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).

Temperate trees locally engineer decomposition and litter-bound microbiomes through differential litter deposits and species-specific soil conditioning.

Leaf decomposition varies widely across temperate forests, shaped by factors like litter quality, climate, soil properties, and decomposers, but forest heterogeneity may mask local tree influences on decomposition and litter-associated microbiomes. We used a 24-yr-old common garden forest to quantify local soil conditioning impacts on decomposition and litter microbiology. We introduced leaf litter bags from 10 tree species (5 arbuscular mycorrhizal; 5 ectomycorrhizal) to soil plots conditioned by all 10 species in a full-factorial design. After 6 months, we assessed litter mass loss, C/N content, and bacterial and fungal composition. We hypothesized that (1) decomposition and litter-associated microbiome composition would be primarily shaped by the mycorrhizal type of litter-producing trees, but (2) modified significantly by underlying soil, based on mycorrhizal type of the conditioning trees. Decomposition and, to a lesser extent, litter-associated microbiome composition, were primarily influenced by the mycorrhizal type of litter-producing trees. Interestingly, however, underlying soils had a significant secondary influence, driven mainly by tree species, not mycorrhizal type. This secondary influence was strongest under trees from the Pinaceae. Temperate trees can locally influence underlying soil to alter decomposition and litter-associated microbiology. Understanding the strength of this effect will help predict biogeochemical responses to forest compositional change.

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.

Functionally discrete fine roots differ in microbial assembly, microbial functional potential, and produced metabolites.

Traditionally, fine roots were grouped using arbitrary size categories, rarely capturing the heterogeneity in physiology, morphology and functionality among different fine root orders. Fine roots with different functional roles are rarely separated in microbiome-focused studies and may result in confounding microbial signals and host-filtering across different root microbiome compartments. Using a 26-year-old common garden, we sampled fine roots from four temperate tree species that varied in root morphology and sorted them into absorptive and transportive fine roots. The rhizoplane and rhizosphere were characterized using 16S rRNA gene and internal transcribed spacer region amplicon sequencing and shotgun metagenomics for the rhizoplane to identify potential microbial functions. Fine roots were subject to metabolomics to spatially characterize resource availability. Both fungi and bacteria differed according to root functional type. We observed additional differences between the bacterial rhizoplane and rhizosphere compartments for absorptive but not transportive fine roots. Rhizoplane bacteria, as well as the root metabolome and potential microbial functions, differed between absorptive and transportive fine roots, but not the rhizosphere bacteria. Functional differences were driven by sugar transport, peptidases and urea transport. Our data highlights the importance of root function when examining root-microbial relationships, emphasizing different host selective pressures imparted on different root microbiome compartments.

Limited evidence of vertical fine-root segregation in a subtropical forest.

Vertical root segregation and the resulting niche partitioning can be a key underpinning of species coexistence. This could result from substantial interspecific variations in root profiles and rooting plasticity in response to soil heterogeneity and neighbours, but they remain largely untested in forest communities. In a diverse forest in subtropical China, we randomly sampled > 4000 root samples from 625 0-30 cm soil profiles. Using morphological and DNA-based methods, we identified 109 woody plant species, determined the degree of vertical fine-root segregation, and examined rooting plasticity in response to soil heterogeneity and neighbour structure. We found no evidence of vertical fine-root segregation among cooccurring species. By contrast, root abundance of different species tended to be positively correlated within soil zones. Underlying these findings was a lack of interspecific variation in fine-root profiles with over 90% of species concentrated in the 0-10 cm soil zone with only one species dominating in the 10-20 cm soil zone. Root profiles exhibited low responsiveness to root neighbours but tended to be shallow in soils with low phosphorus and copper content. These findings suggest that if there is niche differentiation leading to coexistence in this diverse forest, it would be occurring by mechanisms other than vertical fine-root segregation.

Limiting similarity shapes the functional and phylogenetic structure of root neighborhoods in a subtropical forest.

Environmental filtering and limiting similarity mechanisms can simultaneously structure community assemblages. However, how they shape the functional and phylogenetic structure of root neighborhoods remains unclear, hindering the understanding of belowground community assembly processes and diversity maintenance. In a 50-ha plot in a subtropical forest, China, we randomly sampled > 2700 root clusters from 625 soil samples. Focusing on 10 root functional traits measured on 76 woody species, we examined the functional and phylogenetic structure of root neighborhoods and linked their distributions with environmental cues. Functional overdispersion was pervasive among individual root traits (50% of the traits) and accentuated when different traits were combined. Functional clustering (20% of the traits) seemed to be associated with a soil nutrient gradient with thick roots dominating fertile areas whereas thin roots dominated infertile soils. Nevertheless, such traits also were sorted along other environmental cues, showing multidimensional adaptive trait syndromes. Species relatedness also was an important factor defining root neighborhoods, resulting in significant phylogenetic overdispersion. These results suggest that limiting similarity may drive niche differentiation of coexisting species to reduce competition, and that alternative root strategies could be crucial in promoting root neighborhood resource use and species coexistence.

