Using root form to improve our understanding of root function

It has been said – and even written – that the ‘fine roots of perennial plants are a royal pain to study’ (Pregitzer, 2002). This is because the complex branching architecture of ephemeral roots leads to changes in root form and function across sub-millimeter scales (Fig. 1). While painful to consider, the variation in traits from short-lived, absorptive root tips to more proximal, transportive roots, may be our best hope of quantifying and understanding the functional role of living roots throughout the soil profile. Further, inherent variation in root functional traits across plant species may allow us to scale root function from the rhizosphere to the biosphere in order to understand global biogeochemical cycling under current and future climatic conditions. This issue of New Phytologist contains two papers that approach the linkages between root form and function from different, but complementary, directions. Kong et al. (pp. 863–872) take a broad geographic approach, describing patterns of trait variation across the distal root tips of 96 subtropical and tropical tree species in southern China, while Smith et al. (pp. 851–862) worked at the scale of a single site to investigate the relationships among root traits and root decomposition rates of graminoid species across a gradient of soil moisture in grazed ecosystems in central Scotland. ‘… our mechanistic understanding of many of the linkages between root form and function is still in its infancy.’ Natural variation in plant traits is emerging as a powerful tool to understand plant function and its effect on the surrounding environment (Cornwell et al., 2008). Root researchers have long recognized the important linkages between fine-root anatomical and morphological characteristics and their function (e.g. Wilcox, 1968). A number of studies over the past few decades have expanded upon and formalized this earlier work, demonstrating that root traits such as anatomy, morphology, architecture, chemistry, and mycorrhizal colonization are strongly related to root order, changing in predictable ways within a species across the hierarchy of ephemeral, first-order, distal root tips to higher-order roots. Furthermore, traits associated with the most distal, absorptive roots vary substantially across plant species and biomes (Fig. 1). In turn, these traits predict important root functions within and among species, including respiration, water and nutrient acquisition, lifespan, and decomposition (Wilcox, 1968; Pregitzer et al., 2002; Guo et al., 2008; Fan & Guo, 2010; Xia et al., 2010; McCormack et al., 2012). However, our mechanistic understanding of many of the linkages between root form and function is still in its infancy. The insights provided by the Kong et al. and Smith et al. papers can help to improve our understanding and model representation of the important role of fine roots in ecosystem carbon and nutrient cycling. Kong et al. found that the variation in 14 traits across first-order roots of 96 subtropical and tropical tree species were segregated onto two major trait axes. The first axis represented diameter-related traits, while the second, largely independent, axis was related to root branching patterns. The authors suggest that the two orthogonal trait axes represent different root functional strategies; on the first trait axis, the strategy of thicker roots may result in increased structural costs and lower rates of nutrient acquisition that are compensated for by longer root lifespans and higher mycorrhizal colonization rates. The second trait axis, root branching patterns, may be related to nutrient foraging, where species with a higher branching intensity (i.e. more distal root tips per unit of higher-order roots) may be better adapted to rapid proliferation in nutrient-rich patches. While Kong et al. did not measure root function, their extensive quantification of the broad patterns of variation in absorptive root traits among plant species will facilitate the linking of root traits with root function in an economics framework analogous to leaf traits (Cornwell et al., 2008). Smith et al. took a more intensive focus; they used multiple approaches, including litterbags, a common garden, and laboratory incubations, to understand the relationships among plant root traits, environmental conditions, and decomposition at a single grassland site. They found that the decomposition rate of graminoid roots was more related to species-specific differences in root traits (e.g. specific root area, which was related to root diameter) than to variation in environmental conditions, including grazing and soil temperature (though waterlogged soil conditions tended to slow root decomposition rates, no matter the species). The relationship between root traits and root decomposition has been a common theme in recent literature; work in the subarctic indicates that variation in root traits among plant species can strongly affect root decomposition rates, and that linkages among leaves, wood, and roots in plant economics traits, including those related to structure, leads to coordinated litter decomposition across plant organs (Freschet et