Intraspecific diversity of terpenes of Eucalyptus camaldulensis (Myrtaceae) at a continental scale
Carlos Bustos-Segura A B D , Shannon Dillon C , Andras Keszei A , William J. Foley A and Carsten Külheim A
+ Author Affiliations
- Author Affiliations
A Evolution, Ecology and Genetics Division, Research School of Biology, The Australian National University, Canberra, ACT 2601, Australia.
B Present address: Laboratory of Evolutive Entomology, Institute of Biology, University of Neuchâtel, Rue Emile-Argand 11, 2000 Neuchâtel, Switzerland.
C Genetic Diversity and Adaptation, CSIRO Agriculture, Bldg. 2/79, Canberra, ACT 2601, Australia.
D Corresponding author. Email: bustossc@gmail.com
Australian Journal of Botany 65(3) 257-269 https://doi.org/10.1071/BT16183
Submitted: 15 September 2016 Accepted: 6 April 2017 Published: 30 May 2017
Abstract
Plants show a high degree of intraspecific variation in several traits including plant secondary metabolites. This variation can be influenced by genetic and environmental factors that result in geographical structure in their distribution. By growing plants from several populations in a controlled environment, we studied variation in foliar terpenes in Eucalyptus camaldulensis, which is the widest distributed eucalypt, with a large range both latitudinally and longitudinally. We found that the concentration of terpenes is highly variable among subspecies. We identified four chemotypes dominated by 1,8-cineole, γ-terpinene, α- and β-phellandrene. While the 1,8-cineole chemotype is abundant in all populations, the other three chemotypes are rare in the central area and the north-east of Australia. The γ-terpinene chemotype is mainly restricted to the north and west of Australia, whereas the α- and β-phellandrene chemotypes show an opposite distribution in the north and south of the continent. The annual mean temperature and humidity of the source populations correlate with the abundance of the dominant terpenes. We also tested the effects of elevated CO2 concentrations on the terpene concentration and found that elevated CO2 atmosphere reduces the overall accumulation of foliar terpenes. The results suggest that variation in terpene composition in E. camaldulensis can be influenced by environmental variables, mainly favouring the 1,8-cineole chemotype in arid locations.
Additional keywords: chemotypes, elevated CO2, eucalyptus oil, geographical clines, phytochemical diversity, plant secondary metabolites.
References
Ali JG, Alborn HT, Stelinski LL (2010) Subterranean herbivore-induced volatiles released by citrus roots upon feeding by Diaprepes abbreviatus recruit entomopathogenic nematodes. Journal of Chemical Ecology 36, 361–368.| Subterranean herbivore-induced volatiles released by citrus roots upon feeding by Diaprepes abbreviatus recruit entomopathogenic nematodes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXkt12ru7g%3D&md5=920031ec3eefb41efa47d29cba6ee69bCAS |
Alonso WR, Croteau R (1991) Purification and characterization of the monoterpene cyclase γ-terpinene synthase from Thymus vulgaris. Archives of Biochemistry and Biophysics 286, 511–517.
| Purification and characterization of the monoterpene cyclase γ-terpinene synthase from Thymus vulgaris.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3MXitVahtrg%3D&md5=a7bf6bf88ae37dff50fcb6792e1bcf21CAS |
Andrew RL, Keszei A, Foley WJ (2013) Intensive sampling identifies previously unknown chemotypes, population divergence and biosynthetic connections among terpenoids in Eucalyptus tricarpa. Phytochemistry 94, 148–158.
| Intensive sampling identifies previously unknown chemotypes, population divergence and biosynthetic connections among terpenoids in Eucalyptus tricarpa.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXptlGktLw%3D&md5=a3c5137821826714d5e0b65d7d740979CAS |
Atlas of Living Australia (2015) ‘Atlas of Living Australia.’ Available at http://www.ala.org.au/. [Accessed 19 July 2015]
Bates D, Maechler M, Bolker B, Walker S (2015) Fitting linear mixed-effects models using lme4. Journal of Statistical Software 67, 1–48.
| Fitting linear mixed-effects models using lme4.Crossref | GoogleScholarGoogle Scholar |
Boland DJ, Brophy JJ, House APN (1991) ‘Eucalyptus leaf oils: use, chemistry, distillation and marketing.’ (Inkata Press: Melbourne)
Butcher PA, Otero A, McDonald MW, Moran GF (2002) Nuclear RFLP variation in Eucalyptus camaldulensis Dehnh. from northern Australia. Heredity 88, 402–412.
