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      Physical and Functional Constraints on Viable Belowground Acquisition Strategies

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          Abstract

          Since their emergence onto land, terrestrial plants have developed diverse strategies to acquire soil resources. However, we lack a framework that adequately captures how these strategies vary among species. Observations from around the world now allow us to quantify the variation observed in commonly-measured fine-root traits but it is unclear how root traits are interrelated and whether they fall along an “economic” spectrum of acquisitive to conservative strategies. We assessed root trait variation and mycorrhizal colonization rates by leveraging the largest global database of fine-root traits (the Fine-Root Ecology Database; FRED). We also developed a heuristic model to explore the role of mycorrhizal fungi in defining belowground exploration efficiency across a gradient of thin- to thick-diameter roots. In support of the expectations of the “root economic spectrum,” we found that root diameter was negatively related to specific root length (Pearson’s r=-0.76). However, we found an unexpected negative relationship between root diameter and root tissue density (Pearson’s r = -0.40), and we further observed that root nitrogen content was largely unrelated to other economic traits. Mycorrhizal colonization was most closely associated with root diameter (Pearson’s r = 0.62) and was unrelated to root tissue density and root nitrogen. The heuristic model demonstrated that while thinner roots have inherently greater capacity to encounter soil resources based on higher surface area per unit mass, the potential for increased associations with mycorrhizal fungi in thicker roots, combined with greater hyphal growth, can result in equally acquisitive strategies for both thin- and thick roots. Taken together, our assessments of root trait variation, trade-offs with mycorrhizal fungi, and broader connections to root longevity allowed us to propose a series of fundamental constraints on belowground resource acquisition strategies. Physical tradeoffs based on root construction (i.e., economic traits) and functional limitations related to the capacity of a root to encounter and acquire soil resources combine to limit the two-dimensional belowground trait space. Within this trait space there remains a diversity of additional variation in root traits that facilitates a wide range of belowground resource acquisition strategies.

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          Most cited references73

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          A meta-analysis of context-dependency in plant response to inoculation with mycorrhizal fungi.

          Ecology Letters (2010) 13: 394-407 Abstract Mycorrhizal fungi influence plant growth, local biodiversity and ecosystem function. Effects of the symbiosis on plants span the continuum from mutualism to parasitism. We sought to understand this variation in symbiotic function using meta-analysis with information theory-based model selection to assess the relative importance of factors in five categories: (1) identity of the host plant and its functional characteristics, (2) identity and type of mycorrhizal fungi (arbuscular mycorrhizal vs. ectomycorrhizal), (3) soil fertility, (4) biotic complexity of the soil and (5) experimental location (laboratory vs. field). Across most subsets of the data, host plant functional group and N-fertilization were surprisingly much more important in predicting plant responses to mycorrhizal inoculation ('plant response') than other factors. Non-N-fixing forbs and woody plants and C(4) grasses responded more positively to mycorrhizal inoculation than plants with N-fixing bacterial symbionts and C(3) grasses. In laboratory studies of the arbuscular mycorrhizal symbiosis, plant response was more positive when the soil community was more complex. Univariate analyses supported the hypothesis that plant response is most positive when plants are P-limited rather than N-limited. These results emphasize that mycorrhizal function depends on both abiotic and biotic context, and have implications for plant community theory and restoration ecology.
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            Going underground: root traits as drivers of ecosystem processes.

            Ecologists are increasingly adopting trait-based approaches to understand how community change influences ecosystem processes. However, most of this research has focussed on aboveground plant traits, whereas it is becoming clear that root traits are important drivers of many ecosystem processes, such as carbon (C) and nutrient cycling, and the formation and structural stability of soil. Here, we synthesise emerging evidence that illustrates how root traits impact ecosystem processes, and propose a pathway to unravel the complex roles of root traits in driving ecosystem processes and their response to global change. Finally, we identify research challenges and novel technologies to address them.
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              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.
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                Author and article information

                Contributors
                Journal
                Front Plant Sci
                Front Plant Sci
                Front. Plant Sci.
                Frontiers in Plant Science
                Frontiers Media S.A.
                1664-462X
                11 October 2019
                2019
                : 10
                : 1215
                Affiliations
                [1] 1Center for Tree Science, The Morton Arboretum . Lisle, IL, United States
                [2] 2Environmental Sciences Division and Climate Change Science Institute, Oak Ridge National Laboratory . Oak Ridge, TN, United States
                Author notes

                Edited by: Sebastian Leuzinger, Auckland University of Technology, New Zealand

                Reviewed by: Benjamin Delory, Leuphana University, Germany; Friderike Beyer, University of Freiburg, Germany

                *Correspondence: M. Luke McCormack, lmccormack@ 123456mortonarb.org

                This article was submitted to Functional Plant Ecology, a section of the journal Frontiers in Plant Science

                Article
                10.3389/fpls.2019.01215
                6797606
                30723482
                432a171a-aae7-40ad-8865-0748ba2d3562
                Copyright © 2019 McCormack and Iversen

                This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

                History
                : 25 May 2019
                : 03 September 2019
                Page count
                Figures: 5, Tables: 1, Equations: 0, References: 86, Pages: 12, Words: 6286
                Categories
                Plant Science
                Original Research

                Plant science & Botany
                fine roots,plant traits,nutrient acquisition,root economics spectrum (res),mycorrhizal fungi,soil exploration,root lifespan,root diameter

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