Plant Growth Regulation

, Volume 84, Issue 2, pp 383–394 | Cite as

Ecophysiological and phytochemical responses of Salvia sinaloensis Fern. to drought stress

  • Matteo Caser
  • Francesca D’Angiolillo
  • Walter Chitarra
  • Claudio Lovisolo
  • Barbara Ruffoni
  • Luisa Pistelli
  • Laura Pistelli
  • Valentina Scariot
Original paper
  • 71 Downloads

Abstract

Salvia sinaloensis Fern. (sage) is a medicinal plant containing plant secondary metabolites (PSMs) with antioxidant properties. The current study investigated the effects of drought stress on S. sinaloensis morphological and ecophysiological traits, and active constituent production. Sage plants were cultivated in controlled conditions for 34 days and exposed to full irrigation as control, half irrigation, or no irrigation. Changes in growth index (G.I.), dry biomass, leaf water potential (LWP), physiological parameters, active compounds, volatilome (BVOCs) and essential oils (EOs) were determined. Not irrigated plants showed a decrease in total chlorophyll content (~ − 14.7%) and growth (G.I., ~ − 59.4%) from day 18, and dry biomass at day 21 (− 56%), when the complete leaf withering occurred (LWP, − 1.10 MPa). Moderate drought stressed plants showed similar trends for chlorophyll content and growth but kept a constant LWP (− 0.35 MPa) and dry biomass throughout the experiment, as control plants. Carotenoids were not affected by water regimes. The photosynthetic apparatus tolerated mild to severe water deficits, without a complete stomatal closure. Plants under both stress conditions increased the percentage of phenols and flavonoids and showed altered BVOC and EO chemical profiles. Interestingly Camphor, the main EO oxygenated monoterpene, increased in moderate stressed plants while the sesquiterpene hydrocarbon Germacrene D decreased. The same trend was seen in the headspace under stress severity. The data evidenced a possible role of the active molecules in the response of S. sinaloensis plants to drought stress. Taking together, these findings point at S. sinaloensis as a potential drought adaptive species, which could be used in breeding strategies to obtain sages with high quality PSMs, saving irrigation water.

Keywords

Antioxidant activity BVOCs Drought stress EOs Monoterpenes Sage 

Abbreviations

BVOCs

Biogenic volatile organic compounds

EOs

Essential pils

PSMs

Plant secondary metabolites

MAPs

Medicinal and aromatic plants

CC

Container capacity

LWP

Leaf water potential

Ci

Internal CO2 concentration

E

Transpiration rate

gs

Stomatal conductance

A

Net photosynthetic rate

G.I.

Growth index

FRAP

Ferric reducing antioxidant power

Fe3+-TPTZ

Ferric tripyridyl triazine

SPME

Solid phase micro extraction

GC-EIMS

Gas chromatography–electron impact mass spectrometry

WUE

Water use efficiency

FW

Fresh weight

DW

Dry weight

Notes

Acknowledgements

This research was partially funded by the INTERREG-ALCOTRA 2007–2013 Project “AROMA” (n. 68). Authors acknowledged Claudio Cervelli and Paolo Lo Turco for plant furnishing and multiplication.

Supplementary material

10725_2017_349_MOESM1_ESM.docx (30 kb)
Supplementary material 1 (DOCX 29 KB)

