Responses of vascular plant fine roots and associated microbial communities to whole-ecosystem warming and elevated CO2 in northern peatlands.

Warming and elevated CO2 (eCO2) are expected to facilitate vascular plant encroachment in peatlands. The rhizosphere, where microbial activity is fueled by root turnover and exudates, plays a crucial role in biogeochemical cycling, and will likely at least partially dictate the response of the belowground carbon cycle to climate changes. We leveraged the Spruce and Peatland Responses Under Changing Environments (SPRUCE) experiment, to explore the effects of a whole-ecosystem warming gradient (+0°C to 9°C) and eCO2 on vascular plant fine roots and their associated microbes. We combined trait-based approaches with the profiling of fungal and prokaryote communities in plant roots and rhizospheres, through amplicon sequencing. Warming promoted self-reliance for resource uptake in trees and shrubs, while saprophytic fungi and putative chemoorganoheterotrophic bacteria utilizing plant-derived carbon substrates were favored in the root zone. Conversely, eCO2 promoted associations between trees and ectomycorrhizal fungi. Trees mostly associated with short-distance exploration-type fungi that preferentially use labile soil N. Additionally, eCO2 decreased the relative abundance of saprotrophs in tree roots. Our results indicate that plant fine-root trait variation is a crucial mechanism through which vascular plants in peatlands respond to climate change via their influence on microbial communities that regulate biogeochemical cycles.

Embracing fine-root system complexity in terrestrial ecosystem modeling.

Projecting the dynamics and functioning of the biosphere requires a holistic consideration of whole-ecosystem processes. However, biases toward leaf, canopy, and soil modeling since the 1970s have constantly left fine-root systems being rudimentarily treated. As accelerated empirical advances in the last two decades establish clearly functional differentiation conferred by the hierarchical structure of fine-root orders and associations with mycorrhizal fungi, a need emerges to embrace this complexity to bridge the data-model gap in still extremely uncertain models. Here, we propose a three-pool structure comprising transport and absorptive fine roots with mycorrhizal fungi (TAM) to model vertically resolved fine-root systems across organizational and spatial-temporal scales. Emerging from a conceptual shift away from arbitrary homogenization, TAM builds upon theoretical and empirical foundations as an effective and efficient approximation that balances realism and simplicity. A proof-of-concept demonstration of TAM in a big-leaf model both conservatively and radically shows robust impacts of differentiation within fine-root systems on simulating carbon cycling in temperate forests. Theoretical and quantitative support warrants exploiting its rich potentials across ecosystems and models to confront uncertainties and challenges for a predictive understanding of the biosphere. Echoing a broad trend of embracing ecological complexity in integrative ecosystem modeling, TAM may offer a consistent framework where modelers and empiricists can work together toward this grand goal.

Climate drivers alter nitrogen availability in surface peat and decouple N2 fixation from CH4 oxidation in the Sphagnum moss microbiome.

Peat mosses (Sphagnum spp.) are keystone species in boreal peatlands, where they dominate net primary productivity and facilitate the accumulation of carbon in thick peat deposits. Sphagnum mosses harbor a diverse assemblage of microbial partners, including N2 -fixing (diazotrophic) and CH4 -oxidizing (methanotrophic) taxa that support ecosystem function by regulating transformations of carbon and nitrogen. Here, we investigate the response of the Sphagnum phytobiome (plant + constituent microbiome + environment) to a gradient of experimental warming (+0°C to +9°C) and elevated CO2 (+500 ppm) in an ombrotrophic peatland in northern Minnesota (USA). By tracking changes in carbon (CH4 , CO2 ) and nitrogen (NH4 -N) cycling from the belowground environment up to Sphagnum and its associated microbiome, we identified a series of cascading impacts to the Sphagnum phytobiome triggered by warming and elevated CO2 . Under ambient CO2 , warming increased plant-available NH4 -N in surface peat, excess N accumulated in Sphagnum tissue, and N2 fixation activity decreased. Elevated CO2 offset the effects of warming, disrupting the accumulation of N in peat and Sphagnum tissue. Methane concentrations in porewater increased with warming irrespective of CO2 treatment, resulting in a ~10× rise in methanotrophic activity within Sphagnum from the +9°C enclosures. Warming's divergent impacts on diazotrophy and methanotrophy caused these processes to become decoupled at warmer temperatures, as evidenced by declining rates of methane-induced N2 fixation and significant losses of keystone microbial taxa. In addition to changes in the Sphagnum microbiome, we observed ~94% mortality of Sphagnum between the +0°C and +9°C treatments, possibly due to the interactive effects of warming on N-availability and competition from vascular plant species. Collectively, these results highlight the vulnerability of the Sphagnum phytobiome to rising temperatures and atmospheric CO2 concentrations, with significant implications for carbon and nitrogen cycling in boreal peatlands.

