Free Standard AU & NZ Shipping For All Book Orders Over $80!
Register      Login
Australian Journal of Botany Australian Journal of Botany Society
Southern hemisphere botanical ecosystems
RESEARCH ARTICLE

Importance of phenolics in populations of Teucrium chamaedrys (Lamiaceae) from serpentine soils

Miroslava Zhiponova https://orcid.org/0000-0001-7333-6558 A D * , Zhenya Yordanova A * , Dolja Pavlova B , Mariya Rogova A , Milena Dimitrova A , Daniela Dragolova A , Elena Tasheva-Terzieva C and Veneta Kapchina-Toteva A
+ Author Affiliations
- Author Affiliations

A Department of Plant Physiology, Faculty of Biology, Sofia University ‘St Kliment Ohridski’, 8 Dragan Tsankov Boulevard, BG-1164 Sofia, Bulgaria.

B Department of Botany, Faculty of Biology, Sofia University ‘St Kliment Ohridski’, 8 Dragan Tsankov Boulevard, BG-1164 Sofia, Bulgaria.

C Department of Zoology and Anthropology, Faculty of Biology, Sofia University ‘St Kliment Ohridski’, 8 Dragan Tsankov Boulevard, BG-1164 Sofia, Bulgaria.

D Corresponding author. Email: zhiponova@biofac.uni-sofia.bg

Australian Journal of Botany 68(5) 352-362 https://doi.org/10.1071/BT19124
Submitted: 18 July 2019  Accepted: 19 August 2020   Published: 5 October 2020

Abstract

The genus Teucrium includes perennial herbs or shrubs widespread all around the world. The wall germander (Teucrium chamaedrys L.) is widely used in traditional and modern medicine for various health disorders and recent research revealed that serpentine populations of this herb have increased antioxidant and respective medical potential compared with calcareous population. The present study aims to elucidate further the role of phenolic compounds for T. chamaedrys growth on serpentine soil. Methanol extracts from two serpentine and two non-serpentine (calcareous and siliceous) Bulgarian populations were obtained and analysed for total quantity of phenolics and flavonoids, and antioxidant activity. The serpentine soils acted as an elicitor of the antioxidant response in T. chamaedrys plants and the increased phenolics level correlated with enhanced antioxidant activity. The calcareous population had lower values but still higher than the siliceous population which had the lowest antioxidant values, although the flavonoid quantity that was equal to the serpentine populations. A gas chromatography-mass spectrometry (GC-MS) assay for identifying phenolic acids pointed to caffeic acid as a dominant compound, with additional cinnamic and benzoic acid derivatives with putative roles as antioxidants, in cell wall lignification for heavy metals chelation, and for interspecies interactions.

Keywords: antioxidant activity, caffeic acid, GC-MS, Lamiaceae, phenolic acids.


References

Alexander EB, Coleman RG, Keeler-Wolfe T, Harrison SP (2007) ‘Serpentine geoecology of western North America: geology, soils, and vegetation.’ (Oxford University Press: New York, NY, USA)

Batianoff GN, Reeves RD, Specht RL (1990) Stackhousia tryonii Bailey: a nickel-accumulating serpentine-endemic species of central Queensland. Australian Journal of Botany 38, 121–130.
Stackhousia tryonii Bailey: a nickel-accumulating serpentine-endemic species of central Queensland.Crossref | GoogleScholarGoogle Scholar |

Blum U, Gerig TM (2006) Interrelationships between p-coumaric acid, evapotranspiration, soil water content, and leaf expansion. Journal of Chemical Ecology 32, 1817–1834.
Interrelationships between p-coumaric acid, evapotranspiration, soil water content, and leaf expansion.Crossref | GoogleScholarGoogle Scholar | 16865532PubMed |

Brooks RR (1987) ‘Serpentine and its vegetation. A multidisciplinary approach. Vol. 1.’ (Dioscorides Press: Portland, OR, USA)

Bruce MC, Niu Y (2000) Evidence for Palaeozoic magmatism recorded in the Late Neoproterozoic Marlborough ophiolite, New England Fold Belt, central Queensland. Australian Journal of Earth Sciences 47, 1065–1076.
Evidence for Palaeozoic magmatism recorded in the Late Neoproterozoic Marlborough ophiolite, New England Fold Belt, central Queensland.Crossref | GoogleScholarGoogle Scholar |

Chang CC, Yang MH, Wen HM, Chern JC (2002) Estimation of total flavonoid content in propolis by two complementary colorimetric methods. Journal of Food and Drug Analysis 10, 178–182.

