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Title: Are the metabolomic responses to folivory of closely related plant species linked to macroevolutionary and plant-folivore coevolutionary processes?

Abstract

The debate whether the coevolution of plants and insects or macroevolutionary processes (phylogeny) is the main driver determining the arsenal of molecular defensive compounds of plants remains unresolved. Attacks by herbivorous insects affect not only the composition of defensive compounds in plants but the entire metabolome (the set of molecular metabolites), including defensive compounds. Metabolomes are the final products of genotypes and are directly affected by macroevolutionary processes, so closely related species should have similar metabolomic compositions and may respond in similar ways to attacks by folivores. We analyzed the elemental compositions and metabolomes of needles from Pinus pinaster, P. nigra and P. sylvestris to determine if these closely related Pinus species with different coevolutionary histories with the caterpillars of the processionary moth respond similarly to attacks by this lepidopteran. All pines had different metabolomes and metabolic responses to herbivorous attack. The metabolomic variation among the pine species and the responses to folivory reflected their macroevolutionary relationships, with P. pinaster having the most divergent metabolome. The concentrations of phenolic metabolites were generally not higher in the attacked trees, which had lower concentrations of terpenes, suggesting that herbivores avoid individuals with high concentrations of terpenes. Our results suggest that macroevolutionary historymore » plays important roles in the metabolomic responses of these pine species to folivory, but plant-insect coevolution probably constrains those responses. Combinations of different evolutionary factors and trade-offs are likely responsible for the different responses of each species to folivory, which is not necessarily exclusively linked to plant-insect coevolution.« less

Authors:
 [1];  [2];  [3];  [4];  [4];  [5];  [5];  [6];  [3]
  1. Environmental Molecular Sciences Laboratory, Pacific Northwest National Laboratory, Richland Washington 99354 USA; CREAF, Cerdanyola del Vallès 08913 Catalonia Spain
  2. Grupo de Ecología Terrestre, Departamento de Biología Animal y Ecología, Facultad de Ciencias, Universidad de Granada, 18071 Granada Spain
  3. CREAF, Cerdanyola del Vallès 08913 Catalonia Spain; CSIC, Global Ecology Unit CREAF-CEAB-CSIC-UAB, Cerdanyola del Vallès 08913 Catalonia Spain
  4. Biological Sciences Division, Pacific Northwest National Laboratory, Richland Washington 99354 USA
  5. Global Change Research Centre, Academy of Sciences of the Czech Republic, Bĕlidla 4a CZ-603 00 Brno Czech Republic
  6. Department of Earth System Science, University of California, Irvine California 92697 USA
Publication Date:
Research Org.:
Pacific Northwest National Laboratory (PNNL), Richland, WA (US), Environmental Molecular Sciences Laboratory (EMSL)
Sponsoring Org.:
USDOE
OSTI Identifier:
1326144
Report Number(s):
PNNL-SA-116150
Journal ID: ISSN 2045-7758; 48729; KP1704020
DOE Contract Number:
AC05-76RL01830
Resource Type:
Journal Article
Resource Relation:
Journal Name: Ecology and Evolution; Journal Volume: 6; Journal Issue: 13
Country of Publication:
United States
Language:
English
Subject:
Environmental Molecular Sciences Laboratory

