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Environmentally induced changes in antioxidant phenolic compounds levels in wild plants

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Abstract

Different adverse environmental conditions cause oxidative stress in plants by generation of reactive oxygen species (ROS). Accordingly, a general response to abiotic stress is the activation of enzymatic and non-enzymatic antioxidant systems. Many phenolic compounds, especially flavonoids, are known antioxidants and efficient ROS scavengers in vitro, but their exact role in plant stress responses in nature is still under debate. The aim of our work is to investigate this role by correlating the degree of environmental stress with phenolic and flavonoid levels in stress-tolerant plants. Total phenolic and antioxidant flavonoid contents were determined in 19 wild species. Meteorological data and plant and soil samples were collected in three successive seasons from four Mediterranean ecosystems: salt marsh, dune, semiarid and gypsum habitats. Changes in phenolic and flavonoid levels were correlated with the environmental conditions of the plants and were found to depend on both the taxonomy and ecology of the investigated species. Despite species-specific differences, principal component analyses of the results established a positive correlation between plant phenolics and several environmental parameters, such as altitude, and those related to water stress: temperature, evapotranspiration, and soil water deficit. The correlation with salt stress was, however, very weak. The joint analysis of all the species showed the lowest phenolic and flavonoid levels in the halophytes from the salt marsh. This finding supports previous data indicating that the halophytes analysed here do not undergo oxidative stress in their natural habitat and therefore do not need to activate antioxidant systems as a defence against salinity.

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References

  • Agati G, Biricolti S, Guidi L, Ferrini F, Fini A, Tattini M (2011) The biosynthesis of flavonoids is enhanced similarly by UV radiation and root zone salinity in L. vulgare leaves. J Plant Physiol 168:204–212

    Article  CAS  PubMed  Google Scholar 

  • Agati G, Brunetti C, Di Ferdinando M, Ferrini F, Pollastri S, Tattini M (2013) Functional roles of flavonoids in photoprotection: new evidence, lessons from the past. Plant Physiol Biochem 72:35–45

    Article  CAS  PubMed  Google Scholar 

  • Albert A, Sareedenchai V, Heller W, Seidlitz HK, Zidorn C (2009) Temperature is the key to altitudinal variation of phenolics in Arnica montana L. cv. ARBO. Oecologia 160:1–8

    Article  PubMed  Google Scholar 

  • Appel K, Hirt H (2004) Reactive oxygen species: metabolism, oxidative stress, and signal transduction. Annu Rev Plant Biol 55:373–399

    Article  Google Scholar 

  • Bachereau F, Marigo G, Asta J (1998) Effect of solar radiation (UV and visible) at high altitude on CAM-cycling and phenolic compounds biosynthesis in Sedum album. Physiol Plant 104:203–210

    Article  CAS  Google Scholar 

  • Ballizany WL, Hofmann RV, Jahufer MZZ, Barrett BB (2012) Multivariate associations of flavonoid and biomass accumulation in white clover (Trifolium repens) under drought. Funct Plant Biol 39:167–177

    Article  CAS  Google Scholar 

  • Bieza K, Lois R (2001) An Arabidopsis mutant tolerant to lethal ultraviolet-B levels shows constitutively elevated accumulation of flavonoids and other phenolics. Plant Physiol 126:1105–1115

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Bilger W, Rolland M, Nybakken L (2007) UV screening in higher plants induced by low temperature in the absence of UV-B radiation. Photochem Photobiol Sci 6:190–195

    Article  CAS  PubMed  Google Scholar 

  • Blumthaler M, Ambach M, Ellinger R (1997) Increase in solar UV radiation with altitude. J Photochem Photobiol B 39:130–134

    Article  CAS  Google Scholar 

  • Boscaiu M, Lull C, Llinares J, Vicente O, Boira H (2013) Proline as a biochemical marker in relation to the ecology of two halophytic Juncus species. J Plant Ecol 6:177–186

    Article  Google Scholar 

  • Bose J, Rodrigo-Moreno A, Shabala S (2013) ROS homeostasis in halophytes in the context of salinity stress tolerance. J Exp Bot 65:1241–1257

    Article  PubMed  Google Scholar 

  • Brown DE, Rashotte AM, Murphy AS, Normanly J, Tague BW, Peer WA, Taiz L, Muday GK (2001) Flavonoids act as a negative regulators of auxin transport in vivo in Arabidopsis. Plant Physiol 126:524–535

