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Phylogenetically structured traits in root systems influence arbuscular mycorrhizal colonization in woody angiosperms

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Abstract

Background and aim

There is little quantitative information about the relationship between root traits and the extent of arbuscular mycorrhizal fungi (AMF) colonization. We expected that ancestral species with thick roots will maximize AMF habitat by maintaining similar root traits across root orders (i.e., high root trait integration), whereas more derived species are expected to display a sharp transition from acquisition to structural roots. Moreover, we hypothesized that interspecific morphological differences rather than soil conditions will be the main driver of AMF colonization.

Methods

We analyzed 14 root morphological and chemical traits and AMF colonization rates for the first three root orders of 34 temperate tree species grown in two common gardens. We also collected associated soil to measure the effect of soil conditions on AMF colonization.

Results

Thick-root magnoliids showed less variation in root traits along root orders than more-derived angiosperm groups. Variation in stele:root diameter ratio was the best indicator of AMF colonization within and across root orders. Root functional traits rather than soil conditions largely explained the variation in AMF colonization among species.

Conclusions

Not only the traits of first order but the entire structuring of the root system varied among plant lineages, suggesting alternative evolutionary strategies of resource acquisition. Understanding evolutionary pathways in belowground organs could open new avenues to understand tree species influence on soil carbon and nutrient cycling.

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Acknowledgments

The authors would like to thank Scott Kelsey, Suhana Chattopadhyay, Eugene Ryee, Kristine Nissell, Benjamin Villareal, Haren Bonepudi, Josh Lucas, Mariana Romero, Jean Carlo Valverde, Mike Fulp and Carlynn Fulp for their assistance in the field and processing samples. Special thanks to Ethan Johnson from The Holden Arboretum and Kristopher Stone and Josh Selm from Boone County Arboretum for their advice in selecting tree individuals, and to Charlotte Hewins from The Holden Arboretum for sample processing help. This study was funded by startup funds provided by Kent State University, an Art and Margaret Herrick Research Grant, a David and Susan Jarzen Scholarship, The Holden Arboretum Trust, and The Corning Institute for Education and Research, and research grants from US National Science Foundation (DEB-0918240, DEB-0918878) and Department of Energy (DE-SC000433).

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Author notes

  1. Oscar J. Valverde-Barrantes

    Present address: Instituto Nacional de Pesquisa da Amazônia-INPA, Pesquisas Amazônicas de Longa Duraçao, Manaus, Amazonas, 69060-001, Brazil

  2. Amber L. Horning

    Present address: Department of Biology, Mississippi University, University, MS, 38677, USA

  3. Kurt A. Smemo

    Present address: Environmental Studies Program, Skidmore College, Saratoga Springs, NY, 12866, USA

Authors and Affiliations

  1. Department of Biological Sciences, Kent State University, Kent, OH, 44242, USA

    Oscar J. Valverde-Barrantes, Amber L. Horning, Kurt A. Smemo & Christopher B. Blackwood

  2. The Holden Arboretum, 9500 Sperry Rd, Kirtland, OH, 44094, USA

    Kurt A. Smemo

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  1. Oscar J. Valverde-Barrantes
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Correspondence to Oscar J. Valverde-Barrantes.

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Responsible Editor: Duncan D. Cameron.

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Valverde-Barrantes, O.J., Horning, A.L., Smemo, K.A. et al. Phylogenetically structured traits in root systems influence arbuscular mycorrhizal colonization in woody angiosperms. Plant Soil 404, 1–12 (2016). https://doi.org/10.1007/s11104-016-2820-6

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