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Genes, enzymes and chemicals of terpenoid diversity in the constitutive and induced defence of conifers against insects and pathogens*
Author for correspondence: Jörg Bohlmann Tel: (604) 822 0282 Fax: (604) 822 2114 Email: bohlmann@msl.ubc.ca
*
Dedicated to the memory of Dr Vince R. Franceschi, pioneer researcher in conifer plant defence.
Abstract
Contents
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Summary 657
- I.
Introduction 658
- II.
Identification and functional characterization of terpenoid pathway genes 658
- III.
Insect interactions with conifers 667
- IV.
Conclusions and outlook 670
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Acknowledgements 671
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References 671
Summary
Insects select their hosts, but trees cannot select which herbivores will feed upon them. Thus, as long‐lived stationary organisms, conifers must resist the onslaught of varying and multiple attackers over their lifetime. Arguably, the greatest threats to conifers are herbivorous insects and their associated pathogens. Insects such as bark beetles, stem‐ and wood‐boring insects, shoot‐feeding weevils, and foliage‐feeding budworms and sawflies are among the most devastating pests of conifer forests. Conifer trees produce a great diversity of compounds, such as an enormous array of terpenoids and phenolics, that may impart resistance to a variety of herbivores and microorganisms. Insects have evolved to specialize in resistance to these chemicals – choosing, feeding upon, and colonizing hosts they perceive to be best suited to reproduction. This review focuses on the plant–insect interactions mediated by conifer‐produced terpenoids. To understand the role of terpenoids in conifer–insect interactions, we must understand how conifers produce the wide diversity of terpenoids, as well as understand how these specific compounds affect insect behaviour and physiology. This review examines what chemicals are produced, the genes and proteins involved in their biosynthesis, how they work, and how they are regulated. It also examines how insects and their associated pathogens interact with, elicit, and are affected by conifer‐produced terpenoids.
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- Carmen Díaz-Sala, José Antonio Cabezas, Brígida Fernández de Simón, Dolores Abarca, M. Ángeles Guevara, Marina de Miguel, Estrella Cadahía, Ismael Aranda and María-Teresa Cervera, The uniqueness of conifers, From Plant Genomics to Plant Biotechnology, 10.1533/9781908818478.67, (67-96), (2013).
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- María Fernanda López, Claudia Cano-Ramírez, Ana K. Cesar-Ayala, Enrico A. Ruiz and Gerardo Zúñiga, Diversity and expression of P450 genes from Dendroctonus valens LeConte (Curculionidae: Scolytinae) in response to different kairomones, Insect Biochemistry and Molecular Biology, 10.1016/j.ibmb.2013.02.004, 43, 5, (417-432), (2013).
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- Anne Caniard, Philipp Zerbe, Sylvain Legrand, Allison Cohade, Nadine Valot, Jean-Louis Magnard, Jörg Bohlmann and Laurent Legendre, Discovery and functional characterization of two diterpene synthases for sclareol biosynthesis in Salvia sclarea (L.) and their relevance for perfume manufacture, BMC Plant Biology, 10.1186/1471-2229-12-119, 12, 1, (119), (2012).
- Philipp Zerbe, Angela Chiang, Macaire Yuen, Björn Hamberger, Britta Hamberger, Jason A. Draper, Robert Britton and Jörg Bohlmann, Bifunctional cis -Abienol Synthase from Abies balsamea Discovered by Transcriptome Sequencing and Its Implications for Diterpenoid Fragrance Production , Journal of Biological Chemistry, 10.1074/jbc.M111.317669, 287, 15, (12121-12131), (2012).
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- František Kačík, Veronika Veľková, Pavel Šmíra, Andrea Nasswettrová, Danica Kačíková and Ladislav Reinprecht, Release of Terpenes from Fir Wood during Its Long-Term Use and in Thermal Treatment, Molecules, 17, 12, (9990), (2012).
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- Christopher I. Keeling and Jörg Bohlmann, Plant Terpenoids, Natural Products in Chemical Biology, (127-142), (2012).
- N. Erbilgin and L. J. Colgan, Differential effects of plant ontogeny and damage type on phloem and foliage monoterpenes in jack pine (Pinus banksiana), Tree Physiology, 32, 8, (946), (2012).
- Robert P. Adams and Jessica W. Wright, Alkanes and Terpenes in Wood and Leaves ofPinus jeffreyi and P. sabiniana, Journal of Essential Oil Research, 24, 5, (435), (2012).