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Burchard P, Bilger W, Weissenböck G (2000) Contribution of hydroxycinnamates and flavonoids to epidermal shielding of UV-A and UV-B radiation in developing rye primary leaves as assessed by ultraviolet-induced chlorophyll fluorescence measurements. Plant Cell Environ 23:1373–1380

    Article  CAS  Google Scholar 

  • Burriel F, Hernando V (1947) Nuevo método para determinar el fósforo asimilable en los suelos. Anales de Edafología Fisiología Vegetal 9:611–622

    Google Scholar 

  • Cheynier V, Comte G, Davies KM, Lattanzio V, Martens S (2013) Plant phenolics: recent advances on their biosynthesis, genetics, and ecophysiology. Plant Physiol Biochem 72:1–20

    Article  CAS  PubMed  Google Scholar 

  • Coman C, Rugina OD, Socaciu C (2012) Plants and natural compounds with antidiabetic action. Not Bot Horti Agrobo 40:314–325

    CAS  Google Scholar 

  • Di Ferdinando M, Brunetti C, Fini A, Tattini M (2012) Flavonoids as antioxidants in plants under abiotic stresses. In: Ahmad P, Prasad MNV (eds) Abiotic stress responses in plants: metabolism, productivity and sustainability. Springer, New York, pp 159–179

    Chapter  Google Scholar 

  • Di Ferdinando M, Brunetti C, Agati G, Tattini M (2014) Multiple functions of polyphenols in plants inhabiting unfavourable Mediterranean areas. Environ Exper Bot 103:107–116

    Article  Google Scholar 

  • FAO (1990) Management of gypsiferous soils. FAO Soils Bull, p 62

  • Fini A, Brunetti C, Di Ferdinando M, Ferrini F, Tattini M (2011) Stress-induced flavonoid biosynthesis and the antioxidant machinery of plants. Plant Signal Behav 6:709–711

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Gil R, Lull C, Boscaiu M, Bautista I, Lidón A, Vicente O (2011) Soluble carbohydrates as osmolytes in several halophytes from a Mediterranean salt marsh. Not Bot Horti Agrobo 39:9–17

    CAS  Google Scholar 

  • Gil R, Bautista I, Boscaiu M, Lidón A, Wankhade S, Sánchez H, Llinares J, Vicente O (2014) Responses of five Mediterranean halophytes to seasonal changes in environmental conditions. AoB Plants 6: plu049

  • Gould KS, Lister C (2006) Flavonoid function in plants. In: Andersen ØM, Marham KR (eds) Flavonoids, chemistry, biochemistry and application. CRC Press, Boca Raton, pp 397–442

    Google Scholar 

  • Hajimahmoodi M, Moghaddam G, Ranjbar AM, Khazani H, Sadeghi N, Oveisi MR, Jannat B (2013) Total phenolic, flavonoids, tannin content and antioxidant power of some Iranian pomegranate flower cultivars (Punica granatum L.). Am J Plant Sci 4:1815–1820

    Article  Google Scholar 

  • Halliwell B (2006) Reactive species and antioxidants. Redox biology is a fundamental theme of aerobic life. Plant Physiol 141:312–322

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Harborne JB, Williams C (2000) Advances in flavonoid research since 1992. Phytochemistry 55:481–504

    Article  CAS  PubMed  Google Scholar 

  • Hernández I, Alegre L, Munné-Bosch S (2004) Drought-induced changes in flavonoids and other low molecular weight antioxidants in Cistus clusii grown under Mediterranean field conditions. Tree Physiol 24:1303–1311

    Article  PubMed  Google Scholar 

  • Hernández I, Alegre L, Van Breusegem F, Munné-Bosch S (2008) How relevant are flavonoids as antioxidants in plants? Trends Plant Sci 14:125–132

    Article  Google Scholar 

  • Iwashina T (2000) The structure and distribution of the flavonoids in plants. J Plant Res 113:287–299

    Article  CAS  Google Scholar 

  • Jaakola L, Määttä-Riihinen K, Kärenlampi S, Hohtola A (2004) Activation of flavonoid biosynthesis by solar radiation in bilberry (Vaccinium myrtillus L.) leaves. Planta 218:721–728

    Article  CAS  PubMed  Google Scholar 

  • Jenkins GI (2009) Signal transduction in responses to UB-B radiation. Annu Rev Plant Biol 60:407–431

