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Secondary metabolites responses of plants exposed to ozone: an update

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Abstract

Tropospheric ozone (O3) is a secondary pollutant that causes oxidative stress in plants due to the generation of excess reactive oxygen species (ROS). Phenylpropanoid metabolism is induced as a usual response to stress in plants, and induction of key enzyme activities and accumulation of secondary metabolites occur, upon O3 exposure to provide resistance or tolerance. The phenylpropanoid, isoprenoid, and alkaloid pathways are the major secondary metabolic pathways from which plant defense metabolites emerge. Chronic exposure to O3 significantly accelerates the direction of carbon flows toward secondary metabolic pathways, resulting in a resource shift in favor of the synthesis of secondary products. Furthermore, since different cellular compartments have different levels of ROS sensitivity and metabolite sets, intracellular compartmentation of secondary antioxidative metabolites may play a role in O3-induced ROS detoxification. Plants’ responses to resource partitioning often result in a trade-off between growth and defense under O3 stress. These metabolic adjustments help the plants to cope with the stress as well as for achieving new homeostasis. In this review, we discuss secondary metabolic pathways in response to O3 in plant species including crops, trees, and medicinal plants; and how the presence of this stressor affects their role as ROS scavengers and structural defense. Furthermore, we discussed how O3 affects key physiological traits in plants, foliar chemistry, and volatile emission, which affects plant–plant competition (allelopathy), and plant–insect interactions, along with an emphasis on soil dynamics, which affect the composition of soil communities via changing root exudation, litter decomposition, and other related processes.

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References

  • Agathokleous E, Feng Z, Oksanen E, Sicard P, Wang Q, Saitanis CJ, Araminiene V, Blande JD, Hayes F, Calatayud V, Domingos M (2020) Ozone affects plant, insect, and soil microbial communities: a threat to terrestrial ecosystems and biodiversity. Sci Adv 6(33):eabc1176

    CAS  Google Scholar 

  • Agathokleous E, Kitao M, Calabrese EJ (2019a) Hormesis: a compelling platform for sophisticated plant science. Trends Plant Sci 24(4):318–327

    CAS  Google Scholar 

  • Agathokleous E, Saitanis CJ (2020) Plant susceptibility to ozone: a tower of Babel? Sci Total Environ 703:134962

    CAS  Google Scholar 

  • Agathokleous E, Saitanis CJ, Wang X, Watanabe M, Koike T (2016) A review study on past 40 years of research on effects of tropospheric O3 on belowground structure, functioning, and processes of trees: a linkage with potential ecological implications. Water Air Soil Pollut 227(1):1–28

    Google Scholar 

  • Agathokleous E, Sakikawa T, Abu Elela SA, Mochizuki T, Nakamura M, Watanabe M, Kawamura K, Koike T (2017) Ozone alters the feeding behavior of the leaf beetle Agelastica coerulea (Coleoptera: Chrysomelidae) into leaves of Japanese white birch (Betula platyphylla var. japonica). Environ Sci Pollut Res 24(21):17577–17583

    CAS  Google Scholar 

  • Agathokleous E, WaiLi Y, Ntatsi G, Konno K, Saitanis CJ, Kitao M, Koike T (2019b) Effects of ozone and ammonium sulfate on cauliflower: emphasis on the interaction between plants and insect herbivores. Sci Total Environ 659:995–1007

    CAS  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

    CAS  Google Scholar 

  • Agati G, Matteini P, Goti A, Tattini M (2007) Chloroplast-located flavonoids can scavenge singlet oxygen. New Phytol 174(1):77–89

    CAS  Google Scholar 

  • Agati G, Stefano G, Biricolti S, Tattini M (2009) Mesophyll distribution of ‘antioxidant’ flavonoid glycosides in Ligustrum vulgare leaves under contrasting sunlight irradiance. Ann Bot 104(5):853–861

    CAS  Google Scholar 

  • Agrell J, Kopper B, McDonald EP, Lindroth RL (2005) CO2 and O3 effects on host plant preferences of the forest tent caterpillar (Malacosoma disstria). Glob Chang Biol 11(4):588–599

    Google Scholar 

  • Ahuja I, Kissen R, Bones AM (2012) Phytoalexins in defense against pathogens. Trends Plant Sci 17(2):73–90

    CAS  Google Scholar 

  • Ainsworth EA (2017) Understanding and improving global crop response to ozone pollution. Plant J 90(5):886–897

    CAS  Google Scholar 

  • Ali JG, Agrawal AA (2012) Specialist versus generalist insect herbivores and plant defense. Trends Plant Sci 17(5):293–302

    CAS  Google Scholar 

  • Andersen CP (2003) Source–sink balance and carbon allocation below ground in plants exposed to ozone. New Phytol 157(2):213–228

    CAS  Google Scholar 

  • Andersen SO, Halberstadt ML, Borgfucd-Parnell N (2013) Stratospheric ozone, global warming, and the principle of unintended consequences-an ongoing science and policy success story. J Air Waste Manage Assoc 63(6):607–647

    CAS  Google Scholar 

  • Ansari N, Agrawal M, Agrawal SB (2021b) An assessment of growth, floral morphology, and metabolites of a medicinal plant Sida cordifolia L. under the influence of elevated ozone. Environ Sci Pollut Res 28(1):832–845

    CAS  Google Scholar 

  • Ansari N, Yadav DS, Agrawal M, Agrawal SB (2021a) The impact of elevated ozone on growth, secondary metabolites, production of reactive oxygen species and antioxidant response in an anti-diabetic plant Costus pictus. Funct Plant Biol 48(6):597–610

    CAS  Google Scholar 

  • Awmack CS, Harrington R, Lindroth RL (2004) Aphid individual performance may not predict population responses to elevated CO2 or O3. Glob Chang Biol 10(8):1414–1423

    Google Scholar 

  • Azmir J, Zaidul IS, Rahman MM, Sharif KM, Mohamed A, Sahena F, Jahurul MH, Ghafoor K, Norulaini NA, Omar AK (2013) Techniques for extraction of bioactive compounds from plant materials: a review. J Food Eng 117(4):426–436

    CAS  Google Scholar 

  • Badri DV, Vivanco JM (2009) Regulation and function of root exudates. Plant Cell Environ 32(6):666–681

    CAS  Google Scholar 

  • Balmer D, Flors V, Glauser G, Mauch-Mani B (2013) Metabolomics of cereals under biotic stress: current knowledge and techniques. Front Plant Sci 4:82

    Google Scholar 

  • Bardon C, Piola F, Bellvert F, Haichar FE, Comte G, Meiffren G, Pommier T, Puijalon S, Tsafack N, Poly F (2014) Evidence for biological denitrification inhibition (BDI) by plant secondary metabolites. New Phytol 204(3):620–630

    CAS  Google Scholar 

  • Bartram S, Jux A, Gleixner G, Boland W (2006) Dynamic pathway allocation in early terpenoid biosynthesis of stress-induced lima bean leaves. Phytochemistry 67(15):1661–1672

    CAS  Google Scholar 

  • Bartwal A, Mall R, Lohani P, Guru SK, Arora S (2013) Role of secondary metabolites and brassinosteroids in plant defense against environmental stresses. J Plant Growth Regul 32(1):216–232

    CAS  Google Scholar 

  • Batish DR, Singh HP, Kaur S, Kohli RK, Yadav SS (2008) Caffeic acid affects early growth, and morphogenetic response of hypocotyl cuttings of mung bean (Phaseolus aureus). J Plant Physiol 165(3):297–305

    CAS  Google Scholar 

  • Beckman CH (2000) Phenolic-storing cells: keys to programmed cell death and periderm formation in wilt disease resistance and in general defence responses in plants? Physiol Mol Plant Pathol 57(3):101–110

    CAS  Google Scholar 

  • Behnke K, Kleist E, Uerlings R, Wildt J, Rennenberg H, Schnitzler JP (2009) RNAi-mediated suppression of isoprene biosynthesis in hybrid poplar impacts ozone tolerance. Tree Physiol 29(5):725–736

    CAS  Google Scholar 

  • Bender J, Muntifering RB, Lin JC, Weigel HJ (2006) Growth and nutritive quality of Poa pratensis as influenced by ozone and competition. Environ Pollut 142(1):109–115

    CAS  Google Scholar 

  • Betz GA, Knappe C, Lapierre C, Olbrich M, Welzl G, Langebartels C, Heller W, Sandermann H, Ernst D (2009) Ozone affects shikimate pathway transcripts and monomeric lignin composition in European beech (Fagus sylvatica L.). Eur J For Res 128(2):109–116

    CAS  Google Scholar 

  • Betzelberger AM, Gillespie KM, Mcgrath JM, Koester RP, Nelson RL, Ainsworth EA (2010) Effects of chronic elevated ozone concentration on antioxidant capacity, photosynthesis and seed yield of 10 soybean cultivars. Plant Cell Environ 33(9):1569–1581

