Filling gaps in our understanding of belowground plant traits across the world: an introduction to a Virtual Issue
2021; Wiley; Volume: 231; Issue: 6 Linguagem: Inglês
10.1111/nph.17326
ISSN1469-8137
AutoresColleen M. Iversen, Michael McCormack,
Tópico(s)Plant Pathogens and Resistance
ResumoNew PhytologistVolume 231, Issue 6 p. 2097-2103 EditorialFree Access Filling gaps in our understanding of belowground plant traits across the world: an introduction to a Virtual Issue Colleen M. Iversen, Corresponding Author Colleen M. Iversen iversencm@ornl.gov orcid.org/0000-0001-8293-3450 Environmental Sciences Division and Climate Change Science Institute, Oak Ridge National Laboratory, Oak Ridge, TN, 37830-6301 USA Author for correspondence: email iversencm@ornl.govSearch for more papers by this authorM. Luke McCormack, M. Luke McCormack orcid.org/0000-0002-8300-5215 Center for Tree Science, The Morton Arboretum, Liesle, IL, 60515 USASearch for more papers by this author Colleen M. Iversen, Corresponding Author Colleen M. Iversen iversencm@ornl.gov orcid.org/0000-0001-8293-3450 Environmental Sciences Division and Climate Change Science Institute, Oak Ridge National Laboratory, Oak Ridge, TN, 37830-6301 USA Author for correspondence: email iversencm@ornl.govSearch for more papers by this authorM. Luke McCormack, M. Luke McCormack orcid.org/0000-0002-8300-5215 Center for Tree Science, The Morton Arboretum, Liesle, IL, 60515 USASearch for more papers by this author First published: 18 August 2021 https://doi.org/10.1111/nph.17326Citations: 1 This article is an Editorial on the Virtual Issue ‘Filling gaps in our understanding of belowground plant traits across the world’ that includes the following papers: Blume-Werry et al. ( 2019), Boonman et al. ( 2020), Chaudhary et al. ( 2020), Colom & Baucom ( 2021), Courchesne et al. ( 2020), Cuneo et al. ( 2021), de Vries et al. ( 2019), Ehmig & Linder ( 2020), Grünfeld et al. ( 2020), Henneron et al. ( 2020), Hewitt et al. ( 2020), Jiang et al. ( 2021), Kong et al. ( 2021), Lin et al. ( 2020), López-Angulo et al. ( 2020), Lugli et al. ( 2021), Luo et al. ( 2021), Martins et al. ( 2020), McCormack et al. ( 2020), McKay Fletcher et al. ( 2020), Meier et al. ( 2020), Oren et al. ( 2020), Pedersen et al. ( 2021a), Pierick et al. ( 2021), Rodriguez-Dominguez & Brodribb ( 2020), Smith-Martin et al. ( 2020), Sokol et al. ( 2019), Soudzilovskaia et al. ( 2020), Spitzer et al. ( 2021), Sun et al. ( 2021), Suseela et al. ( 2020), Sweeney et al. ( 2021), Valverde-Barrantes et al. ( 2020), van Veelen et al. ( 2020), Wang et al. ( 2020), Wedger et al. ( 2019), Wen et al. ( 2019), Williams & de Vries ( 2020), Yamauchi et al. ( 2021), Yu et al. ( 2020), Zhang et al. ( 2020), Zhou et al. ( 2020). Access the Virtual Issue at www.newphytologist.com/virtualissues. AboutSectionsPDF ToolsRequest permissionExport citationAdd to favoritesTrack citation ShareShare Give accessShare full text accessShare full-text accessPlease review our Terms and Conditions of Use and check box below to share full-text version of article.I have read and accept the Wiley Online Library Terms and Conditions of UseShareable LinkUse the link below to share a full-text version of this article with your friends and colleagues. Learn more.Copy URL Share a linkShare onFacebookTwitterLinked InRedditWechat The belowground world is one of the final frontiers in terrestrial ecology. The tangling of plant roots with the surrounding soil below is a lifeline for the humble forbs and towering trees above, and roots play a key role in shaping ecosystem carbon, water and nutrient cycling (Bardgett et al., 2014). Ecologists have long sought to better understand the ecosystem-scale consequences of differing plant strategies, above- and belowground, by relating plant characteristics, or traits, to plant function (Grime, 1977; Pregitzer, 2002). While developing trait–function linkages is arguably more difficult for plant traits that are hidden belowground, root and rhizosphere ecologists continue to fan out across grasslands and forests with their shovels, isotopes, and specialized cameras, seeking a better understanding of the secret lives of roots. Over the years, New Phytologist has served as a virtual town square for scientists to discuss their hard-won observations on the interplay among belowground plant traits, microbial activity, and edaphic and environmental conditions from biomes around the world (Norby & Jackson, 2000; Pregitzer, 2002; Matamala & Stover, 2013; Norby & Iversen, 2017). Here we highlight the newest papers that update and add to our understanding of the role of root and rhizosphere traits in broader ecosystem processes. We focused on papers published in New Phytologist between 1 January 2019 and 31 December 2020 and extended this window to papers still in ‘early view’ up to the time of writing. Because of the overwhelming number of papers, we did not include those with a decidedly genomic focus or that