    Article  CAS  PubMed  Google Scholar 

  • Jenkins GI, Long JC, Wade HK, Shenton MR, Bibikova TN (2001) UV and blue light signalling: pathways regulating chalcone synthase gene expression in Arabidopsis. New Phytol 151:121–131

    Article  CAS  Google Scholar 

  • Kaulen H, Schell J, Kreuzaler F (1986) Light-induced expression of the chimeric chalcone synthase-NPTII gene in tobacco cells. EMBO J 5:1–8

    PubMed Central  CAS  PubMed  Google Scholar 

  • Kim DO, Jeong SW, Lee CY (2003) Antioxidant capacity of phenolic phytochemicals from various cultivars of plums. Food Chem 81:321–326

    Article  CAS  Google Scholar 

  • Kirakosyan A, Seymour E, Kaufman PB, Warber S, Bolling S, Chang SC (2003) Antioxidant capacity of polyphenolic extracts from leaves of Crataegus laevigata and Crataegus monogyna (Hawthorn) subjected to drought and cold stress. J Agr Food Chem 51:3973–3976

    Article  CAS  Google Scholar 

  • Knudssen D, Peterson GA, Pratt PF (1982) Lithium, Sodium and Potassium. In: Page AL et al (eds) Methods of soil analysis, chemical and microbiological properties. American Society of Agronomy, Madison, pp 225–246

    Google Scholar 

  • Koes RE, Spelt CE, Mol JNM (1989) The chalcone synthase multigene family of Petunia hybrida (V30): differential, light-regulated expression during flower development and UV light induction. Plant Mol Biol 12:213–225

    Article  CAS  PubMed  Google Scholar 

  • Körner C (1999) Alpine plant life. Functional plant ecology of high mountain ecosytems, Berlin

    Book  Google Scholar 

  • Kumar S, Pandey AK (2013) Chemistry and biological activities of flavonoids: an overview. Sci World J 2013:1–16

    Google Scholar 

  • Kuo S (1996) Phosphorus. In: Spark D (ed) Methods of soil analysis: chemical methods, part 3. American Society of Agronomy, Madison, pp 869–919

    Google Scholar 

  • Lavola A (1998) Accumulation of flavonoids and related compounds in birch induced by UV-B irradiance. Tree Physiol 18:53–58

    Article  CAS  PubMed  Google Scholar 

  • Li J, Ou-Lee TM, Raba R, Amundson RG, Last RL (1993) Arabidopsis flavonoid mutants are hypersensitive to UV-B radiation. Plant Cell 5:171–179

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Llinares JV, Bautista I, Donat MP, Lidón A, Lull C, Mayoral O, Wankhade S, Boscaiu M, Vicente O (2015) Responses to environmental stress in plants adapted to Mediterranean gypsum habitats. Not Sci Biol 7:34–44

    Article  Google Scholar 

  • Marinova D, Ribarova F, Atanassova M (2005) Total phenolics and total flavonoids in Bulgarian fruits and vegetables. J Univ Chem Technol Metall 40:255–260

    CAS  Google Scholar 

  • Martens H, Naes T (1989) Multivariate calibration. Wiley, New York

    Google Scholar 

  • Murai Y, Takemura S, Takeda K, Kitajima K, Iwashina T (2009) Altitudinal variation of UV-absorbing compounds in Plantago asiatica. Biochem Syst Ecol 37:78–384

    Google Scholar 

  • Nakabayashi R, Yonekura-Sakakibara K, Urano K, Suzuki M, Yamada Y, Nishizawa T, Matsuda F, Kojima M, Sakakibara H, Shinozaki K, Michael AJ, Tohge T, Yamazaki M, Saito K (2014) Enhancement of oxidative and drought tolerance in Arabidopsis by overaccumulation of antioxidant flavonoids. Plant J 77:367–379

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Napoli CA, Fahy D, Wang HY, Taylor LP (1999) white anther: a petunia mutant that abolishes pollen flavonoid accumulation, induces male sterility, and is complemented by a chalcone synthase transgene. Plant Physiol 120:615–622

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Nechita A, Cotea VV, Nechita CB, Pincu RR, Mihai CT, Colibaba CL (2012) Study of cytostatic and cytotoxic activity of several polyphenolic extracts obtained from Vitis vinifera. Not Bot Horti Agrobo 40:216–221

    CAS  Google Scholar 

  • Nelson DW, Sommers LE (1982) Total carbon, organic carbon, and organic matter. In: Page AL et al (eds) Methods of soil analysis, chemical and microbiological properties. Soil Science Society of America, Madison, pp 539–577