    Google Scholar 

  • Biagioni M, Nali C, Heimler D, Lorenzini G (1997) PAL activity and differential ozone sensitivity in tobacco, bean and poplar. J Phytopathol 145(11-12):533–539

    CAS  Google Scholar 

  • Biere A, Bennett AE (2013) Three-way interactions between plants, microbes and insects. Functional Ecology 27(3):567–573

    Google Scholar 

  • Bison JV, Cardoso-Gustavson P, de Moraes RM, da Silva Pedrosa G, Cruz LS, Freschi L, de Souza SR (2018) Volatile organic compounds and nitric oxide as responses of a Brazilian tropical species to ozone: the emission profile of young and mature leaves. Environ Sci Pollut Res 25:3840–3848

    CAS  Google Scholar 

  • Biswas DK, Xu H, Li YG, Sun JZ, Wang XZ, Han XG, Jiang GM (2008) Genotypic differences in leaf biochemical, physiological and growth responses to ozone in 20 winter wheat cultivars released over the past 60 years. Glob Chang Biol 14(1):46–59

    Google Scholar 

  • Blande JD (2021) Effects of air pollution on plant–insect interactions mediated by olfactory and visual cues. Curr Opin Environ Sci Health 19:100228

    Google Scholar 

  • Blande JD, Holopainen JK, Li T (2010) Air pollution impedes plant-to-plant communication by volatiles. Ecol Lett 13(9):1172–1181

    Google Scholar 

  • Blande JD, Holopainen JK, Niinemets Ü (2014) Plant volatiles in polluted atmospheres: stress responses and signal degradation. Plant Cell Environ 37(8):1892–1904

    CAS  Google Scholar 

  • Bonello P, Heller W, Sandermann H Jr (1993) Ozone effects on root-disease susceptibility and defence responses in mycorrhizal and non-mycorrhizal seedlings of Scots pine (Pinus sylvestris L.). New Phytol 124(4):653–663

    CAS  Google Scholar 

  • Booker FL, Burkey KO, Jones AM (2012) Re-evaluating the role of ascorbic acid and phenolic glycosides in ozone scavenging in the leaf apoplast of Arabidopsis thaliana L. Plant Cell Environ 35(8):1456–1466

    CAS  Google Scholar 

  • Booker FL, Miller JE (1998) Phenylpropanoid metabolism and phenolic composition of soybean [Glycine max (L.) Merr.] leaves following exposure to ozone. J Exp Bot 49(324):1191–1202

    CAS  Google Scholar 

  • Bors W, Langebartels C, Michel C, Sandermann H Jr (1989) Polyamines as radical scavengers and protectants against ozone damage. Phytochemistry 28(6):1589–1595

    CAS  Google Scholar 

  • Bortolin RC, Caregnato FF, Divan AM Jr, Reginatto FH, Gelain DP, Moreira JCF (2014) Effects of chronic elevated ozone concentration on the redox state and fruit yield of red pepper plant Capsicum baccatum. Ecotoxicol Environ Saf 100:114–121

    CAS  Google Scholar 

  • Bortolin RC, Caregnato FF, Junior AM, Zanotto-Filho A, Moresco KS, de Oliveira Rios A, de Oliveira Salvi A, Ortmann CF, de Carvalho P, Reginatto FH, Gelain DP (2016) Chronic ozone exposure alters the secondary metabolite profile, antioxidant potential, anti-inflammatory property, and quality of red pepper fruit from Capsicum baccatum. Ecotoxicol Environ Saf 129:16–24

    CAS  Google Scholar 

  • Bridges M, Jones AM, Bones AM, Hodgson C, Cole R, Bartlet E, Wallsgrove R, Karapapa VK, Watts N, Rossiter JT (2002) Spatial organization of the glucosinolate–myrosinase system in brassica specialist aphids is similar to that of the host plant. Proc R Soc B: Biol Sci 269(1487):187–191

    CAS  Google Scholar 

  • Brown EJ, Khodr H, Hider CR, Rice-Evans CA (1998) Structural dependence of flavonoid interactions with Cu2+ ions: implications for their antioxidant properties. Biochem J 330(3):1173–1178

    CAS  Google Scholar 

  • Buer CS, Muday GK (2004) The transparent testa4 mutation prevents flavonoid synthesis and alters auxin transport and the response of Arabidopsis roots to gravity and light. Plant Cell 16(5):1191–1205

    CAS  Google Scholar 

  • Cabane M, Afif D, Hawkins S (2012) Lignins and abiotic stresses. In: Advances in botanical research, vol 61. Academic Press, pp 219–262

    Google Scholar 

  • Cabané M, Pireaux JC, Léger E, Weber E, Dizengremel P, Pollet B, Lapierre C (2004) Condensed lignins are synthesized in poplar leaves exposed to ozone. Plant Physiol 134(2):586–594

    Google Scholar 

  • Calderon-Montano JM, Burgos-Morón E, Pérez-Guerrero C, López-Lázaro M (2011) A review on the dietary flavonoid kaempferol. Mini Rev Med Chem 11(4):298–344

    CAS  Google Scholar 

  • Calfapietra C, Fares S, Loreto F (2009) Volatile organic compounds from Italian vegetation and their interaction with ozone. Environ Pollut 157(5):1478–1486

    CAS  Google Scholar 

  • Calfapietra C, Fares S, Manes F, Morani A, Sgrigna G, Loreto F (2013) Role of biogenic volatile organic compounds (BVOC) emitted by urban trees on ozone concentration in cities: A review. Environ Pollut 183:71–80

    CAS  Google Scholar 

  • Caretto S, Linsalata V, Colella G, Mita G, Lattanzio V (2015) Carbon fluxes between primary metabolism and phenolic pathway in plant tissues under stress. Int J Mol Sci 16(11):26378–26394

    CAS  Google Scholar 

  • Carqueijeiro I, Noronha H, Duarte P, Gerós H, Sottomayor M (2013) Vacuolar transport of the medicinal alkaloids from Catharanthus roseus is mediated by a proton-driven antiport. Plant Physiol 162(3):1486–1496

    CAS  Google Scholar 

  • Carriero G, Brunetti C, Fares S, Hayes F, Hoshika Y, Mills G, Tattini M, Paoletti E (2016) BVOC responses to realistic nitrogen fertilization and ozone exposure in silver birch. Environ Pollut 213:988–995

    CAS  Google Scholar 

  • Castagna A, Ranieri A (2009) Detoxification and repair process of ozone injury: from O3 uptake to gene expression adjustment. Environ Pollut 157(5):1461–1469

    CAS  Google Scholar 

  • Cesco S, Neumann G, Tomasi N, Pinton R, Weisskopf L (2010) Release of plant-borne flavonoids into the rhizosphere and their role in plant nutrition. Plant and Soil 329(1):1–25

    CAS  Google Scholar 

  • Chai TT, Ooh KF, Ooi PW, Chue PS, Wong FC (2013) Leucaena leucocephala leachate compromised membrane integrity, respiration and antioxidative defence of water hyacinth leaf tissues. Botanical Studies 54(1):1–7

    Google Scholar 

  • Chappelka AH, Grulke NE (2016) Disruption of the ‘disease triangle’ by chemical and physical environmental change. Plant Biology 18:5–12

    CAS  Google Scholar 

  • Chaudhary, I. J., Nigam, B., & Rathore, D. (2022). Effect of elevated ozone on soybean (Glycine max L.) cultivar: role of orange juice and synthetic ascorbic acid.

