Different responses to environmental factors in terpene composition of Pinus heldreichii and P. peuce: ecological and chemotaxonomic considerations



Bosnian pine, Macedonian pine, essential oil, environmental factors, chemotaxonomy


Paper description:

  • There are no studies on the influence of environmental factors and their correlation with pine oleoresin composition from the leaves of several Balkan pines.
  • Oleoresins were isolated from Bosnian and Macedonian pine collected from nine localities, including two sympatric. The obtained composition was analyzed statistically to assess the correlation with bioclimatic, geological and geographical parameters.
  • Three chemotypes were present in Bosnian pine leaf oleoresins, while only one was found in Macedonian pine.
  • While the oleoresin profiles showed strong species-dependent composition and variability, environmental factors, including geological substrate type and exposition must also be taken into account.

Abstract: Many studies show the influence of the environment on terpene composition, but not many of them deal with the terpene composition variability in correlation with environmental factors in Pinus. We chose two endemic species – P. heldreichii Christ. (Bosnian pine) and P. peuce Griseb. (Macedonian pine) – two relict and (sub)endemic species of the Balkan peninsula. They mainly form pure stands but can appear in mixed populations, most commonly with each other. These species belong to different subgenera and thus differ greatly, especially in needle anatomy. α-pinene, limonene and germacrene D predominated in Bosnian pine leaf oleoresins, while Macedonian pine oleoresin contained high amounts of α-pinene. Furthermore, there were three chemotypes present in Bosnian, and only one in Macedonian pine. Oleoresins of Bosnian pine did not show correlation with climate, however, its composition changed in response to geological substrate type. Macedonian pine oleoresin showed a high correlation with the climate but changed only a little in response to geological substrate type. The oleoresin profiles showed strong species-dependent composition and variability. However, since each species expressed different responses to tested environmental conditions, it is important to take into consideration these variables when analyzing natural populations of the species.


Received: July 5, 2019; Revised: July 18, 2019; Accepted: July 24, 2019; Published online: August 1, 2019

How to cite this article: Rajčević N, Nikolić B, Marin PD. Different responses to environmental factors in terpene composition of Pinus heldreichii and P. peuce: Ecological and chemotaxonomic considerations. Arch Biol Sci. 2019;71(4):629-37.


Download data is not yet available.


Adorjan B, Buchbauer G. Biological properties of essential oils: an updated review. Flavour Fragr J. 2010;25(6):407-26.

Baser KHC, Buchbauer G. Handbook of essential oils: science, technology, and applications. Boca Raton, FL: CRC Press; 2009

Cseke LJ, Kirakosyan A, Kaufman PB, Warber S, Duke JA, Brielmann HL. Natural products from plants. Boca Raton, FL: CRC Press; 2006.

Banthorpe DV, Le Patourel GN. The biosynthesis of (+)-alpha-pinene in Pinus species. Biochem J. 1972;130:1055-61.

Bohlmann J, Steele CL, Croteau R. Monoterpene Synthases from Grand Fir (Abies grandis) cDNA isolation, characterization, and functional expression of myrcene synthase,(−)-(4s)-limonene synthase, and (−)-(1s, 5s)-pinene synthase. J Biol Chem. 1997;272(35):21784-92.

Buchanan BB, Gruissem W, Jones RL. Natural Products (Secondary Metabolites). In: Biochemistry & Molecular Biology of Plants. Maryland: American Society of Plant Physiologists; 2009. p. 1251-68.

Langenheim JH. Higher plant terpenoids: a phytocentric overview of their ecological roles. J Chem Ecol. 1994;20(6):1223-80.

McKay SAB. Insect Attack and Wounding Induce Traumatic Resin Duct Development and Gene Expression of (--)-Pinene Synthase in Sitka Spruce. PLANT Physiol. 2003;133(1):368-78.

Phillips MA, Savage TJ, Croteau R. Monoterpene Synthases of Loblolly Pine (Pinus taeda) Produce Pinene Isomers and Enantiomers. Arch Biochem Biophys. 1999;372(1):197-204.

Phillips MA, Croteau RB. Resin-based defenses in conifers. Trends Plant Sci. 1999;4(5):184-90.