| Nuclear RFLP variation in Eucalyptus camaldulensis Dehnh. from northern Australia.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XksFSrs70%3D&md5=f81413aa29bfa9a5df7343c506674645CAS |
Butcher PA, McDonald MW, Bell JC (2009) Congruence between environmental parameters, morphology and genetic structure in Australia’s most widely distributed eucalypt, Eucalyptus camaldulensis. Tree Genetics & Genomes 5, 189–210.
| Congruence between environmental parameters, morphology and genetic structure in Australia’s most widely distributed eucalypt, Eucalyptus camaldulensis.Crossref | GoogleScholarGoogle Scholar |
Chang YT, Chu FH (2011) Molecular cloning and characterization of monoterpene synthases from Litsea cubeba (Lour.) Persoon. Tree Genetics & Genomes 7, 835–844.
| Molecular cloning and characterization of monoterpene synthases from Litsea cubeba (Lour.) Persoon.Crossref | GoogleScholarGoogle Scholar |
Close DC, Beadle CL (2003) The ecophysiology of foliar anthocyanin. Botanical Review 69, 149–161.
| The ecophysiology of foliar anthocyanin.Crossref | GoogleScholarGoogle Scholar |
Coley PD, Massa M, Lovelock CE, Winter K (2002) Effects of elevated CO2 on foliar chemistry of saplings of nine species of tropical tree. Oecologia 133, 62–69.
| Effects of elevated CO2 on foliar chemistry of saplings of nine species of tropical tree.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC2crgs1Cnsg%3D%3D&md5=3a38fac8ea0295d04a6d33f4377989edCAS |
Croteau R, Satterwhite DM, Wheeler CJ, Felton NM (1989) Biosynthesis of monoterpenes: stereochemistry of the enzymatic cyclizations of geranyl pyrophosphate to (+)-alpha-pinene and (–)-beta-pinene. The Journal of Biological Chemistry 264, 2075–2080.
De Frenne P, Graae BJ, Rodríguez-Sánchez F, Kolb A, Chabrerie O, Decocq G, De Kort H, De Schrijver A, Diekmann M, Eriksson O, Gruwez R, Hermy M, Lenoir J, Plue J, Coomes DA, Verheyen K (2013) Latitudinal gradients as natural laboratories to infer species’ responses to temperature. Journal of Ecology 101, 784–795.
| Latitudinal gradients as natural laboratories to infer species’ responses to temperature.Crossref | GoogleScholarGoogle Scholar |
Degenhardt J, Köllner TG, Gershenzon J (2009) Monoterpene and sesquiterpene synthases and the origin of terpene skeletal diversity in plants. Phytochemistry 70, 1621–1637.
| Monoterpene and sesquiterpene synthases and the origin of terpene skeletal diversity in plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhsVWls7bL&md5=3faf0fc8ca1857ef20c0fc0c94fda3eaCAS |
Dobzhansky T (1950) Evolution in the tropics. American Scientist 38, 209–221.
Edwards P, Wanjura W (1993) Selective herbivory by Christmas beetles in response to intraspecific variation in Eucalyptus terpenoids. Oecologia 95, 551–557.
| Selective herbivory by Christmas beetles in response to intraspecific variation in Eucalyptus terpenoids.Crossref | GoogleScholarGoogle Scholar |
Falara V, Akhtar TA, Nguyen TTH, Spyropoulou EA, Bleeker PM, Schauvinhold I, Matsuba Y, Bonini ME, Schilmiller AL, Last RL, Schuurink RC, Pichersky E (2011) The tomato terpene synthase gene family. Plant Physiology 157, 770–789.
| The tomato terpene synthase gene family.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhtlahu7fI&md5=f5d7502db445e9b4f4cd19660af5babaCAS |
Gershenzon J, Dudareva N (2007) The function of terpene natural products in the natural world. Nature Chemical Biology 3, 408–414.
| The function of terpene natural products in the natural world.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXms1SrsLc%3D&md5=9a7dbe4273bc10bab8ec6ed6f88ae1cdCAS |
Gherlenda AN, Haigh AM, Moore BD, Johnson SN, Riegler M (2015) Responses of leaf beetle larvae to elevated [CO2] and temperature depend on Eucalyptus species. Oecologia 177, 607–617.