- Carsten Külheim, Suat Hui Yeoh, Ian R. Wallis, Shawn Laffan, Gavin F. Moran and William J. Foley, The molecular basis of quantitative variation in foliar secondary metabolites in Eucalyptus globulus, New Phytologist, 191, 4, (1041-1053), (2011).
- Celia K. Boone, Brian H. Aukema, Jörg Bohlmann, Allan L. Carroll and Kenneth F. Raffa, Efficacy of tree defense physiology varies with bark beetle population density: a basis for positive feedback in eruptive species, Canadian Journal of Forest Research, 41, 6, (1174), (2011).
- Christopher I. Keeling, Lina L. Madilao, Philipp Zerbe, Harpreet K. Dullat and Jörg Bohlmann, The Primary Diterpene Synthase Products ofPicea abiesLevopimaradiene/Abietadiene Synthase (PaLAS) Are Epimers of a Thermally Unstable Diterpenol, Journal of Biological Chemistry, 286, 24, (21145), (2011).
- Inka Lusebrink, Maya L. Evenden, F. Guillaume Blanchet, Janice E. K. Cooke and Nadir Erbilgin, Effect of Water Stress and Fungal Inoculation on Monoterpene Emission from an Historical and a New Pine Host of the Mountain Pine Beetle, Journal of Chemical Ecology, 37, 9, (1013), (2011).
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- Christopher I Keeling, Sabrina Weisshaar, Steven G Ralph, Sharon Jancsik, Britta Hamberger, Harpreet K Dullat and Jörg Bohlmann, Transcriptome mining, functional characterization, and phylogeny of a large terpene synthase gene family in spruce (Picea spp.), BMC Plant Biology, 11, 1, (43), (2011).
- Feng Chen, Dorothea Tholl, Jörg Bohlmann and Eran Pichersky, The family of terpene synthases in plants: a mid‐size family of genes for specialized metabolism that is highly diversified throughout the kingdom, The Plant Journal, 66, 1, (212-229), (2011).
- Nate G. McDowell, David J. Beerling, David D. Breshears, Rosie A. Fisher, Kenneth F. Raffa and Mark Stitt, The interdependence of mechanisms underlying climate-driven vegetation mortality, Trends in Ecology & Evolution, 26, 10, (523), (2011).
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- G. Elsayed, Plant secondary substances and insects behaviour, Archives Of Phytopathology And Plant Protection, 44, 16, (1534), (2011).
- Alieta Eyles, Pierluigi Bonello, Rebecca Ganley and Caroline Mohammed, Induced resistance to pests and pathogens in trees, New Phytologist, 185, 4, (893-908), (2009).
- Jennifer M. Duringer, Laurence R. Swan, Douglas B. Walker and A. Morrie Craig, Acute aquatic toxicity of western juniper (Juniperus occidentalis) foliage and Port Orford cedar (Chamaecyparis lawsoniana) heartwood oils, Environmental Monitoring and Assessment, 10.1007/s10661-009-1259-0, 170, 1-4, (585-598), (2009).
- Katherine G. Zulak and Jörg Bohlmann, Terpenoid Biosynthesis and Specialized Vascular Cells of Conifer Defense, Journal of Integrative Plant Biology, 52, 1, (86-97), (2010).
- Jeanne A. Robert, Lufiani L. Madilao, Rick White, Alvin Yanchuk, John King and Jörg Bohlmann, Terpenoid metabolite profiling in Sitka spruce identifies association of dehydroabietic acid, (+)-3-carene, and terpinolene with resistance against white pine weevil, Botany, 88, 9, (810), (2010).
- Erin L. Clark, Allan L. Carroll and Dezene P.W. Huber, Differences in the constitutive terpene profile of lodgepole pine across a geographical range in British Columbia, and correlation with historical attack by mountain pine beetle, The Canadian Entomologist, 142, 06, (557), (2010).
- L. Safranyik, A.L. Carroll, J. Régnière, D.W. Langor, W.G. Riel, T.L. Shore, B. Peter, B.J. Cooke, V.G. Nealis and S.W. Taylor, Potential for range expansion of mountain pine beetle into the boreal forest of North America, The Canadian Entomologist, 142, 05, (415), (2010).
- Roland Mumm and Marcel Dicke, Variation in natural plant products and the attraction of bodyguards involved in indirect plant defenseThe present review is one in the special series of reviews on animal–plant interactions., Canadian Journal of Zoology, 10.1139/Z10-032, 88, 7, (628-667), (2010).