    Google Scholar 

  • Nelson RE, Klameth LC, Nettleton WD (1978) Determining soil gypsum content and expressing properties of gypsiferous soils. Soil Sci Soc Am J 42:659–661

    Article  CAS  Google Scholar 

  • Nile SH, Khobragade CN (2010) Antioxidant activity and flavonoid derivatives of Plumbago zeylanica. J Nat Prod 3:130–133

    CAS  Google Scholar 

  • Park HL, Lee SW, Jung KH, Hahn TR, Cho MH (2013) Transcriptomic analysis of UV-treated rice leaves reveals UV-induced phytoalexin biosynthetic pathways and their regulatory networks in rice. Phytochemistry 96:57–71

    Article  CAS  PubMed  Google Scholar 

  • Pękal A, Pyrzynska K (2014) Evaluation of aluminium complexation reaction for flavonoid content assay. Food Anal Method 7:1776–1782

    Article  Google Scholar 

  • Pollastri S, Tattini M (2011) Flavonols: old compounds for old roles. Ann Bot 108:1225–1233

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Ravishankar D, Rajora AK, Greco F, Osborn HM (2013) Flavonoids as prospective compounds for anti-cancer therapy. Int J Biochem Cell B 45:2821–2831

    Article  CAS  Google Scholar 

  • Rice-Evans CA, Miller NJ, Paganga G (1996) Structure-antioxidant activity relationships of flavonoids and phenolic acids. Free Radical Bio Med 20:933–956

    Article  CAS  Google Scholar 

  • Rieger G, Müller M, Guttenberger H, Bucar F (2008) Influence of altitudinal variation on the content of phenolic compounds in wild populations of Calluna vulgaris, Sambucus nigra, and Vaccinium myrtillus. J Agric Food Chem 58:9080–9086

    Article  Google Scholar 

  • Rivas-Martínez S, Rivas-Saenz S (1996–2009) Worldwide bioclimatic classification system. Phytosociological Research Center, Spain. http://www.globalbioclimatics.org. Accessed 1 July 2013

  • Rohman A, Riyanto S, Yuniarti N, Saputra WR, Utami R, Mulatsih W (2010) Antioxidant activity, total phenolic, and total flavonoid of extracts and fractions of red fruit (Pandanus conoideus Lam). Int Food Res J 17:97–106

    CAS  Google Scholar 

  • Romano B, Pagano E, Montanaro V, Fortunato AL, Milic N, Borrelli F (2013) Novel insights into the pharmacology of flavonoids. Phytother Res 27:1588–1596

    Article  CAS  PubMed  Google Scholar 

  • Rozema J, van de Staaij J, Björn LO, Caldwell MM (1997) UV-B as an environmental factor in plant life: stress and regulation. Trends Ecol Evol 12:22–28

    Article  CAS  PubMed  Google Scholar 

  • Rozema J, Bjorn LO, Bornman JF, Gaberščik A, Häder DP, Trošt T, Germ M, Klisch M, Gröniger A, Sinha RP, Lebert M, He YY, Buffoni-Hall R, de Bakker NVJ, van de Staaij J, Meijkamp BB (2002) The role of UV-B radiation in aquatic and terrestrial ecosystems—an experimental and functional analysis of the evolution of UV-absorbing compounds. Photochem Photobiol B Biol 66:2–12

    Article  CAS  Google Scholar 

  • Schulze-Lefert P, Dangl JL, Becker-André M, Hahlbrock K, Schulz W (1989) Inducible in vivo DNA footprints define sequences necessary for UV light activation of the parsley chalcone synthase gene. EMBO J 8:651–656

    PubMed Central  CAS  PubMed  Google Scholar 

  • Sena MM, Frighetto RTS, Valarini PJ, Tokeshi H, Poppi RJ (2002) Discrimination of management effects on soil parameters by using principal component analysis: a multivariate analysis case study. Soil Till Res 67:171–181

    Article  Google Scholar 

  • Shulaev V, Oliver DJ (2006) Metabolic and proteomic markers for oxidative stress. New tools for reactive oxygen species research. Plant Physiol 141:367–372

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Singleton VL, Rossi JA Jr (1965) Colorimetry of total phenolics with phosphomolybdic phosphotungstic acid reagents. Am J EnolVitic 16:144–158