| Responses of leaf beetle larvae to elevated [CO2] and temperature depend on Eucalyptus species.Crossref | GoogleScholarGoogle Scholar |
Heyworth CJ, Iason GR, Temperton V, Jarvis PG, Duncan AJ (1998) The effect of elevated CO2 concentration and nutrient supply on carbon-based plant secondary metabolites in Pinus sylvestris L. Oecologia 115, 344–350.
| The effect of elevated CO2 concentration and nutrient supply on carbon-based plant secondary metabolites in Pinus sylvestris L.Crossref | GoogleScholarGoogle Scholar | 1:STN:280:DC%2BC1czns12gtg%3D%3D&md5=3a56e326bf631564f4d2829b17475d66CAS |
Holeski LM, Keefover-Ring K, Bowers MD, Harnenz ZT, Lindroth RL (2013) Patterns of phytochemical variation in Mimulus guttatus (yellow monkeyflower). Journal of Chemical Ecology 39, 525–536.
| Patterns of phytochemical variation in Mimulus guttatus (yellow monkeyflower).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXlsVGku7o%3D&md5=9e1d80ddb05a10e9836bd369f05555afCAS |
IPCC (2013) ‘Climate change (2013: the physical science basis. Contribution of Working Group I to the fifth assessment report of the Intergovernmental Panel on Climate Change.’ (Eds TF Stocker, D Qin, G-K Plattner, M Tignor, SK Allen, J Boschung, A Nauels, Y Xia, V Bex, PM Midgley) (Cambridge University Press: Cambridge, UK)
Jaakola L, Hohtola A (2010) Effect of latitude on flavonoid biosynthesis in plants. Plant, Cell & Environment 33, 1239–1247.
Johnson RH, Lincoln DE (1991) Sagebrush carbon allocation patterns and grasshopper nutrition: the influence of CO2 enrichment and soil mineral limitation. Oecologia 87, 127–134.
| Sagebrush carbon allocation patterns and grasshopper nutrition: the influence of CO2 enrichment and soil mineral limitation.Crossref | GoogleScholarGoogle Scholar |
Kant MR, Bleeker PM, Van Wijk M, Schuurink RC, Haring MA (2009) Plant volatiles in defence. Advances in Botanical Research 51, 613–666.
| Plant volatiles in defence.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhs1Slsr3N&md5=71cb9a52f2a56c7f0fb352d05d41795fCAS |
Keszei A, Brubaker CL, Foley WJ (2008) A molecular perspective on terpene variation in Australian Myrtaceae. Australian Journal of Botany 56, 197–213.
| A molecular perspective on terpene variation in Australian Myrtaceae.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXmtV2ktL8%3D&md5=69af62be2eaa1ee6fe2f2a52b707b9b4CAS |
Keszei A, Brubaker CL, Carter R, Köllner T, Degenhardt J, Foley WJ (2010) Functional and evolutionary relationships between terpene synthases from Australian Myrtaceae. Phytochemistry 71, 844–852.
| Functional and evolutionary relationships between terpene synthases from Australian Myrtaceae.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXmtFersb4%3D&md5=e1a9e80add629ff45491f768e0fc70d1CAS |
Kleine S, Müller C (2011) Intraspecific plant chemical diversity and its relation to herbivory. Oecologia 166, 175–186.
| Intraspecific plant chemical diversity and its relation to herbivory.Crossref | GoogleScholarGoogle Scholar |
Külheim C, Yeoh SH, Wallis IR, Laffan S, Moran GF, Foley WJ (2011) The molecular basis of quantitative variation in foliar secondary metabolites in Eucalyptus globulus. New Phytologist 191, 1041–1053.
| The molecular basis of quantitative variation in foliar secondary metabolites in Eucalyptus globulus.Crossref | GoogleScholarGoogle Scholar |
Külheim C, Padovan A, Hefer C, Krause ST, Köllner TG, Myburg AA, Degenhardt J, Foley WJ (2015) The Eucalyptus terpene synthase gene family. BMC Genomics 16, 450
| The Eucalyptus terpene synthase gene family.Crossref | GoogleScholarGoogle Scholar |
Langsrud Y (2003) ANOVA for unbalanced data: use Type II instead of Type III sums of squares. Statistics and Computing 13, 163–167.