- Rose L. Andrew, Ian R. Wallis, Chris E. Harwood and William J. Foley, Genetic and environmental contributions to variation and population divergence in a broad-spectrum foliar defence of Eucalyptus tricarpa, Annals of Botany, 105, 5, (707), (2010).
- E. Leonard, P. K. Ajikumar, K. Thayer, W.-H. Xiao, J. D. Mo, B. Tidor, G. Stephanopoulos and K. L. J. Prather, Combining metabolic and protein engineering of a terpenoid biosynthetic pathway for overproduction and selectivity control, Proceedings of the National Academy of Sciences, 10.1073/pnas.1006138107, 107, 31, (13654-13659), (2010).
- Frank Bedon, Claude Bomal, Sébastien Caron, Caroline Levasseur, Brian Boyle, Shawn D. Mansfield, Axel Schmidt, Jonathan Gershenzon, Jacqueline Grima-Pettenati, Armand Séguin and John MacKay, Subgroup 4 R2R3-MYBs in conifer trees: gene family expansion and contribution to the isoprenoid- and flavonoid-oriented responses, Journal of Experimental Botany, 10.1093/jxb/erq196, 61, 14, (3847-3864), (2010).
- Tidiane Aw, Karen Schlauch, Christopher I Keeling, Sharon Young, Jeremy C Bearfield, Gary J Blomquist and Claus Tittiger, Functional genomics of mountain pine beetle (Dendroctonus ponderosae) midguts and fat bodies, BMC Genomics, 11, 1, (215), (2010).
- Tao Zhao, Paal Krokene, Niklas Björklund, Bo Långström, Halvor Solheim, Erik Christiansen and Anna-Karin Borg-Karlson, The influence of Ceratocystis polonica inoculation and methyl jasmonate application on terpene chemistry of Norway spruce, Picea abies, Phytochemistry, 71, 11-12, (1332), (2010).
- Rokneddin Albouyeh, Nima Farzaneh, Jörg Bohlmann and Kermit Ritland, Multivariate analysis of digital gene expression profiles identifies a xylem signature of the vascular tissue of white spruce (Picea glauca), Tree Genetics & Genomes, 6, 4, (601), (2010).
- Jullada Laothawornkitkul, Jane E. Taylor, Nigel D. Paul and C. Nicholas Hewitt, Biogenic volatile organic compounds in the Earth system, New Phytologist, 183, 1, (27-51), (2009).
- Joshua S. Yuan, Sari J. Himanen, Jarmo K. Holopainen, Feng Chen and C. Neal Stewart, Smelling global climate change: mitigation of function for plant volatile organic compounds, Trends in Ecology & Evolution, 10.1016/j.tree.2009.01.012, 24, 6, (323-331), (2009).
- Dustin N. Lippert, Steven G. Ralph, Michael Phillips, Rick White, Derek Smith, Darryl Hardie, Jonathan Gershenzon, Kermit Ritland, Christoph H. Borchers and Jörg Bohlmann, Quantitative iTRAQ proteome and comparative transcriptome analysis of elicitor‐induced Norway spruce () cells reveals elements of calcium signaling in the early conifer defense response, PROTEOMICS, 9, 2, (350-367), (2008).
- Nick Gould, Tony Reglinski, Grant L. Northcott, Mike Spiers and Joe T. Taylor, Physiological and biochemical responses in Pinus radiata seedlings associated with methyl jasmonate-induced resistance to Diplodia pinea, Physiological and Molecular Plant Pathology, 74, 2, (121), (2009).
- Elodie A. Courtois, C. E. Timothy Paine, Pierre-Alain Blandinieres, Didier Stien, Jean-Marie Bessiere, Emeline Houel, Christopher Baraloto and Jerome Chave, Diversity of the Volatile Organic Compounds Emitted by 55 Species of Tropical Trees: a Survey in French Guiana, Journal of Chemical Ecology, 35, 11, (1349), (2009).
- Thomas L. Eberhardt, Philip M. Sheridan and Jolie M. Mahfouz, Monoterpene persistence in the sapwood and heartwood of longleaf pine stumps: assessment of differences in composition and stability under field conditions, Canadian Journal of Forest Research, 39, 7, (1357), (2009).