Peatland warming strongly increases fine-root growth.

Belowground climate change responses remain a key unknown in the Earth system. Plant fine-root response is especially important to understand because fine roots respond quickly to environmental change, are responsible for nutrient and water uptake, and influence carbon cycling. However, fine-root responses to climate change are poorly constrained, especially in northern peatlands, which contain up to two-thirds of the world's soil carbon. We present fine-root responses to warming between +2 °C and 9 °C above ambient conditions in a whole-ecosystem peatland experiment. Warming strongly increased fine-root growth by over an order of magnitude in the warmest treatment, with stronger responses in shrubs than in trees or graminoids. In the first year of treatment, the control (+0 °C) shrub fine-root growth of 0.9 km m-2 y-1 increased linearly by 1.2 km m-2 y-1 (130%) for every degree increase in soil temperature. An extended belowground growing season accounted for 20% of this dramatic increase. In the second growing season of treatment, the shrub warming response rate increased to 2.54 km m-2 °C-1 Soil moisture was negatively correlated with fine-root growth, highlighting that drying of these typically water-saturated ecosystems can fuel a surprising burst in shrub belowground productivity, one possible mechanism explaining the "shrubification" of northern peatlands in response to global change. This previously unrecognized mechanism sheds light on how peatland fine-root response to warming and drying could be strong and rapid, with consequences for the belowground growing season duration, microtopography, vegetation composition, and ultimately, carbon function of these globally relevant carbon sinks.

Assessing dynamic vegetation model parameter uncertainty across Alaskan arctic tundra plant communities.

As the Arctic region moves into uncharted territory under a warming climate, it is important to refine the terrestrial biosphere models (TBMs) that help us understand and predict change. One fundamental uncertainty in TBMs relates to model parameters, configuration variables internal to the model whose value can be estimated from data. We incorporate a version of the Terrestrial Ecosystem Model (TEM) developed for arctic ecosystems into the Predictive Ecosystem Analyzer (PEcAn) framework. PEcAn treats model parameters as probability distributions, estimates parameters based on a synthesis of available field data, and then quantifies both model sensitivity and uncertainty to a given parameter or suite of parameters. We examined how variation in 21 parameters in the equation for gross primary production influenced model sensitivity and uncertainty in terms of two carbon fluxes (net primary productivity and heterotrophic respiration) and two carbon (C) pools (vegetation C and soil C). We set up different parameterizations of TEM across a range of tundra types (tussock tundra, heath tundra, wet sedge tundra, and shrub tundra) in northern Alaska, along a latitudinal transect extending from the coastal plain near Utqiagvik to the southern foothills of the Brooks Range, to the Seward Peninsula. TEM was most sensitive to parameters related to the temperature regulation of photosynthesis. Model uncertainty was mostly due to parameters related to leaf area, temperature regulation of photosynthesis, and the stomatal responses to ambient light conditions. Our analysis also showed that sensitivity and uncertainty to a given parameter varied spatially. At some sites, model sensitivity and uncertainty tended to be connected to a wider range of parameters, underlining the importance of assessing tundra community processes across environmental gradients or geographic locations. Generally, across sites, the flux of net primary productivity (NPP) and pool of vegetation C had about equal uncertainty, while heterotrophic respiration had higher uncertainty than the pool of soil C. Our study illustrates the complexity inherent in evaluating parameter uncertainty across highly heterogeneous arctic tundra plant communities. It also provides a framework for iteratively testing how newly collected field data related to key parameters may result in more effective forecasting of Arctic change.