    CAS  Google Scholar 

  • Spitaler R, Winkler A, Lins I, Yanar S, Stuppner H, Zidorn C (2008) Altitudinal variation of phenolic contents in flowering heads of Arnica montana cv. ARBO: a 3-year comparison. J Chem Ecol 34:369–375

    Article  CAS  PubMed  Google Scholar 

  • Stapleton AE, Walbot V (1994) Flavonoids can protect maize DNA from the induction of UV radiation damage. Plant Physiol 105:881–889

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Takahashi M, Asada K (1988) Superoxide production in aprotic interior of chloroplast thylakoids. Arch Biochem Biophys 267:714–722

    Article  CAS  PubMed  Google Scholar 

  • Tattini M, Gravano E, Pinelli P, Mulinacci N, Romani A (2000) Flavonoids accumulate in leaves and glandular trichomes of Phillyrea latifolia exposed to excess solar radiation. New Phytol 148:69–77

    Article  CAS  Google Scholar 

  • Tattini M, Galardi C, Pinelli P, Massai R, Remorini D, Agati G (2004) Differential accumulation of flavonoids and hydroxycinnamates in leaves of Ligustrum vulgare under excess light and drought stress. New Phytol 163:547–561

    Article  CAS  Google Scholar 

  • Treutter D (2005) Significance of flavonoids in plant resistance and enhancement of their biosynthesis. Plant Biol 7:581–591

    Article  CAS  PubMed  Google Scholar 

  • Treutter D (2006) Significance of flavonoids in plant resistance: a review. Environ Chem Lett 4:147–157

    Article  CAS  Google Scholar 

  • Van Breusegem F, Dat JF (2006) Reactive oxygen species in plant cell death. Plant Physiol 141:384–390

    Article  PubMed Central  PubMed  Google Scholar 

  • Williams CA, Grayer RJ (2004) Anthocyanins and other flavonoids. Nat Prod Rep 21:539–573

    Article  CAS  PubMed  Google Scholar 

  • Winkel-Shirley B (2002) Biosynthesis of flavonoids and effect of stress. Curr Opin Plant Biol 5:218–223

    Article  CAS  PubMed  Google Scholar 

  • Ylstra B, Touraev A, Benito Moreno RM, Stöger E, van Tunen AA, Vicente O, Mol JNM, Heberle-Bors E (1992) Flavonols stimulate development, germination and tube growth of tobacco pollen. Plant Physiol 100:902–907

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Zhishen J, Mengcheng T, Jianming W (1999) The determination of flavonoid contents in mulberry and their scavenging effects on superoxide radicals. Food Chem 64:555–559

    Article  CAS  Google Scholar 

  • Zidorn C, Schubert B, Stuppner H (2005) Altitudinal differences in the contents of phenolics in flowering heads of three members of the tribe Lactuceae (Asteraceae) occurring as introduced species in New Zealand. Biochem Syst Ecol 33:855–872

    Article  CAS  Google Scholar 

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Acknowledgments

This work has been funded by the Spanish Ministry of Science and Innovation (Project CGL2008-00438/BOS), with contribution from the European Regional Development Fund. Thanks to Dr. Rafael Herrera for critical reading of the manuscript.

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Authors and Affiliations

  1. ReForest, Instituto Ingeniería del Agua y Medio Ambiente, Universitat Politècnica de València, Camino de Vera s/n, 46022, Valencia, Spain

    Inmaculada Bautista, Antonio Lidón & Cristina Lull

  2. Instituto Agroforestal Mediterráneo, Universitat Politècnica de València, Camino de Vera s/n, 46022, Valencia, Spain

    Monica Boscaiu & Josep V. Llinares

  3. Instituto de Investigación para la Gestión Integral de Zonas Costeras, Universitat Politècnica de València, C. Paranimf 1, 46730, Grau de Gandía, Spain

    Mª Pilar Donat & Olga Mayoral

  4. Instituto de Biología Molecular y Celular de Plantas (UPV-CSIC), Universitat Politècnica de València, Camino de Vera s/n, 46022, Valencia, Spain

    Oscar Vicente

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  1. Inmaculada Bautista
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  2. Monica Boscaiu
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Correspondence to Antonio Lidón.

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Communicated by M. H. Walter.

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Bautista, I., Boscaiu, M., Lidón, A. et al. Environmentally induced changes in antioxidant phenolic compounds levels in wild plants. Acta Physiol Plant 38, 9 (2016). https://doi.org/10.1007/s11738-015-2025-2

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