foliage and roots, while the effects of fertilization on total C concentrations varied with tree species and organs. Concentrations of NSC (mainly reflected in soluble sugar) were generally negatively correlated with N concentration in fine roots but positively related to N concentration in aboveground woody organs in both control and fertilized treatments. However, fertilization strengthened this correlation in fine roots and weakened this relationship in aboveground organs. This study provides a decade-long insight into the effect of currently increasing N deposition on tree growth and function

Table_1_The Hierarchy of Protoxylem Groupings in Primary Root and Their Plasticity to Nitrogen Addition in Three Tree Species.DOCX

Protoxylem grouping (PG), a classification based on the number of protoxylem poles, is a crucial indicator related to other functional traits in fine roots, affecting growth and survival of individual root. However, within root system, less is known about the arrangement of PG. Moreover, the responses of PG to fertilization are still unclear. Here, we selected three common hardwood species in Northeast China, Juglans mandshurica, Fraxinus mandshurica, and Phellodendron amurense, conducted root pruning and nutrient addition. In this study, we analyzed the PG, morphology, and other anatomy traits of newly formed root branches. The results showed all root length, diameter, and stele, as well as hydraulic conductivity, were significantly positive related to the PG number, and the PG number generally decreased with ascending root developmental order; these patterns were independent of species and fertilization. Additionally, we also found the plasticity of PGs to environmental changes, in terms of the increased frequency of high PG roots after fertilization, significantly in J. mandshurica and F. mandshurica. Therefore, the heterogeneity, hierarchy, and plasticity of individual roots within root system may be widespread in woody plants, which is of great significance to deepen our understanding in root growth and development, as well as the belowground ecological process.</p