    Google Scholar 

  • Chen AY, Chen YC (2013) A review of the dietary flavonoid, kaempferol on human health and cancer chemoprevention. Food Chem 138(4):2099–2107

    CAS  Google Scholar 

  • Chen C, Chen S, Jha RK, Cotrozzi L, Nali C, Lorenzini G, Ma L (2020) Phenol metabolism of two cultivars of durum wheat (Triticum durum Desf.) as affected by ozone and flooding stress. J Agron Crop Sci 206(3):338–351

    CAS  Google Scholar 

  • Chen C, Zhang H, Dong C, Ji H, Zhang X, Li L, Ban Z, Zhang N, Xue W (2019) Effect of ozone treatment on the phenylpropanoid biosynthesis of postharvest strawberries. RSC Adv 9(44):25429–25438

    CAS  Google Scholar 

  • Chen F, Liu CJ, Tschaplinski TJ, Zhao N (2009) Genomics of secondary metabolism in Populus: interactions with biotic and abiotic environments. Crit Rev Plant Sci 28(5):375–392

    CAS  Google Scholar 

  • Cho K, Tiwari S, Agrawal SB, Torres NL, Agrawal M, Sarkar A, Shibato J, Agrawal GK, Kubo A, Rakwal R (2011) Tropospheric ozone and plants: absorption, responses, and consequences. Rev Environ Contam Toxicol 212:61–111

    CAS  Google Scholar 

  • Choi IS, Choi EY, Jin JY, Park HR, Choi JI, Kim SJ (2013) Kaempferol inhibits P. intermedia lipopolysaccharide-induced production of nitric oxide through translational regulation in murine macrophages: critical role of heme oxygenase-1-mediated ROS reduction. J Periodontol 84(4):545–555

    CAS  Google Scholar 

  • Chomel M, Fernandez C, Bousquet‐Mélou A, Gers C, Monnier Y, Santonja M, Gauquelin T, Gros R, Lecareux C, Baldy V (2014) Secondary metabolites of Pinus halepensis alter decomposer organisms and litter decomposition during afforestation of abandoned agricultural zones. J Ecol 102(2):411–424

    Google Scholar 

  • Chomel M, Guittonny‐Larchevêque M, Fernandez C, Gallet C, DesRochers A, Paré D, Jackson BG, Baldy V (2016) Plant secondary metabolites: a key driver of litter decomposition and soil nutrient cycling. J Ecol 104(6):1527–1541

    Google Scholar 

  • Cotrozzi L, Campanella A, Pellegrini E, Lorenzini G, Nali C, Paoletti E (2018) Phenylpropanoids are key players in the antioxidant defense to ozone of European ash, Fraxinus excelsior. Environ Sci Pollut Res 25(9):8137–8147

    CAS  Google Scholar 

  • Cotrozzi L, Conti B, Lorenzini G, Pellegrini E, Nali C (2021) In the tripartite combination ozone-poplar-Chrysomela populi, the pollutant alters the plant-insect interaction via primary metabolites of foliage. Environ Res 201:111581

    CAS  Google Scholar 

  • Cotrozzi L, Nali C (2014) Oxidative stress, phenolic compounds and officinal plants: the case of Melissa officinalis exposed to ozone. Italus Hortus 21(2):35–47

    Google Scholar 

  • Couture JJ (2011) Impact of elevated CO2 and O3 on community herbivory in a northern temperate forest (Ph.D. dissertation). University of Wisconsin, Madison

    Google Scholar 

  • Couture JJ, Holeski LM, Lindroth RL (2014) Long-term exposure to elevated CO2 and O3 alters aspen foliar chemistry across developmental stages. Plant Cell Environ 37(3):758–765

    CAS  Google Scholar 

  • Couture JJ, Lindroth RL (2012) Atmospheric change alters performance of an invasive forest insect. Glob Chang Biol 18(12):3543–3557

    Google Scholar 

  • Couture JJ, Meehan TD, Lindroth RL (2012) Atmospheric change alters foliar quality of host trees and performance of two outbreak insect species. Oecologia 168(3):863–876

    Google Scholar 

  • Croteau R, Kutchan TM, Lewis NG (2000) Natural products (secondary metabolites). Biochem Mol Biol Plants 24:1250–1319

    Google Scholar 

  • Cui H, Su J, Wei J, Hu Y, Ge F (2014) Elevated O3 enhances the attraction of whitefly-infested tomato plants to Encarsia formosa. Sci Rep 4(1):1–6

    Google Scholar 

  • Cui H, Sun Y, Su J, Ren Q, Li C, Ge F (2012) Elevated O3 reduces the fitness of Bemisia tabaci via enhancement of the SA-dependent defense of the tomato plant. Arthropod-Plant Interactions 6(3):425–437

    Google Scholar 

  • da Rosa Santos AC, Furlan CM (2013) Levels of phenolic compounds in Tibouchina pulchra after fumigation with ozone. Atmos Pollut Res 4(3):250–256

    Google Scholar 

  • da Silva Engela MR, Furlan CM, Esposito MP, Fernandes FF, Carrari E, Domingos M, Paoletti E, Hoshika Y (2021) Metabolic and physiological alterations indicate that the tropical broadleaf tree Eugenia uniflora L. is sensitive to ozone. Sci Total Environ 769:145080

    Google Scholar 

  • De Luca V, Salim V, Thamm A, Masada SA, Yu F (2014) Making iridoids/secoiridoids and monoterpenoid indole alkaloids: progress on pathway elucidation. Curr Opin Plant Biol 19:35–42

    Google Scholar 

  • Demos EK, Woolwine M, Wilson RH, McMillan C (1975) The effects of ten phenolic compounds on hypocotyl growth and mitochondrial metabolism of mung bean. Am J Bot 62(1):97–102

    CAS  Google Scholar 

  • Denisov ET, Afanas' ev IB (2005) Oxidation and antioxidants in organic chemistry and biology. CRC press

    Google Scholar 

  • D'Haese D, Horemans N, Coen WD, Guisez Y (2006) Identification of late O3 responsive genes in Arabidopsis thaliana by cDNA microarray analysis. Physiol Plant 128(1):70–79

    CAS  Google Scholar 

  • Di Baccio D, Castagna A, Paoletti E, Sebastiani L, Ranieri A (2008) Could the differences in O3 sensitivity between two poplar clones be related to a difference in antioxidant defense and secondary metabolic response to O3 influx? Tree Physiol 28(12):1761–1772

    Google Scholar 

  • Ditchkoff SS, Lewis JS, Lin JC, Muntifering RB, Chappelka AH (2009) Nutritive quality of highbush blackberry (Rubus argutus) exposed to tropospheric ozone. Rangel Ecol Manage 62(4):364–370

    Google Scholar 

  • Divekar PA, Narayana S, Divekar BA, Kumar R, Gadratagi BG, Ray A, Singh AK, Rani V, Singh V, Singh AK, Kumar A (2022) Plant secondary metabolites as defense tools against herbivores for sustainable crop protection. Int J Mol Sci 23(5):2690

    CAS  Google Scholar 

  • Dixon RA, Paiva NL (1995) Stress-induced phenylpropanoid metabolism. Plant Cell 7(7):1085

    CAS  Google Scholar 

  • Dizengremel P (2001) Effects of ozone on the carbon metabolism of forest trees. Plant Physiol Biochem 39(9):729–742

    CAS  Google Scholar 

  • Dolker T, Agrawal M (2019) Negative impacts of elevated ozone on dominant species of semi-natural grassland vegetation in Indo-Gangetic plain. Ecotoxicol Environ Saf 182:109404

    CAS  Google Scholar 

  • Dolker T, Mukherjee A, Agrawal SB, Agrawal M (2020) Responses of a semi-natural grassland community of tropical region to elevated ozone: an assessment of soil dynamics and biomass accumulation. Sci Total Environ 718:137141

    CAS  Google Scholar 

  • Dong D, Shi C, Yan S, Ashraf MA (2019) Effects of elevated atmospheric CO2, O3 and soil phenanthrene on soil enzyme activities and microbial biomass. Appl Ecol Environ Res 17(4):8501–8512

    Google Scholar 

  • dos Santos Nascimento LB, Leal-Costa MV, Menezes EA, Lopes VR, Muzitano MF, Costa SS, Tavares ES (2015) Ultraviolet-B radiation effects on phenolic profile and flavonoid content of Kalanchoe pinnata. J Photochem Photobiol B Biol 148:73–81

    Google Scholar 

  • Duke SO, Oliva A, Macias F, Galindo J, Molinillo J, Cutler H (2004) Mode of action of phytotoxic terpenoids. CRC Press, Boca Raton, FL, USA, pp 201–206

    Google Scholar 

  • Duque LMR (2022) Effects of ozone on plants and plant-insect interactions (Doctoral dissertation. Universität Würzburg

    Google Scholar 

  • Dusart N, Gandin A, Vaultier MN, Joffe R, Cabané M, Dizengremel P, Jolivet Y (2019) Importance of detoxification processes in ozone risk assessment: need to integrate the cellular compartmentation of antioxidants? Frontiers in Forests and Global Change 2:45

    Google Scholar 

  • Einhellig FA, Galindo JCG, Molinillo JMG, Cutler HG (2004) Mode of allelochemical action of phenolic compounds. In: Allelopathy: chemistry and mode of action of allelochemicals, pp 217–238

    Google Scholar 

  • Eyles A, Davies NW, Yuan ZQ, Mohammed C (2003) Host responses to natural infection by Cytonaema sp. in the aerial bark of Eucalyptus globulus. Forest Pathology 33(5):317–331

    Google Scholar 

  • Faoro F, Iriti M (2009) Plant cell death and cellular alterations induced by ozone: key studies in Mediterranean conditions. Environ Pollut 157(5):1470–1477

    CAS  Google Scholar 

  • Farré-Armengol G, Peñuelas J, Li T, Yli-Pirilä P, Filella I, Llusia J, Blande JD (2016) Ozone degrades floral scent and reduces pollinator attraction to flowers. New Phytol 209(1):152–160