References

  1. Abreu ME, Munné-Bosch S (2008) Salicylic acid may be involved in the regulation of drought-induced leaf senescence in perennials: a case study in field-grown Salvia officinalis L. plants. Env Exp Bot 64:105–112CrossRefGoogle Scholar
  2. Abreu ME, Müller M, Alegre L, Munné-Bosch S (2008) Phenolic diterpene and α-tocopherol contents in leaf extracts of 60 Salvia species. J Sci Food Agric 88:2648–2653CrossRefGoogle Scholar
  3. Abu-Darwish MS, Cabral C, Ferreira IV, Gonçalves MJ, Cavaleiro C, Cruz MT, Al-bdour TH, Salgueiro L (2013) Essential oil of common sage (Salvia officinalis L.) from Jordan: assessment of safety in mammalian cells and its antifungal and anti-inflammatory potential. Biomed Res Int 2013:538940PubMedPubMedCentralCrossRefGoogle Scholar
  4. Adams RP (1995) Identification of essential oil components by gas chromatography-mass spectroscopy. Allured, Carol StreamGoogle Scholar
  5. Alfieri A, Maione F, Bisio A, Romussi G, Mascolo N, Cicala C (2007) Effect of a diterpenoid from Salvia cinnabarina on arterial blood pressure in rats. Phytother Res 21:690–692PubMedCrossRefGoogle Scholar
  6. Ali F, Bano A, Fazal A (2017) Recent methods of drought stress tolerance in plants. Plant Growth Regul 82:363–375CrossRefGoogle Scholar
  7. Alvarez S, Navarro A, Nicolas E, Sanchez-Blanco MJ (2011) Transpiration, photosynthetic responses, tissue water relations and dry mass partitioning in Callistemon plants during drought conditions. Sci Hortic 129(2):306–312CrossRefGoogle Scholar
  8. Azhar N, Hussain B, Ashraf MY, Abbasi KY (2011) Water stress mediated changes in growth, physiology and secondary metabolites of desi ajwain (Trachyspermum ammi L.). Pak J Bot 43:15–19Google Scholar
  9. Baher ZF, Mirza M, Ghorbanli M, Rezaii MB (2002) The influence of water stress on plant height, herbal and essential oil yield and composition in Satureja hortensis L. Flavour Frag J 17:275–277CrossRefGoogle Scholar
  10. Ben Farhat M, Landoulsi A, Chaouch-Hamada R, Sotomayor JA, Jordán MJ (2013) Characterization and quantification of phenolic compounds and antioxidant properties of Salvia species growing in different habitats. Ind Crop Prod 49:904–914CrossRefGoogle Scholar
  11. Ben Taarit M, Msaada K, Hosni K, Hammami M, Kchouk ME, Marzouk B (2009) Plant growth, essential oil yield and composition of sage (Salvia officinalis L.) fruits cultivated under salt stress conditions. Ind Crops Prod 30:333–337CrossRefGoogle Scholar
  12. Bertin N, Staudt M (1996) Effect of water stress on monoterpene emissions from young potted holm oak (Quercus ilex L.) trees. Oecologia 107:456–462PubMedCrossRefGoogle Scholar
  13. Bettaieb I, Zakhama N, Aidi Wannes W, Kchouk ME, Marzouk B (2009) Water deficit effects on Salvia officinalis fatty acids and essential oils composition. Sci Hortic 120:271–275CrossRefGoogle Scholar
  14. Bettaieb I, Hamrouni-Sellami I, Bourgou S, Limam F, Marzouk B (2011) Drought effects on polyphenol composition and antioxidant activities in aerial parts of Salvia officinalis L. Acta Physiol Plant 33:1103–1111CrossRefGoogle Scholar
  15. Bor M, Özdemir F, Türkan I (2003) The effect of salt stress on lipid peroxidation and antioxidants in leaves of sugar beet Beta vulgaris L. and wild beet Beta maritima L. Plant Sci 164:77–84CrossRefGoogle Scholar
  16. Bretzel F, Benvenuti S, Pistelli L (2014) Metal contamination in urban street sediment in Pisa (Italy) can affect the production of antioxidant metabolites in Taraxacum officinale Weber. Environ Sci Pollut Res 21:2325–2333CrossRefGoogle Scholar
  17. Burnett SE, Pennisi SV, Thomas PA, van Iersel MW (2005) Controlled drought affects morphology and anatomy of Salvia splendens. J Am Soc Hortic Sci 130:775–781Google Scholar
  18. Cai X, Starman T, Niu G, Hall C, Lombardini L (2012) Response of selected garden rose to drought stress. HortScience 47:1050–1055Google Scholar