An integrated framework of plant form and function: the belowground perspective.

Plant trait variation drives plant function, community composition and ecosystem processes. However, our current understanding of trait variation disproportionately relies on aboveground observations. Here we integrate root traits into the global framework of plant form and function. We developed and tested an overarching conceptual framework that integrates two recently identified root trait gradients with a well-established aboveground plant trait framework. We confronted our novel framework with published relationships between above- and belowground trait analogues and with multivariate analyses of above- and belowground traits of 2510 species. Our traits represent the leaf and root conservation gradients (specific leaf area, leaf and root nitrogen concentration, and root tissue density), the root collaboration gradient (root diameter and specific root length) and the plant size gradient (plant height and rooting depth). We found that an integrated, whole-plant trait space required as much as four axes. The two main axes represented the fast-slow 'conservation' gradient on which leaf and fine-root traits were well aligned, and the 'collaboration' gradient in roots. The two additional axes were separate, orthogonal plant size axes for height and rooting depth. This perspective on the multidimensional nature of plant trait variation better encompasses plant function and influence on the surrounding environment.

Root traits as drivers of plant and ecosystem functioning: current understanding, pitfalls and future research needs.

The effects of plants on the biosphere, atmosphere and geosphere are key determinants of terrestrial ecosystem functioning. However, despite substantial progress made regarding plant belowground components, we are still only beginning to explore the complex relationships between root traits and functions. Drawing on the literature in plant physiology, ecophysiology, ecology, agronomy and soil science, we reviewed 24 aspects of plant and ecosystem functioning and their relationships with a number of root system traits, including aspects of architecture, physiology, morphology, anatomy, chemistry, biomechanics and biotic interactions. Based on this assessment, we critically evaluated the current strengths and gaps in our knowledge, and identify future research challenges in the field of root ecology. Most importantly, we found that belowground traits with the broadest importance in plant and ecosystem functioning are not those most commonly measured. Also, the estimation of trait relative importance for functioning requires us to consider a more comprehensive range of functionally relevant traits from a diverse range of species, across environments and over time series. We also advocate that establishing causal hierarchical links among root traits will provide a hypothesis-based framework to identify the most parsimonious sets of traits with the strongest links on functions, and to link genotypes to plant and ecosystem functioning.

A starting guide to root ecology: strengthening ecological concepts and standardising root classification, sampling, processing and trait measurements.

In the context of a recent massive increase in research on plant root functions and their impact on the environment, root ecologists currently face many important challenges to keep on generating cutting-edge, meaningful and integrated knowledge. Consideration of the below-ground components in plant and ecosystem studies has been consistently called for in recent decades, but methodology is disparate and sometimes inappropriate. This handbook, based on the collective effort of a large team of experts, will improve trait comparisons across studies and integration of information across databases by providing standardised methods and controlled vocabularies. It is meant to be used not only as starting point by students and scientists who desire working on below-ground ecosystems, but also by experts for consolidating and broadening their views on multiple aspects of root ecology. Beyond the classical compilation of measurement protocols, we have synthesised recommendations from the literature to provide key background knowledge useful for: (1) defining below-ground plant entities and giving keys for their meaningful dissection, classification and naming beyond the classical fine-root vs coarse-root approach; (2) considering the specificity of root research to produce sound laboratory and field data; (3) describing typical, but overlooked steps for studying roots (e.g. root handling, cleaning and storage); and (4) gathering metadata necessary for the interpretation of results and their reuse. Most importantly, all root traits have been introduced with some degree of ecological context that will be a foundation for understanding their ecological meaning, their typical use and uncertainties, and some methodological and conceptual perspectives for future research. Considering all of this, we urge readers not to solely extract protocol recommendations for trait measurements from this work, but to take a moment to read and reflect on the extensive information contained in this broader guide to root ecology, including sections I-VII and the many introductions to each section and root trait description. Finally, it is critical to understand that a major aim of this guide is to help break down barriers between the many subdisciplines of root ecology and ecophysiology, broaden researchers' views on the multiple aspects of root study and create favourable conditions for the inception of comprehensive experiments on the role of roots in plant and ecosystem functioning.

