Evolutionary history resolves global organization of root functional traits

  • An Erratum to this article was published on 05 April 2018
  • An Author Correction to this article was published on 17 May 2019

Abstract

Plant roots have greatly diversified in form and function since the emergence of the first land plants1,2, but the global organization of functional traits in roots remains poorly understood3,4. 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 studies5,6 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.

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Figure 1: Root trait dimensions organized by root diameter and growth form.
Figure 2: Density distributions of first-order root diameter across seven biomes.

Change history

  • 04 April 2018

    Please see accompanying Erratum (https://doi.org/10.1038/nature26163). Both authors D.G. and L.O.H. should have been listed as corresponding authors. This has been corrected online.

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Acknowledgements

We thank C. Ma, L. Li, Y. Yue, M. Liu, F. Ma, H. Li, D. Kong, B. Liu and K. Sun for collecting data; X. Liu and X. Deng for their assistance in field sampling; and all members of field research stations of the Chinese Academy of Sciences for their support. This study was funded by the Natural Science Foundation of China (NSFC Grants 31325006, 31530011, and 41571130041).

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Z.M., D.G. and L.O.H. developed the overall conceptual approach and analysis. Z.M. compiled and analysed the data, and X.X. provided nitrogen-uptake-rate data. R.D.B., D.M.E. and M.L.M. contributed to the formulation of research questions and interpretations. Z.M., D.G., M.L. and L.O.H. wrote the paper and all authors contributed to revisions.

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Correspondence to Dali Guo or Lars O. Hedin.

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Extended data figures and tables

Extended Data Figure 1 Principal component analysis of 7 root functional traits across 104 species.

Trait loading on the plane defined by principal components 1 and 2 (PC1 and PC2). Brown arrows indicate four morphological traits; diameter, length, SRL and root tissue density (RTD). Green arrows indicate two physiological–chemical traits; root carbon (RootC) and root nitrogen (RootN). The yellow arrow shows mycorrhizal colonization. Three different analyses confirm the results shown here (detailed in Extended Data Table 2): (i) all data excluding the mycorrhizal colonization trait (n = 217 species); (ii) gaps in mycorrhizal colonization data interpolated using the regression from Fig. 1c (n = 217 species); and (iii) gaps in any trait value interpolated (n = 369) using the regressions in Fig. 1a, c or the multiple imputation method in the MICE R package).

Extended Data Figure 2 Root nitrogen concentration and root nitrogen uptake rate.

a, There is no correlation between root nitrogen and SRL (r2 = 0.002, P = 0.81, n = 269). b, There is no correlation between root nitrogen and diameter (r2 = 0.02, P = 0.01, n = 274). Each point represents one species: brown, woody plants; green, herbaceous plants (a, b). c, Across plant growth forms, nitrogen uptake rates per root biomass did not vary significantly (P > 0.05) based on hydroponic measurements (brown). For in situ experiments (green) we observed a growth-form effect (P < 0.01), which was caused solely by higher root uptake in graminoid species compared to trees. All other growth forms were statistically indistinguishable. The letters ‘a’ and ‘b’ indicate significant difference based on an ANOVA across growth forms. d, Summary table of nitrogen uptake rates across different biomes by two approaches. This dataset included previously unpublished data from 22 species. A detailed description of these two approaches can be found in the Methods. Additional data were collected from refs 59, 60, 61, 62, 63, 64, 65, 66, 67, 68, 69, 70, 71, 72, 73, 74, 75, 76, 77, 78, 79, 80, 81, 82, 83, 84, 85, 86, 87, 88, 89, 90, 91, 92, 93, 94, 95, 96, 97, 98, 99, 100, 101.

Extended Data Figure 3 First-order-root nitrogen concentration across biomes and plant functional groups.

a, We did not detect a distinct pattern in first-order-root nitrogen concentration across biomes (a) (ANOVA; P > 0.14, n = 284 species). b, We detected a slight difference in first-order-root nitrogen concentration among plant functional groups (b) (ANOVA; P < 0.01, n = 284 species), which was mostly driven by the higher root nitrogen concentrations found in legumes. Each point represents one species; brown, woody plants; green, herbaceous plants. The letters ‘a’, ‘b’ and ‘ab’ indicate significant differences between categories.

Extended Data Figure 4 Relationship between root functional and morphological traits.

a, c, Root median lifespan is significantly correlated with root diameter (a, r2 = 0.14, P < 0.01, linear regression) and SRL (c, r2 = 0.17, P < 0.01, linear regression). b, d, Root nitrogen uptake rate is not correlated with root diameter (b, r2 = 0.07, P > 0.05, linear regression) or with SRL (d, r2 = 0.07, P = 0.29, linear regression) in woody plants. Data are presented on a logarithmic scale (log10), with each point representing one species.

Extended Data Figure 5 Distribution of first-order-root diameter for woody and herbaceous plants across biomes.

a, Woody plant root diameter deceases from tropical to desert biomes, with the most frequent occurrence of coarse-root ancestral woody species in tropical and subtropical biomes. b, Herbaceous plant root diameters do not display a clear trend across biomes. In both panels, the letters ‘a’, ‘b’ and ‘c’ denote significant differences (P < 0.05) between biomes based on a linear mixed effects model (generated using the lmer function in R) with species included as a random effect. Diameter was first log10-transformed to correct for non-normality. Each point represents a species-specific observation at one site. The background violin plot characterizes the distribution of points in each biome. c, Pairwise comparisons for equal variance in first-order-root diameter using Levene’s test. Levene’s test is used for testing the homogeneity of variance, and is used here to explain biome differences in variance of root diameter.

Extended Data Figure 6 Frequency distributions of nine root functional traits.

ac, Cyan bars identify the distribution of herbaceous plants, yellow bars identify woody plants, and green colour is where two distributions overlap. n, total number of species; s, skewness of all data.

Extended Data Figure 7 Phylogenetic tree of 365 taxa in the study.

The oldest taxonomic groups are highlighted in orange (gymnosperms), yellow (monocotyledons) and green (for example, Magnoliales, Lauraceae). The youngest taxonomic groups are highlighted in purple (for example, Betulaceae, Fagaceae).

Extended Data Table 1 Summary of ten functional traits of first order roots
Extended Data Table 2 Principal component analyses of global root functional trait data
Extended Data Table 3 Spearman’s correlation coefficients and phylogenetically independent contrasts among eight root functional traits

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Ma, Z., Guo, D., Xu, X. et al. Evolutionary history resolves global organization of root functional traits. Nature 555, 94–97 (2018). https://doi.org/10.1038/nature25783

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