  19. Caser M, Ruffoni B, Scariot V (2012) Screening for drought tolerance in Salvia spp. and Helichrysum petiolare: a way to select low maintenance ornamental plants. Acta Hortic 953:239–246CrossRefGoogle Scholar
  20. Caser M, Scariot V, Gaino W, Larcher F, Devecchi M (2013) The effects of sodium chloride on the aesthetic value of Buxus spp. Eur J Hortic Sci 78:153–159Google Scholar
  21. Caser M, D’Angiolillo F, Chitarra W, Lovisolo C, Ruffoni B, Pistelli L, Pistelli L, Scariot V (2016) Water deficit trigger changes in valuable physiological and phytochemical parameters in Helichrysum petiolare Hilliard & B.L. Burtt. Ind Crops Prod 83:680–692CrossRefGoogle Scholar
  22. Caser M, Lovisolo C, Scariot V (2017) The influence of water stress on growth, ecophysiology and ornamental quality of potted Primula vulgaris ‘Heidy’ plants. New insights to increase water use efficiency in plant production. Plant Growth Regul 83:361–373CrossRefGoogle Scholar
  23. Castelli F, Contillo R, Miceli F (1996) Non-destructive determination of leaf chlorophyll content in four crop species. J Agric Crop Sci 4:275–283CrossRefGoogle Scholar
  24. Comas L, Becker S, Cruz VMV, Byrne PF, Dierig DA (2013) Root traits contributing to plant productivity under drought. Front Plant Sci 4:442PubMedPubMedCentralCrossRefGoogle Scholar
  25. Davies NW (1990) Gas chromatographic retention indexes of monoterpenes and sesquiterpenes on methyl silicone and carbowx20M phases. J Chrom 503:1–24CrossRefGoogle Scholar
  26. de Abreu IN, Mazzafera P (2005) Effect of water and temperature stress on the content of active constituents of Hypericum brasiliense Choisy. Plant Physiol Biochem 43(3):241–248CrossRefGoogle Scholar
  27. di Ferdinando M, Brunetti C, Agati G, Tattini M (2014) Multiple functions of polyphenols in plants inhabiting unfavorable Mediterranean areas. Environ Exp Bot 103:107–116CrossRefGoogle Scholar
  28. Dicke M, Baldwin IT (2010) The evolutionary context for herbivore-induced plant volatiles: beyond the ‘cry for help’. Trends Plant Sci 15:167–175PubMedCrossRefGoogle Scholar
  29. Du GH, Zhang JT (2004) The general situation and progress of the modern research of red sage root (Radix Salviae miltiorrhizae). II. Yiyao Daobao 23:435–440Google Scholar
  30. Dunford NT, Vazquez RS (2005) Effect of water stress on plant growth and thymol and carvacrol concentrations in Mexican oregano grown under controlled conditions. J Appl Hortic 7:20–22Google Scholar
  31. Eakes DJ, Wright RD, Seiler JR (1991) Moisture stress conditioning effects on Salvia splendens ‘Bonfire’. J Am Soc Hortic Sci 116:716–719Google Scholar
  32. Farmacopea Ufficiale della Repubblica Italiana (1991) 9th edn. Istituto Poligrafico Zecca dello Stato, RomaGoogle Scholar
  33. Farooq M, Wahid A, Kobayashi N, Fujita D, Basra SMA (2009) Plant drought stress: effects, mechanisms and management. Agric Sustain Dev 29:185–212CrossRefGoogle Scholar
  34. Fleta-Soriano E, Munné-Bosch S (2016) Stress memory and the inevitable effects of drought: a physiological perspective. Front Plant Sci 7:143PubMedPubMedCentralCrossRefGoogle Scholar
  35. Galmés J, Medrano H, Flexas J (2007) Photosynthetic limitations in response to water stress and recovery in Mediterranean plants with different growth forms. New Phytol 175:81–93PubMedCrossRefGoogle Scholar
  36. Gray DE, Pallardy SG, Garrett HE, Rottinghaus G (2003) Acute drought stress and plant age effects on alkamide and phenolic acid content in purple coneflower roots. Planta Med 69:50–55PubMedCrossRefGoogle Scholar
  37. Guerfel M, Baccouri O, Boujnah D, Chaibi W, Zarrouk M (2009) Impacts of water stress on gas exchange, water relations, chlorophyll content and leaf structure in the two main Tunisian olive (Olea europaea L.) cultivars. Sci Hortic 119:257–263CrossRefGoogle Scholar