    Google Scholar 

  • Fatima A, Singh AA, Agrawal M, Agrawal SB (2018b) Effect of elevated O3 on rhizospheric enzymatic activities of ozone sensitive and tolerant wheat cultivars. Arch Agron Soil Sci 64(12):1768–1776

    CAS  Google Scholar 

  • Fatima A, Singh AA, Mukherjee A, Agrawal M, Agrawal SB (2018a) Variability in defence mechanism operating in three wheat cultivars having different levels of sensitivity against elevated ozone. Environ Exp Bot 155:66–78

    CAS  Google Scholar 

  • Fatima A, Singh AA, Mukherjee A, Dolker T, Agrawal M, Agrawal SB (2019) Assessment of ozone sensitivity in three wheat cultivars using ethylenediurea. Plants 8(4):80

    CAS  Google Scholar 

  • Feng Y, Lin X, Yu Y, Zhang H, Chu H, Zhu J (2013) Elevated ground-level O3 negatively influences paddy methanogenic archaeal community. Sci Rep 3(1):1–9

    Google Scholar 

  • Feng Z, Sun J, Wan W, Hu E, Calatayud V (2014) Evidence of widespread ozone-induced visible injury on plants in Beijing, China. Environ Pollut 193:296–301

    CAS  Google Scholar 

  • Feng Z, Yuan X, Fares S, Loreto F, Li P, Hoshika Y, Paoletti E (2019) Isoprene is more affected by climate drivers than monoterpenes: a meta-analytic review on plant isoprenoid emissions. Plant Cell Environ 42(6):1939–1949

    CAS  Google Scholar 

  • Ferdinando MD, Brunetti C, Fini A, Tattini M (2012) Flavonoids as antioxidants in plants under abiotic stresses. In: Abiotic stress responses in plants, pp 159–179

    Google Scholar 

  • Fernandes FF, Cardoso-Gustavson P, Alves ES (2016) Synergism between ozone and light stress: structural responses of polyphenols in a woody Brazilian species. Chemosphere 155:573–582

    CAS  Google Scholar 

  • Findlay S, Carreiro M, Krischik V, Jones CG (1996) Effects of damage to living plants on leaf litter quality. Ecol Appl 6(1):269–275

    Google Scholar 

  • Fiscus EL, Booker FL, Burkey KO (2005) Crop responses to ozone: uptake, modes of action, carbon assimilation and partitioning. Plant Cell Environ 28(8):997–1011

    CAS  Google Scholar 

  • Flores G, Hubbes M (1979) Phytoalexin production by Aspen (Populus tremuloides Michx.) in response to infection by Hypoxylon mammatum (Wahl.) Mill and Alternaria spp. Eur J Forest Pathol 9(5):280–288

    Google Scholar 

  • Fontaine V, Cabané M, Dizengremel P (2003) Regulation of phosphoenolpyruvate carboxylase in Pinus halepensis needles submitted to ozone and water stress. Physiol Plant 117(4):445–452

    CAS  Google Scholar 

  • Foster‐Hartnett DA, Danesh D, Penuela S, Sharopova N, Endre G, Vandenbosch KA, Young ND, Samac DA (2007) Molecular and cytological responses of Medicago truncatula to Erysiphe pisi. Mol Plant Pathol 8(3):307–319

    Google Scholar 

  • Foyer CH, Noctor G (2005) Oxidant and antioxidant signalling in plants: a re-evaluation of the concept of oxidative stress in a physiological context. Plant Cell Environ 28(8):1056–1071

    CAS  Google Scholar 

  • Frei M (2015) Breeding of ozone resistant rice: relevance, approaches and challenges. Environ Pollut 197:144–155

    CAS  Google Scholar 

  • Frei M, Kohno Y, Wissuwa M, Makkar HP, Becker K (2011) Negative effects of tropospheric ozone on the feed value of rice straw are mitigated by an ozone tolerance QTL. Glob Chang Biol 17(7):2319–2329

    Google Scholar 

  • Frei M, Makkar HP, Becker K, Wissuwa M (2010) Ozone exposure during growth affects the feeding value of rice shoots. Anim Feed Sci Technol 155(1):74–79

    CAS  Google Scholar 

  • Frei M, Wissuwa M, Pariasca-Tanaka J, Chen CP, Südekum KH, Kohno Y (2012) Leaf ascorbic acid level–is it really important for ozone tolerance in rice? Plant Physiol Biochem 59:63–70

    CAS  Google Scholar 

  • Freiwald V, Häikiö E, Julkunen-Tiitto R, Holopainen JK, Oksanen E (2008) Elevated ozone modifies the feeding behaviour of the common leaf weevil on hybrid aspen through shifts in developmental, chemical, and structural properties of leaves. Entomol Exp Appl 128(1):66–72

    CAS  Google Scholar 

  • Fuhrer J, Shariat-Madari H, Perler R, Tschannen W, Grub A (1994) Effects of ozone on managed pasture: II. yield, species compostion, canopy structure, and forage quality. Environ Pollut 86(3):307–314

    CAS  Google Scholar 

  • Galey JB (1996) Potential use of iron chelators against oxidative damage. Adv Pharmacol 38:167–203

    Google Scholar 

  • Gani U, Vishwakarma RA, Misra P (2021) Membrane transporters: the key drivers of transport of secondary metabolites in plants. Plant Cell Rep 40(1):1–18

    CAS  Google Scholar 

  • Ghimire RP, Kasurinen A, Häikiö E, Holopainen JK, Julkunen-Tiitto R, Holopainen T, Kivimäenpää M (2019) Combined effects of elevated ozone, temperature, and nitrogen on stem phenolic concentrations of Scots pine (Pinus sylvestris) seedlings. Can J For Res 49(3):246–255

    CAS  Google Scholar 

  • Ghimire RP, Kivimäenpää M, Kasurinen A, Häikiö E, Holopainen T, Holopainen JK (2017) Herbivore-induced BVOC emissions of Scots pine under warming, elevated ozone and increased nitrogen availability in an open-field exposure. Agric For Meteorol 242:21–32

    Google Scholar 

  • Ghorbani A, Esmaeilizadeh M (2017) Pharmacological properties of Salvia officinalis and its components. J Tradit Complement Med 7(4):433–440

    Google Scholar 

  • Ghosh A, Agrawal M, Agrawal SB (2020a) Effect of water deficit stress on an Indian wheat cultivar (Triticum aestivum L. HD 2967) under ambient and elevated level of ozone. Sci Total Environ 714:136837

    CAS  Google Scholar 

  • Ghosh A, Agrawal M, Agrawal SB (2021a) Examining the effectiveness of biomass-derived biochar for the amelioration of tropospheric ozone-induced phytotoxicity in the Indian wheat cultivar HD 2967. J Hazard Mater 408:124968

    CAS  Google Scholar 

  • Ghosh A, Pandey B, Agrawal M, Agrawal SB (2020b) Interactive effects and competitive shift between Triticum aestivum L.(wheat) and Chenopodium album L.(fat-hen) under ambient and elevated ozone. Environ Pollut 265:114764

    CAS  Google Scholar 

  • Ghosh A, Pandey B, Yadav DS (2021c) Chapter twelve implications of ozone on ecosystem services. In: Tropospheric Ozone: A Hazard for Vegetation and Human Health, p 426

    Google Scholar 

  • Ghosh A, Singh AA, Agrawal M, Agrawal SB (2018) Ozone toxicity and remediation in crop plants. In: Sustainable Agriculture Reviews, vol 27. Springer, Cham, pp 129–169

    Google Scholar 

  • Ghosh A, Singh P, Agrawal M, Agrawal S (2021b) Chapter eleven response of crop plants to tropospheric ozone under different agronomic practices: an insight into the mechanisms. In: Tropospheric Ozone: A Hazard for Vegetation and Human Health, p 380

    Google Scholar 

  • Gill SS, Tuteja N (2010) Reactive oxygen species and antioxidant machinery in abiotic stress tolerance in crop plants. Plant Physiol Biochem 48(12):909–930

    CAS  Google Scholar 

  • Gillespie KM, Rogers A, Ainsworth EA (2011) Growth at elevated ozone or elevated carbon dioxide concentration alters antioxidant capacity and response to acute oxidative stress in soybean (Glycine max). J Exp Bot 62(8):2667–2678

    CAS  Google Scholar 

  • Girón-Calva PS, Li T, Blande JD (2016) Plant-plant interactions affect the susceptibility of plants to oviposition by pests but are disrupted by ozone pollution. Agr Ecosyst Environ 233:352–360

    Google Scholar 

  • Giron-Calva PS, Li T, Blande JD (2017) Volatile-mediated interactions between cabbage plants in the field and the impact of ozone pollution. J Chem Ecol 43(4):339–350