Bohlmann J, Meyer-Gauen G, Croteau R. Plant terpenoid synthases: molecular biology and phylogenetic analysis. Proc Natl Acad Sci. 1998;95(8):4126-33.

Martin DM. Functional Characterization of Nine Norway Spruce TPS Genes and Evolution of Gymnosperm Terpene Synthases of the TPS-d Subfamily. PLANT Physiol. 2004;135(4):1908-27.

Adams RP. Systematics of the one seeded Juniperus of the eastern hemisphere based on leaf essential oils and random amplified polymorphic DNAs (RAPDs). Biochem Syst Ecol. 2000;28(6):529-543.

Adams RP. The serrate leaf margined Juniperus (Section Sabina) of the western hemisphere: systematics and evolution based on leaf essential oils and Random Amplified Polymorphic DNAs (RAPDs). Biochem Syst Ecol. 2000;28(10):975-89.

Iloff PM, Mirov NT. Composition of gum turpentines of pines XXV. A report on two white pines: Pinus koraiensis from Korea and P. peuce from Macedonia. J Pharm Sci. 1956;45(2):77-81.

Rudloff E von. Chemosystematic Studies in the Genus Picea (Pinaceae): I. Introduction. Can J Bot. 1967;45(6):891-901.

Rudloff E von. Chemosystematic studies in the genus Picea (Pinaceae): II. The leaf oil of Picea glauca and P. mariana. Can J Bot. 1967;45(9):1703-14.

Von Rudloff E. Volatile leaf oil analysis in chemosystematic studies of North American conifers. Biochem Syst Ecol. 1975;2(3):131-67.

Yatagai M, Sato T. Terpenes of leaf oils from conifers. Biochem Syst Ecol. 1986;14(5):469-78.

Zavarin E, Snajberk K, Reichert T, Tsien E. On the geographic variability of the monoterpenes from the cortical blister oleoresin of Abies lasiocarpa. Phytochemistry. 1970;9(2):377-95.

Cates RG. The role of mixtures and variation in the production of terpenoids in conifer-insect-pathogen interactions. In: Romeo JT, Saunders JA, Barbosa P, editors. Phytochemical diversity and redundancy in ecological interactions. Springer; 1996. p. 179-216.

Lakušić DV, Ristić MS, Slavkovska VN, Šinžar-Sekulić JB, Lakušić BS. Environment-related variations of the composition of the essential oils of rosemary (Rosmarinus officinalis L.) in the Balkan Peninsula. Chem Biodivers. 2012;9(7):1286-302.

Marčetić M, Kovačević N, Lakušić D, Lakušić B. Habitat-related variation in composition of the essential oil of Seseli rigidum Waldst. & Kit. (Apiaceae). Phytochemistry. 2017 135:80-92

Ložienė K, Labokas J. Effects of abiotic environmental conditions on amount and enantiomeric composition of α-pinene in Juniperus communis L. Biochem Syst Ecol. 2012;44:36-43.

Kallio H, Junger-Mannermaa K. Maritime influence on the volatile terpenes in the berries of different ecotypes of juniper (Juniperus communis L.) in Finland. J Agric Food Chem. 1989;37(4):1013-16.

Djerrad Z, Kadik L, Djouahri A. Chemical variability and antioxidant activities among Pinus halepensis Mill. essential oils provenances, depending on geographic variation and environmental conditions. Ind Crops Prod. 2015;74:440-9.

Jud A. Characteristics of essential oil composition in the needles of young stand of Scots pine (Pinus sylvestris L.) growing along aerial ammonia gradient. Chemija. 2006;17(4):67-73.

Kupcinskiene E, Stikliene A, Judzentiene A. The essential oil qualitative and quantitative composition in the needles of Pinus sylvestris L. growing along industrial transects. Environ Pollut. 2008;155(3):481-91.

Farjon A, Filer D. An Atlas of the World’s Conifers: An Analysis of Their Distribution, Biogeography, Diversity and Conservation Status. Leiden ; Boston: Brill; 2013.

Diklić N, Janković M. Šume munike. In: Sarić M, editor. Vegetacija Srbije II. Belgrade: Serbian Academy of Sciences and Arts; 1997. p. 155-65.