  38. Gulen H, Eris A (2004) Effect of heat stress on peroxidase activity and total protein content in strawberry plants. Plant Sci 166:739–744CrossRefGoogle Scholar
  39. Hamerlynck EP, McAllister CA, Knapp AK, Ham JM, Owensby CE (1997) Photosynthetic gas exchange and water relation responses of three tallgrass prairie species to elevated carbon dioxide and moderate drought. Int J Plant Sci 158:608–616CrossRefGoogle Scholar
  40. Hansen U, van Eijk J, Bertin N, Staudt M, Kotzias D, Seufert G, Fugit JL, Torres L, Cecinato A, Brancaleoni E, Ciccioli P, Bomboi T (1997) Biogenic emissions and CO2 gas exchange investigated on four Mediterranean shrubs. Atmos Environ 31:157–166CrossRefGoogle Scholar
  41. Hargrave KR, Kolb KJ, Ewers FW, Davis SD (1994) Conduit diameter and drought-induced embolism in Salvia mellifera Greene (Labiatae). New Phytol 126:695–705CrossRefGoogle Scholar
  42. Hessini K, Martinez JP, Gandour M, Albouchi A, Soltani A, Abdelly C (2009) Effect of water stress on growth, osmotic adjustment, cell wall elasticity and water-use efficiency in Spartina alterniflora. Environ Exp Bot 67:312–319CrossRefGoogle Scholar
  43. Hidalgo PR, Harkess RL (2002) Earthworm castings as a substrate for poinsettia production. HortScience 37:304–308Google Scholar
  44. Holopainen JK, Gershenzon J (2010) Multiple stress factors and the emission of plant VOCs. Trends Plant Sci 15:176–184PubMedCrossRefGoogle Scholar
  45. Hosseinzadeh H, Arabsanavi J (2001) Anticonvulsant effect of Salvia leriifolia Benth. Seed and leaf extracts in mice. Iran J Basic Med Sci 3:163–170Google Scholar
  46. Imanshahidi M, Hosseinzadeh H (2006) The pharmacological effects of Salvia species on the central nervous system. Phytother Res 20:427–437PubMedCrossRefGoogle Scholar
  47. Jaafar HZE, Ibrahim MH, Fakri NFM (2012) Impact of soil field water capacity in secondary metabolites, phenylalanine ammonia-lyase (PAL), maliondialdehyde (MDA) and photosynthetic responses of Malaysian kacip Fatimah (Labisia pumila Benth). Molecules 17:7305–7322PubMedCrossRefGoogle Scholar
  48. Jaleel CA, Gopi R, Sankar B, Gomathinayagam M, Panneerselvam R (2008) Differential responses in water use efficiency in two varieties of Catharanthus roseus under drought stress. C R Biologies 331:42–47PubMedCrossRefGoogle Scholar
  49. Jaleel CA, Manivannan P, Wahid A, Farooq M, Somasundaram R, Panneerselvam R (2009) Drought stress in plants: a review on morphological characteristics and pigments composition. Int J Agric Biol 11:100–105Google Scholar
  50. Kachenko AG, Bhatia N, Singh B (2011) Influence of drought stress on the nickel-hyperaccumulating shrub Hybanthus floribundus (Lindl.) F. Muell. Subsp. floribundus. Int J Plant Sci 172(3):315–322CrossRefGoogle Scholar
  51. Kamatou GPP, Van Vuuren SF, Van Heerden FR, Seaman T, Viljoen AM (2007) Antibacterial and antimycobacterial activities of South African Salvia species and isolated compounds from S. chamelaegnea. South Afr J Bot 73:552–557CrossRefGoogle Scholar
  52. Kaminska-Rozek E, Pukacki PM (2004) Effect of water deficit on oxidative stress and degradation of cell membranes in needles of Norway spruce (Picea abies (L.) Karst.). Acta Physiol Plant 26:431–442CrossRefGoogle Scholar
  53. Kavar T, Maras M, Kidric M, Sustar-Vozlic J, Meglic V (2007) Identification of genes involved in the response of leaves of Phaseolus vulgaris to drought stress. Mol Breed 21:159–172CrossRefGoogle Scholar
  54. Kim DO, Jeong SW, Lee CY (2003) Antioxidant capacity of phenolic phytochemicals from various cultivars of plums. Food Chem 81(3):321–326CrossRefGoogle Scholar
  55. Kleinwächter M, Paulsen J, Bloem E, Schnug E, Selmar D (2015) Moderate drought and signal transducer induced biosynthesis of relevant secondary metabolite in thyme (Thymus vulgaris), greater celandine (Chelidonium majus) and parsley (Petroselinum crispum). Ind Crops Prod 64:158–166CrossRefGoogle Scholar