| ANOVA for unbalanced data: use Type II instead of Type III sums of squares.Crossref | GoogleScholarGoogle Scholar |
Lawler IR, Foley WJ, Woodrow IE, Cork SJ (1997) The effects of elevated CO2 atmospheres on the nutritional quality of eucalyptus foliage and its interaction with soil nutrient and light availability. Oecologia 109, 59–68.
| The effects of elevated CO2 atmospheres on the nutritional quality of eucalyptus foliage and its interaction with soil nutrient and light availability.Crossref | GoogleScholarGoogle Scholar |
Lawler I, Stapley J, Foley W, Eschler B (1999) Ecological example of conditioned flavor aversion in plant–herbivore interactions: effect of terpenes of Eucalyptus leaves on feeding by common ringtail and brushtail possums. Journal of Chemical Ecology 25, 401–415.
| Ecological example of conditioned flavor aversion in plant–herbivore interactions: effect of terpenes of Eucalyptus leaves on feeding by common ringtail and brushtail possums.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXht1CjtL8%3D&md5=7e8cc6e6dcff8704744e406f2ed54708CAS |
Levin DA (1976) Alkaloid-bearing plants: an ecogeographic perspective. American Naturalist 110, 261–284.
| Alkaloid-bearing plants: an ecogeographic perspective.Crossref | GoogleScholarGoogle Scholar |
Liaw E-T, Liu K-J (2010) Synthesis of terpinyl acetate by lipase-catalyzed esterification in supercritical carbon dioxide. Bioresource Technology 101, 3320–3324.
| Synthesis of terpinyl acetate by lipase-catalyzed esterification in supercritical carbon dioxide.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhvFyjsLg%3D&md5=aa67e0a56fc73ad8a810e0c43b850033CAS |
McDonald MW, Brooker MIH, Butcher PA (2009) A taxonomic revision of Eucalyptus camaldulensis (Myrtaceae). Australian Systematic Botany 22, 257–285.
| A taxonomic revision of Eucalyptus camaldulensis (Myrtaceae).Crossref | GoogleScholarGoogle Scholar |
McKiernan AB, O’Reilly-Wapstra JM, Price C, Davies NW, Potts BM, Hovenden MJ (2012) Stability of plant defensive traits among populations in two Eucalyptus species under elevated carbon dioxide. Journal of Chemical Ecology 38, 204–212.
| Stability of plant defensive traits among populations in two Eucalyptus species under elevated carbon dioxide.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC38Xjt1agtbw%3D&md5=6c705a2e322d6c2b5afc1b54e1a7c480CAS |
Misra BB, Chen S (2015) Advances in understanding CO2 responsive plant metabolomes in the era of climate change. Metabolomics 11, 1478–1491.
| Advances in understanding CO2 responsive plant metabolomes in the era of climate change.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2MXhtV2hs7nM&md5=93c8d6bdbe8f34ac75647976346e3480CAS |
Moles AT, Bonser SP, Poore AGB, Wallis IR, Foley WJ (2011a) Assessing the evidence for latitudinal gradients in plant defence and herbivory. Functional Ecology 25, 380–388.
| Assessing the evidence for latitudinal gradients in plant defence and herbivory.Crossref | GoogleScholarGoogle Scholar |
Moles AT, Wallis IR, Foley WJ, Warton DI, Stegen JC, Bisigato AJ, Cella-Pizarro L, Clark CJ, Cohen PS, Cornwell WK, Edwards W, Ejrnæs R, Gonzales-Ojeda T, Graae BJ, Hay G, Lumbwe FC, Magaña-Rodríguez B, Moore BD, Peri PL, Poulsen JR, Veldtman R, von Zeipel H, Andrew NR, Boulter SL, Borer ET, Campón FF, Coll M, Farji-Brener AG, de Gabriel J, Jurado E, Kyhn LA, Low B, Mulder CPH, Reardon-Smith K, Rodríguez-Velázquez J,, Seabloom EW, Vesk PA, van Cauter A, Waldram MS, Zheng Z, Blendinger PG, Enquist BJ, Facelli JM, Knight T, Majer JD, Martínez-Ramos M, McQuillan P, Prior LD (2011b) Putting plant resistance traits on the map: a test of the idea that plants are better defended at lower latitudes. New Phytologist 191, 777–788.
| Putting plant resistance traits on the map: a test of the idea that plants are better defended at lower latitudes.Crossref | GoogleScholarGoogle Scholar |
Moore BD, Andrew RL, Külheim C, Foley WJ (2014) Explaining intraspecific diversity in plant secondary metabolites in an ecological context. New Phytologist 201, 733–750.
