Register      Login
Australian Journal of Botany Australian Journal of Botany Society
Southern hemisphere botanical ecosystems
RESEARCH ARTICLE

Genetic and environmental parameters show associations with essential oil composition in West Australian sandalwood (Santalum spicatum)

Jessie Moniodis A D , Michael Renton A B , Christopher G. Jones A , E. Liz Barbour A and Margaret Byrne A C
+ Author Affiliations
- Author Affiliations

A School of Biological Sciences (M084), University of Western Australia, 35 Stirling Highway, Crawley, WA 6009, Australia.

B School of Agriculture and Environment, University of Western Australia, 35 Stirling Highway, Crawley, WA 6009, Australia.

C Science and Conservation, Department of Biodiversity, Conservation and Attractions, Locked Bag 104, Bentley Delivery Centre, WA 6983, Australia.

D Corresponding author. Email: jess.moniodis@uwa.edu.au

Australian Journal of Botany 66(1) 48-58 https://doi.org/10.1071/BT17116
Submitted: 18 June 2017  Accepted: 5 December 2017   Published: 9 January 2018

Abstract

Santalum spicatum (R.Br.) A.DC is a West Australian sandalwood species highly valued for the sesquiterpene-rich oil in mature heartwood. The oil composition, particularly levels of the valuable sesquiterpenoids α- and β-santalol and the allergenic E,E-farnesol, are known to vary across its natural distribution. Our study investigated associations of oil characteristics in 186 S. spicatum trees in semiarid and arid regions of Western Australia with genetic structure, environmental parameters and morphological features. We found associations between oil composition and genetic structure, as well as between oil composition and environmental factors. Analysis of individuals using STRUCTURE revealed two major genetic clusters (K = 2), comprising trees from the arid north clustered together, and the semiarid south-west clustered separately. Mantel tests revealed a significant association between oil characteristics and genetic distance (r = 0.129, P = 0.02). There was considerable variation in the growing environment of S. spicatum. An Adonis test showed a significant association between oil composition and provenance (P = 0.001) and between oil composition and soil type (P = 0.002) but not oil composition and other environmental characters. Soil type was significantly related to santalol and E,E-farnesol content. No significant associations between oil composition and morphological features were identified.

Additional keywords: essential oil variation, genetic distance, microsatellites, Santalaceae, Santalum, sesquiterpenes.


References

Anderson MJ (2001) A new method for non-parametric multivariate analysis of variance. Austral Ecology 26, 32–46.

Andrew RL, Wallis IR, Harwood CE, Foley WJ (2010) Genetic and environmental contributions to variation and population divergence in a broad-spectrum foliar defence of Eucalyptus tricarpa. Annals of Botany 105, 707–717.
Genetic and environmental contributions to variation and population divergence in a broad-spectrum foliar defence of Eucalyptus tricarpa.Crossref | GoogleScholarGoogle Scholar |

Applegate GB, Chamberlain J, Daruhi G, Feigelson JL, Hamilton L, McKinnell FH, Neil PE, Rai SN, Rodehn P, Statham P, Stemmermann L (1990) A state of knowledge synthesis and summary from the April 1990 symposium. In ‘Proceedings of the symposium on sandalwood in the Pacific. Vol. PSW-122’. (Eds L Hamilton, CE Conrad) pp. 1–11. (US Forest Service: Honolulu, HI, USA)

Barrett DR (1987) Initial observations on flowering and fruiting in Santalum spicatum (R.Br.) A.D.C. the Western Australian Sandalwood. Mulga Research Center Journal 9, 33–37.

Boira H, Blanquer A (1998) Environmental factors affecting chemical variability of essential oils in Thymus piperella L. Biochemical Systematics and Ecology 26, 811–822.
Environmental factors affecting chemical variability of essential oils in Thymus piperella L.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK1cXmslWrtrk%3D&md5=01960b3fa001df00bef3ee1f00612c46CAS |

Bottin L, Vaillant A, Sire P, Cardi C, Bouvet JM (2005) Isolation and characterization of microsatellite loci in Santalum austrocaledonicum, Santalaceae. Molecular Ecology Notes 5, 800–802.
Isolation and characterization of microsatellite loci in Santalum austrocaledonicum, Santalaceae.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28Xjs1Wiug%3D%3D&md5=96865350218a20a18db473f0b0c584caCAS |