Integrating the evidence for a terrestrial carbon sink caused by increasing atmospheric CO2.

Atmospheric carbon dioxide concentration ([CO2 ]) is increasing, which increases leaf-scale photosynthesis and intrinsic water-use efficiency. These direct responses have the potential to increase plant growth, vegetation biomass, and soil organic matter; transferring carbon from the atmosphere into terrestrial ecosystems (a carbon sink). A substantial global terrestrial carbon sink would slow the rate of [CO2 ] increase and thus climate change. However, ecosystem CO2 responses are complex or confounded by concurrent changes in multiple agents of global change and evidence for a [CO2 ]-driven terrestrial carbon sink can appear contradictory. Here we synthesize theory and broad, multidisciplinary evidence for the effects of increasing [CO2 ] (iCO2 ) on the global terrestrial carbon sink. Evidence suggests a substantial increase in global photosynthesis since pre-industrial times. Established theory, supported by experiments, indicates that iCO2 is likely responsible for about half of the increase. Global carbon budgeting, atmospheric data, and forest inventories indicate a historical carbon sink, and these apparent iCO2 responses are high in comparison to experiments and predictions from theory. Plant mortality and soil carbon iCO2 responses are highly uncertain. In conclusion, a range of evidence supports a positive terrestrial carbon sink in response to iCO2 , albeit with uncertain magnitude and strong suggestion of a role for additional agents of global change.

Experimental warming alters the community composition, diversity, and N2 fixation activity of peat moss (Sphagnum fallax) microbiomes.

Sphagnum-dominated peatlands comprise a globally important pool of soil carbon (C) and are vulnerable to climate change. While peat mosses of the genus Sphagnum are known to harbor diverse microbial communities that mediate C and nitrogen (N) cycling in peatlands, the effects of climate change on Sphagnum microbiome composition and functioning are largely unknown. We investigated the impacts of experimental whole-ecosystem warming on the Sphagnum moss microbiome, focusing on N2 fixing microorganisms (diazotrophs). To characterize the microbiome response to warming, we performed next-generation sequencing of small subunit (SSU) rRNA and nitrogenase (nifH) gene amplicons and quantified rates of N2 fixation activity in Sphagnum fallax individuals sampled from experimental enclosures over 2 years in a northern Minnesota, USA bog. The taxonomic diversity of overall microbial communities and diazotroph communities, as well as N2 fixation rates, decreased with warming (p < 0.05). Following warming, diazotrophs shifted from a mixed community of Nostocales (Cyanobacteria) and Rhizobiales (Alphaproteobacteria) to predominance of Nostocales. Microbiome community composition differed between years, with some diazotroph populations persisting while others declined in relative abundance in warmed plots in the second year. Our results demonstrate that warming substantially alters the community composition, diversity, and N2 fixation activity of peat moss microbiomes, which may ultimately impact host fitness, ecosystem productivity, and C storage potential in peatlands.

A global Fine-Root Ecology Database to address below-ground challenges in plant ecology.

Variation and tradeoffs within and among plant traits are increasingly being harnessed by empiricists and modelers to understand and predict ecosystem processes under changing environmental conditions. While fine roots play an important role in ecosystem functioning, fine-root traits are underrepresented in global trait databases. This has hindered efforts to analyze fine-root trait variation and link it with plant function and environmental conditions at a global scale. This Viewpoint addresses the need for a centralized fine-root trait database, and introduces the Fine-Root Ecology Database (FRED, http://roots.ornl.gov) which so far includes > 70 000 observations encompassing a broad range of root traits and also includes associated environmental data. FRED represents a critical step toward improving our understanding of below-ground plant ecology. For example, FRED facilitates the quantification of variation in fine-root traits across root orders, species, biomes, and environmental gradients while also providing a platform for assessments of covariation among root, leaf, and wood traits, the role of fine roots in ecosystem functioning, and the representation of fine roots in terrestrial biosphere models. Continued input of observations into FRED to fill gaps in trait coverage will improve our understanding of changes in fine-root traits across space and time.