| Explaining intraspecific diversity in plant secondary metabolites in an ecological context.Crossref | GoogleScholarGoogle Scholar |
Moudachirou M, Gbénou JD, Chalchat JC, Chabard JL, Lartigue C (1999) Chemical composition of essential oils of Eucalyptus from Bénin: Eucalyptus citriodora and E. camaldulensis. Influence of location, harvest time, storage of plants and time of steam distillation. Journal of Essential Oil Research 11, 109–118.
| Chemical composition of essential oils of Eucalyptus from Bénin: Eucalyptus citriodora and E. camaldulensis. Influence of location, harvest time, storage of plants and time of steam distillation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1MXhtlyhu7c%3D&md5=854635d6487c25e358bc0dbe86c9a054CAS |
O’Callaghan S, De Souza DP, Isaac A, Wang Q, Hodkinson L, Olshansky M, Erwin T, Appelbe B, Tull DL, Roessner U, Bacic A, McConville MJ, Likić VA (2012) PyMS: a Python toolkit for processing of gas chromatography-mass spectrometry (GC–MS) data. Application and comparative study of selected tools. BMC Bioinformatics 13, 115
| PyMS: a Python toolkit for processing of gas chromatography-mass spectrometry (GC–MS) data. Application and comparative study of selected tools.Crossref | GoogleScholarGoogle Scholar |
Oates CN, Külheim C, Myburg AA, Slippers B, Naidoo S (2015) The transcriptome and terpene profile of Eucalyptus grandis reveals mechanisms of defense against the insect pest, Leptocybe invasa. Plant & Cell Physiology 56, 1418–1428.
| The transcriptome and terpene profile of Eucalyptus grandis reveals mechanisms of defense against the insect pest, Leptocybe invasa.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC28XhslWksrvI&md5=3df38f819c063d611c1649160e639b6fCAS |
Padovan A, Keszei A, Külheim C, Foley WJ (2014) The evolution of foliar terpene diversity in Myrtaceae. Phytochemistry Reviews 13, 695–716.
| The evolution of foliar terpene diversity in Myrtaceae.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXhs1Sgt7fE&md5=bc4bf99794c7df811689ee8cfc13aff9CAS |
Pazouki L, Niinemets Ü (2016) Multi-substrate terpene synthases: their occurrence and physiological significance. Frontiers in Plant Science 7, 1019
| Multi-substrate terpene synthases: their occurrence and physiological significance.Crossref | GoogleScholarGoogle Scholar |
Peñuelas J, Llusia J (1997) Effects of carbon dioxide, water supply, and seasonality on terpene content and emission by Rosmarinus officinalis. Journal of Chemical Ecology 23, 979–993.
| Effects of carbon dioxide, water supply, and seasonality on terpene content and emission by Rosmarinus officinalis.Crossref | GoogleScholarGoogle Scholar |
Pettit NE, Froend RH (2001) Availability of seed for recruitment of riparian vegetation: a comparison of a tropical and a temperate river ecosystem in Australia. Australian Journal of Botany 49, 515–525.
| Availability of seed for recruitment of riparian vegetation: a comparison of a tropical and a temperate river ecosystem in Australia.Crossref | GoogleScholarGoogle Scholar |
Poulose AJ, Croteau R (1978) Biosynthesis of aromatic monoterpenes. Conversion of γ-terpinene to p-cymene and thymol in Thymus vulgaris L. Archives of Biochemistry and Biophysics 187, 307–314.
| Biosynthesis of aromatic monoterpenes. Conversion of γ-terpinene to p-cymene and thymol in Thymus vulgaris L.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaE1cXhs1Kku74%3D&md5=94341ccdd2463b37573d5a1a567ed6e2CAS |
Pratt JD, Keefover-Ring K, Liu LY, Mooney KA (2014) Genetically based latitudinal variation in Artemisia californica secondary chemistry. Oikos 123, 953–963.
| Genetically based latitudinal variation in Artemisia californica secondary chemistry.Crossref | GoogleScholarGoogle Scholar |
Rasmann S, Agrawal AA (2011) Latitudinal patterns in plant defense: evolution of cardenolides, their toxicity and induction following herbivory. Ecology Letters 14, 476–483.