Chathuranga PKD, Dharmasena SKAT, Rajakaruna N, Iqbal MCM (2015) Growth and nickel uptake by serpentine and non-serpentine populations of Fimbristylis ovata (Cyperaceae) from Sri Lanka. Australian Journal of Botany 63, 128–133.
Growth and nickel uptake by serpentine and non-serpentine populations of Fimbristylis ovata (Cyperaceae) from Sri Lanka.Crossref | GoogleScholarGoogle Scholar |

Dias CN, Picoli EAT, Souza GA, Farag MA, Scotti MT, Filho JMB, Silva MS, Tavares JF (2017) Phenolics metabolism provides a tool for screening drought tolerant Eucalyptus grandis hybrids. Australian Journal of Crop Science 11, 1016–1024.
Phenolics metabolism provides a tool for screening drought tolerant Eucalyptus grandis hybrids.Crossref | GoogleScholarGoogle Scholar |

Díaz J, Bernal A, Pomar F, Merino F (2001) Induction of shikimate dehydrogenase and peroxidase in pepper (Capsicum annuum L.) seedlings in response to copper stress and its relation to lignification. Plant Science 161, 179–188.
Induction of shikimate dehydrogenase and peroxidase in pepper (Capsicum annuum L.) seedlings in response to copper stress and its relation to lignification.Crossref | GoogleScholarGoogle Scholar |

Elmasri WA, Hegazy MEF, Mechref Y, Paré PW (2016) Structure-antioxidant and anti-tumor activity of Teucrium polium phytochemicals. Phytochemistry Letters 15, 81–87.
Structure-antioxidant and anti-tumor activity of Teucrium polium phytochemicals.Crossref | GoogleScholarGoogle Scholar |

Fiehn O (2002) Metabolomics – the link between genotypes and phenotypes. Plant Molecular Biology 48, 155–171.
Metabolomics – the link between genotypes and phenotypes.Crossref | GoogleScholarGoogle Scholar | 11860207PubMed |

González-Chávez MCA, Carrillo-González R, Cuellar-Sánchez A, Delgado-Alvarado A, Suárez-Espinosa J, Ríos-Leal E, Solís-Domínguez FA, Maldonado-Mendoza IE (2019) Phytoremediation assisted by mycorrhizal fungi of a Mexican defunct lead-acid battery recycling site. Science of the Total Environment 650, 3134–3144.
Phytoremediation assisted by mycorrhizal fungi of a Mexican defunct lead-acid battery recycling site.Crossref | GoogleScholarGoogle Scholar |

Gursoy N, Tepe B (2009) Determination of the antimicrobial and antioxidative properties and total phenolics of two ‘endemic’ Lamiaceae species from Turkey: Ballota rotundifolia L. and Teucrium chamaedrys C. Koch. Plant Foods for Human Nutrition 64, 135–140.
Determination of the antimicrobial and antioxidative properties and total phenolics of two ‘endemic’ Lamiaceae species from Turkey: Ballota rotundifolia L. and Teucrium chamaedrys C. Koch.Crossref | GoogleScholarGoogle Scholar | 19455424PubMed |

Harrison SP, Rajakaruna N (2011) ‘Serpentine: the evolution and ecology of a model system.’ (University of California Press: Berkeley, CA, USA)

Hasanuzzaman M, Nahar K, Bhuiyan TH, Anee TI, Inafuku M, Oku H, Fujita M (2018) Salicylic acid: an all-rounder in regulating abiotic stress responses in plants. In ‘Phytohormones – signaling mechanisms and crosstalk in plant development and stress responses’. (Ed. MA El-Esawi) pp. 31–75. (IntechOpen) 10.5772/intechopen.68213