Bottin L, Isnard C, Lagrange A, Jeann Marc B (2007) Comparative molecular and phytochemical study of the tree species Santalum austrocaledonicum (Santalaceae) distributed in the New Caledonian archipelago. Chemistry & Biodiversity 4, 1541–1556.
Comparative molecular and phytochemical study of the tree species Santalum austrocaledonicum (Santalaceae) distributed in the New Caledonian archipelago.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXosFeqs74%3D&md5=ae02cad7e2902cd206181d17da201af9CAS |

Braun NA, Butaud J-F, Bianchini J-P, Kohlenberg B, Hammerschmidt F-J, Meier M, Raharivelomanana P (2007) Eastern Polynesian sandalwood oil (Santalum insulare Bertero ex A. DC.) – a detailed investigation. Natural Product Communications 2, 695–699.

Brennan P, Merlin M (1993) Biogeography and traditional use of Santalum in the Pacific region. In ‘Sandalwood in the Pacific region: proceedings of a symposium held on 2 June 1991 at the XVII Pacific Science Congress, Honolulu, Hawaii’. (Ed. FH McKinnel) pp. 30–38. (US Forest Service: Honolulu, HI, USA)

Butcher PA, Matheson AC, Slee MU (1996) Potential for genetic improvement of oil production in Melaleuca alternifolia and M. linariifolia. New Forests 11, 31–51.

Byrne M, Moran GF (1994) Population divergence in the chloroplast genome of Eucalyptus nitens. Heredity 73, 18–28.
Population divergence in the chloroplast genome of Eucalyptus nitens.Crossref | GoogleScholarGoogle Scholar |

Byrne M, Macdonald B, Francki M (2001) Incorporation of sodium sulphite into extraction protocol minimizes degradation of Acacia DNA. BioTechniques 30, 742–744.

Byrne M, Macdonald B, Brand JE (2003a) Regional genetic differentiation in Western Australian sandalwood (Santalum spicatum) as revealed by nuclear RFLP analysis. Theoretical and Applied Genetics 107, 1208–1214.
Regional genetic differentiation in Western Australian sandalwood (Santalum spicatum) as revealed by nuclear RFLP analysis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXos1Okuro%3D&md5=af13aa7294c8653a8de46403aaa0312aCAS |

Byrne M, Macdonald B, Brand JE (2003b) Phylogeography and divergence in the chloroplast genome of Western Australian sandalwood (Santalum spicatum). Heredity 91, 389–395.
Phylogeography and divergence in the chloroplast genome of Western Australian sandalwood (Santalum spicatum).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3sXnsF2msbY%3D&md5=181612dbcddf04b99bf00afe96f01a07CAS |

Cavalli-Sforza LL, Edwards AW (1967) Phylogenetic analysis. Models and estimation procedures. American Journal of Human Genetics 19, 233–257.

Celedon JM, Chiang A, Yuen M, Diaz‐Chavez ML, Madilao LL, Finnegan PM, Barbour EL, Bohlmann J (2016) Heartwood‐specific transcriptome and metabolite signatures of tropical sandalwood (Santalum album) reveal the final step of (Z)‐santalol fragrance biosynthesis. The Plant Journal 86, 289–299.
Heartwood‐specific transcriptome and metabolite signatures of tropical sandalwood (Santalum album) reveal the final step of (Z)‐santalol fragrance biosynthesis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC28XmtVenurs%3D&md5=c12fe54222ac148abaa551c7dd7e3d1bCAS |

Chakrabarti R, Schutt CE (2002) Novel sulfoxides facilitate GC-rich template amplification. BioTechniques 32, 866–874.