    CAS  Google Scholar 

  • González-Fernández I, Bass D, Muntifering R, Mills G, Barnes J (2008) Impacts of ozone pollution on productivity and forage quality of grass/clover swards. Atmos Environ 42(38):8755–8769

    Google Scholar 

  • Gorelick J, Bernstein N (2014) Elicitation: an underutilized tool in the development of medicinal plants as a source of therapeutic secondary metabolites. Adv Agron 124:201–230

    CAS  Google Scholar 

  • Gould KS, Lister C (2006) Flavonoid functions in plants. In: Flavonoids: Chemistry, biochemistry and applications, pp 397–441

    Google Scholar 

  • Grace SC (2005) Phenolics as antioxidants. In: Antioxidants and reactive oxygen species in plants, vol 141, p 168

    Google Scholar 

  • Guidi L, Degl’Innocenti E, Genovesi S, Soldatini GF (2005) Photosynthetic process and activities of enzymes involved in the phenylpropanoid pathway in resistant and sensitive genotypes of Lycopersicon esculentum L. exposed to ozone. Plant Sci 168(1):153–160

    CAS  Google Scholar 

  • Guidi L, Degl’Innocenti E, Martinelli F, Piras M (2009) Ozone effects on carbon metabolism in sensitive and insensitive Phaseolus cultivars. Environ Exp Bot 66(1):117–125

    CAS  Google Scholar 

  • Guirimand G, Guihur A, Poutrain P, Héricourt F, Mahroug S, St-Pierre B, Burlat V, Courdavault V (2011) Spatial organization of the vindoline biosynthetic pathway in Catharanthus roseus. J Plant Physiol 168(6):549–557

    CAS  Google Scholar 

  • Gupta P, De B (2017) Differential responses of cell wall bound phenolic compounds in sensitive and tolerant varieties of rice in response to salinity. Plant Signal Behav 12(10):e1379643

    Google Scholar 

  • Haig T (2008) Allelochemicals in plants. In: Allelopathy in sustainable agriculture and forestry. Springer, New York, NY, pp 63–104

    Google Scholar 

  • Häikiö E, Freiwald V, Julkunen-Tiitto R, Beuker E, Holopainen T, Oksanen E (2009) Differences in leaf characteristics between ozone-sensitive and ozone-tolerant hybrid aspen (Populus tremula× Populus tremuloides) clones. Tree Physiol 29(1):53–66

    Google Scholar 

  • Halkier BA, Gershenzon J (2006) Biology and biochemistry of glucosinolates. Annu Rev Plant Biol 57(1):303–333

    CAS  Google Scholar 

  • Han YJ, Gharibeshghi A, Mewis I, Förster N, Beck W, Ulrichs C (2021) Effect of different durations of moderate ozone exposure on secondary metabolites of Brassica campestris L. ssp. chinensis. J Hortic Sci Biotech 96(1):110–120

    CAS  Google Scholar 

  • Haraguchi H, Tanimoto K, Tamura Y, Mizutani K, Kinoshita T (1998) Mode of antibacterial action of retrochalcones from Glycyrrhiza inflata. Phytochemistry 48(1):125–129

    CAS  Google Scholar 

  • Harborne JB, Williams CA (2000) Advances in flavonoid research since 1992. Phytochemistry 55(6):481–504

    CAS  Google Scholar 

  • Hashimoto T, Yamada Y (2003) New genes in alkaloid metabolism and transport. Curr Opin Biotechnol 14(2):163–168

    CAS  Google Scholar 

  • Hättenschwiler S, Vitousek PM (2000) The role of polyphenols in terrestrial ecosystem nutrient cycling. Trends Ecol Evol 15(6):238–243

    Google Scholar 

  • Hayes F, Jones MLM, Mills G, Ashmore M (2007) Meta-analysis of the relative sensitivity of semi-natural vegetation species to ozone. Environ Pollut 146(3):754–762

    CAS  Google Scholar 

  • Hayes F, Mills G, Ashmore M (2009) Effects of ozone on inter-and intra-species competition and photosynthesis in mesocosms of Lolium perenne and Trifolium repens. Environ Pollut 157(1):208–214

    CAS  Google Scholar 

  • Hayes F, Mills G, Jones L, Abbott J, Ashmore M, Barnes J, Cape JN, Coyle M, Peacock S, Rintoul N, Toet S (2016) Consistent ozone-induced decreases in pasture forage quality across several grassland types and consequences for UK lamb production. Sci Total Environ 543:336–346

    CAS  Google Scholar 

  • Hewitt DKL, Mills G, Hayes F, Norris D, Coyle M, Wilkinson S, Davies W (2016) N-fixation in legumes–an assessment of the potential threat posed by ozone pollution. Environ Pollut 208:909–918

    CAS  Google Scholar 

  • Hewitt DKL, Mills G, Hayes F, Wilkinson S, Davies W (2014) Highlighting the threat from current and near-future ozone pollution to clover in pasture. Environ Pollut 189:111–117

    CAS  Google Scholar 

  • Hillstrom ML, Lindroth RL (2008) Elevated atmospheric carbon dioxide and ozone alter forest insect abundance and community composition. Insect Conserv Divers 1(4):233–241

    Google Scholar 

  • Hoang Anh L, Van Quan N, Tuan Nghia L, Dang Xuan T (2021) Phenolic allelochemicals: achievements, limitations, and prospective approaches in weed management. Weed Biol Manag 21(2):37–67

    Google Scholar 

  • Holmes WE, Zak DR, Pregitzer KS, King JS (2003) Soil nitrogen transformations under Populus tremuloides, Betula papyrifera and Acer saccharum following 3 years exposure to elevated CO2 and O3. Glob Chang Biol 9(12):1743–1750

    Google Scholar 

  • Holmes WE, Zak DR, Pregitzer KS, King JS (2006) Elevated CO2 and O3 alter soil nitrogen transformations beneath trembling aspen, paper birch, and sugar maple. Ecosystems 9(8):1354–1363

    CAS  Google Scholar 

  • Holstein SA, Hohl RJ (2004) Isoprenoids: remarkable diversity of form and function. Lipids 39(4):293–309

    CAS  Google Scholar 

  • Holton MK, Lindroth RL, Nordheim EV (2003) Foliar quality influences tree-herbivore-parasitoid interactions: effects of elevated CO2, O3, and plant genotype. Oecologia 137(2):233–244

    Google Scholar 

  • Huang XF, Chaparro JM, Reardon KF, Zhang R, Shen Q, Vivanco JM (2014) Rhizosphere interactions: root exudates, microbes, and microbial communities. Botany 92(4):267–275

    Google Scholar 

  • Hussain MI, Reigosa MJ (2021) Secondary metabolites, ferulic acid and p-hydroxybenzoic acid induced toxic effects on photosynthetic process in Rumex acetosa L. Biomolecules 11(2):233

    CAS  Google Scholar 

  • Inderjit (1996) Plant phenolics in allelopathy. Bot Rev 62:186–202

    Google Scholar 

  • Iriti M, Faoro F (2004) Plant defense and human nutrition: phenylpropanoids on the menu. Curr Top Nutraceutical Res 2(1):47–65

    CAS  Google Scholar 

  • Iriti M, Faoro F (2009) Chemical diversity and defence metabolism: how plants cope with pathogens and ozone pollution. Int J Mol Sci 10(8):3371–3399

    CAS  Google Scholar 

  • Jabran K, Mahajan G, Sardana V, Chauhan BS (2015) Allelopathy for weed control in agricultural systems. Crop Prot 72:57–65

    Google Scholar 

  • Jackson DM, Heagle AS, Eckel RVW (1999) Ovipositional response of tobacco hornworm moths (Lepidoptera: Sphingidae) to tobacco plants grown under elevated levels of ozone. Environ Entomol 28(4):566–571

    CAS  Google Scholar 

  • Janzik I, Preiskowski S, Kneifel H (2005) Ozone has dramatic effects on the regulation of the prechorismate pathway in tobacco (Nicotiana tabacum L. cv. Bel W3). Planta 223(1):20–27

    CAS  Google Scholar 

  • Jones CG, Coleman JS (1988) Plant stress and insect behavior: cottonwood, ozone and the feeding and oviposition preference of a beetle. Oecologia 76(1):51–56

    Google Scholar 

  • Kacienė G, Miškelytė D, AbdElgawad H, Beemster G, Asard H, Dikšaitytė A, Žaltauskaitė J, Sujetovienė G, Januškaitienė I, Juknys R (2019) O3 pollution in a future climate increases the competition between summer rape and wild mustard. Plant Physiol Biochem 135:194–205

    Google Scholar 

  • Kanagendran A, Chatterjee P, Liu B, Sa T, Pazouki L, Niinemets Ü (2019) Foliage inoculation by Burkholderia vietnamiensis CBMB40 antagonizes methyl jasmonate-mediated stress in Eucalyptus grandis. J Plant Physiol 242:153032