On characterizing root function in perennial horticultural crops.

PREMISE: While root-order approaches to fine-root classification have shown wide utility among wild plants, they have seen limited use for perennial crop plants. Moreover, inadequate characterization of fine roots across species of domesticated perennial crops has led to a knowledge gap in the understanding of evolutionary and functional patterns associated with different fine-root orders. METHODS: We examined fine-root traits of common horticultural fruit and nut crops: Malus ×domestica, Prunus persica, Vitus vinifera, Prunus dulcis, and Citrus ×clementina. Additional roots were sampled from 33 common perennial horticultural crops, native to tropical, subtropical, and temperate regions, to examine variation in 1st- and 2nd-order absorptive roots. RESULTS: First-order roots of grape and 1st- and 2nd-order roots of apple and peach were consistently thin, nonwoody, mycorrhizal, and had high N:C ratios. In contrast, 4th- and 5th-order roots of grape and 5th-order roots of apple and peach were woody, nonmycorrhizal, had low N:C ratios, and were thicker than lower-order roots. Among the 33 horticultural species, diameter of 1st- and 2nd-order roots varied about 15-fold, ranging from 0.04 to 0.60 mm and 0.05 to 0.89 mm respectively. This variation generally was phylogenetically conserved across plant lineages. CONCLUSIONS: Collectively, our research shows that root-order characterization has considerably more utility than an arbitrary diameter cutoff for identifying roots of different functions in perennial horticultural crops. In addition, much of the variation in root diameter among species can be predicted by evolutionary relationships.

Asymmetry in above- and belowground productivity responses to N addition in a semi-arid temperate steppe.

Nitrogen (N) enrichment often increases aboveground net primary productivity (ANPP) of the ecosystem, but it is unclear if belowground net primary productivity (BNPP) track responses of ANPP. Moreover, the frequency of N inputs may affect primary productivity but is rarely studied. To assess the response patterns of above- and belowground productivity to rates of N addition under different addition frequencies, we manipulated the rate (0-50 g N m-2  year-1 ) and frequency (twice vs. monthly additions per year) of NH4 NO3 inputs for six consecutive years in a temperate grassland in northern China and measured ANPP and BNPP from 2012 to 2014. In the low range of N addition rates, BNPP showed the greatest negative response and ANPP showed the greatest positive responses with increases in N addition (<10 g N m-2  year-1 ). As N addition increased beyond 10 g N m-2  year-1 , increases in ANPP dampened and decreases in BNPP ceased altogether. The response pattern of net primary productivity (combined above- and belowground; NPP) corresponded more closely to ANPP than to BNPP. The N effects on BNPP and BNPP/NPP (fBNPP ) were not dependent on N addition frequency in the range of N additions typically associated with N deposition. BNPP was more sensitive to N addition frequency than ANPP, especially at low rates of N addition. Our findings provide new insights into how plants regulate carbon allocation to different organs with increasing N rates and changing addition frequencies. These root response patterns, if incorporated into Earth system models, may improve the predictive power of C dynamics in dryland ecosystems in the face of global atmospheric N deposition.

Soil organic carbon stability in forests: Distinct effects of tree species identity and traits.

Rising atmospheric CO2 concentrations have increased interest in the potential for forest ecosystems and soils to act as carbon (C) sinks. While soil organic C contents often vary with tree species identity, little is known about if, and how, tree species influence the stability of C in soil. Using a 40 year old common garden experiment with replicated plots of eleven temperate tree species, we investigated relationships between soil organic matter (SOM) stability in mineral soils and 17 ecological factors (including tree tissue chemistry, magnitude of organic matter inputs to the soil and their turnover, microbial community descriptors, and soil physicochemical properties). We measured five SOM stability indices, including heterotrophic respiration, C in aggregate occluded particulate organic matter (POM) and mineral associated SOM, and bulk SOM δ15 N and ∆14 C. The stability of SOM varied substantially among tree species, and this variability was independent of the amount of organic C in soils. Thus, when considering forest soils as C sinks, the stability of C stocks must be considered in addition to their size. Further, our results suggest tree species regulate soil C stability via the composition of their tissues, especially roots. Stability of SOM appeared to be greater (as indicated by higher δ15 N and reduced respiration) beneath species with higher concentrations of nitrogen and lower amounts of acid insoluble compounds in their roots, while SOM stability appeared to be lower (as indicated by higher respiration and lower proportions of C in aggregate occluded POM) beneath species with higher tissue calcium contents. The proportion of C in mineral associated SOM and bulk soil ∆14 C, though, were negligibly dependent on tree species traits, likely reflecting an insensitivity of some SOM pools to decadal scale shifts in ecological factors. Strategies aiming to increase soil C stocks may thus focus on particulate C pools, which can more easily be manipulated and are most sensitive to climate change.

