00 MONTH 2018 | VOL 000 | NATURE | 1 LETTER doi:10.1038/nature25783 Evolutionary history resolves global organization of root functional traits Zeqing Ma 1 *, Dali Guo 1 ‡*, Xingliang Xu 1 , Mingzhen Lu 2 , Richard D. Bardgett 3 , David M. Eissenstat 4 , M. Luke McCormack 1,5 & Lars O. Hedin 2 * Plant roots have greatly diversified in form and function since the emergence of the first land plants 1,2 , but the global organization of functional traits in roots remains poorly understood 3,4 . 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 5,6 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. Recent efforts to understand how functional traits are organized across land plants have revealed notable patterns across the leaf economic spectrum 5,6 , but whether such a high degree of organization is also seen in root traits remains controversial 4,7 . A key factor that has limited progress has been the paucity of data on root traits across plant species and biomes, as roots are difficult to sample and characterize 8,9 . Yet, roots are vital for the ability of plants to acquire nutrients and water—two functions of fundamental importance to whole-plant performance and for predicting how plants respond to elevated CO 2 levels and to climate change 10–12 . Roots face ecological and physiological challenges that differ fundamentally from those encountered by leaves. Roots must compete for and acquire nutrients and water in environments that greatly vary across global biomes, with biophysical conditions ranging from relatively stable (for example, tropical rainforests) to highly seasonal (for example, deserts or boreal forests). The high diversity that exists in root form and function, and in the degree of association with sym- biotic mycorrhizal fungi, raises a fundamental question: how are root traits organized across the diverse taxa that inhabit different ecological conditions worldwide? Here we propose a model of root trait organization that is function- ally decoupled from the leaf economic spectrum and that derives from the phylogenetic history of root diameter and its evolutionary conse- quences for plant resource acquisition. We evaluated a species- and biome-specific dataset of 10 root traits in 3 major categories 3,13 (morphology, physiology and mycorrhizal association; Supplementary Information, note 1), collected from over 1,200 individual plants of 369 species (from 210 genera and 79 families), distributed across 7 major biomes and 3 continents (Extended Data Table 1). The observations in our dataset: (i) derive solely from native plant communities with natural soil and nutrient conditions; (ii) focus on first-order roots (the most distal and absorptive roots of the branching system) that are subject to strong selection by the local environment 8,9,14 ; (iii) accurately identify species and root order (that is, measure of branching hierarchy 8 ) in mixed-species ecosystems, by tracing roots to parent trees 15 ; and (iv) apply consistent analytical methods to trait measures across all species and biomes. We collected 94% of the total observations used in our dataset (see Methods). We first investigated whether first-order root traits are globally organized in a manner analogous to the leaf economic spectrum 5,6 , a composite axis of trait variation that ranges from nitrogen-rich leaves with high specific leaf area and short leaf lifespan to nitrogen-poor leaves with low specific leaf area and long leaf lifespan. In roots, nitrogen supports metabolic activity, including nutrient and water transport, enzyme functioning and mycorrhizal symbiosis 16 . As a result, nitrogen has previously been proposed to serve a similarly central role in the trait organization of roots, with high levels of nitrogen in roots occurring in species with high levels of nitrogen in their leaves, rapid growth and short root lifespans 4,17 . Our results do not support the idea of an analogous organizing role for nitrogen in a global root economic spectrum, expanding on similar previous conclusions drawn from taxonomically and geographically smaller datasets 4,18,19 . First, a principal component analysis failed to identify root nitrogen, which is analogous to leaf nitrogen, as a significant contributor to the primary axis of trait variation (Extended Data Fig. 1 and Extended Data Table 2). Instead, root traits were most strongly explained by root diameter and by a group of traits associated with root construction and mycorrhizal association (principal compo- nent 1, 46%; Extended Data Fig. 1). Second, root nitrogen was not correlated to specific root length (SRL, the length of root per unit of biomass invested) in a manner analo- gous to the relationship between specific leaf area and leaf nitrogen 1 Center for Forest Ecosystem Studies and Qianyanzhou Ecological Station, Key Laboratory of Ecosystem Network Observation and Modeling, Institute of Geographic Sciences and Natural Resources Research, Chinese Academy of Sciences, Beijing 100101, China. 2 Department of Ecology and Evolutionary Biology, Princeton University, New Jersey 08544, USA. 3 School of Earth and Environmental Sciences, The University of Manchester, Manchester M13 9PT, UK. 4 Department of Ecosystem Science and Management, The Pennsylvania State University, University Park, Pennsylvania 16802, USA. 5 Department of Plant and Microbial Biology, University of Minnesota, St Paul, Minnesota 55108, USA. *These authors contributed equally to this work. ‡Deceased. © 2018 Macmillan Publishers Limited, part of Springer Nature. All rights reserved.