- G.-i. Arimura, K. Matsui and J. Takabayashi, Chemical and Molecular Ecology of Herbivore-Induced Plant Volatiles: Proximate Factors and Their Ultimate Functions, Plant and Cell Physiology, 50, 5, (911), (2009).
- Fang-Hua Chu, Pei-Min Kuo, Yu-Rong Chen and Sheng-Yang Wang, Cloning and characterization of α-pinene synthase from Chamaecyparis formosensis Matsum, Holzforschung, 63, 1, (2009).
- G. Wang and R. A. Dixon, Heterodimeric geranyl(geranyl)diphosphate synthase from hop (Humulus lupulus) and the evolution of monoterpene biosynthesis, Proceedings of the National Academy of Sciences, 106, 24, (9914), (2009).
- L. G. Eckhardt, R. D. Menard and E. D. Gray, Effects of oleoresins and monoterpenes onin vitrogrowth of fungi associated with pine decline in the Southern United States, Forest Pathology, 39, 3, (157), (2009).
- Jacques Joyard, Myriam Ferro, Christophe Masselon, Daphné Seigneurin-Berny, Daniel Salvi, Jérôme Garin and Norbert Rolland, Chloroplast Proteomics and the Compartmentation of Plastidial Isoprenoid Biosynthetic Pathways, Molecular Plant, 2, 6, (1154), (2009).
- James D. Blande, Katariina Turunen and Jarmo K. Holopainen, Pine weevil feeding on Norway spruce bark has a stronger impact on needle VOC emissions than enhanced ultraviolet-B radiation, Environmental Pollution, 157, 1, (174), (2009).
- Anita Giglio, Pietro Brandmayr, Renato Dalpozzo, Giovanni Sindona, Antonio Tagarelli, Federica Talarico, Tullia Zetto Brandmayr and Enrico A. Ferrero, The defensive secretion ofCarabus lefebvreiDejean 1826 pupa (Coleoptera, Carabidae): Gland ultrastructure and chemical identification, Microscopy Research and Technique, 72, 5, (351), (2009).
- Wayra G. Navia-Giné, Joshua S. Yuan, Andy Mauromoustakos, J. Brad Murphy, Feng Chen and Kenneth L. Korth, Medicago truncatula (E)-β-ocimene synthase is induced by insect herbivory with corresponding increases in emission of volatile ocimene, Plant Physiology and Biochemistry, 47, 5, (416), (2009).
- Katherine G. Zulak, Dustin N. Lippert, Michael A. Kuzyk, Dominik Domanski, Tina Chou, Christoph H. Borchers and Jörg Bohlmann, Targeted proteomics using selected reaction monitoring reveals the induction of specific terpene synthases in a multi‐level study of methyl jasmonate‐treated Norway spruce (Picea abies), The Plant Journal, 60, 6, (1015-1030), (2009).
- Nina‐Alexandra Lehr, Silvia D. Schrey, Rüdiger Hampp and Mika T. Tarkka, Root inoculation with a forest soil streptomycete leads to locally and systemically increased resistance against phytopathogens in Norway spruce, New Phytologist, 177, 4, (965-976), (2007).
- ROLAND MUMM, MAARTEN A. POSTHUMUS and MARCEL DICKE, Significance of terpenoids in induced indirect plant defence against herbivorous arthropods, Plant, Cell & Environment, 31, 4, (575-585), (2008).
- C. Wallis, A. Eyles, R. Chorbadjian, B. McSpadden Gardener, R. Hansen, D. Cipollini, D. A. Herms and P. Bonello, Systemic induction of phloem secondary metabolism and its relationship to resistance to a canker pathogen in Austrian pine, New Phytologist, 177, 3, (767-778), (2007).
- Joshua S. Yuan, Tobias G. Köllner, Greg Wiggins, Jerome Grant, Jörg Degenhardt and Feng Chen, Molecular and genomic basis of volatile-mediated indirect defense against insects in rice, The Plant Journal, 55, 3, (491), (2008).
- C. I. Keeling, S. Weisshaar, R. P. C. Lin and J. Bohlmann, Functional plasticity of paralogous diterpene synthases involved in conifer defense, Proceedings of the National Academy of Sciences, 105, 3, (1085), (2008).
- Stefan Opitz, Grit Kunert and Jonathan Gershenzon, Increased Terpenoid Accumulation in Cotton (Gossypium hirsutum) Foliage is a General Wound Response, Journal of Chemical Ecology, 34, 4, (508), (2008).