Hendry RA, Wormington KR (2013) Eucalypt forests as indicators of the gradients within the central Queensland serpentine landscape of Australia. Australian Journal of Botany 61, 544–551.
Eucalypt forests as indicators of the gradients within the central Queensland serpentine landscape of Australia.Crossref | GoogleScholarGoogle Scholar |

Huang JQ, Liao Y-C, Chen H-J, Zhang Z (2017) Chemical solution is an efficient method to induce the formation of 2-(2-phenylethyl) chromone derivatives in Aquilaria sinensis Phytochemistry Letters 19, 64–70.
Chemical solution is an efficient method to induce the formation of 2-(2-phenylethyl) chromone derivatives in Aquilaria sinensisCrossref | GoogleScholarGoogle Scholar |

Hussain MI, Reigosa MJ (2012) Seedling growth, leaf water status and signature of stable carbon isotopes in C3 perennials exposed to natural phytochemicals. Australian Journal of Botany 60, 676–684.
Seedling growth, leaf water status and signature of stable carbon isotopes in C3 perennials exposed to natural phytochemicals.Crossref | GoogleScholarGoogle Scholar |

Hussain MI, González L, Souto C, Reigosa MJ (2011) Ecophysiological responses of native plants to phytotoxic effect of Acacia melanoxylon R.Br. Agroforestry Systems 83, 149–166.
Ecophysiological responses of native plants to phytotoxic effect of Acacia melanoxylon R.Br.Crossref | GoogleScholarGoogle Scholar |

Inderjit , Duke SO (2003) Ecophysiological aspects of allelopathy. Planta 217, 529–539.
Ecophysiological aspects of allelopathy.Crossref | GoogleScholarGoogle Scholar | 12811559PubMed |

Kapchina-Toteva V, Dimitrova MA, Stefanova M, Koleva D, Kostov K, Yordanova ZhP, Stefanov D, Zhiponova MK (2014) Adaptive changes in photosynthetic performance and secondary metabolites during white dead nettle micropropagation. Journal of Plant Physiology 171, 1344–1353.
Adaptive changes in photosynthetic performance and secondary metabolites during white dead nettle micropropagation.Crossref | GoogleScholarGoogle Scholar | 25046755PubMed |

Kayama M, Sasa K, Koike T (2002) Needle life span, photosynthetic rate and nutrient concentration of Picea glehnii, P. jezoensis and P. abies planted on serpentine soil in northern Japan. Tree Physiology 22, 707–716.
Needle life span, photosynthetic rate and nutrient concentration of Picea glehnii, P. jezoensis and P. abies planted on serpentine soil in northern Japan.Crossref | GoogleScholarGoogle Scholar | 12091152PubMed |

Khan AG, Kuek C, Chaudhry TM, Khoo CS, Hayes WJ (2000) Role of plants, mycorrhizae and phytochelators in heavy metal contaminated land remediation. Chemosphere 41, 197–207.
Role of plants, mycorrhizae and phytochelators in heavy metal contaminated land remediation.Crossref | GoogleScholarGoogle Scholar | 10819202PubMed |

Khosh-Khui M, Ashiri F, Saharkhiz MJ (2012) Effects of irrigation regimes on antioxidant activity and total phenolic content of thyme (Thymus vulgaris L.). Medicinal & Aromatic Plants 1, 1000114

Klessig DF, Choi HW, Dempsey DA (2018) Systemic acquired resistance and salicylic acid: past, present, and future. Molecular Plant-Microbe Interactions 31, 871–888.
Systemic acquired resistance and salicylic acid: past, present, and future.Crossref | GoogleScholarGoogle Scholar | 29781762PubMed |

Kováčik J, Klejdus B, Bačkor M, Repčák M (2007) Phenylalanine ammonialyase activity and phenolic compounds accumulation in nitrogen-deficient Matricaria chamomilla leaf rosettes. Plant Science 172, 393–399.
Phenylalanine ammonialyase activity and phenolic compounds accumulation in nitrogen-deficient Matricaria chamomilla leaf rosettes.Crossref | GoogleScholarGoogle Scholar |

