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Convergence of a specialized root trait in plants from nutrient-impoverished soils: phosphorus-acquisition strategy in a nonmycorrhizal cactus

Abstract

In old, phosphorus (P)-impoverished habitats, root specializations such as cluster roots efficiently mobilize and acquire P by releasing large amounts of carboxylates in the rhizosphere. These specialized roots are rarely mycorrhizal. We investigated whether Discocactus placentiformis (Cactaceae), a common species in nutrient-poor campos rupestres over white sands, operates in the same way as other root specializations. Discocactus placentiformis showed no mycorrhizal colonization, but exhibited a sand-binding root specialization with rhizosheath formation. We first provide circumstantial evidence for carboxylate exudation in field material, based on its very high shoot manganese (Mn) concentrations, and then firm evidence, based on exudate analysis. We identified predominantly oxalic acid, but also malic, citric, lactic, succinic, fumaric, and malonic acids. When grown in nutrient solution with P concentrations ranging from 0 to 100 μM, we observed an increase in total carboxylate exudation with decreasing P supply, showing that P deficiency stimulated carboxylate release. Additionally, we tested P solubilization by citric, malic and oxalic acids, and found that they solubilized P from the strongly P-sorbing soil in its native habitat, when the acids were added in combination and in relatively low concentrations. We conclude that the sand-binding root specialization in this nonmycorrhizal cactus functions similar to that of cluster roots, which efficiently enhance P acquisition in other habitats with very low P availability.

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Acknowledgments

This work was supported by the Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq, grant CNPq 474670/2008-2), Fundação de Apoio à Pesquisa do Estado de São Paulo (FAPESP, grant 10/17204-0) and Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (Capes). We thank H.G. Cândido, C. Pereira and A.V. Scatigna for the support in collecting the plants in the field. Additionally, we thank M.C. Campos, S.M. Carmello-Guerreiro, N. Urquiza, J. Tamashiro, J.C. Galvão, L. Pereira, D.C. da Silva and D.P. de Souza for the methodological support and F.S.C. Takahashi for the help with statistical analyses. We also thank P.B. Costa, S.M.S. Costa, L. Franci and A. Dias, for their assistance. Finally, we thank the anonymous reviewers for their useful reviews of this manuscript.

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Communicated by Jason P. Kaye.

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Abrahão, A., Lambers, H., Sawaya, A.C.H.F. et al. Convergence of a specialized root trait in plants from nutrient-impoverished soils: phosphorus-acquisition strategy in a nonmycorrhizal cactus. Oecologia 176, 345–355 (2014). https://doi.org/10.1007/s00442-014-3033-4

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Keywords

  • Carboxylates
  • Cerrado
  • Manganese
  • Root exudates
  • Root hairs