    CAS  Google Scholar 

  • Kanagendran A, Pazouki L, Niinemets Ü (2018) Differential regulation of volatile emission from Eucalyptus globulus leaves upon single and combined ozone and wounding treatments through recovery and relationships with ozone uptake. Environ Exp Bot 145:21–38

    CAS  Google Scholar 

  • Kangasjärvi J, Jaspers P, Kollist H (2005) Signalling and cell death in ozone-exposed plants. Plant Cell Environ 28(8):1021–1036

    Google Scholar 

  • Kannan E, Palayian L (2022) Allelopathic potential of Annona muricata (L.) on physiological and biochemical changes of Vigna radiata (L.) and Eleusine coracana (L.) Gaertn. J Appl Biol Biotechnol 10(3):1–5

    Google Scholar 

  • Keski-Saari S (2005) Phenolic compounds in birch seedlings during early ontogeny: regulation of biosynthesis and accumulation in response to nutrient availability and UV-B radiation. University of Joensuu

    Google Scholar 

  • Khaling E, Agyei T, Jokinen S, Holopainen JK, Blande JD (2020) The phytotoxic air-pollutant O3 enhances the emission of herbivore-induced volatile organic compounds (VOCs) and affects the susceptibility of black mustard plants to pest attack. Environ Pollut 265:115030

    CAS  Google Scholar 

  • Khaling E, Papazian S, Poelman EH, Holopainen JK, Albrectsen BR, Blande JD (2015) Ozone affects growth and development of Pieris brassicae on the wild host plant Brassica nigra. Environ Pollut 199:119–129

    CAS  Google Scholar 

  • Kim JS, Chappelka AH, Miller-Goodman MS (1998) Decomposition of blackberry and broomsedge bluestem as influenced by ozone (Vol. 27, No. 4, pp. 953-960). American Society of Agronomy, Crop Science Society of America, and Soil Science Society of America

    Google Scholar 

  • Kivimäenpää M, Ghimire RP, Sutinen S, Häikiö E, Kasurinen A, Holopainen T, Holopainen JK (2016) Increases in volatile organic compound emissions of Scots pine in response to elevated ozone and warming are modified by herbivory and soil nitrogen availability. Eur J For Res 135(2):343–360

    Google Scholar 

  • Kleanthous S, Vrekoussis M, Mihalopoulos N, Kalabokas P, Lelieveld J (2014) On the temporal and spatial variation of ozone in Cyprus. Sci Total Environ 476:677–687

    Google Scholar 

  • Kluth S, Kruess A, Tscharntke T (2002) Insects as vectors of plant pathogens: mutualistic and antagonistic interactions. Oecologia 133(2):193–199

    Google Scholar 

  • Koffler BE, Luschin-Ebengreuth N, Stabentheiner E, Müller M, Zechmann B (2014) Compartment specific response of antioxidants to drought stress in Arabidopsis. Plant Sci 227:133–144

    CAS  Google Scholar 

  • Kontunen-Soppela SARI, Ossipov V, Ossipova S, Oksanen E (2007) Shift in birch leaf metabolome and carbon allocation during long-term open-field ozone exposure. Glob Chang Biol 13(5):1053–1067

    Google Scholar 

  • Kopper BJ, Lindroth RL (2003) Effects of elevated carbon dioxide and ozone on the phytochemistry of aspen and performance of an herbivore. Oecologia 134(1):95–103

    Google Scholar 

  • Koricheva J, Larsson S, Haukioja E (1998) Insect performance on experimentally stressed woody plants: a meta-analysis. Annu Rev Entomol 43(1):195–216

    CAS  Google Scholar 

  • Korkina LG (2007) Phenylpropanoids as naturally occurring antioxidants: from plant defense to human health. Cell Mol Biol 53(1):15–25

    CAS  Google Scholar 

  • Korkina LG, Afanas'Ev IB (1996) Antioxidant and chelating properties of flavonoids. Adv Pharmacol 38:151–163

    Google Scholar 

  • Krupa S, Muntifering R, Chappelka A (2004) Effects of ozone on plant nutritive quality characteristics for ruminant animals. The Botanica 54:1–12

    Google Scholar 

  • Laine AL (2004) A powdery mildew infection on a shared host plant affects the dynamics of the Glanville fritillary butterfly populations. Oikos 107(2):329–337

    Google Scholar 

  • Laisk A, Kull O, Moldau H (1989) Ozone concentration in leaf intercellular air spaces is close to zero. Plant Physiol 90(3):1163–1167

    CAS  Google Scholar 

  • Lake JA, Field KJ, Davey MP, Beerling DJ, Lomax BH (2009) Metabolomic and physiological responses reveal multi-phasic acclimation of Arabidopsis thaliana to chronic UV radiation. Plant Cell Environ 32(10):1377–1389

    CAS  Google Scholar 

  • Langebartels C, Wohlgemuth H, Kschieschan S, Grün S, Sandermann H (2002) Oxidative burst and cell death in ozone-exposed plants. Plant Physiol Biochem 40(6-8):567–575

    CAS  Google Scholar 

  • Latif S, Chiapusio G, Weston LA (2017) Allelopathy and the role of allelochemicals in plant defence. In: Advances in botanical research, vol 82. Academic Press, pp 19–54

    Google Scholar 

  • Lattanzio V, Lattanzio VM, Cardinali A (2006) Role of phenolics in the resistance mechanisms of plants against fungal pathogens and insects. Phytochem: Adv Res 661(2):23–67

    Google Scholar 

  • Lazebnik J, Frago E, Dicke M, van Loon JJ (2014) Phytohormone mediation of interactions between herbivores and plant pathogens. J Chem Ecol 40(7):730–741

    CAS  Google Scholar 

  • Lerdau, M., Shugart, H., & Fuentes, J. (2007). COS 7-10: isoprene, ozone, and biodiversity: a positive feedback loop with negative consequences.

    Google Scholar 

  • Leszczynski B, Tjallingii WF, Dixon AFG, Swiderski R (1995) Effect of methoxyphenols on grain aphid feeding behaviour. Entomol Exp Appl 76(2):157–162

    CAS  Google Scholar 

  • Li G, Shi Y, Chen X (2008) Effects of elevated CO2 and O3 on phenolic compounds in spring wheat and maize leaves. Bull Environ Contam Toxicol 81(5):436–439

    CAS  Google Scholar 

  • Li T, Blande JD (2015) Associational susceptibility in broccoli: mediated by plant volatiles, impeded by ozone. Glob Chang Biol 21(5):1993–2004

    Google Scholar 

  • Li ZH, Wang Q, Ruan X, Pan CD, Jiang DA (2010) Phenolics and plant allelopathy. Molecules 15(12):8933–8952

    CAS  Google Scholar 

  • Lindroth RL (2010) Impacts of elevated atmospheric CO2 and O3 on forests: phytochemistry, trophic interactions, and ecosystem dynamics. J Chem Ecol 36(1):2–21

    CAS  Google Scholar 

  • Lindroth RL, Kopper BJ, Parsons WF, Bockheim JG, Karnosky DF, Hendrey GR, Pregitzer KS, Isebrands JG, Sober J (2001) Consequences of elevated carbon dioxide and ozone for foliar chemical composition and dynamics in trembling aspen (Populus tremuloides) and paper birch (Betula papyrifera). Environ Pollut 115(3):395–404

    CAS  Google Scholar 

  • Liu L, King JS, Giardina CP (2005) Effects of elevated concentrations of atmospheric CO2 and tropospheric O3 on leaf litter production and chemistry in trembling aspen and paper birch communities. Tree Physiol 25(12):1511–1522

    CAS  Google Scholar 

  • Logemann E, Tavernaro A, Schulz W, Somssich IE, Hahlbrock K (2000) UV light selectively coinduces supply pathways from primary metabolism and flavonoid secondary product formation in parsley. Proc Natl Acad Sci 97(4):1903–1907

    CAS  Google Scholar 

  • Loreto F, Förster A, Dürr M, Csiky O, Seufert G (1998) On the monoterpene emission under heat stress and on the increased thermotolerance of leaves of Quercus ilex L. fumigated with selected monoterpenes. Plant Cell Environ 21(1):101–107

    CAS  Google Scholar 

  • Loreto F, Mannozzi M, Maris C, Nascetti P, Ferranti F, Pasqualini S (2001) Ozone quenching properties of isoprene and its antioxidant role in leaves. Plant Physiol 126(3):993–1000

    CAS  Google Scholar 

  • Loreto F, Schnitzler JP (2010) Abiotic stresses and induced BVOCs. Trends Plant Sci 15(3):154–166

    CAS  Google Scholar 

  • Lupini A, Sorgona A, Princi MP, Sunseri F, Abenavoli MR (2016) Morphological and physiological effects of trans-cinnamic acid and its hydroxylated derivatives on maize root types. Plant Growth Regul 78(2):263–273