Root morphology and mycorrhizal symbioses together shape nutrient foraging strategies of temperate trees.

Photosynthesis by leaves and acquisition of water and minerals by roots are required for plant growth, which is a key component of many ecosystem functions. Although the role of leaf functional traits in photosynthesis is generally well understood, the relationship of root functional traits to nutrient uptake is not. In particular, predictions of nutrient acquisition strategies from specific root traits are often vague. Roots of nearly all plants cooperate with mycorrhizal fungi in nutrient acquisition. Most tree species form symbioses with either arbuscular mycorrhizal (AM) or ectomycorrhizal (EM) fungi. Nutrients are distributed heterogeneously in the soil, and nutrient-rich "hotspots" can be a key source for plants. Thus, predicting the foraging strategies that enable mycorrhizal root systems to exploit these hotspots can be critical to the understanding of plant nutrition and ecosystem carbon and nutrient cycling. Here, we show that in 13 sympatric temperate tree species, when nutrient availability is patchy, thinner root species alter their foraging to exploit patches, whereas thicker root species do not. Moreover, there appear to be two distinct pathways by which thinner root tree species enhance foraging in nutrient-rich patches: AM trees produce more roots, whereas EM trees produce more mycorrhizal fungal hyphae. Our results indicate that strategies of nutrient foraging are complementary among tree species with contrasting mycorrhiza types and root morphologies, and that predictable relationships between below-ground traits and nutrient acquisition emerge only when both roots and mycorrhizal fungi are considered together.

Linking fine root morphology, hydraulic functioning and shade tolerance of trees.

Background and Aims: Understanding root traits and their trade-off with other plant processes is important for understanding plant functioning in natural ecosystems as well as agricultural systems. The aim of the present study was to determine the relationship between root morphology and the hydraulic characteristics of several orders of fine roots (<2 mm) for species differing in shade tolerance (low, moderate and high). Methods: The morphological, anatomical and hydraulic traits across five distal root orders were measured in species with different levels of shade tolerance and life history strategies. The species studied were Acer negundo, Acer rubrum, Acer saccharum, Betula alleghaniensis, Betula lenta, Quercus alba, Quercus rubra, Pinus strobus and Pinus virginiana. Key Results: Compared with shade-tolerant species, shade-intolerant species produced thinner absorptive roots with smaller xylem lumen diameters and underwent secondary development less frequently, suggesting that they had shorter life spans. Shade-tolerant species had greater root specific hydraulic conductance among these roots due to having larger diameter xylems, although these roots had a lower calculated critical tension for conduit collapse. In addition, shade-intolerant species exhibited greater variation in hydraulic conductance across different root growth rings in woody transport roots of the same root order as compared with shade-tolerant species. Conclusions: Plant growth strategies were extended to include root hydraulic properties. It was found that shade intolerance in trees was associated with conservative root hydraulics but greater plasticity in number of xylem conduits and hydraulic conductance. Root traits of shade-intolerant species were consistent with the ability to proliferate roots quickly for rapid water uptake needed to support rapid shoot growth, while minimizing risk in uncertain environments.

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.

Mycorrhizal fungi and roots are complementary in foraging within nutrient patches.