Citation Formats

Rivas-Ubach, Albert, Hódar, José A., Sardans, Jordi, Kyle, Jennifer E., Kim, Young-Mo, Oravec, Michal, Urban, Otmar, Guenther, Alex, and Peñuelas, Josep. Are the metabolomic responses to folivory of closely related plant species linked to macroevolutionary and plant-folivore coevolutionary processes?. United States: N. p., 2016. Web. doi:10.1002/ece3.2206.
Rivas-Ubach, Albert, Hódar, José A., Sardans, Jordi, Kyle, Jennifer E., Kim, Young-Mo, Oravec, Michal, Urban, Otmar, Guenther, Alex, & Peñuelas, Josep. Are the metabolomic responses to folivory of closely related plant species linked to macroevolutionary and plant-folivore coevolutionary processes?. United States. doi:10.1002/ece3.2206.
Rivas-Ubach, Albert, Hódar, José A., Sardans, Jordi, Kyle, Jennifer E., Kim, Young-Mo, Oravec, Michal, Urban, Otmar, Guenther, Alex, and Peñuelas, Josep. 2016. "Are the metabolomic responses to folivory of closely related plant species linked to macroevolutionary and plant-folivore coevolutionary processes?". United States. doi:10.1002/ece3.2206.
@article{osti_1326144,
title = {Are the metabolomic responses to folivory of closely related plant species linked to macroevolutionary and plant-folivore coevolutionary processes?},
author = {Rivas-Ubach, Albert and Hódar, José A. and Sardans, Jordi and Kyle, Jennifer E. and Kim, Young-Mo and Oravec, Michal and Urban, Otmar and Guenther, Alex and Peñuelas, Josep},
abstractNote = {The debate whether the coevolution of plants and insects or macroevolutionary processes (phylogeny) is the main driver determining the arsenal of molecular defensive compounds of plants remains unresolved. Attacks by herbivorous insects affect not only the composition of defensive compounds in plants but the entire metabolome (the set of molecular metabolites), including defensive compounds. Metabolomes are the final products of genotypes and are directly affected by macroevolutionary processes, so closely related species should have similar metabolomic compositions and may respond in similar ways to attacks by folivores. We analyzed the elemental compositions and metabolomes of needles from Pinus pinaster, P. nigra and P. sylvestris to determine if these closely related Pinus species with different coevolutionary histories with the caterpillars of the processionary moth respond similarly to attacks by this lepidopteran. All pines had different metabolomes and metabolic responses to herbivorous attack. The metabolomic variation among the pine species and the responses to folivory reflected their macroevolutionary relationships, with P. pinaster having the most divergent metabolome. The concentrations of phenolic metabolites were generally not higher in the attacked trees, which had lower concentrations of terpenes, suggesting that herbivores avoid individuals with high concentrations of terpenes. Our results suggest that macroevolutionary history plays important roles in the metabolomic responses of these pine species to folivory, but plant-insect coevolution probably constrains those responses. Combinations of different evolutionary factors and trade-offs are likely responsible for the different responses of each species to folivory, which is not necessarily exclusively linked to plant-insect coevolution.},
doi = {10.1002/ece3.2206},
journal = {Ecology and Evolution},
number = 13,
volume = 6,
place = {United States},
year = 2016,
month = 6
}
  • Plants respond locally and systemically to herbivore attack. Most of the research conducted on plant-herbivore relationships at elemental and molecular levels have focused on nutrients or/and certain molecular compounds or specific families of defensive metabolites showing that herbivores tend to select plant individuals or species with higher nutrient concentrations and to avoid those with higher levels of phenolics and terpenes. Unfortunately, the defensive role of phenolics in conifers is still unclear. We performed stoichiometric and metabolomics, local and systemic, analyses in two subspecies of Pinus sylvestris under the herbivorous attack by the caterpillars of the pine processionary moth, an importantmore » pest in the Mediterranean Basin. Herbivorous attack was not associated with any of the elements analyzed. Both pine subspecies responded locally to folivory mainly by increasing the concentrations of various terpenes and phenolics. Systemic responses differed between subspecies and most of the metabolites presented intermediate concentrations between those of the affected parts and unattacked trees. Contrary as usually thought, foliar nutrient concentrations did not show to be a main factor of an alleged plant selection by adult female processionary moths for oviposition. Local increases in phenolics were more associated with antioxidant function for protection against oxidative damage produced by folivory. On the other hand, terpenes were directly related to defense against herbivores. Herbivory attack produced a general systemic shift in pines, including both primary and secondary metabolisms, that was, however, less intense and chemically different from the local responses. Subspecies responded similarly locally but differently to folivory at systemic level.« less
  • The metabolome, the chemical phenotype of an organism, should be shaped by evolution. Metabolomes depend on genetic composition and expression, which can be sources of evolutionary inertia, so most aspects of metabolomes should be similar in closely related sympatric species. We examined the metabolomes of two sympatric subspecies of Pinus sylvestris in Sierra Nevada (southern Iberian Peninsula), one introduced (ssp. iberica) and one autochthonous (ssp. nevadensis), in summer and winter and exposed to folivory by the pine processionary moth. The overall metabolomes differed between the subspecies but both tended to respond more similarly to folivory. The metabolomes of the subspeciesmore » were more dissimilar in summer than in winter, and iberica trees had higher concentrations of metabolites directly related to drought stress. Our results suggest that certain plant metabolic responses associated with folivory have been conserved throughout evolutionary history. The larger divergence between subspecies metabolomes in summer is likely due to the warmer and drier conditions that the northern iberica subspecies experience in Sierra Nevada. Our results provide crucial insights into how iberica populations would respond to the predicted conditions of climate change under an increased defoliation, two recent severe issues in the Mediterranean Basin.« less
  • Specific human subtelomeric DNA probes were used to reveal cryptic chromosomal rearrangements that cannot be detected by conventional high resolution cytogenetic techniques, or by chromosomal in situ suppression hybridization using whole chromosome paint analysis. Two cosmids containing different subtelomeric DNA sequences were derived from human chromosome 19 and designated as 7501 and 16432. Cosmid 7501 was hybridized to chromosomes from humans, chimpanzee, gorilla and orangutan. In humans, 7501 consistently labeled chromosomes 3q, 15q, and 19p. Additional chromosomes were labeled in different individuals, indicating a polymorphic distribution of this sequence in the human genome. In contrast, 7501 consistently and strongly labeledmore » only the q arm terminus of chromosome 3 in both chimp and gorilla. The identification of the chromosome was made by two-color FISH analysis using human chromosome 4-specific paint and homologous to human chromosome 4. None of the human subjects showed labeling of chromosome 4 with 7501. This finding suggests that in the course of human evolution, subsequent to the divergence of humans and African apes, a cryptic translocation occurred between the ancestral human chromosome 4 and one or more of the other human chromosomes that now contain this DNA segment. In orangutan, 7501 labeled a single acrocentric chromosome pair, a distinctly different chromosome than that labeled in chimp and gorilla. Comparison of chromosome sites labeled with cosmid 16432 showed the distribution of signals on chromosome 1q arm is the same for humans and chimp, but different in the gorilla. Humans and chimps show distinct labeling on sites 1q terminus and 1q41-42. In gorilla, there is instead a large cluster of intense signal near the terminus of 1q that clearly does not extend all the way to the terminus. A paracentric inversion or an unequal cross-over event may account for the observed difference between these species.« less