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Front. Plant Sci. | doi: 10.3389/fpls.2018.01651

Inducibility of plant secondary metabolites in the stem predicts genetic variation in resistance against a key insect herbivore in maritime pine

  • 1Misión Biológica de Galicia (MBG), Spain
  • 2Department of Plant Pathology, College of Food, Agricultural, and Environmental Sciences, The Ohio State University, United States
  • 3Department of Chemistry, Royal Institute of Technology, Sweden
  • 4Centro de Investigación Forestal (INIA), Spain
  • 5Warnell School of Forestry and Natural Resources, University of Georgia, United States
  • 6Instituto de Investigación en Manejo Forestal Sostenible, Universidad de Valladolid, Spain

Resistance to herbivores and pathogens is considered a key plant trait with strong adaptive value in trees, usually involving high concentrations of a diverse array of plant secondary metabolites (PSM). Intraspecific genetic variation and plasticity of PSM are widely known, however, their ecology and evolution are unclear, and even the implication of PSM as traits that provide direct effective resistance against herbivores is currently questioned. We used control and methyl jasmonate (MJ)-induced clonal copies of genotypes within families from ten populations of the main distribution range of maritime pine to exhaustively characterize the constitutive and induced profile and concentration of PSM in the stem phloem, and to measure insect herbivory damage as a proxy of resistance. Then, we explored whether genetic variation in resistance to herbivory may be predicted by the constitutive concentration of PSM, and the role of its inducibility to predict the increase in resistance once the plant is induced. We found large and structured genetic variation among populations but not between families within populations in resistance to herbivory. The MJ-induction treatment strongly increased resistance to the weevil in the species, and the genetic variation in the inducibility of resistance was significantly structured among populations, with greater inducibility in the Atlantic populations. Genetic variation in resistance was largely explained by the multivariate concentration and profile of PSM at the genotypic level, rather than by bivariate correlations with individual PSM, after accounting for genetic relatedness among genotypes. While the constitutive concentration of the PSM blend did not show a clear pattern of resistance to herbivory, specific changes in the chemical profile and the increase in concentration of the PSM blend after MJ induction were related to increased resistance. To date, this is the first example of a comprehensive and rigorous approach in which inducibility of PSM in trees and its implication in resistance was analyzed excluding spurious associations due to genetic relatedness, often overlooked in intraspecific studies. Here we provide evidences that multivariate analyses of PSM, rather than bivariate correlations, provide more realistic information about the potentially causal relationships between PSM and resistance to herbivory in pine trees.

Keywords: Genetic Variation, Herbivory, inducibility, Maritime pine (Pinus pinaster), plant secondary metabolites (PSMs), phenolics, Resistance, Terpenes

Received: 07 Aug 2018; Accepted: 24 Oct 2018.

Edited by:

Judy Simon, Universität Konstanz, Germany

Reviewed by:

Stefanie Wienkoop, Universität Wien, Austria
Axel Schmidt, Max Planck Institute for Chemical Ecology, Germany  

Copyright: © 2018 López-Goldar, Villari, Bonello, Borg-Karlson, Grivet, Zas and Sampedro. This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

* Correspondence: Mr. Xosé López-Goldar, Misión Biológica de Galicia (MBG), Pontevedra, 36143, Spain,