Phenolics lie at the centre of functional versatility in the responses of two phytochemically diverse tropical trees to canopy thinning

Schneider, Gerald F.; Coley, Phyllis D.; Younkin, Gordon C.; Forrister, Dale L.; Mills, Anthony G.; Kursar, Thomas A.

doi:10.1093/jxb/erz308

Title: Phenolics lie at the centre of functional versatility in the responses of two phytochemically diverse tropical trees to canopy thinning

Journal Article · 28 June 2019 · Journal of Experimental Botany

DOI: https://doi.org/10.1093/jxb/erz308 · OSTI ID:1625390

^[1];

^[1]; Younkin, Gordon C. ^[2]; Forrister, Dale L. ^[2]; Mills, Anthony G. ^[2]; Kursar, Thomas A. ^[1]

Univ. of Utah, Salt Lake City, UT (United States); Smithsonian Tropical Research Institute, Panama City (Panama)
Univ. of Utah, Salt Lake City, UT (United States)

Saplings in the shade of the tropical understorey face the challenge of acquiring sufficient carbon for growth as well as defence against intense pest pressure. A minor increase in light availability via canopy thinning may allow for increased investment in chemical defence against pests, but it may also necessitate additional biochemical investment to prevent light-induced oxidative stress. The shifts in secondary metabolite composition that increased sun exposure may precipitate in such tree species present an ideal milieu for evaluating the potential of a single suite of phenolic secondary metabolites to be used in mitigating both abiotic and biotic stressors. To conduct such an evaluation, we exposed saplings of two unrelated species to a range of light environments and compared changes in their foliar secondary metabolome alongside corresponding changes in the abiotic and biotic activity of their secondary metabolite suites. Among the numerous classes of secondary metabolites found in both species, phenolics accounted for the majority of increases in antioxidant and UV-absorbing properties as well as activity against an invertebrate herbivore and a fungal pathogen. Our results support the hypothesis that phenolics contribute to the capacity of plants to resist co-occurring abiotic and biotic stressors in resource-limited conditions.

View Accepted Manuscript (DOE)

Cite

Export

Save

Research Organization:: Univ. of Utah, Salt Lake City, UT (United States)

Sponsoring Organization:: USDOE Office of Science (SC); National Science Foundation (NSF); USEPA

Grant/Contract Number:: 1148698; DEB-1405637; DEB-1135733; F13F31245

OSTI ID:: 1625390

Journal Information:: Journal of Experimental Botany, Vol. 70, Issue 20; ISSN 0022-0957

Publisher:: Oxford University PressCopyright Statement

Country of Publication:: United States

Language:: English

References (51)