Krasteva I, Nedelcheva A, Pavlova D, Zdraveva P, Nikolov S (2013) Influence of the serpentine on the content of flavonoids in Hypericum populations growing in Bulgaria. African Journal of Pharmacy and Pharmacology 7, 1762–1765.
Influence of the serpentine on the content of flavonoids in Hypericum populations growing in Bulgaria.Crossref | GoogleScholarGoogle Scholar |

Kruckeberg A (1985) ‘California serpentines: flora, vegetation, geology, soil and management problems.’ (University of California Press: Berkeley, CA, USA)

Lavid N, Schwartz A, Yarden O, Tel-Or E (2001) The involvement of polyphenols and peroxidase activities in heavy metal accumulation by epidermal glands of the waterlily (Nymphaeaceae). Planta Medica 212, 323–331.

Li XJ, Xia ZC, Kong CH, Xu XH (2013) Mobility and microbial activity of allelochemicals in soil. Journal of Agricultural and Food Chemistry 61, 5072–5079.
Mobility and microbial activity of allelochemicals in soil.Crossref | GoogleScholarGoogle Scholar | 23647315PubMed |

Maksymiec W (1998) Effect of copper on cellular processes in higher plants. Photosynthetica 34, 321–342.
Effect of copper on cellular processes in higher plants.Crossref | GoogleScholarGoogle Scholar |

Masarovičová E, Králová K (2012) Plant–heavy metal interaction: phytoremediation, biofortification and nanoparticles. In ‘Advances in selected plant physiology aspect’. (Eds G Montanaro, B Dichio) pp. 75–102. (InTech: Rijeka, Croatia)

Michalak A (2006) Phenolic compounds and their antioxidant activity in plants growing under heavy metal stress. Polish Journal of Environmental Studies 15, 523–530.

Mitreski I, Stanoeva J, Stefova M, Stefkov G, Kulevanova S (2014) Polyphenols in representative Teucrium species in the flora of R. Macedonia: LC/DAD/ESI-MSn profile and content. Natural Product Communications 9, 175–180.
Polyphenols in representative Teucrium species in the flora of R. Macedonia: LC/DAD/ESI-MSn profile and content.Crossref | GoogleScholarGoogle Scholar | 24689284PubMed |

Moores EM (2011) Serpentinites and other ultramafic rocks. Why they are important for earth’s history and possibly for its future. In ‘Serpentine: the evolution and ecology of a model system’. (Eds SP Harrison, N Rajakaruna) pp. 3–28. (University of California Press: Berkeley, CA, USA)

Moyankova D, Mladenov P, Berkov S, Peshev D, Georgieva D, Djilianov D (2014) Metabolic profiling of the resurrection plant Haberlea rhodopensis during desiccation and recovery. Physiologia Plantarum 152, 675–687.
Metabolic profiling of the resurrection plant Haberlea rhodopensis during desiccation and recovery.Crossref | GoogleScholarGoogle Scholar | 24735127PubMed |

Murray CG (2007) Devonian supra-subduction zone setting for the Princhester and Northumberland serpentinites: implications for the tectonic evolution of the northern New England Orogen. Australian Journal of Earth Sciences 54, 899–925.
Devonian supra-subduction zone setting for the Princhester and Northumberland serpentinites: implications for the tectonic evolution of the northern New England Orogen.Crossref | GoogleScholarGoogle Scholar |

Nikolova MT, Berkov SH, Doycheva IV, Stoyanov SS, Stanilova MI (2018) GC/MS based metabolite profiling of five populations of Glaucium flavum (Ranunculales: Papaveraceae) from the Black Sea coast of Bulgaria. Acta Zoologica Bulgarica 11, 91–94.

