Author Correction: Evolutionary history resolves global organization of root functional traits.

We thank reader Joseph Craine for pointing out three inadvertent errors in this Letter. First, 4 of the 71 divergence dates extracted from ref. 1 of this Amendment and used in Fig. 1b of the original Letter were overestimated. The correct values are 45 million years ago (Ma) for Apocynaceae, 51 Ma for Anacardiaceae, 40 Ma for Primulaceae, and 53 Ma for Amaryllidaceae. These errors had little influence on the overall trend of Fig. 1b (r2 is now 0.48 rather than 0.54, with no change to P < 0.001) and do not change our conclusion and inferences. Second, we neglected to note that since refs. 1 and 2 of this Amendment considered only angiosperms, our Fig. 1b necessarily did not include gymnosperm taxa. The in-text reference to Fig. 1b should therefore read "all major angiosperm plant families in our dataset" rather than "all major vascular plant families in our dataset". Third, in Fig. 1c the trait value of mycorrhizal colonization for Machilus kwangtungensis was erroneously given the value 0.25 instead of 1.0. This error had little influence on the overall Fig. 1c trend, reducing r2 from 0.64 to 0.63 (with no change to P < 0.001).

Evolutionary history resolves global organization of root functional traits.

Plant roots have greatly diversified in form and function since the emergence of the first land plants, but the global organization of functional traits in roots remains poorly understood. Here we analyse a global dataset of 10 functionally important root traits in metabolically active first-order roots, collected from 369 species distributed across the natural plant communities of 7 biomes. Our results identify a high degree of organization of root traits across species and biomes, and reveal a pattern that differs from expectations based on previous studies of leaf traits. Root diameter exerts the strongest influence on root trait variation across plant species, growth forms and biomes. Our analysis suggests that plants have evolved thinner roots since they first emerged in land ecosystems, which has enabled them to markedly improve their efficiency of soil exploration per unit of carbon invested and to reduce their dependence on symbiotic mycorrhizal fungi. We also found that diversity in root morphological traits is greatest in the tropics, where plant diversity is highest and many ancestral phylogenetic groups are preserved. Diversity in root morphology declines sharply across the sequence of tropical, temperate and desert biomes, presumably owing to changes in resource supply caused by seasonally inhospitable abiotic conditions. Our results suggest that root traits have evolved along a spectrum bounded by two contrasting strategies of root life: an ancestral 'conservative' strategy in which plants with thick roots depend on symbiosis with mycorrhizal fungi for soil resources and a more-derived 'opportunistic' strategy in which thin roots enable plants to more efficiently leverage photosynthetic carbon for soil exploration. These findings imply that innovations of belowground traits have had an important role in preparing plants to colonize new habitats, and in generating biodiversity within and across biomes.

Erratum: Evolutionary history resolves global organization of root functional traits.

This corrects the article DOI: 10.1038/nature25783.

Drivers of nematode diversity in forest soils across climatic zones.

Nematodes are the most abundant multi-cellular animals in soil, influencing key processes and functions in terrestrial ecosystems. Yet, little is known about the drivers of nematode abundance and diversity in forest soils across climatic zones. This is despite forests covering approximately 30% of the Earth's land surface, providing many crucial ecosystem services but strongly varying in climatic conditions and associated ecosystem properties across biogeographic zones. Here, we collected nematode samples from 13 forests across a latitudinal gradient. We divided this gradient into temperate, warm-temperate and tropical climatic zones and found that, across the gradient, nematode abundance and diversity were mainly influenced by soil organic carbon content. However, mean annual temperature and total soil phosphorus content in temperate zones, soil pH in warm-temperate zones, and mean annual precipitation in tropical zones were more important in driving nematode alpha-diversity, biomass and abundance. Additionally, nematode beta-diversity was higher in temperate than in warm-temperate and tropical zones. Together, our findings demonstrate that the drivers of nematode diversity in forested ecosystems are affected by the spatial scale and climatic conditions considered. This implies that high resolution studies are needed to accurately predict how soil functions respond if climate conditions move beyond the coping range of soil organisms.

Mechanical traits of fine roots as a function of topology and anatomy.