Multiple functional roles of flavonoids in photoprotection: Letters Agati, Giovanni; Tattini, Massimiliano New Phytologist, Vol. 186, Issue 4 https://doi.org/10.1111/j.1469-8137.2010.03269.x	journal	May 2010
Functional roles of flavonoids in photoprotection: New evidence, lessons from the past Agati, Giovanni; Brunetti, Cecilia; Di Ferdinando, Martina Plant Physiology and Biochemistry, Vol. 72 https://doi.org/10.1016/j.plaphy.2013.03.014	journal	November 2013
Competitive fragmentation modeling of ESI-MS/MS spectra for putative metabolite identification Allen, Felicity; Greiner, Russ; Wishart, David Metabolomics, Vol. 11, Issue 1 https://doi.org/10.1007/s11306-014-0676-4	journal	June 2014
Metabolomics as a Tool to Investigate Abiotic Stress Tolerance in Plants Arbona, Vicent; Manzi, Matías; Ollas, Carlos International Journal of Molecular Sciences, Vol. 14, Issue 3 https://doi.org/10.3390/ijms14034885	journal	March 2013
Light environment and the impacts of foliage quality on herbivorous insect attack and bird predation Barber, Nicholas A.; Marquis, Robert J. Oecologia, Vol. 166, Issue 2 https://doi.org/10.1007/s00442-010-1840-9	journal	November 2010
The Distribution of Fruit and Seed Toxicity during Development for Eleven Neotropical Trees and Vines in Central Panama Beckman, Noelle G. PLoS ONE, Vol. 8, Issue 7 https://doi.org/10.1371/journal.pone.0066764	journal	July 2013
Secondary metabolites in plant defence mechanisms Bennett, Richard N.; Wallsgrove, Roger M. New Phytologist, Vol. 127, Issue 4 https://doi.org/10.1111/j.1469-8137.1994.tb02968.x	journal	August 1994
Is extrafloral nectar production induced by herbivores or ants in a tropical facultative ant–plant mutualism? Bixenmann, R. J.; Coley, P. D.; Kursar, T. A. Oecologia, Vol. 165, Issue 2 https://doi.org/10.1007/s00442-010-1787-x	journal	September 2010
High herbivore pressure favors constitutive over induced defense Bixenmann, Ryan J.; Coley, Phyllis D.; Weinhold, Alexander Ecology and Evolution, Vol. 6, Issue 17 https://doi.org/10.1002/ece3.2208	journal	July 2016
Contribution of hydroxycinnamates and flavonoids to epidermal shielding of UV-A and UV-B radiation in developing rye primary leaves as assessed by ultraviolet-induced chlorophyll fluorescence measurements Burchard, P.; Bilger, W.; Weissenbock, G. Plant, Cell and Environment, Vol. 23, Issue 12 https://doi.org/10.1046/j.1365-3040.2000.00633.x	journal	December 2000
Antioxidant activities of six natural phenolics against lipid oxidation induced by Fe²⁺or ultraviolet light Chen, Xiaoying; Ahn, Dong U. Journal of the American Oil Chemists' Society, Vol. 75, Issue 12 https://doi.org/10.1007/s11746-998-0322-2	journal	December 1998
Herbivory and Plant Defenses in Tropical Forests Coley, P. D.; Barone, J. A. Annual Review of Ecology and Systematics, Vol. 27, Issue 1 https://doi.org/10.1146/annurev.ecolsys.27.1.305	journal	November 1996
Artefacts of the pot environment on soil nutrient availability: implications for the interpretation of ecological studies Dalling, J. W.; Winter, K.; Andersen, K. M. Plant Ecology, Vol. 214, Issue 2 https://doi.org/10.1007/s11258-013-0172-3	journal	January 2013
Propagating annotations of molecular networks using in silico fragmentation da Silva, Ricardo R.; Wang, Mingxun; Nothias, Louis-Félix PLOS Computational Biology, Vol. 14, Issue 4 https://doi.org/10.1371/journal.pcbi.1006089	journal	April 2018
Divergent evolution in antiherbivore defences within species complexes at a single Amazonian site Endara, María-José; Weinhold, Alexander; Cox, James E. Journal of Ecology, Vol. 103, Issue 5 https://doi.org/10.1111/1365-2745.12431	journal	June 2015
Identification of phenolic compounds in isolated vacuoles of the medicinal plant Catharanthus roseus and their interaction with vacuolar class III peroxidase: an H2O2 affair? Ferreres, Federico; Figueiredo, Raquel; Bettencourt, Sara Journal of Experimental Botany, Vol. 62, Issue 8 https://doi.org/10.1093/jxb/erq458	journal	February 2011
Solar UV‐B and visible radiation in tropical forest gaps: measurements partitioning direct and diffuse radiation Flint, Stephan D.; Caldwell, Martyn M. Global Change Biology, Vol. 4, Issue 8 https://doi.org/10.1046/j.1365-2486.1998.00191.x	journal	December 1998
Energy dissipation and radical scavenging by the plant phenylpropanoid pathway Grace, Stephen C.; Logan, Barry A. Philosophical Transactions of the Royal Society of London. Series B: Biological Sciences, Vol. 355, Issue 1402 https://doi.org/10.1098/rstb.2000.0710	journal	October 2000
A survey of antifungal compounds from higher plants, 1982–1993 Grayer, Renée J.; Harborne, Jeffrey B. Phytochemistry, Vol. 37, Issue 1 https://doi.org/10.1016/0031-9422(94)85005-4	journal	January 1994
Use of Natural Products as Chemical Library for Drug Discovery and Network Pharmacology Gu, Jiangyong; Gui, Yuanshen; Chen, Lirong PLoS ONE, Vol. 8, Issue 4 https://doi.org/10.1371/journal.pone.0062839	journal	April 2013
MetaboLights—an open-access general-purpose repository for metabolomics studies and associated meta-data Haug, Kenneth; Salek, Reza M.; Conesa, Pablo Nucleic Acids Research, Vol. 41, Issue D1 https://doi.org/10.1093/nar/gks1004	journal	October 2012
Metabolomic analysis of the interaction between plants and herbivores Jansen, Jeroen J.; Allwood, J. William; Marsden-Edwards, Emma Metabolomics, Vol. 5, Issue 1 https://doi.org/10.1007/s11306-008-0124-4	journal	August 2008
Higher plants and UV-B radiation: balancing damage, repair and acclimation Jansen, Marcel A. K.; Gaba, Victor; Greenberg, Bruce M. Trends in Plant Science, Vol. 3, Issue 4 https://doi.org/10.1016/S1360-1385(98)01215-1	journal	April 1998
Effects of Natural Intensities of Visible and Ultraviolet Radiation on Epidermal Ultraviolet Screening and Photosynthesis in Grape Leaves Kolb, Christiane A.; Käser, Martin A.; Kopecký, Jiri Plant Physiology, Vol. 127, Issue 3 https://doi.org/10.1104/pp.010373	journal	November 2001
Regulation of Woody Plant Secondary Metabolism by Resource Availability: Hypothesis Testing by Means of Meta-Analysis Koricheva, Julia; Larsson, Stig; Haukioja, Erkki Oikos, Vol. 83, Issue 2 https://doi.org/10.2307/3546833	journal	November 1998