O’Dell RE, Rajakaruna N (2011) Intraspecific variation, adaptation, and evolution. In ‘Serpentine: the evolution and ecology of a model system’. (Eds SP Harrison, N Rajakaruna) pp. 97–137. (University of California Press: Berkeley, CA, USA)

Palm E, Brady K, Van Volkenburgh E (2012) Serpentine tolerance in Mimulus guttatus does not rely on exclusion of magnesium. Functional Plant Biology 39, 679–688.
Serpentine tolerance in Mimulus guttatus does not rely on exclusion of magnesium.Crossref | GoogleScholarGoogle Scholar | 32480819PubMed |

Park SB, Kim JY, Han JY, Ahn CH, Park EJ, Choi YE (2017) Exploring genes involved in benzoic acid biosynthesis in the Populus davidiana transcriptome and their transcriptional activity upon methyl jasmonate treatment. Journal of Chemical Ecology 43, 1097–1108.
Exploring genes involved in benzoic acid biosynthesis in the Populus davidiana transcriptome and their transcriptional activity upon methyl jasmonate treatment.Crossref | GoogleScholarGoogle Scholar | 29129016PubMed |

Parry AD, Tiller SA, Edwards R (1994) The effects of heavy metals and root immersion on isoflavonoid metabolism in alfalfa (Medicago sativa L.). Plant Physiology 106, 195–202.
The effects of heavy metals and root immersion on isoflavonoid metabolism in alfalfa (Medicago sativa L.).Crossref | GoogleScholarGoogle Scholar | 12232319PubMed |

Pavlova D (2009) Morphological variation in Teucrium chamaedrys from serpentine and non-serpentine populations, soil and biota of serpentine: a world view. Northeastern Naturalist 16, 39–55.
Morphological variation in Teucrium chamaedrys from serpentine and non-serpentine populations, soil and biota of serpentine: a world view.Crossref | GoogleScholarGoogle Scholar |

Pavlova D, Karadjova I, Krasteva I (2015) Essential and toxic element concentrations in Hypericum perforatum. Australian Journal of Botany 63, 152–158.
Essential and toxic element concentrations in Hypericum perforatum.Crossref | GoogleScholarGoogle Scholar |

Prieto P, Pineda M, Aguilar M (1999) Spectrophotometric quantitation of antioxidant capacity through the formation of a phosphomolybdenum complex: Specific application to the determination of vitamin E1. Analytical Biochemistry 269, 337–341.
Spectrophotometric quantitation of antioxidant capacity through the formation of a phosphomolybdenum complex: Specific application to the determination of vitamin E1.Crossref | GoogleScholarGoogle Scholar | 10222007PubMed |

Racovita RC, Hen-Avivi S, Fernandez-Moreno JP, Granell A, Aharoni A, Jetter R (2016) Composition of cuticular waxes coating flag leaf blades and peduncles of Triticum aestivum cv. Bethlehem. Phytochemistry 130, 182–192.
Composition of cuticular waxes coating flag leaf blades and peduncles of Triticum aestivum cv. Bethlehem.Crossref | GoogleScholarGoogle Scholar | 27264640PubMed |

Radanović D, Mladenović S, Jakovljević M (2002) Influence of some soil characteristics on heavy metal content in Hypericum perforatum L. and Achillea millefolium L. Acta Horticulturae 576, 295–301.
Influence of some soil characteristics on heavy metal content in Hypericum perforatum L. and Achillea millefolium L.Crossref | GoogleScholarGoogle Scholar |

Rajakaruna N, Harris TB, Alexander EB (2009) Serpentine geoecology of eastern North America: a review. Rhodora 111, 21–108.
Serpentine geoecology of eastern North America: a review.Crossref | GoogleScholarGoogle Scholar |

Rajakaruna N, Knudsen KA, Fryday RE, O’Dell N, Pope F, Olday C, Woolhouse S (2012) Investigation of the importance of rock chemistry for saxicolous lichen communities of the New Idria serpentinite mass, San Benito County, California, USA. Lichenologist 44, 695–714.
Investigation of the importance of rock chemistry for saxicolous lichen communities of the New Idria serpentinite mass, San Benito County, California, USA.Crossref | GoogleScholarGoogle Scholar |