    CAS  Google Scholar 

  • Makoi JH, Ndakidemi PA (2007) Biological, ecological and agronomic significance of plant phenolic compounds in rhizosphere of the symbiotic legumes. Afr J Biotechnol 6(12)

  • Mao B, Yin H, Wang Y, Zhao TH, Tian RR, Wang W, Ye JS (2017) Combined effects of O3 and UV radiation on secondary metabolites and endogenous hormones of soybean leaves. PloS One 12(8):e0183147

    Google Scholar 

  • Marchica A, Ascrizzi R, Flamini G, Cotrozzi L, Tonelli M, Lorenzini G, Nali C, Pellegrini E (2021) Ozone as eustress for enhancing secondary metabolites and bioactive properties in Salvia officinalis. Ind Crop Prod 170:113730

    CAS  Google Scholar 

  • Marquardt J, Hanelt D (2004) Carotenoid composition of Delesseria lancifolia and other marine red algae from polar and temperate habitats. Eur J Phycol 39(3):285–292

    CAS  Google Scholar 

  • Martins N, Barros L, Santos-Buelga C, Henriques M, Silva S, Ferreira IC (2015) Evaluation of bioactive properties and phenolic compounds in different extracts prepared from Salvia officinalis L. Food Chem 170:378–385

    CAS  Google Scholar 

  • Masui N, Mochizuki T, Tani A, Matsuura H, Agathokleous E, Watanabe T, Koike T (2020) Does ozone alter the attractiveness of Japanese white birch leaves to the leaf beetle Agelastica coerulea via changes in biogenic volatile organic compounds (BVOCs): an examination with the Y-tube test. Forests 11(1):58

    Google Scholar 

  • Matyssek R, Sandermann H (2003) Impact of ozone on trees: an ecophysiological perspective. Progress in botany:349–404

  • McCrady JK, Andersen CP (2000) The effect of ozone on below-ground carbon allocation in wheat. Environ Pollut 107(3):465–472

    CAS  Google Scholar 

  • Mierziak J, Kostyn K, Kulma A (2014) Flavonoids as important molecules of plant interactions with the environment. Molecules 19(10):16240–16265

    Google Scholar 

  • Mikkelsen BL, Jørgensen RB, Lyngkjær MF (2015b) Complex interplay of future climate levels of CO2, ozone and temperature on susceptibility to fungal diseases in barley. Plant pathology 64(2):319–327

    CAS  Google Scholar 

  • Mikkelsen BL, Olsen CE, Lyngkjær MF (2015a) Accumulation of secondary metabolites in healthy and diseased barley, grown under future climate levels of CO2, ozone and temperature. Phytochemistry 118:162–173

    CAS  Google Scholar 

  • Miranda M, Ralph SG, Mellway R, White R, Heath MC, Bohlmann J, Constabel CP (2007) The transcriptional response of hybrid poplar (Populus trichocarpa x P. deltoids) to infection by Melampsora medusae leaf rust involves induction of flavonoid pathway genes leading to the accumulation of proanthocyanidins. Mol Plant Microbe Interact 20(7):816–831

    CAS  Google Scholar 

  • Mishra AK, Agrawal SB (2015) Biochemical and physiological characteristics of tropical mung bean (Vigna radiata L.) cultivars against chronic ozone stress: an insight to cultivar-specific response. Protoplasma 252(3):797–811

    CAS  Google Scholar 

  • Mishra AK, Mishra A, Kehri HK, Sharma B, Pandey AK (2009) Inhibitory activity of Indian spice plant Cinnamomum zeylanicum extracts against Alternaria solani and Curvularia lunata, the pathogenic dematiaceous moulds. Ann Clin Microbiol Antimicrob 8(1):1–7

    Google Scholar 

  • Mittler R (2017) ROS are good. Trends Plant Sci 22(1):11–19

    CAS  Google Scholar 

  • Mochizuki T, Watanabe M, Koike T, Tani A (2017) Monoterpene emissions from needles of hybrid larch F1 (Larix gmelinii var. japonica× Larix kaempferi) grown under elevated carbon dioxide and ozone. Atmos Environ 148:197–202

    CAS  Google Scholar 

  • Mofikoya AO, Bui TNT, Kivimäenpää M, Holopainen JK, Himanen SJ, Blande JD (2019) Foliar behaviour of biogenic semi-volatiles: potential applications in sustainable pest management. Arthropod-Plant Interactions 13(2):193–212

    Google Scholar 

  • Møller BL (2010) Functional diversifications of cyanogenic glucosides. Curr Opin Plant Biol 13(3):337–346

    Google Scholar 

  • Munné-Bosch S, Alegre L (2002) The function of tocopherols and tocotrienols in plants. Crit Rev Plant Sci 21(1):31–57

    Google Scholar 

  • Munné-Bosch S, Falk J (2004) New insights into the function of tocopherols in plants. Planta 218(3):323–326

    Google Scholar 

  • Muntifering RB, Chappelka AH, Lin JC, Karnosky DF, Somers GL (2006) Chemical composition and digestibility of Trifolium exposed to elevated ozone and carbon dioxide in a free-air (FACE) fumigation system. Funct Ecol 20(2):269–275

    Google Scholar 

  • Murata J, Roepke J, Gordon H, De Luca V (2008) The leaf epidermome of Catharanthus roseus reveals its biochemical specialization. Plant Cell 20(3):524–542

    CAS  Google Scholar 

  • Nakayama M, Tateno R (2018) Solar radiation strongly influences the quantity of forest tree root exudates. Trees 32(3):871–879

    CAS  Google Scholar 

  • Ogawa D, Nakajima N, Sano T, Tamaoki M, Aono M, Kubo A (2005) Regulation of salicylic acid synthesis in ozone-exposed tobacco and Arabidopsis. Phyton-Horn 45(4):169

    CAS  Google Scholar 

  • Oksanen E, Manninen S, Vapaavuori E, Holopainen T (2009) Near-ambient ozone concentrations reduce the vigor of Betula and Populus species in Finland. Ambio 38:413–417

    CAS  Google Scholar 

  • Olsen KM, Lea US, Slimestad R, Verheul M, Lillo C (2008) Differential expression of four Arabidopsis PAL genes; PAL1 and PAL2 have functional specialization in abiotic environmental-triggered flavonoid synthesis. J Plant Physiol 165(14):1491–1499

    CAS  Google Scholar 

  • Osier TL, Lindroth RL (2006) Genotype and environment determine allocation to and costs of resistance in quaking aspen. Oecologia 148(2):293–303

    Google Scholar 

  • Pant P, Pandey S, Dall'Acqua S (2021) The influence of environmental conditions on secondary metabolites in medicinal plants: a literature review. Chem Biodivers 18(11):e2100345

    CAS  Google Scholar 

  • Paolacci AR, D'Ovidio R, Marabottini R, Nali C, Lorenzini G, Abenavoli MR, Badiani M (2001) Research note: ozone induces a differential accumulation of phenyalanine ammonia-lyase, chalcone synthase and chalcone isomerase RNA transcripts in sensitive and resistant bean cultivars. Funct Plant Biol 28(5):425–428

    CAS  Google Scholar 

  • Peer WA, Brown DE, Tague BW, Muday GK, Taiz L, Murphy AS (2001) Flavonoid accumulation patterns of transparent test a mutant of Arabidopsis. Plant Physiol 126(2):536–548

    CAS  Google Scholar 

  • Pellegrini E, Campanella A, Cotrozzi L, Tonelli M, Nali C, Lorenzini G (2018a) Ozone primes changes in phytochemical parameters in the medicinal herb Hypericum perforatum (St. John’s wort). Ind Crop Prod 126:119–128

    CAS  Google Scholar 

  • Pellegrini E, Campanella A, Cotrozzi L, Tonelli M, Nali C, Lorenzini G (2018b) What about the detoxification mechanisms underlying ozone sensitivity in Liriodendron tulipifera? Environ Sci Pollut Res 25(9):8148–8160

    CAS  Google Scholar 

  • Pellegrini E, Cioni PL, Francini A, Lorenzini G, Nali C, Flamini G (2012) Volatiles emission patterns in poplar clones varying in response to ozone. J Chem Ecol 38(7):924–932

    CAS  Google Scholar 

  • Pellegrini E, Cotrozzi L, Neri L, Baraldi R, Carrari E, Nali C, Lorenzini G, Paoletti E, Hoshika Y (2021) Stress markers and physiochemical responses of the Mediterranean shrub Phillyrea angustifolia under current and future drought and ozone scenarios. Environ Res 201:111615

    CAS  Google Scholar 

  • Peñuelas J, Staudt M (2010) BVOCs and global change. Trends Plant Sci 15(3):133–144