CAMERA: An Integrated Strategy for Compound Spectra Extraction and Annotation of Liquid Chromatography/Mass Spectrometry Data Sets Kuhl, Carsten; Tautenhahn, Ralf; Böttcher, Christoph Analytical Chemistry, Vol. 84, Issue 1 https://doi.org/10.1021/ac202450g	journal	December 2011
Arabidopsis Mutants Lacking Phenolic Sunscreens Exhibit Enhanced Ultraviolet-B Injury and Oxidative Damage Landry, L. G.; Chapple, Ccs.; Last, R. L. Plant Physiology, Vol. 109, Issue 4 https://doi.org/10.1104/pp.109.4.1159	journal	December 1995
Plant Phenolics: An Ecological Perspective Levin, Donald A. The American Naturalist, Vol. 105, Issue 942 https://doi.org/10.1086/282712	journal	March 1971
The Shikimate Pathway and Aromatic Amino Acid Biosynthesis in Plants Maeda, Hiroshi; Dudareva, Natalia Annual Review of Plant Biology, Vol. 63, Issue 1 https://doi.org/10.1146/annurev-arplant-042811-105439	journal	June 2012
Seasonal and habitat differences affect the impact of food and predation on herbivores: a comparison between gaps and understory of a tropical forest Richards, Lora A.; Coley, Phyllis D. Oikos, Vol. 116, Issue 1 https://doi.org/10.1111/j.2006.0030-1299.15043.x	journal	November 2006
Dose-Response Analysis Using R Ritz, Christian; Baty, Florent; Streibig, Jens C. PLOS ONE, Vol. 10, Issue 12 https://doi.org/10.1371/journal.pone.0146021	journal	December 2015
Flavonoids and UV Photoprotection in Arabidopsis Mutants Ryan, Ken G.; Swinny, Ewald E.; Winefield, Chris Zeitschrift für Naturforschung C, Vol. 56, Issue 9-10 https://doi.org/10.1515/znc-2001-9-1013	journal	October 2001
Herbivory on Temperate Rainforest Seedlings in Sun and Shade: Resistance, Tolerance and Habitat Distribution Salgado-Luarte, Cristian; Gianoli, Ernesto PLoS ONE, Vol. 5, Issue 7 https://doi.org/10.1371/journal.pone.0011460	journal	July 2010
Sources of variation in foliar secondary chemistry in a tropical forest tree community Sedio, Brian E.; Rojas Echeverri, Juan C.; Boya P., Cristopher A. Ecology, Vol. 98, Issue 3 https://doi.org/10.1002/ecy.1689	journal	March 2017
Cytoscape: A Software Environment for Integrated Models of Biomolecular Interaction Networks Shannon, P. Genome Research, Vol. 13, Issue 11 https://doi.org/10.1101/gr.1239303	journal	November 2003
Do the antiherbivore traits of expanding leaves in the Neotropical tree Inga paraensis (Fabaceae) vary with light availability? Sinimbu, G.; Coley, P. D.; Lemes, M. R. Oecologia, Vol. 170, Issue 3 https://doi.org/10.1007/s00442-012-2353-5	journal	May 2012
XCMS: Processing Mass Spectrometry Data for Metabolite Profiling Using Nonlinear Peak Alignment, Matching, and Identification Smith, Colin A.; Want, Elizabeth J.; O'Maille, Grace Analytical Chemistry, Vol. 78, Issue 3 https://doi.org/10.1021/ac051437y	journal	February 2006
A peroxidase/phenolics/ascorbate system can scavenge hydrogen peroxide in plant cells Takahama, Umeo; Oniki, Takayuki Physiologia Plantarum, Vol. 101, Issue 4 https://doi.org/10.1111/j.1399-3054.1997.tb01072.x	journal	December 1997
Sharing and community curation of mass spectrometry data with Global Natural Products Social Molecular Networking Wang, Mingxun; Carver, Jeremy J.; Phelan, Vanessa V. Nature Biotechnology, Vol. 34, Issue 8 https://doi.org/10.1038/nbt.3597	journal	August 2016
Quantitative and qualitative shifts in defensive metabolites define chemical defense investment during leaf development inInga, a genus of tropical trees Wiggins, Natasha L.; Forrister, Dale L.; Endara, María‐José Ecology and Evolution, Vol. 6, Issue 2 https://doi.org/10.1002/ece3.1896	journal	January 2016
Data from: Phenolics lie at the center of functional versatility in the responses of two phytochemically diverse tropical trees to canopy thinning Schneider, Gerald F.; Coley, Phyllis D.; Younkin, Gordon C. Dryad https://doi.org/10.5061/dryad.t469v60	dataset	January 2020
Data from: Phenolics lie at the center of functional versatility in the responses of two phytochemically diverse tropical trees to canopy thinning Schneider, Gerald F.; Coley, Phyllis D.; Younkin, Gordon C. Dryad https://doi.org/10.5061/dryad.t469v60	dataset	January 2020
Competitive fragmentation modeling of ESI-MS/MS spectra for putative metabolite identification Allen, Felicity; Greiner, Russ; Wishart, David Metabolomics, Vol. 11, Issue 1 https://doi.org/10.1007/s11306-014-0676-4	journal	June 2014
Hydrogen peroxide scavenging systems in vacuoles of mesophyll cells of Vicia faba Takahama, Umeo Phytochemistry, Vol. 31, Issue 4 https://doi.org/10.1016/0031-9422(92)80246-b	journal	April 1992
Cytoscape: A Software Environment for Integrated Models of Biomolecular Interaction Networks Shannon, P. Genome Research, Vol. 13, Issue 11 https://doi.org/10.1101/gr.1239303	journal	November 2003
Arabidopsis Mutants Lacking Phenolic Sunscreens Exhibit Enhanced Ultraviolet-B Injury and Oxidative Damage Landry, L. G.; Chapple, Ccs.; Last, R. L. Plant Physiology, Vol. 109, Issue 4 https://doi.org/10.1104/pp.109.4.1159	journal	December 1995
Secondary metabolites in plant defence mechanisms Bennett, Richard N.; Wallsgrove, Roger M. New Phytologist, Vol. 127, Issue 4 https://doi.org/10.1111/j.1469-8137.1994.tb02968.x	journal	August 1994
Multiple functional roles of flavonoids in photoprotection: Letters Agati, Giovanni; Tattini, Massimiliano New Phytologist, Vol. 186, Issue 4 https://doi.org/10.1111/j.1469-8137.2010.03269.x	journal	May 2010
The Shikimate Pathway and Aromatic Amino Acid Biosynthesis in Plants Maeda, Hiroshi; Dudareva, Natalia Annual Review of Plant Biology, Vol. 63, Issue 1 https://doi.org/10.1146/annurev-arplant-042811-105439	journal	June 2012
Flavonoids and UV Photoprotection in Arabidopsis Mutants Ryan, Ken G.; Swinny, Ewald E.; Winefield, Chris Zeitschrift für Naturforschung C, Vol. 56, Issue 9-10 https://doi.org/10.1515/znc-2001-9-1013	journal	October 2001
Metabolomics as a Tool to Investigate Abiotic Stress Tolerance in Plants Arbona, Vicent; Manzi, Matías; Ollas, Carlos International Journal of Molecular Sciences, Vol. 14, Issue 3 https://doi.org/10.3390/ijms14034885	journal	March 2013