Background and Aims: Root mechanical traits, including tensile strength (Tr), tensile strain (εr) and modulus of elasticity (Er), are key functional traits that help characterize plant anchorage and the physical contribution of vegetation to landslides and erosion. The variability in these traits is high among tree fine roots and is poorly understood. Here, we explore the variation in root mechanical traits as well as their underlying links with morphological (diameter), architectural (topological order) and anatomical (stele and cortex sizes) traits. Methods: We investigated the four tropical tree species Pometia tomentosa, Barringtonia fusicarpa, Baccaurea ramiflora and Pittosporopsis kerrii in Xishuangbanna, Yunnan, China. For each species, we excavated intact, fresh, fine roots and measured mechanical and anatomical traits for each branching order. Key Results: Mechanical traits varied enormously among the four species within a narrow range of diameters (<2 mm): <0.1-65 MPa for Tr, 4-1135 MPa for Er and 0.4-37 % for εr. Across species, Tr and Er were strongly correlated with stele area ratio, which was also better correlated with topological order than with root diameter, especially at interspecific levels. Conclusions: Root topological order plays an important role in explaining variability in fine-root mechanical traits due to its reflection of root tissue development. Accounting for topological order when measuring fine-root traits therefore leads to greater empirical understanding of plant functions (e.g. anchorage) within and across species.

Diverse belowground resource strategies underlie plant species coexistence and spatial distribution in three grasslands along a precipitation gradient.

Functional traits and their variation mediate plant species coexistence and spatial distribution. Yet, how patterns of variation in belowground traits influence resource acquisition across species and plant communities remains obscure. To characterize diverse belowground strategies in relation to species coexistence and abundance, we assessed four key belowground traits - root diameter, root branching intensity, first-order root length and mycorrhizal colonization - in 27 coexisting species from three grassland communities along a precipitation gradient. Species with thinner roots had higher root branching intensity, but shorter first-order root length and consistently low mycorrhizal colonization, whereas species with thicker roots enhanced their capacity for resource acquisition by producing longer first-order roots and maintaining high mycorrhizal colonization. Plant species observed across multiple sites consistently decreased root branching and/or mycorrhizal colonization, but increased lateral root length with decreasing precipitation. Additionally, the degree of intraspecific trait variation was positively correlated with species abundance across the gradient, indicating that high intraspecific trait variation belowground may facilitate greater fitness and chances of survival across multiple habitats. These results suggest that a small set of critical belowground traits can effectively define diverse resource acquisition strategies in different environments and may forecast species survival and range shifts under climate change.

Similar below-ground carbon cycling dynamics but contrasting modes of nitrogen cycling between arbuscular mycorrhizal and ectomycorrhizal forests.

Compared with ectomycorrhizal (ECM) forests, arbuscular mycorrhizal (AM) forests are hypothesized to have higher carbon (C) cycling rates and a more open nitrogen (N) cycle. To test this hypothesis, we synthesized 645 observations, including 22 variables related to below-ground C and N dynamics from 100 sites, where AM and ECM forests co-occurred at the same site. Leaf litter quality was lower in ECM than in AM trees, leading to greater forest floor C stocks in ECM forests. By contrast, AM forests had significantly higher mineral soil C concentrations, and this result was strongly mediated by plant traits and climate. No significant differences were found between AM and ECM forests in C fluxes and labile C concentrations. Furthermore, inorganic N concentrations, net N mineralization and nitrification rates were all higher in AM than in ECM forests, indicating 'mineral' N economy in AM but 'organic' N economy in ECM trees. AM and ECM forests show systematic differences in mineral vs organic N cycling, and thus mycorrhizal type may be useful in predicting how different tree species respond to multiple environmental change factors. By contrast, mycorrhizal type alone cannot reliably predict below-ground C dynamics without considering plant traits and climate.

Building a better foundation: improving root-trait measurements to understand and model plant and ecosystem processes.