Clarke KR (1993) Non-parametric multivariate analyses of changes in community structure. Australian Journal of Ecology 18, 117–143.
Non-parametric multivariate analyses of changes in community structure.Crossref | GoogleScholarGoogle Scholar |

Clarke M (2006) ‘Australia’s sandalwood industry, an overview and analysis of research needs.’ (Rural Industries Research and Development Corporation: Sydney, NSW)

Clarke KR, Gorley RN (2006) ‘PRIMER ver. 6: user manual/tutorial.’ (PRIMER-E, Plymouth, UK)

Diaz-Chavez ML, Moniodis J, Madilao LL, Jancsik S, Keeling CI, Barbour EL, Ghisalberti EL, Plummer JA, Jones CG, Bohlmann J (2013) Biosynthesis of sandalwood oil: Santalum album CYP76F cytochromes P450 produce santalols and bergamotol. PLoS One 8, e75053
Biosynthesis of sandalwood oil: Santalum album CYP76F cytochromes P450 produce santalols and bergamotol.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXhsFeitb3K&md5=42bf0230853874e24f90f63801399518CAS |

Duarte AR, Santos SC, Seraphin JC, Ferri PH (2010) Environmental influence on phenols and essential oils of Myrciaria cauliflora leaves. Journal of the Brazilian Chemical Society 21, 1672–1680.
Environmental influence on phenols and essential oils of Myrciaria cauliflora leaves.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXht1Cnu7nK&md5=678ad773a68e72c678eee93510825e28CAS |

Faith DP, Minchin PR, Belbin L (1987) Compositional dissimilarity as a robust measure of ecological distance. Vegetatio 69, 57–68.
Compositional dissimilarity as a robust measure of ecological distance.Crossref | GoogleScholarGoogle Scholar |

Falush D, Stephens M, Pritchard JK (2003) Inference of population structure using multilocus genotype data: linked loci and correlated allele frequencies. Genetics 164, 1567–1587.

Fox JED, Brand JE (1993) Preliminary observations on ecotypic variation in Santalum spicatum. Mulga Research Centre Journal 11, 1–12.

Hewson HJ, George AS (1984) ‘Santalaceae. Flora of Australia. Vol. 22.’ (Australian Government Publishing Service: Canberra, ACT)

Howes M-JR, Simmonds MSJ, Kite GC (2004) Evaluation of the quality of sandalwood essential oils by gas chromatography-mass spectrometry. Journal of Chromatography. A 1028, 307–312.
Evaluation of the quality of sandalwood essential oils by gas chromatography-mass spectrometry.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXmvFyntg%3D%3D&md5=e4c359c19da23fd7a22035769710de8cCAS |

Jones CG, Plummer JA, Barbour EL (2007) Non-destructive sampling of Indian sandalwood (Santalum album L.) for oil content and composition. Journal of Essential Oil Research 19, 157–164.
Non-destructive sampling of Indian sandalwood (Santalum album L.) for oil content and composition.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXlvVSksLg%3D&md5=4303a4f7950bf485f8f4fa5fb86e85cfCAS |

Jones CG, Keeling CI, Ghisalberti EL, Barbour EL, Plummer JA, Bohlmann J (2008) Isolation of cDNAs and functional characterisation of two multi-product terpene synthase enzymes from sandalwood, Santalum album L. Archives of Biochemistry and Biophysics 477, 121–130.
Isolation of cDNAs and functional characterisation of two multi-product terpene synthase enzymes from sandalwood, Santalum album L.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXpslWmuro%3D&md5=ce6a0d4edfb8a8ed81e855578cd2a636CAS |

Jones C, Plummer J, Barbour E, Byrne M (2009) Genetic diversity of an Australian Santalumalbum collection – implications for tree improvement potential. Silvae Genetica 58, 279–286.
Genetic diversity of an Australian Santalumalbum collection – implications for tree improvement potential.Crossref | GoogleScholarGoogle Scholar |

Jones CG, Moniodis J, Zulak KG, Scaffidi A, Plummer JA, Ghisalberti EL, Barbour EL, Bohlmann J (2011) Sandalwood fragrance biosynthesis involves sesquiterpene synthases of both the terpene synthase (TPS) a and TPS-b subfamilies, including santalene synthases. Journal of Biological Chemistry 286, 17445–17454.
Sandalwood fragrance biosynthesis involves sesquiterpene synthases of both the terpene synthase (TPS) a and TPS-b subfamilies, including santalene synthases.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXmtVGjsbo%3D&md5=cea6f5b6a458c67228fa5c754443dd5eCAS |