| Latitudinal patterns in plant defense: evolution of cardenolides, their toxicity and induction following herbivory.Crossref | GoogleScholarGoogle Scholar |
Rasmann S, Köllner TG, Degenhardt J, Hiltpold I, Toepfer S, Kuhlmann U, Gershenzon J, Turlings TCJ, (2005) Recruitment of entomopathogenic nematodes by insect-damaged maize roots. Nature 434, 732–737.
| Recruitment of entomopathogenic nematodes by insect-damaged maize roots.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXivFCgur0%3D&md5=a7800edbd736ce6e9c5706463ecb339dCAS |
Rosenstiel TN, Potosnak MJ, Griffin KL, Fall R, Monson RK (2003) Increased CO2 uncouples growth from isoprene emission in an agriforest ecosystem. Nature 421, 256–259.
| Increased CO2 uncouples growth from isoprene emission in an agriforest ecosystem.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXjsF2gsg%3D%3D&md5=b9caa52b2c49be552abccb5d50e2222cCAS |
Sadeghi H, Niazmand AR, Yoosefi S (2014) Essential leaf oil and nuclear ribosomal DNA sequence variation in six Eucalyptus populations. Journal of Essential Oil Research 26, 377–384.
| Essential leaf oil and nuclear ribosomal DNA sequence variation in six Eucalyptus populations.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXhtFaktb7E&md5=60ed5b25c8c51dbef89ad5c2717306ceCAS |
Sallas L, Kainulainen P, Utriainen J, Holopainen T, Holopainen JK (2001) The influence of elevated O3 and CO2 concentrations on secondary metabolites of Scots pine (Pinus sylvestris L.) seedlings. Global Change Biology 7, 303–311.
| The influence of elevated O3 and CO2 concentrations on secondary metabolites of Scots pine (Pinus sylvestris L.) seedlings.Crossref | GoogleScholarGoogle Scholar |
Schemske DW, Mittelbach GG, Cornell HV, Sobel JM, Roy K (2009) Is there a latitudinal gradient in the importance of biotic interactions? Annual Review of Ecology Evolution and Systematics 40, 245–269.
| Is there a latitudinal gradient in the importance of biotic interactions?Crossref | GoogleScholarGoogle Scholar |
Schilmiller AL, Schauvinhold I, Larson M, Xu R, Charbonneau AL, Schmidt A, Wilkerson C, Last RL, Pichersky E (2009) Monoterpenes in the glandular trichomes of tomato are synthesized from a neryl diphosphate precursor rather than geranyl diphosphate. Proceedings of the National Academy of Sciences, USA 106, 10865–10870.
| Monoterpenes in the glandular trichomes of tomato are synthesized from a neryl diphosphate precursor rather than geranyl diphosphate.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXos1Sjuro%3D&md5=81c3afbe17f47bb82b92d1a3bbb10a4fCAS |
Sharkey TD, Monson RK (2014) The future of isoprene emission from leaves, canopies and landscapes. Plant, Cell & Environment 37, 1727–1740.
| The future of isoprene emission from leaves, canopies and landscapes.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXhtFOlsLvF&md5=3ad4129037bfe35de82688f0fcbab26bCAS |
Sharkey TD, Wiberley AE, Donohue AR (2008) Isoprene emission from plants: why and how. Annals of Botany 101, 5–18.
| Isoprene emission from plants: why and how.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXitlansrg%3D&md5=5657c11ed6d1f417e813e25fcf851aedCAS |
Southwell IA, Russell MF (2002) Volatile oil comparison of cotyledon leaves of chemotypes of Melaleuca alternifolia. Phytochemistry 59, 391–393.
| Volatile oil comparison of cotyledon leaves of chemotypes of Melaleuca alternifolia.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD38XhtVKgtL0%3D&md5=33f1f3a165ebea84eef23be9c985bee7CAS |
Staudt M, Joffre R, Rambal S, Kesselmeier J (2001) Effect of elevated CO2 on monoterpene emission of young Quercus ilex trees and its relation to structural and ecophysiological parameters. Tree Physiology 21, 437–445.
| Effect of elevated CO2 on monoterpene emission of young Quercus ilex trees and its relation to structural and ecophysiological parameters.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXktVSgu78%3D&md5=45d710d193d5ad772dfa7c76d0a75166CAS |
Stone C, Bacon P (1994) Relationships among moisture stress, insect herbivory, foliar cineole content and the growth of river red gum Eucalyptus camaldulensis. Journal of Applied Ecology 31, 604–612.
| Relationships among moisture stress, insect herbivory, foliar cineole content and the growth of river red gum Eucalyptus camaldulensis.Crossref | GoogleScholarGoogle Scholar |
Suzuki R, Shimodaira H (2006) Pvclust: an R package for assessing the uncertainty in hierarchical clustering. Bioinformatics 22, 1540–1542.