  56. Kramer PJ, Boyer JS (1995) Water relations of plants and soils. Academic Press, New YorkGoogle Scholar
  57. Kubota N, Mimura H, Shimamura K (1988) The effects of drought and flooding on the phenolic compounds in peach fruits. Sci Rep Fac Agric Okayama Univ 171:17–21Google Scholar
  58. Lambrecht SC, Santiago LS, DeVan CM, Cervera JC, Stripe CM, Buckingham LA, Pasquini SC (2011) Plant water status and hydraulic conductance during flowering in the southern California coastal sage shrub Salvia mellifera (Lamiaceae). Am J Bot 98:1286–1292PubMedCrossRefGoogle Scholar
  59. Lazaridou M, Koutroubas SD (2004) Drought effect on water use efficiency of berseem clover at various growth stages. In: New directions for a diverse planet: Proceedings of the 4th International Crop Science Congress Brisbane, Australia, vol. 26Google Scholar
  60. Lichtenthaler HK (1987) Chlorophylls and carotenoids: pigments of photosynthetic biomembranes. Meth Enzymol 148:350–382CrossRefGoogle Scholar
  61. Liu F, Stützel H (2004) Biomass partitioning, specific leaf area, and water use efficiency of vegetable amaranth (Amaranthus spp.) in response to drought stress. Sci Hortic 102:15–27CrossRefGoogle Scholar
  62. Liu F, Andersen MN, Jacobsen SE, Jensen CR (2005) Stomatal control and water use efficiency of soybean (Glycine max L. Merr.) during progressive soil drying. Environ Exp Bot 54:33–40CrossRefGoogle Scholar
  63. Liu H, Wang X, Wang D, Zou Z, Liang Z (2011) Effect of drought stress on growth and accumulation of active constituents in Salvia miltiorrhiza Bunge. Ind Crops Prod 33:84–88CrossRefGoogle Scholar
  64. Llusia J, Peñuelas J (1998) Changes in terpene content and emission in potted Mediterranean woody plants under severe drought. Can J Bot 76:1366–1373Google Scholar
  65. Loreto F, Schnitzler JP (2010) Abiotic stresses and induced BVOCs. Trends Plant Sci 15:154–166PubMedCrossRefGoogle Scholar
  66. Loreto F, Fischbach RJ, Schnitzler JP, Ciccioli P, Brancaleoni E, Calfapietra C, Seufer G (2001) Monoterpene emission and monoterpene synthase activities in the Mediterranean evergreen oak Quercus ilex L. grown at elevated CO2 concentrations. Glob Change Biol 7:709–717CrossRefGoogle Scholar
  67. Loreto F, Dicke M, Schnitzler JP, Turlings TCJ (2014) Plant volatiles and the environment. Plant Cell Environ 37:1905–1908PubMedCrossRefGoogle Scholar
  68. Lovisolo C, Perrone I, Carra A, Ferrandino A, Flexas J, Medrano H, Schubert A (2010) Drought-induced changes in development and function of grapevine (Vitis spp.) organs and in their hydraulic and non hydraulic interactions at the whole plant level: a physiological and molecular update. Funct Plant Biol 37:98–116CrossRefGoogle Scholar
  69. Lubbe A, Verpoorte R (2011) Cultivation of medicinal and aromatic plants for specialty industrial materials. Ind Crops Prod 34:785–801CrossRefGoogle Scholar
  70. Maatallah S, Nasri N, Hajlaoui H, Albouchi A, Elaissi A (2016) Evaluation changing of essential oil of laurel (Laurus nobilis L.) under water deficit stress conditions. Ind Crops Prod 91:170–178CrossRefGoogle Scholar
  71. Medrano H, Tomas M, Martorell S, Flexas J, Hernandez E, Rossello J, Pou A, Escalona JM, Bota J (2015) From leaf to whole-plant water use efficiency (WUE) in complex canopies: limitations of leaf WUE as a selection target. Crop J 3(3):220–228CrossRefGoogle Scholar
  72. Monclus R, Dreyer E, Villar M, Delmotte FM, Delay D, Petit JM, Barbaroux C, Thiec D, Bréchet C, Brignolas F (2006) Impact of drought on productivity and water use efficiency in 29 genotypes of Populus deltoides × Populus nigra. New Phytol 169:765–777PubMedCrossRefGoogle Scholar
  73. Munné-Bosch S, Peñuelas J (2003) Photo- and antioxidative protection, and a role for salicyclic acid during drought and recovery in field-grown Phillyrea angustifolia plants. Planta 217:758–766PubMedCrossRefGoogle Scholar