Karousou R, Koureas DN, Kokkini S (2005) Essential oil composition is related to the natural habitats: Coridothymus capitatus and Satureja thymbra in NATURA 2000 sites of Crete. Phytochemistry 66, 2668–2673.
Essential oil composition is related to the natural habitats: Coridothymus capitatus and Satureja thymbra in NATURA 2000 sites of Crete.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXht1ars7jO&md5=634054f0bc596e7ad7b88692e350bbc2CAS |

Kruskal JB (1964a) Multidimensional scaling by optimizing goodness-of-fit to a nonmetric hypothesis. Psychometrika 29, 1–27.
Multidimensional scaling by optimizing goodness-of-fit to a nonmetric hypothesis.Crossref | GoogleScholarGoogle Scholar |

Kruskal JB (1964b) Nonmetric multidimensional scaling: a numerical method. Psychometrika 29, 115–129.
Nonmetric multidimensional scaling: a numerical method.Crossref | GoogleScholarGoogle Scholar |

Legendre P, Anderson MJ (1999) Distance-based redundancy analysis: testing multispecies responses in multifactorial ecological experiments. Ecological Monographs 69, 1–24.
Distance-based redundancy analysis: testing multispecies responses in multifactorial ecological experiments.Crossref | GoogleScholarGoogle Scholar |

Lhuillier E, Butaud J-F, Bouvet JM (2006) Extensive clonality and strong differentiation in the insular Pacific tree Santalum insulare: implications for its conservation. Annals of Botany 98, 1061–1072.
Extensive clonality and strong differentiation in the insular Pacific tree Santalum insulare: implications for its conservation.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XhtlantbfM&md5=8ba99fcaf815f997cf6e950a686ed3feCAS |

Liu K, Muse SV (2005) PowerMarker: an integrated analysis environment for genetic marker analysis. Bioinformatics 21, 2128–2129.
PowerMarker: an integrated analysis environment for genetic marker analysis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2MXjsl2nsbg%3D&md5=71e8434fe6655511dd37230f0e408f32CAS |

Loneragan OW (1990) Historical review of sandalwood (Santalum spicatum) research in Western Australia. Research Bulletin No. 4. Department of Conservation and Land Management, Perth, WA.

Maffei M, Mucciarelli M, Scannerini S (1993) Environmental factors affecting the lipid metabolism in Rosmarinus officinalis L. Biochemical Systematics and Ecology 21, 765–784.
Environmental factors affecting the lipid metabolism in Rosmarinus officinalis L.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK2cXhsFyrtbg%3D&md5=8d8eeb7bf98986fc3d789ab9f58fbbd5CAS |

Mantel N (1967) The detection of disease clustering and a generalized regression approach. Cancer Research 27, 209–220.

McArdle BH, Anderson MJ (2001) Fitting multivariate models to community data: a comment on distance-based redundancy analysis. Ecology 82, 290–297.
Fitting multivariate models to community data: a comment on distance-based redundancy analysis.Crossref | GoogleScholarGoogle Scholar |

Millar MA, Byrne M, Barbour E (2012) Characterisation of eleven polymorphic microsatellite DNA markers for Australian sandalwood (Santalum spicatum) (R.Br.) A.DC. (Santalaceae). Conservation Genetics Resources 4, 51–53.
Characterisation of eleven polymorphic microsatellite DNA markers for Australian sandalwood (Santalum spicatum) (R.Br.) A.DC. (Santalaceae).Crossref | GoogleScholarGoogle Scholar |

Minchin PR (1987) An evaluation of relative robustness of techniques for ecological ordinations. Vegetatio 69, 89–107.
An evaluation of relative robustness of techniques for ecological ordinations.Crossref | GoogleScholarGoogle Scholar |

Moniodis J, Jones CG, Barbour EL, Plummer JA, Ghisalberti EL, Bohlmann J (2015) The transcriptome of sesquiterpenoid biosynthesis in heartwood xylem of Western Australian sandalwood (Santalum spicatum). Phytochemistry 113, 79–86.
The transcriptome of sesquiterpenoid biosynthesis in heartwood xylem of Western Australian sandalwood (Santalum spicatum).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2MXntVOnsw%3D%3D&md5=2f88e161dc6d74c085de2663e8b68d28CAS |

Moniodis J, Jones CG, Renton M, Plummer JA, Barbour EL, Ghisalberti EL, Bohlmann J (2017) Sesquiterpene variation in West Australian sandalwood (Santalum spicatum). Molecules 22, 940
Sesquiterpene variation in West Australian sandalwood (Santalum spicatum).Crossref | GoogleScholarGoogle Scholar |

Moretta P (2001) Extraction and variation of the essential oil from Western Australian sandalwood (Santalum spicatum). PhD thesis. School of Chemistry and Biochemistry, University of Western Australia, Perth, WA.