al., 2012a,b). Root form, and its links with root function, may be better understood over geological timeframes. Kong et al. found that diameter-related root traits, which also included mycorrhizal colonization, were highly-conserved phylogenetically, where more modern lineages tended to have thinner first-order roots than more primitive lineages. The evolution of thinner roots, with fewer layers of cortex, in response to drier climates likely altered root–soil interactions and feedbacks of CO2 to the atmosphere (Comas et al., 2012; Chen et al., 2013; Gu et al., 2014). The relationship between species phylogeny and root traits is important for two reasons: (1) it may allow us to predict root traits for broad groups of species with similar phylogenetic history, and (2) it may help to explain differences in root form among biomes. For example, there appears to be a much greater variation among species in root traits in the tropics, compared with the temperate zone (Chen et al., 2013; Gu et al., 2014). In contrast to the phylogenetic conservation of diameter-related root traits, Kong et al. found that root branching patterns were only weakly conserved across phylogenetic lineages, suggesting that these traits are strongly influenced by environmental variables like soil resource availability. Therefore, many species may not be able to change phylogenetically-conserved traits such as root morphology, but have capacity to substantially alter root architecture and root tip density to adapt to a changing environment. Fine roots are an important component of ecosystem carbon, water, and nutrient cycling. Living roots constitute a large fraction of annual net primary production, contribute to fluxes of CO2 and CH4 through respiration and the release of labile root exudates, and acquire limited water and nutrients to sustain plant growth, while dead and decaying roots contribute carbon and nutrients throughout the soil profile in the form of root litter (reviewed in Jackson et al., 1997). Further, fine roots have shown some of the most dynamic responses to global climate change factors in large-scale experiments (reviewed in Norby & Jackson, 2000; Iversen, 2010). As a community, root and rhizosphere ecologists have been slowly, but steadily, moving away from a categorical classification of fine roots as < 2 mm in diameter, and toward a more functional classification of fine roots based on root form (Pregitzer et al., 2002). For example, a major goal of a recent meeting hosted at the Chinese Academy of Sciences, Institute of Geographic Sciences and Natural Resources Research, in Beijing, China, was to develop a path forward for linking root form with function, beginning with establishment of a network of intensively-measured sites distributed across China. An improved understanding of the important role that fine roots have in ecosystem carbon and nutrient fluxes will require the combined approaches of both Kong et al. and Smith et al.; the establishment of geographical patterns in root trait variation will allow for the development of more mechanistic experiments to investigate the linkages among root form and function. Furthermore, these papers underline the necessity of considering a broad framework for understanding the linkages between root form and function that includes both woody and non-woody plant species. Root traits are poorly represented by large-scale terrestrial biosphere models that are used to characterize ecosystem processes and functions, and their feedbacks to the atmosphere, across the diverse biomes of Earth (Iversen, 2010; Matamala & Stover, 2013). The overly-simplistic representation of roots in terrestrial biosphere models is due in part to a lack of root trait data from ecosystems spanning the globe. While the papers summarized here build upon an increasing foundation of understanding of the links among root form and important ecosystem processes, more work is needed. Given the difficulty in measuring root form and function, the phylogenetic patterns in root traits described in Kong et al. could be combined with the plant economics spectrum (Freschet et al., 2013) to link belowground plant traits with more easily-measured aboveground plant traits. Also, recent work has found that root orders can be grouped into modules that have a similar function (Xia et al., 2010), making it easier to both measure and model fine-root traits. Ultimately, root and rhizosphere ecologists need to be proactive advocates for the inclusion of their data in models; the increased population of root traits, and their relationship with root form and function, in a global database (e.g. the TRY database, http://www.try-db.org/TryWeb/Home.php), could provide a direct pathway from empirical measurements to model representation. A good starting place might be the data contained within the Kong et al. and Smith et al. papers. Oak Ridge National Laboratory is managed by UT-Battelle, LLC, for the US Department of Energy under contract DE-AC05-00OR22725. The SPRUCE experiment in an ombrotrophic bog in northern Minnesota, USA (http://mnspruce.ornl.gov/) is supported by the Office of Biological and Environmental Research in the US Department of Energy Office of Science.