  74. Munné-Bosch S, Mueller M, Schwarz K, Alegre L (2001) Diterpenes and antioxidative protection in drought-stressed Salvia officinalis plants. J Plant Physiol 11:1431–1437CrossRefGoogle Scholar
  75. Niinemets Ü, Loreto F, Reichstein M (2004) Physiological and physicochemical controls on foliar volatile organic compound emissions. Trends Plant Sci 9:180–186PubMedCrossRefGoogle Scholar
  76. Niinemets Ü, Kännaste A, Copolovici L (2013) Quantitative patterns between plant volatile emissions induced by biotic stresses and the degree of damage. Front Plant Sci 4:262PubMedPubMedCentralCrossRefGoogle Scholar
  77. Nogués S, Allen DJ, Morison JIL, Baker NR (1998) Ultraviolet-B radiation effects on water relations, leaf development, and photosynthesis in droughted pea plants. Plant Physiol 117:173–181PubMedPubMedCentralCrossRefGoogle Scholar
  78. Nogués I, Muzzini V, Loreto F, Bustamante MA (2015) Drought and soil amendment effects on monoterpene emission in rosemary plants. Sci Total Environ 538:768–778PubMedCrossRefGoogle Scholar
  79. Novak J (2017) Letter to the Editor on “How to implement GACP of MAPs? A practical implementation guide to Good Agricultural and Wild Collection Practices (GACP)”. J Appl Res Med Aromat Plants.  https://doi.org/10.1016/j.jarmap.2016.12.003 Google Scholar
  80. Nowak M, Kleinwächter M, Manderscheid R, Weigel HJ, Selmar D (2010) Drought stress increases the accumulation of monoterpenes in sage (Salvia officinalis), an effect that is compensated by elevated carbon dioxide concentration. J Appl Bot Food Qual 83:133–136Google Scholar
  81. Oren R, Sperry JS, Katul GG, Pataki DE, Ewers BE, Phillips N, Schäfer KVR (1999) Survey and synthesis of intra- and interspecific variation in stomatal sensitivity to vapour pressure deficit. Plant Cell Env 22:1515–1526CrossRefGoogle Scholar
  82. Ormeño E, Mévy JP, Vila B, Bousquet Mélou A, Greff S, Bonin G, Fernandez C (2007) Water deficit stress induces different monoterpene and sesquiterpene emission changes in Mediterranean species. Relationship between terpene emissions and plant water potential. Chemosphere 67:276–284PubMedCrossRefGoogle Scholar
  83. Ormeño E, Romain O, Mevy JP, Baldy V, Fernandez C (2009) Compost may affect volatile and semi-volatile plant emissions through nitrogen supply and chlorophyll fluorescence. Chemosphere 77:94–104PubMedCrossRefGoogle Scholar
  84. Paquin R, Mehuys GR (1980) Influence of soil moisture on cold tolerance of alfalfa. Can J Plant Sci 60:139–147CrossRefGoogle Scholar
  85. Pastenes C, Pimentel P, Lillo J (2005) Leaf movements and photoinhibition in relation to water stress in field-grown beans. J Exp Bot 56:425–433PubMedCrossRefGoogle Scholar
  86. Paulsen J, Selmar D (2016) The difficulty of correct reference values when evaluating the effects of drought stress: a case study with Thymus vulgaris. J Appl Bot Food Qual 89:287–289Google Scholar
  87. Petropoulos SA, Daferera D, Polissiou MG, Passam HC (2008) The effect of water deficit stress on the growth, yield and composition of essential oils of parsley. Sci Hortic 115:393–397CrossRefGoogle Scholar
  88. Pirbalouti AG, Samani MR, Hashemi M, Zeinali H (2014) Salicylic acid affects growth, essential oil and chemical compositions of thyme (Thymus daenensis Celak.) under reduced irrigation. Plant Growth Regul 72:289–301CrossRefGoogle Scholar
  89. Pistelli L, Noccioli C, D’Angiolillo F, Pistelli L (2013) Composition of volatile in micropropagated and field grown aromatic plants from Tuscany Islands. Acta Biochim Pol 60:43–50PubMedGoogle Scholar
  90. Possell M, Loreto F (2013) The role of volatile organic compounds in plant resistance to abiotic stresses: responses and mechanisms. In: Biology, controls and models of tree volatile organic compound emissions (Eds Ü. Niinemets, RK Monson). Springer, Berlin, pp 209–235CrossRefGoogle Scholar