Muir K, Byrne M, Barbour E, Cox MC, Fox JED (2007) High levels of outcrossing in a family trial of Western Australian sandalwood (Santalum spicatum). Silvae Genetica 56, 222–230.
High levels of outcrossing in a family trial of Western Australian sandalwood (Santalum spicatum).Crossref | GoogleScholarGoogle Scholar |

Murphy MT, Garkaklis MJ, Hardy GESJ (2005) Seed caching by woylies Bettongia penicillata can increase sandalwood Santalum spicatum regeneration in Western Australia. Austral Ecology 30, 747–755.
Seed caching by woylies Bettongia penicillata can increase sandalwood Santalum spicatum regeneration in Western Australia.Crossref | GoogleScholarGoogle Scholar |

O’Reilly-Wapstra JM, Alison M, Miller AM, Hamilton MG, Dean Williams D, Glancy-Dean N, Potts BM (2013) Chemical variation in a dominant tree species: population divergence, selection and genetic stability across environments. PLoS One 8, e58416
Chemical variation in a dominant tree species: population divergence, selection and genetic stability across environments.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3sXltFyqtLg%3D&md5=c7d5119fb26b8f9ca5ffa9d17b78aa09CAS |

Oksanen J, Blanchet FG, Kindt R, Legendre P, Minchin PR, O’hara RB, Simpson GL, Solymos P, Stevens MHH, Wagner H, Oksanen MJ (2013) Package ‘vegan’ Community ecology package, ver. 2.9. Available at https://CRAN.R-project.org/package=vegan [Verified 8 December 2017].

Page T, Southwell I, Russell M, Tate H, Tungon J, Sam C, Dickinson G, Robson K, Leakey RRB (2010) Geographic and phenotypic variation in heartwood and essential-oil characters in natural populations of Santalum austrocaledonicum in Vanuatu. Chemistry & Biodiversity 7, 1990–2006.
Geographic and phenotypic variation in heartwood and essential-oil characters in natural populations of Santalum austrocaledonicum in Vanuatu.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhtVKjsbfL&md5=c174590549b712dcf5e19f2380c6b501CAS |

Peakall R, Smouse P (2006) GENALEX 6: genetic analysis in Excel. Population genetic software for teaching and research. Molecular Ecology Notes 6, 288–295.
GENALEX 6: genetic analysis in Excel. Population genetic software for teaching and research.Crossref | GoogleScholarGoogle Scholar |

Pritchard JK, Stephens M, Donnelly P (2000) Inference of population structure using multilocus genotype data. Genetics 155, 945–959.

R Core Team (2016) R: A language and environment for statistical computing. R Foundation for Statistical Computing, Vienna, Austria. Available at: https://www.R-project.org/ [verified 11 December 2017].

Radomiljac A, McComb JA, Pate JS (1999a) Gas exchange and water relations of the root hemiparasite Santalum album L. in association with legume and non-legume hosts. Annals of Botany 83, 215–224.
Gas exchange and water relations of the root hemiparasite Santalum album L. in association with legume and non-legume hosts.Crossref | GoogleScholarGoogle Scholar |

Radomiljac A, McComb JA, McGrath J (1999b) Intermediate host influences on the root hemiparasite Santalum album L. biomass partitioning. Forest Ecology and Management 113, 143–153.
Intermediate host influences on the root hemiparasite Santalum album L. biomass partitioning.Crossref | GoogleScholarGoogle Scholar |

Rosenberg NA (2004) DISTRUCT: a program for the graphical display of population structure. Molecular Ecology Notes 4, 137–138.
DISTRUCT: a program for the graphical display of population structure.Crossref | GoogleScholarGoogle Scholar |

Steffen W, Burbidge AA, Hughes L, Kitching R, Lindenmayer D, Musgrave W, Smith MS, Werner PA (2009) ‘Australia’s biodiversity and climate change.’ (CSIRO Publishing: Melbourne, Vic.)