Rajkumar M, Ma Y, Freitas H (2008) Characterization of metal-resistant plant growth promoting Bacillus weihenstephanensis isolated from serpentine soil in Portugal. Journal of Basic Microbiology 48, 500–508.
Characterization of metal-resistant plant growth promoting Bacillus weihenstephanensis isolated from serpentine soil in Portugal.Crossref | GoogleScholarGoogle Scholar | 18785659PubMed |

Re R, Pellegrini N, Proteggente A, Pannala A, Yang M, Rice-Evans CA (1999) Antioxidant activity applying an improved ABTS radical cation decolorization assay. Free Radical Biology & Medicine 26, 1231–1237.
Antioxidant activity applying an improved ABTS radical cation decolorization assay.Crossref | GoogleScholarGoogle Scholar |

Riaz U, Kharal MA, Murtaza G, Zaman Q, Javaid S, Malik HA, Aziz H, Abbas Z (2019) Prospective roles and mechanisms of caffeic acid in counter plant stress: a mini review. Pakistan Journal of Agricultural Research 32, 8–19.

Rice-Evans CA, Miller NJ, Paganga G (1997) Antioxidant properties of phenolic compounds. Trends in Plant Science 2, 152–159.
Antioxidant properties of phenolic compounds.Crossref | GoogleScholarGoogle Scholar |

Rivero RM, Ruiz JM, Garcia PC, Lopez-Lefebre LR, Sanchez E, Romero L (2001) Resistance to cold and heat stress: accumulation of phenolic compounds in tomato and watermelon plants. Plant Science 160, 315–321.
Resistance to cold and heat stress: accumulation of phenolic compounds in tomato and watermelon plants.Crossref | GoogleScholarGoogle Scholar | 11164603PubMed |

Salam MMA, Mohsin M, Pulkkinen P, Pelkonen P, Pappinen A (2019) Effects of soil amendments on the growth response and phytoextraction capability of a willow variety (S. viminalis × S. schwerinii × S. dasyclados) grown in contaminated soils. Ecotoxicology and Environmental Safety 171, 753–770.
Effects of soil amendments on the growth response and phytoextraction capability of a willow variety (S. viminalis × S. schwerinii × S. dasyclados) grown in contaminated soils.Crossref | GoogleScholarGoogle Scholar | 30660969PubMed |

Santiago LJM, Louro RP, De Oliveira DE (2000) Compartmentation of phenolic compounds and phenylalanine ammonia-lyase in leaves of Phyllanthus tenellus Roxb. and their induction by copper sulphate. Annals of Botany 86, 1023–1032.
Compartmentation of phenolic compounds and phenylalanine ammonia-lyase in leaves of Phyllanthus tenellus Roxb. and their induction by copper sulphate.Crossref | GoogleScholarGoogle Scholar |

Schinella GR, Tournier HA, Pietro JM, Mordujovich de Buschiazzo P, Rios JL (2002) Antioxidant activity of anti-inflamatory plant extracts. Life Sciences 70, 1023–1033.
Antioxidant activity of anti-inflamatory plant extracts.Crossref | GoogleScholarGoogle Scholar | 11860151PubMed |

Singleton VL, Orthofer R, Lamuela-Raventós RM (1999) [14] Analysis of total phenols and other oxidation substrates and antioxidants by means of Folin–Ciocalteu reagent. Methods in Enzymology 299, 152–178.
[14] Analysis of total phenols and other oxidation substrates and antioxidants by means of Folin–Ciocalteu reagent.Crossref | GoogleScholarGoogle Scholar |

Solovchenko AE, Merzlyak MN (2008) Screening of visible and UV radiation as a photoprotective mechanism in plants. Russian Journal of Plant Physiology: a Comprehensive Russian Journal on Modern Phytophysiology 55, 719–737.
Screening of visible and UV radiation as a photoprotective mechanism in plants.Crossref | GoogleScholarGoogle Scholar |