served primarily as data syntheses, reviews, insights or commentaries. Filling gaps in our understanding of root trait variation among species The Fine-Root Ecology Database (FRED) has been at the forefront of efforts in recent years to fill gaps in our understanding of fine-root trait variation. FRED serves as a repository for the focused and collaborative curation of root trait data and provides a foundation to improve both empirical understanding and model representation of root form and function (Iversen et al., 2017). The third version of FRED is now available online at https://roots.ornl.gov as a searchable database, where global coverage of fine-root traits ranging from the anatomy of individual roots to root dynamics and distribution can be filtered according to the specific interests of each scientist. While FRED houses root trait observations from across c. 4600 unique plant species, this is only a fraction of the roughly 350 000 species of known vascular plants around the world (Antonelli et al., 2020). And like many databases, the observations in FRED are unequally distributed around the world (Fig. 1a,b) and among root traits (Fig. 1c), hindering our ability to predict global root trait variation. However, phylogenetic relationships are providing a useful means to infer broad patterns of trait variation across the plant kingdom. For example, Valverde-Barrantes et al. (2020) confirmed a strong shift in root morphology among angiosperms over evolutionary time , and demonstrated that these changes were largely independent from changes in leaves and mycorrhizal association. Interestingly, with narrower phylogenetic ranges, scientists have observed that both phylogenetic conservatism (McCormack et al., 2020) as well as phylogenetic lability (Ehmig & Linder, 2020; Colom & Baucom, 2021) may contribute to the success of woody and nonwoody species spanning environmental gradients. Fig. 1Open in figure viewerPowerPoint FRED 3.0 is now freely available to the broader community of root and rhizosphere ecologists via a new user interface that allows data filtering (Iversen et al., 2021; see more on the details of FRED 3.0 at https://roots.ornl.gov). (a) FRED 3.0 observations are distributed unevenly across the globe. For the purposes of this map, land cover within a Köppen–Geiger climate classification zone (Kottek et al., 2006) was aggregated into hex bins that are extruded in three-dimensional space based on the number of root trait samples collected in each bin. (Map courtesy of Chris DeRolph.) (b) The number of root trait samples collected from each Köppen–Geiger climate subclass (e.g. Kottek et al., 2006) is summed within each climate class. (c) The distribution of observations in FRED 3.0 across broad categories of root traits. FRED 3.0 has 45% more root trait observations than FRED 2.0, particularly in the categories of root anatomy, root morphology and root microbial associations; the increase in the microbial associations category is largely related to an increase in studies reporting mycorrhizal associations; for more information about the broad root trait categories, see Iversen et al. (2017). Despite the rapidly growing number of root trait observations in FRED, there are still notable gaps in coverage for many trait types. For example, anatomical traits represent less than 3% of the root trait observations in FRED 3.0 (Fig. 1c), yet these traits may provide a better approximation of root function and construction cost than more commonly-measured morphological traits (Pedersen et al., 2021b; Zhou et al., 2021). A framework presented by Kong et al., (2021) to estimate theoretical rates of root carbon supply and consumption based on root anatomical composition may help explain observed variation and limits on individual root diameter, including across the phylogenetic tree and around the world (Kong et al., 2014; Bergmann et al., 2020). Linking root form with function While assessments of fine-root trait variation are critically important, our ultimate goal is to link root traits with root function and whole-plant strategies. However, direct measurements of root function remain challenging, as evidenced by the relatively low number of observations of root physiological traits in FRED 3.0 (Fig. 1c). Fortunately, an increasing number of scientists have taken on the challenge of linking one important aspect of root function, exudation, with a number of other root traits in the context of ecosystem carbon, water and nutrient cycling. For example, belowground ecologists have linked root exudation rates with suites of competitive or conservative root traits in a multidimensional framework that spans the phylogenetic tree (Sun et al., 2021) and soil gradients (Meier et al., 2020), and have established linkages between exudate production, microbial activity and plant drought stress (de Vries et al., 2019; Williams & de Vries, 2020). Further, they have established relationships among exudate