Research ArticlePLANT SCIENCES

The fungal collaboration gradient dominates the root economics space in plants

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Science Advances  01 Jul 2020:
Vol. 6, no. 27, eaba3756
DOI: 10.1126/sciadv.aba3756
  • Fig. 1 Conceptual framework of the root economics space.

    On the basis of this concept, we hypothesize (i) a collaboration gradient ranging from do-it-yourself soil exploration by high specific root length (SRL) to outsourcing by investing carbon into the mycorrhizal partner and hence extraradical hypheae, which requires a large cortex fraction (CF) and root diameter (D) and (ii) a conservation gradient ranging from roots with high root tissue density (RTD) that show a slow resource return on investment but are long-lived and well-protected, to fast roots with a high nitrogen content (N) and metabolic rate for fast resource return on investment but a short life span. Arrows indicate negative correlations between the single traits (see Table 1).

  • Fig. 2 The root economics space.

    Phylogenetically informed principal component analyses (PCAs) of core traits of (A) 748 global species, (B) 621 arbuscular mycorrhizal (AM) species (blue), and (C) 94 ectomycorrhizal (EM) species (red). NM, nonmycorrhizal. The collaboration gradient (44%) ranges from do-it-yourself roots with high SRL to outsourcing roots with “thick diameters” (D). The conservation gradient (33%) ranges from fast (N) to slow (RTD). For each corner of the root economics space, in (A) we highlight two representative plant species: QV, Quercus virginiana Mill.; CH, Carex humilis Leyss.; CO, Cornus officinalis Siebold & Zucc.; ZM, Zea mays L.; LP, Lathyrus pratensis L.; GB, Ginkgo biloba L.; BL, Betula lenta L.; CP, Cardamine pratensis L. (D) Woody (ocher) and nonwoody (green) species show no distinct pattern within the root economics space (see fig. S4 and table S4). (E) PCA based on bivariate trait relationships. The percentage mycorrhizal colonization (%M) and the CF are positively correlated with D along the collaboration gradient, while root life span is negatively correlated with N along the conservation gradient. See table S1 for PCA scores.

  • Fig. 3 The root economics space is present in different biomes.

    Root traits and trait relations are known to vary across biomes (14). We found no respective between group variation within the root economics space (table S4). Still, to test whether the concept is broadly generalizable, we present separate PCAs for biomes spanning arid to tropical. We found that the root economics space was apparent in all of the biomes represented by our species (panels A, B, C, and D). In continental systems, the conservation gradient was represented by principal component 3 (D) instead of principal component 2 (E). See table S1 for principal component analyses. pc, principal component.

  • Fig. 4 The collaboration gradient is phylogenetically conserved.

    On the left, we display the phylogenetic tree of 1810 species aggregated at a family level with the standardized family mean trait values of the four core traits (center) ranging from low (yellow) to medium (green) to high (blue). The collaboration gradient shows a strong phylogenetic pattern (λ = 0.8, P < 0.001) with a transition from families with thick D to those with high SRL. The phylogenetic signal in the conservation gradient is less pronounced (λ = 0.5, P < 0.001), although still significant (see also table S3). For detailed information about specific clades, see table S5, and for family distribution across clades, see table S6. Pie charts (right) depict the fraction of different mycorrhizal association types within the broader plant phylogenetic clades (indicated by corresponding background colors).

  • Table 1 Rationale of the conceptual framework of root trait correlations depicted in Fig. 1.

    Expected correlations are based on mathematical and ecological rationale and empirical support from the literature. De facto correlations (see also fig. S1) are phylogenetically informed correlation coefficients of species subsets with the respective trait coverage. D, root diameter; SRL, specific root length; RTD, root tissue density; N, root nitrogen content; CF, cortex fraction.

    Trait pairExpected correlationRationaleEmpirical supportDe facto correlationPn species
    SRL - DNegativeA thicker root is shorter
    per unit mass.
    (9, 14, 1820)−0.70<0.00011402
    RTD - NNegativeRTD increases with cell wall
    stabilization, which is poor
    in nitrogen.
    (9, 14, 19)−0.26<0.0001851
    CF - DPositiveCF increases with increasing D at a
    higher rate than stele fraction.
    (10, 19, 22)0.22<0.0001317
    SRL - RTDNegativeA root with a higher tissue density
    is shorter per unit mass.
    RTD - CFNegativeCortex tissue is less dense than
    stele tissue.
    RTD - DNegativeD scales positively with CF.
    Cortex tissue is less dense than
    stele tissue.
    (14, 19)−0.20<0.00011318

Supplementary Materials

  • Supplementary Materials

    The fungal collaboration gradient dominates the root economics space in plants

    Joana Bergmann, Alexandra Weigelt, Fons van der Plas, Daniel C. Laughlin, Thom W. Kuyper, Nathaly Guerrero-Ramirez, Oscar J. Valverde-Barrantes, Helge Bruelheide, Grégoire T. Freschet, Colleen M. Iversen, Jens Kattge, M. Luke McCormack, Ina C. Meier, Matthias C. Rillig, Catherine Roumet, Marina Semchenko, Christopher J. Sweeney, Jasper van Ruijven, Larry M. York, Liesje Mommer

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