- Kenneth F. Raffa, Brian H. Aukema, Barbara J. Bentz, Allan L. Carroll, Jeffrey A. Hicke, Monica G. Turner and William H. Romme, Cross-scale Drivers of Natural Disturbances Prone to Anthropogenic Amplification: The Dynamics of Bark Beetle Eruptions, BioScience, 58, 6, (501), (2008).
- Jay J. Emerick, Aaron I. Snyder, Nathan W. Bower and Marc A. Snyder, Mountain Pine Beetle Attack Associated with Low Levels of 4-Allylanisole in Ponderosa Pine, Environmental Entomology, 37, 4, (871), (2008).
- Christopher G. Jones, Christopher I. Keeling, Emilio L. Ghisalberti, Elizabeth L. Barbour, Julie A. Plummer and Jörg Bohlmann, Isolation of cDNAs and functional characterisation of two multi-product terpene synthase enzymes from sandalwood, Santalum album L., Archives of Biochemistry and Biophysics, 477, 1, (121), (2008).
- Diana Köpke, Roland Schröder, Hanna M. Fischer, Jonathan Gershenzon, Monika Hilker and Axel Schmidt, Does egg deposition by herbivorous pine sawflies affect transcription of sesquiterpene synthases in pine?, Planta, 228, 3, (427), (2008).
- Axel Schmidt and Jonathan Gershenzon, Cloning and characterization of two different types of geranyl diphosphate synthases from Norway spruce (Picea abies), Phytochemistry, 69, 1, (49), (2008).
- Susan D. Lawrence, Nicole G. Novak, Chelsea J.-T. Ju and Janice E.K. Cooke, Examining the molecular interaction between potato (Solanum tuberosum) and Colorado potato beetle Leptinotarsa decemlineata, Botany, 86, 9, (1080), (2008).
- Elena Ormeño, Virginie Baldy, Christine Ballini and Catherine Fernandez, Production and Diversity of Volatile Terpenes from Plants on Calcareous and Siliceous Soils: Effect of Soil Nutrients, Journal of Chemical Ecology, 34, 9, (1219), (2008).
- M. Aminul Islam, Rona N. Sturrock and Abul K.M. Ekramoddoullah, A proteomics approach to identify proteins differentially expressed in Douglas-fir seedlings infected by Phellinus sulphurascens, Journal of Proteomics, 10.1016/j.jprot.2008.06.004, 71, 4, (425-438), (2008).
- Sang-Min Kim, Yeon-Bok Kim, Tomohisa Kuzuyama and Soo-Un Kim, Two copies of 4-(cytidine 5′-diphospho)-2-C-methyl-d-erythritol kinase (CMK) gene in Ginkgo biloba: molecular cloning and functional characterization, Planta, 10.1007/s00425-008-0794-1, 228, 6, (941-950), (2008).
- Marie Pettersson, C. Rikard Unelius, Irena Valterová and Anna-Karin Borg-Karlson, Semiochemicals related to the aphid Cinara pilicornis and its host, Picea abies: A method to assign nepetalactone diastereomers, Journal of Chromatography A, 1180, 1-2, (165), (2008).
- Jörg Bohlmann and Christopher I. Keeling, Terpenoid biomaterials, The Plant Journal, 54, 4, (656-669), (2008).
- Victor Busov and Chung‐Jui Tsai, Perennial challenges and opportunities, New Phytologist, 176, 1, (3-6), (2007).
- Dustin Lippert, Sunita Chowrira, Steven Gregory Ralph, Jun Zhuang, Dana Aeschliman, Carol Ritland, Kermit Ritland and Jörg Bohlmann, Conifer defense against insects: Proteome analysis of Sitka spruce () bark induced by mechanical wounding or feeding by white pine weevils (), PROTEOMICS, 7, 2, (248-270), (2007).
- Kimberley-Ann Godard, Ashley Byun-McKay, Caroline Levasseur, Aine Plant, Armand Séguin and Jörg Bohlmann, Testing of a heterologous, wound- and insect-inducible promoter for functional genomics studies in conifer defense, Plant Cell Reports, 26, 12, (2083), (2007).
- M.J. Giertych, P. Karolewski, J. Grzebyta and J. Oleksyn, Feeding behavior and performance of Neodiprion sertifer larvae reared on Pinus sylvestris needles, Forest Ecology and Management, 242, 2-3, (700), (2007).
- Christopher I. Keeling and Jörg Bohlmann, Plant Terpenoids, Wiley Encyclopedia of Chemical Biology, (1-10), (2008).