Veljković V, Radulović S. Prirodno podmlađivanje molike u raznim uslovima stanita i sastojinskih prilika u SR Srbiji. In: Pejoski B, editor. Zbornik na simpoziumot za molikata. Bitola: Pelister; 1969:351-362

Hijmans RJ, Cameron SE, Parra JL, Jones PG, Jarvis A. Very high resolution interpolated climate surfaces for global land areas. Int J Climatol. 2005;25(15):1965-78.

Hammer Ø, Harper DAT, Ryan PD. PAST: paleontological statistics software package for education and data analysis. Palaeontol Electron. 2001;4(1):1-9.

Nikolić B, Ristić M, Bojović S, Marin PD. Variability of the needle essential oils of Pinus heldreichii from different populations in Montenegro and Serbia. Chem Biodivers. 2007;4(5):905-16.

Nikolić B, Ristić M, Bojović S, Krivošej Z, Matevski V, Marin PD. Population Variability of Essential Oils of Pinus heldreichii from the Scardo‐Pindic Mountains Ošljak and Galičica. Chem Biodivers. 2015;12(2):295-308.

Nikolic B, Ristic M, Bojovic S, Marin PD. Variability of the needle essential oils of Pinus peuce from different Populations in Montenegro and Serbia. Chem Biodivers. 2008;5(7):1377-88.

Nikolic B, Ristic M, Bojovic S, Matevski V, Krivosej Z, Marin PD. Essential-oil composition of the needles collected from natural populations of Macedonian Pine (Pinus peuce GRISEB.) from the Scardo-Pindic Mountain System. Chem Biodivers. 2014;11(6):934-48.

Mitić ZS, Jovanović SČ, Zlatković BK, Nikolić BM, Stojanović GS, Marin PD. Needle terpenes as chemotaxonomic markers in Pinus: subsections Pinus and Pinaster. Chem Biodivers. 2017;14(5): e1600453.

Šarac Z, Bojović S, Nikolić B, Tešević V, Ðorđević I, Marin PD. Chemotaxonomic significance of the terpene composition in natural populations of Pinus nigra JF Arnold from Serbia. Chem Biodivers. 2013;10(8):1507-20.

Nikolić B, Ristić M, Tešević V, Marin PD, Bojović S. Terpene Chemodiversity of Relict Conifers Picea omorika, Pinus heldreichii, and Pinus peuce, Endemic to Balkan. Chem Biodivers. 2011;8(12):2247-60.

Kaundun SS, Lebreton P. Taxonomy and systematics of the genus Pinus based on morphological, biogeographical and biochemical characters. Plant Syst Evol. 2010;284(1-2):1-15.

Otto A, Wilde V. Sesqui-, di-, and triterpenoids as chemosystematic markers in extant conifers—A review. Bot Rev. 2001;67(2):141-238.

Adams RP. The leaf essential oils and chemotaxonomy of Juniperus sect. Juniperus. Biochem Syst Ecol. 1998;26(6):637-45.

Hanover JW. Applications of terpene analysis in forest genetics. In: Adams WT, Strauss SH, Copes DL, Griffin AL, editors. Population Genetics of Forest Trees. Springer; 1992. p. 159-78.

Adams RP. Chemosystematics-Analyses of populational differentiation and variability of ancestral and recent populations of Juniperus ashei. Ann Mo Bot Gard. 1977;64(2):184-209.

Nikolić B, Bojović S, Marin P. Morpho-anatomical properties of Pinus heldreichii needles from natural populations in Montenegro and Serbia. Plant Biosyst. 2016;150(2):254-63.

Nikolić B, Bojović S, Marin PD. Morpho-anatomical traits of Pinus peuce needles from natural populations in Montenegro and Serbia. Plant Biosyst. 2015;150(5):1038-45.




How to Cite

Rajčević N, Nikolić B, Marin PD. Different responses to environmental factors in terpene composition of Pinus heldreichii and P. peuce: ecological and chemotaxonomic considerations. Arch Biol Sci [Internet]. 2019Dec.19 [cited 2024Apr.22];71(4):629-37. Available from: https://serbiosoc.org.rs/arch/index.php/abs/article/view/4458




Most read articles by the same author(s)