Cited By (2)

Data from: Phenolics lie at the center of functional versatility in the responses of two phytochemically diverse tropical trees to canopy thinning Schneider, Gerald F.; Coley, Phyllis D.; Younkin, Gordon C. Dryad https://doi.org/10.5061/dryad.t469v60	dataset	January 2020
Data from: Phenolics lie at the center of functional versatility in the responses of two phytochemically diverse tropical trees to canopy thinning Schneider, Gerald F.; Coley, Phyllis D.; Younkin, Gordon C. Dryad https://doi.org/10.5061/dryad.t469v60	dataset	January 2020

Similar Records

Similar local, but different systemic, metabolomics responses of closely related pine subspecies to folivory by caterpillars of the processionary moth

Journal Article · 2016 · Plant Biology, 18(3):484-494 · OSTI ID:1259940

Rivas-Ubach, A.; Sardans, J.; Hódar, J. A.; +6 more

Plant myo-inositol transport influences bacterial colonization phenotypes

Journal Article · 2023 · Current Biology · OSTI ID:1988343

O’Banion, Bridget S.; Jones, Piet; Demetros, Alexander A.; +8 more

Potential biological control agents of Geosmithia morbida restrict fungal pathogen growth via mycoparasitism and antibiosis

Journal Article · 2024 · Biocontrol · OSTI ID:2428020

Onufrak, Aaron J.; Gazis, Romina; Gwinn, Kimberly; +8 more

Related Subjects

59 BASIC BIOLOGICAL SCIENCES
plant sciences
abiotic stress
biotic stress
chemical defence
light environment
metabolomics
multiple stressors
secondary metabolites
sunflecks
tropical forest
UV radiation

Title: Phenolics lie at the centre of functional versatility in the responses of two phytochemically diverse tropical trees to canopy thinning

Citation Formats

References (51)

Cited By (2)

Linked Research (1)

Similar Records

Related Subjects