production, root branchiness and proliferation, and mycorrhizal colonization in empirical and modeling frameworks with implications for root phosphorus acquisition and the availability of soil phosphorus to adjacent plants (Wen et al., 2019; McKay Fletcher et al., 2020; Yu et al., 2020; Zhang et al., 2020). We note that these studies, which encompass different plant functional types and ecosystems, observed different and sometimes contrasting relationships among root exudation rates and root morphological traits – highlighting an opportunity for further synthesis or study. Linking root traits with fungal traits Belowground plant strategies encompass more than just root traits, and complex plant interactions with the surrounding rhizosphere microbial community – especially mycorrhizal fungi – are important for plant root survival and resource acquisition (Strullu-Derrien et al., 2018). In recent years, a number of empirical, synthesis and heuristic modeling studies have found species-specific tradeoffs in mycorrhizal association and root characteristics encompassing strategies ranging from ‘do it yourself’ to ‘outsourcing’ of resource acquisition (e.g. McCormack & Iversen, 2019; Wen et al., 2019; Bergmann et al., 2020). Furthermore, Hewitt et al. (2020) found that root-associated fungi could extend plant foraging below maximum rooting depth to reach available nutrients at the thaw front in tundra ecosystems underlain by permafrost. New global database initiatives in recent years include rich data sets on plant association with colonization by mycorrhizal fungi (e.g. FungalRoot; Soudzilovskaia et al., 2020), as well as fungal traits (Fig. 2); these new initiatives hold promise for improving our understanding of plant–fungal interactions. Fig. 2Open in figure viewerPowerPoint The shape of the Belowground Data Revolution. Ongoing belowground trait data mobilization initiatives (that the authors of this Editorial are aware of) that have a concerted belowground focus. Image created with BioRender.com. The belowground trait initiatives are: Arctic Underground (R. Hewitt & M. Mack, Northern Arizona University, https://www.assw2020.is/program-iasc/open-meetings); BBB (Belowground Bud Bank database, Pausas et al., 2018, https://www.uv.es/jgpausas/bbb.htm); CLO-PLA (Klimešová et al., 2017, http://clopla.butbn.cas.cz); FRED (Fine-Root Ecology Database, Iversen et al., 2017, http://roots.ornl.gov); FunFun (Zanne et al., 2020, https://github.com/traitecoevo/fungaltraits); FUNGuild (Nguyen et al., 2016, http://www.funguild.org); FungalRoot (Soudzilovskaia et al., 2020, 10.15468/a7ujmj); GlobalFungi (Větrovský et al., 2020, https://globalfungi.com); GRooT (Guerrero-Ramírez et al., 2021, http://groot-database.github.io/GRooT); Kutschera Drawings (Kutschera, 2010, https://images.wur.nl/digital/collection/coll13/search); MAPS (S. Kivlin, University of Tennessee); MycoDB (Chaudhary et al., 2016, 10.5061/dryad.723m1); MyCoPortal (Miller & Bates, 2017, https://mycoportal.org); NodDB (Tedersoo et al., 2018, 10.15156/BIO/587469); Open Traits (Gallagher et al., 2020, http://opentraits.org); PFI (Plant-Fungal Interactions, S. Kivlin, University of Tennessee, A. Zanne, George Washington University); Rhizopolis (Freschet et al., 2017, www.researchgate.net/project/Rhizopolis-Exploring-global-variation-in-fine-root-traits); Rooty (Rooty: A Root Ideotype Toolbox to Support Improved Wheat Yields, E. Ober, National Institute of Agricultural Botany, https://iwyp.org/wp-content/uploads/sites/34/2018/08/Eric-Ober-Project.pdf); sROOT (Bergmann et al., 2020, www.idiv.de/en/sroot.html); TraitAM (B. Chaudhary, DePaul University & C. Aguilar-Trigueros, Freie Universität Berlin); TropiRoot (D. Cusack, Colorado State University, https://tropiroottrait.github.io/TropiRootTrait); TRY (Kattge et al., 2020, www.try-db.org), UNITE (Nilsson et al., 2019, https://unite.ut.ee). All websites were accessed on 11 January 2021. Root–rhizosphere interactions Living roots contribute disproportionately to the formation of soil organic matter (Sokol et al., 2019) via synergistic and antagonistic interactions with fungal and bacterial communities in the surrounding rhizosphere. For example, the amount, composition and diversity of living roots can affect microbial community richness and diversity (López-Angulo et al., 2020; Spitzer et al., 2021; Sweeney et al., 2021), as well as nitrogen cycling in the rhizosphere (Henneron et al., 2020). Furthermore, root traits control growth patterns in response to deflecting soil particles (Martins et al., 2020), and in turn root-induced soil deformation affects soil properties ranging from compaction to chemical composition (van Veelen et al., 2020). Even after roots die, the decomposition of roots by soil microbial communities is often mediated by root traits and root associations with mycorrhizal fungi, in addition to the surrounding environment (Lin et al., 2020; Jiang et al., 2021). Our understanding of root