Trait-based approaches provide a useful framework to investigate plant strategies for resource acquisition, growth, and competition, as well as plant impacts on ecosystem processes. Despite significant progress capturing trait variation within and among stems and leaves, identification of trait syndromes within fine-root systems and between fine roots and other plant organs is limited. Here we discuss three underappreciated areas where focused measurements of fine-root traits can make significant contributions to ecosystem science. These include assessment of spatiotemporal variation in fine-root traits, integration of mycorrhizal fungi into fine-root-trait frameworks, and the need for improved scaling of traits measured on individual roots to ecosystem-level processes. Progress in each of these areas is providing opportunities to revisit how below-ground processes are represented in terrestrial biosphere models. Targeted measurements of fine-root traits with clear linkages to ecosystem processes and plant responses to environmental change are strongly needed to reduce empirical and model uncertainties. Further identifying how and when suites of root and whole-plant traits are coordinated or decoupled will ultimately provide a powerful tool for modeling plant form and function at local and global scales.

A novel soil manganese mechanism drives plant species loss with increased nitrogen deposition in a temperate steppe.

Loss of plant diversity with increased anthropogenic nitrogen (N) deposition in grasslands has occurred globally. In most cases, competitive exclusion driven by preemption of light or space is invoked as a key mechanism. Here, we provide evidence from a 9-yr N-addition experiment for an alternative mechanism: differential sensitivity of forbs and grasses to increased soil manganese (Mn) levels. In Inner Mongolia steppes, increasing the N supply shifted plant community composition from grass-forb codominance (primarily Stipa krylovii and Artemisia frigida, respectively) to exclusive dominance by grass, with associated declines in overall species richness. Reduced abundance of forbs was linked to soil acidification that increased mobilization of soil Mn, with a 10-fold greater accumulation of Mn in forbs than in grasses. The enhanced accumulation of Mn in forbs was correlated with reduced photosynthetic rates and growth, and is consistent with the loss of forb species. Differential accumulation of Mn between forbs and grasses can be linked to fundamental differences between dicots and monocots in the biochemical pathways regulating metal transport. These findings provide a mechanistic explanation for N-induced species loss in temperate grasslands by linking metal mobilization in soil to differential metal acquisition and impacts on key functional groups in these ecosystems.

Leaf economics and hydraulic traits are decoupled in five species-rich tropical-subtropical forests.

Leaf economics and hydraulic traits are critical to leaf photosynthesis, yet it is debated whether these two sets of traits vary in a fully coordinated manner or there is room for independent variation. Here, we tested the relationship between leaf economics traits, including leaf nitrogen concentration and leaf dry mass per area, and leaf hydraulic traits including stomatal density and vein density in five tropical-subtropical forests. Surprisingly, these two suites of traits were statistically decoupled. This decoupling suggests that independent trait dimensions exist within a leaf, with leaf economics dimension corresponding to light capture and tissue longevity, and the hydraulic dimension to water-use and leaf temperature maintenance. Clearly, leaf economics and hydraulic traits can vary independently, thus allowing for more possible plant trait combinations. Compared with a single trait dimension, multiple trait dimensions may better enable species adaptations to multifarious niche dimensions, promote diverse plant strategies and facilitate species coexistence.

Complementarity in nutrient foraging strategies of absorptive fine roots and arbuscular mycorrhizal fungi across 14 coexisting subtropical tree species.

In most cases, both roots and mycorrhizal fungi are needed for plant nutrient foraging. Frequently, the colonization of roots by arbuscular mycorrhizal (AM) fungi seems to be greater in species with thick and sparsely branched roots than in species with thin and densely branched roots. Yet, whether a complementarity exists between roots and mycorrhizal fungi across these two types of root system remains unclear. We measured traits related to nutrient foraging (root morphology, architecture and proliferation, AM colonization and extramatrical hyphal length) across 14 coexisting AM subtropical tree species following root pruning and nutrient addition treatments. After root pruning, species with thinner roots showed more root growth, but lower mycorrhizal colonization, than species with thicker roots. Under multi-nutrient (NPK) addition, root growth increased, but mycorrhizal colonization decreased significantly, whereas no significant changes were found under nitrogen or phosphate additions. Moreover, root length proliferation was mainly achieved by altering root architecture, but not root morphology. Thin-root species seem to forage nutrients mainly via roots, whereas thick-root species rely more on mycorrhizal fungi. In addition, the reliance on mycorrhizal fungi was reduced by nutrient additions across all species. These findings highlight complementary strategies for nutrient foraging across coexisting species with contrasting root traits.