Specht RL, Batianoff GN, Reeves RD (2002) The vegetation continuum on the Serpentine soil catena in the Rockhampton-Marlborough area. In ‘Marlborough serpentine, landscape management and conservation’. (Eds A Exelby, K Wormington, A Melzer) pp. 23–40. (Centre for Environmental Management, Central Queensland University: Rockhampton, Qld, Australia)

Specht R, Batianoff G, Reeves R (2006) Vegetation structure and biodiversity along the eucalypt forest to rainforest continuum on the serpentinite soil catena in a subhumid area of central Queensland, Australia. Austral Ecology 31, 394–407.
Vegetation structure and biodiversity along the eucalypt forest to rainforest continuum on the serpentinite soil catena in a subhumid area of central Queensland, Australia.Crossref | GoogleScholarGoogle Scholar |

Sreekanth TVM, Nagajyothi PC, Lee KD, Prasad TNVKV (2013) Occurrence, physiological responses and toxicity of nickel in plants. International Journal of Environmental Science and Technology 10, 1129–1140.
Occurrence, physiological responses and toxicity of nickel in plants.Crossref | GoogleScholarGoogle Scholar |

Stanković M, Topuzović M, Solujic S, Mihailović V (2010) Antioxidant activity and concentration of phenols and flavonoids in the whole plant and plant parts of Teucrium chamaerdys L. var. glanduliferum Haussk. Journal of Medicinal Plants Research 4, 2092–2098.

Stanković M, Curcić M, Zizić J, Topuzović M, Solujić S, Marković S (2011) Teucrium plant species as natural sources of novel anticancer compounds: antiproliferative, proapoptotic and antioxidant properties. International Journal of Molecular Sciences 12, 4190–4205.
Teucrium plant species as natural sources of novel anticancer compounds: antiproliferative, proapoptotic and antioxidant properties.Crossref | GoogleScholarGoogle Scholar | 21845072PubMed |

Stanković M, Stefanović O, Čomić L, Topuzović M, Radojević I, Solujić S (2012) Antimicrobial activity, total phenolic content and flavonoid concentrations of Teucrium species. Central European Journal of Biology 7, 664–671.

Sytar O, Cai Zh, Brestic M, Kumar A, Prasad MNV, Taran N, Smetanska I (2013) Foliar applied nickel on buckwheat (Fagopyrum esculentum) induced phenolic compounds as potential antioxidants. CLEAN – Soil, Air. Water 41, 1129–1137.
Foliar applied nickel on buckwheat (Fagopyrum esculentum) induced phenolic compounds as potential antioxidants.Crossref | GoogleScholarGoogle Scholar |

Szepesi A, Csiszár J, Gémes K, Horváth E, Horváth F, Simon ML, Tari I (2009) Salicylic acid improves acclimation to salt stress by stimulating abscisic aldehyde oxidase activity and abscisic acid accumulation, and increases Na+ content in leaves without toxicity symptoms in Solanum lycopersicum L. Journal of Plant Physiology 166, 914–925.
Salicylic acid improves acclimation to salt stress by stimulating abscisic aldehyde oxidase activity and abscisic acid accumulation, and increases Na+ content in leaves without toxicity symptoms in Solanum lycopersicum L.Crossref | GoogleScholarGoogle Scholar | 19185387PubMed |

Todorov D, Pavlova D, Hinkov A, Shishkova K, Dragolova D, Kapchina-Toteva V, Shishkov S (2015) Effect of extracts derived from Teucrium chamaedrys L. on Herpes simplex virus type 2. Dokladi na Bulgarskata Akademiâ na Naukite 68, 1519–1526.

Treutter D (2005) Significance of flavonoids in plant resistance and enhancement of their biosynthesis. Plant Biology 7, 581–591.
Significance of flavonoids in plant resistance and enhancement of their biosynthesis.Crossref | GoogleScholarGoogle Scholar | 16388461PubMed |