trait variation is limited beyond temperate ecosystems Historically, much of our understanding (and quantification) of root trait variation has been limited to temperate grasslands and forests (Fig. 1a,b). But under-studied ecosystems, from the tundra to the tropics, have unique species and trait combinations and are changing rapidly in response to changing environmental conditions (Malhi et al., 2011; Thomas et al., 2020). New efforts in recent years have sought to clarify some long-held assumptions about belowground plant strategies in these ecosystems. At the top of the world, Blume-Werry et al. (2019) found that tundra plant roots may gain a competitive advantage by growing more deeply towards the thawing permafrost boundary, and Spitzer et al. (2021) found that tundra plant root characteristics can predict some aspects of soil microbial community composition. In turn, Courchesne et al. (2020) found that temperature likely constrains the occurrence of boreal wetland species, depending on their root overwintering strategy. At lower latitudes, Boonman et al. (2020) found that tropical seedlings were characterized by syndromes of related root traits characteristic of vegetation types spanning environmental gradients in tropical Africa. In turn, Smith-Martin et al. (2020) debunked the long-held assumption that lianas are deeply-rooted in dry tropical forests by the use of shovelomics and modeling approaches. In recognizing the substantial difficulty of quantifying maximum rooting depth in savannas, Zhou et al. (2020) focused on new ways of predicting and validating the distribution of the total rooting system. Furthermore, gradients of water and nutrient availability in tropical and subtropical forests shape both the distribution of tree species and their associated root trait syndromes (Luo et al., 2021; Pierick et al., 2021). Understanding root responses to changing environmental conditions Some of the species-specific root traits listed above can help us to better predict how belowground plant trait strategies may change in response to changing environmental conditions, but we must also validate these predictions in plants experiencing warming, CO2-enrichment, altered precipitation regimes, or the associated changes in the availability of nutrients and water. For example, Wang et al. (2020) found that woody and herbaceous plant species tended to vary in the relative amount of fine-root biomass produced along manipulated precipitation gradients, while Lugli et al. (2021) found that increased nutrient availability – including the availability of rock-derived nutrients – increased root production and altered root traits. In turn, Williams & de Vries (2020) proposed that plants use root exudates, and the resulting influence on surrounding microbial communities, as a way to mediate plant responses to stressors such as drought conditions. Others found that changes in the quality and composition of heteropolymers such as lignin, suberin and tannins could help to sustain the function of the most distal roots during drought (Suseela et al., 2020; Cuneo et al., 2021). At the wetter end of the soil moisture curve, Pedersen et al. (2021a,b) found that plants, in particular crop plants, can adapt to waterlogging and low soil oxygen availability through changes in root anatomy, morphology, and architecture, while Yamauchi et al. (2021) found that the relative amounts of root anatomical tissues can explain the adaptation of Poaceae species to gradients of soil water. Understanding plant trait variation across a whole-plant economics spectrum A unified whole-plant economic spectrum where leaves, wood and fine roots have parallel strategies within a species has been the subject of ecological manifestos (e.g. Reich, 2014). While ecologists have yet to discover generalizable linkages among the most commonly measured above- and belowground plant traits (Weemstra et al., 2016), in part because roots can outsource resource acquisition to mycorrhizal fungi (McCormack & Iversen, 2019; Bergmann et al., 2020), recent evidence indicates that some physiological functions may be coupled across the whole plant. For example, in tropical saplings Oren et al. (2020) found that root respiration was coupled with canopy photosynthetic patterns in response to changing light conditions, while in turn, Zhou et al. (2021) found that syndromes of root anatomical traits could be used to group plant functional types that differed in leaf physiological responses to changing precipitation regimes. Furthermore, Rodriguez-Dominguez & Brodribb (2020) found that declining root water transport associated with soil drying was directly linked to stomatal closure in olive plants. To facilitate whole-plant trait investigations that span leaf, wood and fine-root traits, each new version of FRED is submitted to the TRY plant trait database (Kattge et al., 2020). Harnessing the belowground data revolution We are experiencing a ‘Belowground Data