Redefining fine roots improves understanding of below-ground contributions to terrestrial biosphere processes.

Fine roots acquire essential soil resources and mediate biogeochemical cycling in terrestrial ecosystems. Estimates of carbon and nutrient allocation to build and maintain these structures remain uncertain because of the challenges of consistently measuring and interpreting fine-root systems. Traditionally, fine roots have been defined as all roots ≤ 2 mm in diameter, yet it is now recognized that this approach fails to capture the diversity of form and function observed among fine-root orders. Here, we demonstrate how order-based and functional classification frameworks improve our understanding of dynamic root processes in ecosystems dominated by perennial plants. In these frameworks, fine roots are either separated into individual root orders or functionally defined into a shorter-lived absorptive pool and a longer-lived transport fine-root pool. Using these frameworks, we estimate that fine-root production and turnover represent 22% of terrestrial net primary production globally - a c. 30% reduction from previous estimates assuming a single fine-root pool. Future work developing tools to rapidly differentiate functional fine-root classes, explicit incorporation of mycorrhizal fungi into fine-root studies, and wider adoption of a two-pool approach to model fine roots provide opportunities to better understand below-ground processes in the terrestrial biosphere.

Whole-tree dynamics of non-structural carbohydrate and nitrogen pools across different seasons and in response to girdling in two temperate trees.

Despite extensive research on the seasonal dynamics of non-structural carbohydrate (NSC) and nitrogen (N) concentrations, the size and relative contributions of NSC and N pools across different tree organs are not well understood. We have measured the changes in NSC and N concentrations in leaves, branches, stems and all root branch orders at monthly intervals in control and girdled trees of larch (Larix gmelinii) and ash (Fraxinus mandshurica). The biomass of each plant compartment was also determined to calculate the size of the NSC and N pools. In both species, 13-37% of the NSC and N pools were mobilized at the beginning of the growing season. Among the mobilized pools, stems and non-absorptive roots (branch orders 4-9) acted as the largest NSC sources in larch and ash, respectively, while branches served as the largest N source in both species. After stem girdling, 22 and 50% of the root NSC stores in larch and ash, respectively, were mobilized to maintain root activities during the growing season. Tree mortality was observed 1 year after girdling, at which time there was still an abundant NSC pool in the roots. We conclude that (1) different storage organs differ in their contribution to new tissue growth at the beginning of the growing season and that those storage organs holding higher fractions of the NSC or N pool are not necessarily those which mobilize more NSC or N; (2) tree growth may not be limited by carbon (C) availability; (3) C storage in non-absorptive roots plays an important role in maintaining tree survival after the termination of photosynthate flow from aboveground sources.

Leading dimensions in absorptive root trait variation across 96 subtropical forest species.

Absorptive root traits show remarkable cross-species variation, but major root trait dimensions across species have not been defined. We sampled first-order roots and measured 14 root traits for 96 angiosperm woody species from subtropical China, including root diameter, specific root length, stele diameter, cortex thickness, root vessel size and density, mycorrhizal colonization rate, root branching intensity, tissue density, and concentrations of carbon and nitrogen ([N]). Root traits differed in the degree of variation and phylogenetic conservatism, but showed predictable patterns of cross-trait coordination. Root diameter, cortex thickness and stele diameter displayed high variation across species (coefficient of variation (CV)=0.51-0.69), whereas the stele:root diameter ratio and [N] showed low variation (CV<0.32). Root diameter, cortex thickness and stele diameter showed a strong phylogenetic signal across species, whereas root branching traits did not, and these two sets of traits were segregated onto two nearly orthogonal (independent) principal component analysis (PCA) axes. Two major dimensions of root trait variation were found: a diameter-related dimension potentially integrating root construction, maintenance, and persistence with mycorrhizal colonization, and a branching architecture dimension expressing root plastic responses to the environment. These two dimensions may offer a promising path for better understanding root trait economics and root ecological strategies world-wide.

Fine root branch orders contribute differentially to uptake, allocation, and return of potentially toxic metals.