Tommasi L, Negro C, Cerfeda A, Nutricati E, Zuccarello V, De Bellis L, Miceli A (2007) Influence of environmental factors on essential oil variability in Thymbra capitata (L.) cav. growing wild in southern Puglia (Italy). Journal of Essential Oil Research 19, 572–580.
Influence of environmental factors on essential oil variability in Thymbra capitata (L.) cav. growing wild in southern Puglia (Italy).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2sXhsVyjur7L&md5=81f7860bb8dbcb53a8c284763fe8242eCAS |

Tonk FA, Yüce S, Bayram E, Giachino RRA, Sönmez Ç, Telci İ, Furan MA (2010) Chemical and genetic variability of selected Turkish oregano (Origanum onites L.) clones. Plant Systematics and Evolution 288, 157–165.
Chemical and genetic variability of selected Turkish oregano (Origanum onites L.) clones.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhtVKhurnF&md5=89ea2a63d4a86ff78a763f95735cf742CAS |

Tonts M, Selwood J (2003) Niche markets, regional diversification and the reinvention of Western Australia’s sandalwood industry. Tijdschrift voor Economische en Sociale Geografie 94, 564–575.
Niche markets, regional diversification and the reinvention of Western Australia’s sandalwood industry.Crossref | GoogleScholarGoogle Scholar |

Van Oosterhout C, Hutchinson WF, Wills DP, Shipley P (2004) MICRO‐CHECKER: software for identifying and correcting genotyping errors in microsatellite data. Molecular Ecology Notes 4, 535–538.
MICRO‐CHECKER: software for identifying and correcting genotyping errors in microsatellite data.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD2cXnvFOktb8%3D&md5=3adc1ae5486b5c9a86fa815707d6e622CAS |

Verghese J, Sunny TP, Balakrishnan KV (1990) (Z)-(+)-a-santalol and (Z)-(–)-b-santalol concentration, a new quality determinant of east Indian sandalwood oil. Flavour and Fragrance Journal 5, 223–226.
(Z)-(+)-a-santalol and (Z)-(–)-b-santalol concentration, a new quality determinant of east Indian sandalwood oil.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3MXktFGhtbw%3D&md5=ccf6d7dda1bc1f31a915c3e2858f1679CAS |

Vieira RF, Grayer RJ, Paton A, Simon JE (2001) Genetic diversity of Ocimum gratissimum L. based on volatile oil constituents, flavonoids and RAPD markers. Biochemical Systematics and Ecology 29, 287–304.
Genetic diversity of Ocimum gratissimum L. based on volatile oil constituents, flavonoids and RAPD markers.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD3MXhsF2qtb8%3D&md5=0819f994ba383553848e70ae1a73fc11CAS |

Vokou D, Kokkini S, Bessiere J-M (1993) Geographic variation of Greek oregano (Origanumvulgare ssp. hirtum) essential oils. Biochemical Systematics and Ecology 21, 287–295.
Geographic variation of Greek oregano (Origanumvulgare ssp. hirtum) essential oils.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DyaK3sXks1yjurw%3D&md5=eb0e95f0f90d003ecd12e56c36450f32CAS |

Webb H, Foley WJ, Külheim C (2014) The genetic basis of foliar terpene yield: Implications for breeding and profitability of Australian essential oil crops. Plant Biotechnology 31, 363–376.
The genetic basis of foliar terpene yield: Implications for breeding and profitability of Australian essential oil crops.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2MXntFegtr4%3D&md5=e762e077e0c71f74e350467ab1a16216CAS |

Woodall GS, Robinson CJ (2003) Natural diversity of Santalum spicatum host species in south-coast river systems and their incorporation into profitable and biodiverse revegetation. Australian Journal of Botany 51, 741–753.
Natural diversity of Santalum spicatum host species in south-coast river systems and their incorporation into profitable and biodiverse revegetation.Crossref | GoogleScholarGoogle Scholar |