Revolution’ (Defrenne et al., 2021); the open sharing of belowground plant trait observations from around the world has greatly improved our understanding of the intricate connections in the hidden world beneath our feet. However, the data revolution is just beginning. For example, the FRED initiative is relatively young, and there are still opportunities to incorporate rich and currently underutilized sources of data, especially those originating from horticultural and agricultural studies. Although their metrics often use different terminology and methodology than traditional ecological research, these studies have important and far-reaching implications (Lynch, 2019; Arsova et al., 2020). Furthermore, an advantage of horticultural and agricultural systems is the often detailed characterization of intraspecific variation (i.e. of varietals or lines) in root physiology, morphology and root system architecture, as well as the genetic underpinning of root traits (Wedger et al., 2019), and explicit links between root traits and the function of individual roots (Martins et al., 2020; van Veelen et al., 2020; Pedersen et al., 2021a) and root systems (Wen et al., 2019; McKay Fletcher et al., 2020). While the FRED team – in collaboration with the broader ecological community – plans to continue curating and sharing root trait data for the foreseeable future, FRED is just one of the many contributors to the Belowground Data Revolution (Fig. 2). New data mobilization efforts focused on belowground processes from plant interactions with mycorrhizal fungi (Soudzilovskaia et al., 2020), to root traits in understudied biomes like the tundra and tropics (Hewitt et al., 2020), to fungal dispersal in the air and on land (Chaudhary et al., 2020; Grünfeld et al., 2020) each provide new belowground understanding for empiricists and modelers alike. Furthermore, new tools such as OpenSimRoot (Postma et al., 2017) and RhizoVision Explorer (Seethepalli & York, 2020) allow for in-depth exploration of root architecture, while predictive analyzers like PEcAn allow for trait-informed model sensitivity analyses (Dietze et al., 2014). Lastly, linkages between data mobilization efforts are facilitating a new understanding (e.g. the FRED–TRY synergy allows for an investigation of above- and belowground trait relationships; Kattge et al., 2020), or new ways to subset data to focus on a question of interest (e.g. the GRooT database subset portions of FRED to allow for a narrowed focus on species-specific patterns in commonly-measured root traits around the world; Guerrero-Ramírez et al., 2021). As we move forward together, we note several overarching ideas that can guide future observations of the belowground world: (1) Community consensus. A new root trait handbook (Freschet et al., 2021a) and companion paper (Freschet et al., 2021b) led by an international community of root and rhizosphere ecologists are available to guide future root trait measurements, in the hope that we can fill existing data gaps as well as standardize our terminology and methodology in a way that allows broader inference. (2) Inclusion in belowground ecology. As the belowground science endeavour is global, so too should belowground ecologists actively create an inclusive culture that welcomes scientists from across a range of different backgrounds and experiences (Chaudhary & Berhe, 2020; Defrenne et al., 2021). And (3) Data sharing. As part of a global community of belowground enthusiasts, we advance our understanding of the intricate and complex world beneath our feet much more rapidly by openly sharing our data. To that end, the papers featured in this Virtual Issue are freely available for the next 2 months, and all New Phytologist papers become freely available 1 yr after publication. We hope that you will contribute your new belowground understanding to a growing list of papers and to FRED – join us in the Belowground Data Revolution! Acknowledgements Congratulations to the authors of the Virtual Issue articles for their excellent work; we enjoyed reading about your observations of the belowground world and we sincerely apologize if we have misrepresented any of your findings. Thank you also to the reviewers who invested their time and expertise to help shape these manuscripts; we appreciate your service to advance the scientific endeavor. Organization of this Virtual Issue and this introductory article were supported by the Biological and Environmental Research program in the US Department of Energy's Office of Science.The Fine-Root Ecology Database (FRED) is also supported by the Biological and Environmental Research program in the Department of Energy’s Office of Science; thank you to the FRED team: A. Shafer Powell, J. Katie Baer, Dave Connerth, Derek Brownlee, Chris DeRolph and Les Hook. Oak Ridge National Laboratory is managed by UT-Battelle, LLC, under contract number DE-AC05-00OR22725. 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