Growing evidence has revealed high heterogeneity of fine root networks in both structure and function, with different root orders corporately maintaining trees' physiological activities. However, little information is available on how fine root heterogeneity of trees responds to environmental stresses. We examined concentrations of seven potentially toxic metals (Cr, Ni, Cu, Zn, As, Cd, and Pb) within fine root networks and their correlations with root morphological and macro-elemental traits in six Chinese subtropical trees. The contributions of different orders of roots to fine-root metal storage and return were also estimated. Results showed no consistent pattern for the correlation among different metal concentration against root traits. Unlike root metal concentration that generally decreased with root order, root metal storage was commonly lowest in middle root orders. Root senescence was at least comparable to leaf senescence contributing to metal removal. Although the first-order roots constituted 7.2-22.3% of total fine root biomass, they disproportionately contributed to most of metal return fluxes via root senescence. The two distinct root functional modules contributed differentially to metal uptake, allocation, and return, with defensive (lower-order) roots effectively stabilizing and removing toxic metals and bulk buffering (higher-order) roots possessing a persistent but diluted metal pool. Our results suggest a strong association of physiological functions of metal detoxification and metal homeostasis with the structural heterogeneity in fine root architecture.

Fine root mercury heterogeneity: metabolism of lower-order roots as an effective route for mercury removal.

Fine roots are critical components for plant mercury (Hg) uptake and removal, but the patterns of Hg distribution and turnover within the heterogeneous fine root components and their potential limiting factors are poorly understood. Based on root branching structure, we studied the total Hg (THg) and its cellular partitioning in fine roots in 6 Chinese subtropical trees species and the impacts of root morphological and stoichiometric traits on Hg partitioning. The THg concentration generally decreased with increasing root order, and was higher in cortex than in stele. This concentration significantly correlated with root length, diameter, specific root length, specific root area, and nitrogen concentration, whereas its cytosolic fraction (accounting for <10% of THg) correlated with root carbon and sulfur concentrations. The estimated Hg return flux from dead fine roots outweighed that from leaf litter, and ephemeral first-order roots that constituted 7.2-22.3% of total fine root biomass may have contributed most to this flux (39-71%, depending on tree species and environmental substrate). Our results highlight the high capacity of Hg stabilization and Hg return by lower-order roots and demonstrate that turnover of lower-order roots may be an effective strategy of detoxification in perennial tree species.

Relationships Between Leaf Carbon and Macronutrients Across Woody Species and Forest Ecosystems Highlight How Carbon Is Allocated to Leaf Structural Function.

Stoichiometry of leaf macronutrients can provide insight into the tradeoffs between leaf structural and metabolic investments. Structural carbon (C) in cell walls is contained in lignin and polysaccharides (cellulose, hemicellulose, and pectins). Much of leaf calcium (Ca) and a fraction of magnesium (Mg) were further bounded with cell wall pectins. The macronutrients phosphorus (P), potassium (K), and nitrogen (N) are primarily involved in cell metabolic functions. There is limited information on the functional interrelations among leaf C and macronutrients, and the functional dimensions characterizing the leaf structural and metabolic tradeoffs are not widely appreciated. We investigated the relationships between leaf C and macronutrient (N, P, K, Ca, Mg) concentrations in two widespread broad-leaved deciduous woody species Quercus wutaishanica (90 individuals) and Betula platyphylla (47 individuals), and further tested the generality of the observed relationships in 222 woody eudicots from 15 forest ecosystems. In a subsample of 20 broad-leaved species, we also analyzed the relationships among C, Ca, lignin, and pectin concentrations in leaf cell walls. We found a significant leaf C-Ca tradeoff operating within and across species and across ecosystems. This basic relationship was explained by variations in the share of cell wall lignin and pectin investments at the cell scale. The C-Ca tradeoffs were mainly driven by soil pH and mean annual temperature and precipitation, suggesting that leaves were more economically built with less C and more Ca as soil pH increased and at lower temperature and lower precipitation. However, we did not detect consistent patterns among C-N, and C-Mg at different levels of biological organization, suggesting substantial plasticity in N and Mg distribution among cell organelles and cell protoplast and cell wall. We observed two major axes of macronutrient differentiation: the cell-wall structural axis consisting of protein-free C and Ca and the protoplasm metabolic axis consisting of P and K, underscoring the decoupling of structural and metabolic elements inherently linked with cell wall from protoplasm investment strategies. We conclude that the tradeoffs between leaf C and Ca highlight how carbon is allocated to leaf structural function and suggest that this might indicate biogeochemical niche differentiation of species.