Taft S, Najar A, Godbout J, Bousquet J, Erbilgin N (2015) Variations in foliar monoterpenes across the range of jack pine reveal three widespread chemotypes: implications to host expansion of invasive mountain pine beetle. Frontiers in Plant Science 6, 342
| Variations in foliar monoterpenes across the range of jack pine reveal three widespread chemotypes: implications to host expansion of invasive mountain pine beetle.Crossref | GoogleScholarGoogle Scholar |
Tholl D (2006) Terpene synthases and the regulation, diversity and biological roles of terpene metabolism. Current Opinion in Plant Biology 9, 297–304.
| Terpene synthases and the regulation, diversity and biological roles of terpene metabolism.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XktVGgur4%3D&md5=5c57b343ef3021f882bc02684dd8605dCAS |
Thompson J, Charpentier A, Bouguet G, Charmasson F, Roset S, Buatois B, Vernet P, Gouyon PH (2013) Evolution of a genetic polymorphism with climate change in a Mediterranean landscape. Proceedings of the National Academy of Sciences of the United States of America 110, 2893–2897.
| Evolution of a genetic polymorphism with climate change in a Mediterranean landscape.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXjvFeltrk%3D&md5=80b0ce038e7f403024e31c9a18a8743cCAS |
Valkama E, Koricheva J, Oksanen E (2007) Effects of elevated O3, alone and in combination with elevated CO2, on tree leaf chemistry and insect herbivore performance: A meta-analysis. Global Change Biology 13, 184–201.
| Effects of elevated O3, alone and in combination with elevated CO2, on tree leaf chemistry and insect herbivore performance: A meta-analysis.Crossref | GoogleScholarGoogle Scholar |
van Schie CCN, Haring MA, Schuurink RC (2007) Tomato linalool synthase is induced in trichomes by jasmonic acid. Plant Molecular Biology 64, 251–263.
| Tomato linalool synthase is induced in trichomes by jasmonic acid.Crossref | GoogleScholarGoogle Scholar |
Vernet P, Gouyon R, Valdeyron G (1986) Genetic control of the oil content in Thymus vulgaris L: a case of polymorphism in a biosynthetic chain. Genetica 69, 227–231.
| Genetic control of the oil content in Thymus vulgaris L: a case of polymorphism in a biosynthetic chain.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaL28XltlSrsLg%3D&md5=2d8b440c89bb07f0332d728556fffec0CAS |
Wallis IR, Keszei A, Henery ML, Moran GF, Forrester R, Maintz J, Marsh KJ, Andrew RL, Foley WJ, (2011) A chemical perspective on the evolution of variation in Eucalyptus globulus. Perspectives in Plant Ecology, Evolution and Systematics 13, 305–318.
| A chemical perspective on the evolution of variation in Eucalyptus globulus.Crossref | GoogleScholarGoogle Scholar |
Webb H, Lanfear R, Hamill J, Foley WJ, Külheim C (2013) The yield of essential oils in Melaleuca alternifolia (Myrtaceae) is regulated through transcript abundance of genes in the MEP pathway. PLoS One 8, e60631
| The yield of essential oils in Melaleuca alternifolia (Myrtaceae) is regulated through transcript abundance of genes in the MEP pathway.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXlslClsr4%3D&md5=c47d51bd6b76bd1a592c4c0f4db4aef1CAS |
Woods EC, Hastings AP, Turley NE, Heard SB, Agrawal AA (2012) Adaptive geographical clines in the growth and defense of a native plant. Ecological Monographs 82, 149–168.
| Adaptive geographical clines in the growth and defense of a native plant.Crossref | GoogleScholarGoogle Scholar |
Zvereva EL, Kozlov MV (2006) Consequences of simultaneous elevation of carbon dioxide and temperature for plant-herbivore interactions: a meta-analysis. Global Change Biology 12, 27–41.
| Consequences of simultaneous elevation of carbon dioxide and temperature for plant-herbivore interactions: a meta-analysis.Crossref | GoogleScholarGoogle Scholar |