Tutin T, Wood D (1972) Teucrium. In ‘Flora Europaea’. (Eds T Tutin, VH Heywood, NA Burges, DH Valentine, DM Moore, PW Ball, SM Walters, AO Chater, DA Webb, RA DeFilipps, IK Ferguson, IBK Richardson) pp. 129–135. (Cambridge University Press: Cambridge, UK)

van der Ent A, Rajakaruna N, Boyd RS, Echevarria G, Repin R, Williams D (2015) Global research on ultramafic (serpentine) ecosystems (8th International Conference on Serpentine Ecology in Sabah, Malaysia). Australian Journal of Botany 63, iii–iv.
Global research on ultramafic (serpentine) ecosystems (8th International Conference on Serpentine Ecology in Sabah, Malaysia).Crossref | GoogleScholarGoogle Scholar |

Venter A, Levanets A, Siebert S, Rajakaruna N (2015) A preliminary survey of the diversity of soil algae and cyanoprokaryotes on mafic and ultramafic substrates in South Africa. Australian Journal of Botany 63, 341–352.
A preliminary survey of the diversity of soil algae and cyanoprokaryotes on mafic and ultramafic substrates in South Africa.Crossref | GoogleScholarGoogle Scholar |

Vicić DD, Stoiljković MM, Sabovljević MS, Stevanović BM (2015) Seasonal changes in photosynthetic 1 rate and pigment content in two populations of the monotypic Balkan serpentine endemic Halacsya sendtneri. Australian Journal of Botany 63, 167–171.
Seasonal changes in photosynthetic 1 rate and pigment content in two populations of the monotypic Balkan serpentine endemic Halacsya sendtneri.Crossref | GoogleScholarGoogle Scholar |

Vlase L, Benedec D, Hanganu D, Damian G, Csillag I (2014) Evaluation of antioxidant and antimicrobial activities and phenolic profile for Hyssopus officinalis, Ocimum basilicum and Teucrium chamaedrys. Molecules 19, 5490–5507.
Evaluation of antioxidant and antimicrobial activities and phenolic profile for Hyssopus officinalis, Ocimum basilicum and Teucrium chamaedrys.Crossref | GoogleScholarGoogle Scholar | 24786688PubMed |

Yordanova ZP, Rogova MA, Zhiponova MK, Georgiev MI, Kapchina-Toteva VM (2017) Comparative determination of the essential oil composition in Bulgarian endemic plant Achillea thracica Velen. during the process of ex situ conservation. Phytochemistry Letters 20, 456–461.
Comparative determination of the essential oil composition in Bulgarian endemic plant Achillea thracica Velen. during the process of ex situ conservation.Crossref | GoogleScholarGoogle Scholar |

Zdraveva P, Pavlova D, Krasteva I, Pencheva I (2018) Phytochemical analysis on populations of Teucrium chamaedrys from serpentine sites in Bulgaria. Dokladi na Bulgarskata Akademiâ na Naukite 71, 185–192.

Zhu H, Zhang R, Chen W, Gu Z, Xie X, Zhao H, Yao Q (2015) The possible involvement of salicylic acid and hydrogen peroxide in the systemic promotion of phenolic biosynthesis in clover roots colonized by arbuscular mycorrhizal fungus. Journal of Plant Physiology 178, 27–34.
The possible involvement of salicylic acid and hydrogen peroxide in the systemic promotion of phenolic biosynthesis in clover roots colonized by arbuscular mycorrhizal fungus.Crossref | GoogleScholarGoogle Scholar | 25765360PubMed |

Zlatić NM, Stanković MS, Simić ZS (2017) Secondary metabolites and metal content dynamics in Teucrium montanum L. and Teucrium chamaedrys L. from habitats with serpentine and calcareous substrate. Environmental Monitoring and Assessment 189, 110
Secondary metabolites and metal content dynamics in Teucrium montanum L. and Teucrium chamaedrys L. from habitats with serpentine and calcareous substrate.Crossref | GoogleScholarGoogle Scholar | 28210892PubMed |

Zornoza P, Vázquez S, Esteban E, Fernández-Pascual M, Carpena R (2002) Cadmium-stress in nodulated white lupin: strategies to avoid toxicity. Plant Physiology and Biochemistry 40, 1003–1009.
Cadmium-stress in nodulated white lupin: strategies to avoid toxicity.Crossref | GoogleScholarGoogle Scholar |