The roots of the majority of tree species are associated with either arbuscular mycorrhizal (AM) or ectomycorrhizal (EM) fungi. The absorptive roots of tree species also vary widely in their diameter. The linkages between root thickness, mycorrhiza type and nutrient foraging are poorly understood. We conducted a large root ingrowth experiment in the field to investigate how absorptive roots of varying thickness and their associated fungi (AM vs. EM) exploit different nutrient patches (inorganic and organic) in a common garden. In nutrient-rich patches, thin-root tree species more effectively proliferated absorptive roots than thick-root tree species, whereas thick-root tree species proliferated more mycorrhizal fungal biomass than thin-root tree species. Moreover, nutrient patches enriched with organic materials resulted in greater root and mycorrhizal fungal proliferation compared to those enriched with inorganic nutrients. Irrespective of root morphology, AM tree species had higher root foraging precision than mycorrhizal hyphae foraging precision within organic patches, whereas EM tree species exhibited the opposite. Our findings that roots and mycorrhizal fungi are complementary in foraging within nutrient patches provide new insights into species coexistence and element cycling in terrestrial ecosystems.

Root phenology in a changing climate.

Plant phenology is one of the strongest indicators of ecological responses to climate change, and altered phenology can have pronounced effects on net primary production, species composition in local communities, greenhouse gas fluxes, and ecosystem processes. Although many studies have shown that aboveground plant phenology advances with warmer temperatures, demonstration of a comparable association for belowground phenology has been lacking because the factors that influence root phenology are poorly understood. Because roots can constitute a large fraction of plant biomass, and root phenology may not respond to warming in the same way as shoots, this represents an important knowledge gap in our understanding of how climate change will influence phenology and plant performance. We review studies of root phenology and provide suggestions to direct future research. Only 29% of examined studies approached root phenology quantitatively, strongly limiting interpretation of results across studies. Therefore, we suggest that researchers emphasize quantitative analyses in future phenological studies. We suggest that root initiation, peak growth, and root cessation may be under different controls. Root initiation and cessation may be more constrained by soil temperature and the timing of carbon availability, whereas the timing of peak root growth may represent trade-offs among competing plant sinks. Roots probably do not experience winter dormancy in the same way as shoots: 89% of the studies that examined winter phenology found evidence of growth during winter months. More research is needed to observe root phenology, and future studies should be careful to capture winter and early season phenology. This should be done quantitatively, with direct observations of root growth utilizing rhizotrons or minirhizotrons.

Limited linkages of aboveground and belowground phenology: A study in grape.

PREMISE OF THE STUDY: Plant phenology influences resource utilization, carbon fluxes, and interspecific interactions. Although controls on aboveground phenology have been studied to some degree, controls on root phenology are exceptionally poorly understood. METHODS: We used minirhizotrons to examine the timing of grape root production over 5 yr in Fredonia, New York, USA, in a humid continental climate; and over 3 yr in Oakville, California, USA, in a Mediterranean climate. We used data from previous experiments to examine the relationship of root phenology with aboveground phenology. We compared interannual variability in root and shoot growth and determined the influence of abiotic factors on the timing of root initiation, peak root standing crop, peak root growth rate, and cessation of root growth. KEY RESULTS: Root phenology was not tightly coupled with aboveground phenological periods. Both sites typically had one yearly root flush and high interannual variability in root growth. Root phenology was more variable in California than in New York. In this and other published studies, interannual variation in root phenology was greater than variation in aboveground phenology. The three phenological phases of root growth-root initiation, peak root growth, and root cessation-were related to different suites of abiotic factors. CONCLUSIONS: Root phenology is highly variable among years. Analysis of potential controlling factors over several years suggest that belowground phenological phases should be analyzed separately from each other. If aboveground grape phenology responds differently than belowground phenology to changes in air temperature, global warming may further uncouple the timing of aboveground and belowground growth.

Linking root traits to nutrient foraging in arbuscular mycorrhizal trees in a temperate forest.

The identification of plant functional traits that can be linked to ecosystem processes is of wide interest, especially for predicting vegetational responses to climate change. Root diameter of the finest absorptive roots may be one plant trait that has wide significance. Do species with relatively thick absorptive roots forage in nutrient-rich patches differently from species with relatively fine absorptive roots? We measured traits related to nutrient foraging (root morphology and architecture, root proliferation, and mycorrhizal colonization) across six coexisting arbuscular mycorrhizal (AM) temperate tree species with and without nutrient addition. Root traits such as root diameter and specific root length were highly correlated with root branching intensity, with thin-root species having higher branching intensity than thick-root species. In both fertilized and unfertilized soil, species with thin absorptive roots and high branching intensity showed much greater root length and mass proliferation but lower mycorrhizal colonization than species with thick absorptive roots. Across all species, fertilization led to increased root proliferation and reduced mycorrhizal colonization. These results suggest that thin-root species forage more by root proliferation, whereas thick-root species forage more by mycorrhizal fungi. In mineral nutrient-rich patches, AM trees seem to forage more by proliferating roots than by mycorrhizal fungi.

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.