Earliest rooting system and root : shoot ratio from a new Zosterophyllum plant.

The enhanced chemical weathering by rooted vascular plants during the Silurian-Devonian period played a crucial role in altering global biogeochemical cycles and atmospheric environments; however, the documentation of early root morphology and physiology is scarce because the existing fossils are mostly incomplete. Here, we report an entire, uprooted specimen of a new Zosterophyllum Penhallow, named as Z. shengfengense, from the Early Devonian Xitun Formation (Lochkovian, c. 413 Myr old) of Yunnan, south China. This plant has the most ancient known record of a rooting system. The plant consists of aerial axes of 98 mm in height, showing a tufted habit, and a rhizome bearing a fibrous-like rooting system, c. 20 mm in length. The rhizome shows masses of branchings, which produce upwardly directed aerial axes and downwardly directed root-like axes. The completeness of Z. shengfengense made it possible to estimate the biomass allocation and root : shoot ratio. The root : shoot ratio of this early plant is estimated at a mean value of 0.028, and the root-like axes constitute only c. 3% of the total biomass. Zosterophyllum shengfengense was probably a semi-aquatic plant with efficient water use or a strong uptake capacity of the root-like axes.

Ephemeral root modules in Fraxinus mandshurica.

Historically, ephemeral roots have been equated with 'fine roots' (i.e. all roots of less than an arbitrary diameter, such as 2 mm), but evidence shows that 'fine roots' in woody species are complex branching systems with both rapid-cycling and slow-cycling components. A precise definition of ephemeral roots is therefore needed. Using a branch-order classification, a rhizotron method and sequential sampling of a root cohort, we tested the hypothesis that ephemeral root modules exist within the branching Fraxinus mandshurica (Manchurian ash) root system as distal nonwoody lateral branches, which show anatomical, nutritional and physiological patterns distinct from their woody mother roots. Our results showed that in F. mandshurica, distal nonwoody root branch orders die rapidly as intact lateral branches (or modules). These nonwoody branch orders exhibited highly synchronous changes in tissue nitrogen concentrations and respiration, dominated root turnover, nutrient flux and root respiration, and never underwent secondary development. The ephemeral root modules proposed here may provide a functional basis for differentiating and sampling short-lived absorptive roots in woody plants, and represent a conceptual leap over the traditional coarse-fine root dichotomies based on arbitrary size classes.

Slow decomposition of lower order roots: a key mechanism of root carbon and nutrient retention in the soil.

Among tree fine roots, the distal small-diameter lateral branches comprising first- and second-order roots lack secondary (wood) development. Therefore, these roots are expected to decompose more rapidly than higher order woody roots. But this prediction has not been tested and may not be correct. Current evidence suggests that lower order roots may decompose more slowly than higher order roots in tree species associated with ectomycorrhizal (EM) fungi because they are preferentially colonized by fungi and encased by a fungal sheath rich in chitin (a recalcitrant compound). In trees associated with arbuscular mycorrhizal (AM) fungi, lower order roots do not form fungal sheaths, but they may have poorer C quality, e.g. lower concentrations of soluble carbohydrates and higher concentrations of acid-insolubles than higher order roots, thus may decompose more slowly. In addition, litter with high concentrations of acid insolubles decomposes more slowly under higher N concentrations (such as lower order roots). Therefore, we propose that in both AM and EM trees, lower order roots decompose more slowly than higher order roots due to the combination of poor C quality and high N concentrations. To test this hypothesis, we examined decomposition of the first six root orders in Fraxinus mandshurica (an AM species) and Larix gmelinii (an EM species) using litterbag method in northeastern China. We found that lower order roots of both species decomposed more slowly than higher order roots, and this pattern appears to be associated mainly with initial C quality and N concentrations. Because these lower order roots have short life spans and thus dominate root mortality, their slow decomposition implies that a substantial fraction of the stable soil organic matter pool is derived from these lower order roots, at least in the two species we studied.