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.

Root structural and functional dynamics in terrestrial biosphere models--evaluation and recommendations.

There is wide breadth of root function within ecosystems that should be considered when modeling the terrestrial biosphere. Root structure and function are closely associated with control of plant water and nutrient uptake from the soil, plant carbon (C) assimilation, partitioning and release to the soils, and control of biogeochemical cycles through interactions within the rhizosphere. Root function is extremely dynamic and dependent on internal plant signals, root traits and morphology, and the physical, chemical and biotic soil environment. While plant roots have significant structural and functional plasticity to changing environmental conditions, their dynamics are noticeably absent from the land component of process-based Earth system models used to simulate global biogeochemical cycling. Their dynamic representation in large-scale models should improve model veracity. Here, we describe current root inclusion in models across scales, ranging from mechanistic processes of single roots to parameterized root processes operating at the landscape scale. With this foundation we discuss how existing and future root functional knowledge, new data compilation efforts, and novel modeling platforms can be leveraged to enhance root functionality in large-scale terrestrial biosphere models by improving parameterization within models, and introducing new components such as dynamic root distribution and root functional traits linked to resource extraction.

The unseen iceberg: plant roots in arctic tundra.

Plant roots play a critical role in ecosystem function in arctic tundra, but root dynamics in these ecosystems are poorly understood. To address this knowledge gap, we synthesized available literature on tundra roots, including their distribution, dynamics and contribution to ecosystem carbon and nutrient fluxes, and highlighted key aspects of their representation in terrestrial biosphere models. Across all tundra ecosystems, belowground plant biomass exceeded aboveground biomass, with the exception of polar desert tundra. Roots were shallowly distributed in the thin layer of soil that thaws annually, and were often found in surface organic soil horizons. Root traits - including distribution, chemistry, anatomy and resource partitioning - play an important role in controlling plant species competition, and therefore ecosystem carbon and nutrient fluxes, under changing climatic conditions, but have only been quantified for a small fraction of tundra plants. Further, the annual production and mortality of fine roots are key components of ecosystem processes in tundra, but extant data are sparse. Tundra root traits and dynamics should be the focus of future research efforts. Better representation of the dynamics and characteristics of tundra roots will improve the utility of models for the evaluation of the responses of tundra ecosystems to changing environmental conditions.

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.

Genomics in a changing arctic: critical questions await the molecular ecologist.

Molecular ecology is poised to tackle a host of interesting questions in the coming years. The Arctic provides a unique and rapidly changing environment with a suite of emerging research needs that can be addressed through genetics and genomics. Here we highlight recent research on boreal and tundra ecosystems and put forth a series of questions related to plant and microbial responses to climate change that can benefit from technologies and analytical approaches contained within the molecular ecologist's toolbox. These questions include understanding (i) the mechanisms of plant acquisition and uptake of N in cold soils, (ii) how these processes are mediated by root traits, (iii) the role played by the plant microbiome in cycling C and nutrients within high-latitude ecosystems and (iv) plant adaptation to extreme Arctic climates. We highlight how contributions can be made in these areas through studies that target model and nonmodel organisms and emphasize that the sequencing of the Populus and Salix genomes provides a valuable resource for scientific discoveries related to the plant microbiome and plant adaptation in the Arctic. Moreover, there exists an exciting role to play in model development, including incorporating genetic and evolutionary knowledge into ecosystem and Earth System Models. In this regard, the molecular ecologist provides a valuable perspective on plant genetics as a driver for community biodiversity, and how ecological and evolutionary forces govern community dynamics in a rapidly changing climate.