  91. Radwan A, Kleinwachter M, Selmar D (2017) Impact of drought stress on specialised metabolism: biosynthesis and the expression of monoterpene synthases in sage (Salvia officinalis). Phytochemistry 141:20–26PubMedCrossRefGoogle Scholar
  92. Raut JS, Karuppayil SM (2014) A status review on the medicinal properties of essential oils. Ind Crops Prod 62:250–264CrossRefGoogle Scholar
  93. Rauter AP, Dias C, Martins A, Branco I, Neng NR, Nogueira JM, Goulart M, Silva FVM, Justino J, Trevitt C, Waltho JP (2012) Non-toxic Salvia sclareoides Brot. extracts as a source of functional food ingredients: phenolic profile, antioxidant activity and prion binding properties. Food Chem 132:1930–1935CrossRefGoogle Scholar
  94. Rinnan R, Steinke M, McGenity T, Loreto F (2014) Plant volatiles in extreme terrestrial and marine environments. Plant Cell Environ 37:1776–1789PubMedCrossRefGoogle Scholar
  95. Ruberto G, Baratta MT (2000) Antioxidant activity of selected essential oil components in two lipid model systems. Food Chem 69:167–174CrossRefGoogle Scholar
  96. Schachtman DP, Goodger JQD (2008) Chemical root to shoot signaling under drought. Trends Plant Sci 13:281–287PubMedCrossRefGoogle Scholar
  97. Scholander PF, Hammel HT, Bradstreet ED, Hemmingsen EA (1965) Sap pressure in vascular plants. Negative hydrostatic pressure can be measured in plants. Science 148:339–346PubMedCrossRefGoogle Scholar
  98. Selmar D, Kleinwachter M (2013) Influencing the product quality by deliberately applying drought stress during the cultivation of medicinal plants. Ind Crops Prod 42:558–666CrossRefGoogle Scholar
  99. Singleton VL, Rossi JAJ (1965) Colorimetry of total phenolics with phosphomolybdic–phosphotungstic acid reagent. Am J Enol Vitic 16:144–158Google Scholar
  100. Skirycz A, Inzé D (2010) More from less: plant growth under limited water. Curr Opin Biotechnol 21:197–203PubMedCrossRefGoogle Scholar
  101. Steinbrecher F, Hauff K, Hakola H, Rössler J (1999) A revised parameterization for emission modeling of isoprenoids for boreal plants. In: Laurilla T, Lindfors V (eds) Biogenic VOC emissions and phytochemistry in the boreal regions of Europe air pollution research report 70. Commission of European Communities, Luxembourg, pp 29–43Google Scholar
  102. Swigar AA, Silverstein RM (1981) Monoterpenes. Aldrich, MilwaukeeGoogle Scholar
  103. Szôllôsi R, Szôllôsi Varga I (2002) Total antioxidant power in some species of Labiatae (adaptation of FRAP method). Acta Biol Szegediensis 46:125–127Google Scholar
  104. Turtola S, Manninen A, Rikal R, Kainulainen P (2003) Drought stress alters the concentration of wood terpenoids in scots pine and Norway spruce seedling. J Chem Ecol 29:1981–1995PubMedCrossRefGoogle Scholar
  105. Viera HJ, Bergamaschi H, Angelocci LR, Libardi PL (1991) Performance of two bean cultivars under two water availability regimes. II. Stomatal resistance to vapour diffusion, transpiration flux density and water potential in the plant (in Portugal). Pesqui Agropecu Bras 9:1035–1045Google Scholar
  106. Zhao J, Davis LC, Verpoorte R (2005) Elicitor signal transduction leading to production of plant secondary metabolites. Biotechnol Adv 23:283–333PubMedCrossRefGoogle Scholar

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Authors and Affiliations

  1. 1.Department of Agricultural, Forest and Food SciencesUniversity of TorinoGrugliasco (TO)Italy
  2. 2.Department of Agriculture, Food, and EnvironmentUniversity of PisaPisaItaly
  3. 3.CREA-OF, Ornamental Species Research UnitSanremo (IM)Italy
  4. 4.Department of PharmacyUniversity of PisaPisaItaly
  5. 5.Institute for Sustainable Plant ProtectionNational Research Council (IPSP-CNR)Torino (TO)Italy
  6. 6.CREA-VE, Viticulture and Enology Research CentreConegliano (TV)Italy

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