- D. P. W. Huber, M. L. Erickson, C. M. Leutenegger, J. Bohlmann and S. J. Seybold, Isolation and extreme sex-specific expression of cytochrome P450 genes in the bark beetle, Ips paraconfusus, following feeding on the phloem of host ponderosa pine, Pinus ponderosa, Insect Molecular Biology, 16, 3, (335), (2007).
- Michael A. Phillips, Michael H. Walter, Steven G. Ralph, Paulina Dabrowska, Katrin Luck, Eva Maria Urós, Wilhelm Boland, Dieter Strack, Manuel Rodríguez-Concepción, Jörg Bohlmann and Jonathan Gershenzon, Functional identification and differential expression of 1-deoxy-d-xylulose 5-phosphate synthase in induced terpenoid resin formation of Norway spruce (Picea abies), Plant Molecular Biology, 65, 3, (243), (2007).
- Axel Schmidt and Jonathan Gershenzon, Cloning and characterization of isoprenyl diphosphate synthases with farnesyl diphosphate and geranylgeranyl diphosphate synthase activity from Norway spruce (Picea abies) and their relation to induced oleoresin formation, Phytochemistry, 68, 21, (2649), (2007).
- Michael Friedmann, Steven G. Ralph, Dana Aeschliman, Jun Zhuang, Kermit Ritland, Brian E. Ellis, Joerg Bohlmann and Carl J. Douglas, Microarray gene expression profiling of developmental transitions in Sitka spruce (Picea sitchensis) apical shoots, Journal of Experimental Botany, 58, 3, (593), (2007).
- Marcelo Carnier Dornelas and Paulo Mazzafera, A genomic approach to characterization of the Citrus terpene synthase gene family, Genetics and Molecular Biology, 30, 3 suppl, (832), (2007).
- Ryan N. Philippe and Jörg Bohlmann, Poplar defense against insect herbivoresThis review is one of a selection of papers published in the Special Issue on Poplar Research in Canada., Canadian Journal of Botany, 85, 12, (1111), (2007).
- Sang-Min Kim, Tomohisa Kuzuyama, Akio Kobayashi, Tomoki Sando, Yung-Jin Chang and Soo-Un Kim, 1-Hydroxy-2-methyl-2-(E)-butenyl 4-diphosphate reductase (IDS) is encoded by multicopy genes in gymnosperms Ginkgo biloba and Pinus taeda, Planta, 227, 2, (287), (2007).
- Christopher I. Keeling and Jörg Bohlmann, Diterpene resin acids in conifers, Phytochemistry, 67, 22, (2415), (2006).
- Natalia Dudareva, Florence Negre, Dinesh A. Nagegowda and Irina Orlova, Plant Volatiles: Recent Advances and Future Perspectives, Critical Reviews in Plant Sciences, 25, 5, (417), (2006).
- Michael A Phillips and Manuel Rodríguez Concepción, Terpenoids: Lower, eLS, (2010).
- Wanda Vélez-Carrasco, Carol E. Green, Paul Catz, Anna Furimsky, Kathleen O’Loughlin, Vesna A. Eterović, P. A. Ferchmin and Jinglu Ai, Pharmacokinetics and Metabolism of 4R-Cembranoid, PLOS ONE, 10.1371/journal.pone.0121540, 10, 3, (e0121540), (2015).
- Sibongile Mafu and Philipp Zerbe, Plant diterpenoid metabolism for manufacturing the biopharmaceuticals of tomorrow: prospects and challenges, Phytochemistry Reviews, 10.1007/s11101-017-9513-5, (2017).
- Vivek R. Yadav, Sahdeo Prasad, Bokyung Sung, Ramaswamy Kannappan and Bharat B. Aggarwal, Targeting Inflammatory Pathways by Triterpenoids for Prevention and Treatment of Cancer, Toxins, 10.3390/toxins2102428, 2, 10, (2428-2466), (2010).
- Daniel Flø, Hans Ragnar Norli, Bjørn Økland and Paal Krokene, Successful reproduction and pheromone production by the spruce bark beetle in evolutionary naïve spruce hosts with familiar terpenoid defences, Agricultural and Forest Entomology, , (2018).
- David T. Williams and Gillian Jonusas, The influence of tree species and edge effects on pheromone trap catches of oak processionary moth Thaumetopoea processionea (L.) in the U.K., Agricultural and Forest Entomology, , (2018).