    Google Scholar 

  • Pinto DM, Blande JD, Nykänen R, Dong WX, Nerg AM, Holopainen JK (2007) Ozone degrades common herbivore-induced plant volatiles: does this affect herbivore prey location by predators and parasitoids? J Chem Ecol 33(4):683–694

    CAS  Google Scholar 

  • Pinto DM, Blande JD, Souza SR, Nerg AM, Holopainen JK (2010) Plant volatile organic compounds (VOCs) in ozone (O3) polluted atmospheres: the ecological effects. J Chem Ecol 36(1):22–34

    CAS  Google Scholar 

  • Pleijel H, Karlsson GP, Sild E, Danielsson H, Skärby L, Selldén G (1996) Exposure of a grass-clover mixture to ozone in open-top chambers—effects on yield, quality and botanical composition. Agr Ecosyst Environ 59(1-2):55–62

    CAS  Google Scholar 

  • Pollastri S, Tattini M (2011) Flavonols: old compounds for old roles. Ann Bot 108(7):1225–1233

    CAS  Google Scholar 

  • Powell MC, Muntifering RB, Lin JC, Chappelka AH (2003) Yield and nutritive quality of sericea lespedeza (Lespedeza cuneata) and little bluestem (Schizachyrium scoparium) exposed to ground-level ozone. Environ Pollut 122(3):313–322

    CAS  Google Scholar 

  • Rai R, Singh AA, Agrawal SB, Agrawal M (2016) Tropospheric O3: a cause of concern for terrestrial plants. In: Plant responses to air pollution. Springer, Singapore, pp 165–195

    Google Scholar 

  • Renaut J, Bohler S, Hausman JF, Hoffmann L, Sergeant K, Ahsan N, Jolivet Y, Dizengremel P (2009) The impact of atmospheric composition on plants: a case study of ozone and poplar. Mass Spectrom Rev 28(3):495–516

    CAS  Google Scholar 

  • Richet N, Afif D, Huber F, Pollet B, Banvoy J, El Zein R, Lapierre C, Dizengremel P, Perre P, Cabane M (2011) Cellulose and lignin biosynthesis is altered by ozone in wood of hybrid poplar (Populus tremula× alba). J Exp Bot 62(10):3575–3586

    CAS  Google Scholar 

  • Richet N, Afif D, Tozo K, Pollet B, Maillard P, Huber F, Priault P, Banvoy J, Gross P, Dizengremel P, Lapierre C (2012) Elevated CO2 and/or ozone modify lignification in the wood of poplars (Populus tremula x alba). J Exp Bot 63(11):4291–4301

    CAS  Google Scholar 

  • Rosa E, Woestmann L, Biere A, Saastamoinen M (2018) A plant pathogen modulates the effects of secondary metabolites on the performance and immune function of an insect herbivore. Oikos 127(10):1539–1549

    CAS  Google Scholar 

  • Rosemann D, Heller W, Sandermann H Jr (1991) Biochemical plant responses to ozone: II. Induction of stilbene biosynthesis in Scots pine (Pinus sylvestris L.) seedlings. Plant Physiol 97(4):1280–1286

    CAS  Google Scholar 

  • Sakihama Y, Cohen MF, Grace SC, Yamasaki H (2002) Plant phenolic antioxidant and prooxidant activities: phenolics-induced oxidative damage mediated by metals in plants. Toxicology 177(1):67–80

    CAS  Google Scholar 

  • Saleem A, Loponen J, Pihlaja K, Oksanen E (2001) Effects of long-term open-field ozone exposure on leaf phenolics of European silver birch (Betula pendula Roth). J Chem Ecol 27(5):1049–1062

    CAS  Google Scholar 

  • Sampedro J, Waldhoff ST, Van de Ven DJ, Pardo G, Van Dingenen R, Arto I, del Prado A, Sanz MJ (2020) Future impacts of ozone driven damages on agricultural systems. Atmos Environ 231:117538

    CAS  Google Scholar 

  • Sanz J, Muntifering RB, Bermejo V, Gimeno BS, Elvira S (2005) Ozone and increased nitrogen supply effects on the yield and nutritive quality of Trifolium subterraneum. Atmos Environ 39(32):5899–5907

    CAS  Google Scholar 

  • Sarkar A, Singh AA, Agrawal SB, Ahmad A, Rai SP (2015) Cultivar specific variations in antioxidative defense system, genome and proteome of two tropical rice cultivars against ambient and elevated ozone. Ecotoxicol Environ Saf 115:101–111

    CAS  Google Scholar 

  • Saslowsky D, Winkel-Shirley B (2001) Localization of flavonoid enzymes in Arabidopsis roots. Plant J 27(1):37–48

    CAS  Google Scholar 

  • Sato F, Hashimoto T, Hachiya A, Tamura KI, Choi KB, Morishige T, Fujimoto H, Yamada Y (2001) Metabolic engineering of plant alkaloid biosynthesis. Proc Natl Acad Sci 98(1):367–372

    CAS  Google Scholar 

  • Saunders JA, McClure JW (1976) The distribution of flavonoids in chloroplasts of twenty five species of vascular plants. Phytochemistry 15(5):809–810

    CAS  Google Scholar 

  • Saunders JA, O’neill NR, Romeo JT (1992) Alkaloid chemistry and feeding specificity of insect herbivores. In: Alkaloids: chemical and biological perspectives. Springer, New York, NY, pp 151–196

    Google Scholar 

  • Saviranta NM, Julkunen-Tiitto R, Oksanen E, Karjalainen RO (2010) Leaf phenolic compounds in red clover (Trifolium pratense L.) induced by exposure to moderately elevated ozone. Environ Pollut 158(2):440–446

    CAS  Google Scholar 

  • Schmeizer HG (1988) Polyurethanes for “two-dimensional” applications. Materials & Design 9(5):276–286

    Google Scholar 

  • Schneider GF, Cheesman AW, Winter K, Turner BL, Sitch S, Kursar TA (2017) Current ambient concentrations of ozone in Panama modulate the leaf chemistry of the tropical tree Ficus insipida. Chemosphere 172:363–372

    CAS  Google Scholar 

  • Sgarbi E, Fornasiero RB, Lins AP, Bonatti PM (2003) Phenol metabolism is differentially affected by ozone in two cell lines from grape (Vitis vinifera L.) leaf. Plant Sci 165(5):951–957

    CAS  Google Scholar 

  • Shamay Y, Raskin VI, Brandis AS, Steinberger HE, Marder JB, Schwartz A (2001) Ozone treatment affects pigment precursor metabolism in pine seedlings. Physiol Plant 112(2):285–292

    CAS  Google Scholar 

  • Shang B, Xu Y, Dai L, Yuan X, Feng Z (2019) Elevated ozone reduced leaf nitrogen allocation to photosynthesis in poplar. Sci Total Environ 657:169–178

    CAS  Google Scholar 

  • Sharma P, Jha AB, Dubey RS, Pessarakli M (2012) Reactive oxygen species, oxidative damage, and antioxidative defense mechanism in plants under stressful conditions. J Bot 2012:217037

    Google Scholar 

  • Sharma YK, Davis KR (1994) Ozone-induced expression of stress-related genes in Arabidopsis thaliana. Plant Physiol 105(4):1089–1096

    CAS  Google Scholar 

  • Shen Z, Haslam E, Falshaw CP, Begley MJ (1986) Procyanidins and polyphenols of Larix gmelini bark. Phytochemistry 25(11):2629–2635

    CAS  Google Scholar 

  • Shetty R, Fretté X, Jensen B, Shetty NP, Jensen JD, Jørgensen HJ, Newman MA, Christensen LP (2011) Silicon-induced changes in antifungal phenolic acids, flavonoids, and key phenylpropanoid pathway genes during the interaction between miniature roses and the biotrophic pathogen Podosphaera pannosa. Plant Physiol 157(4):2194–2205

    CAS  Google Scholar 

  • Shi C, Watanabe T, Koike T (2017) Leaf stoichiometry of deciduous tree species in different soils exposed to free-air O3 enrichment over two growing seasons. Environ Exp Bot 138:148–163

    CAS  Google Scholar 

  • Shitan N, Yazaki K (2007) Accumulation and membrane transport of plant alkaloids. Curr Pharm Biotechnol 8(4):244–252

    CAS  Google Scholar 

  • Singh AA (2022) Biomonitoring potential of tropospheric ozone in plants utilizing visible injury and biomarkers. In: New Paradigms in Environmental Biomonitoring Using Plants. Elsevier, pp 181–224

    Google Scholar 

  • Singh AA, Agrawal S (2021) Chapter ten analysis of transcriptome, proteome, and metabolome approaches to overview the ozone responses in plants. In: Tropospheric Ozone: A Hazard for Vegetation and Human Health, p 335

    Google Scholar 

  • Singh AA, Agrawal SB (2017) Tropospheric ozone pollution in India: effects on crop yield and product quality. Environ Sci Pollut Res 24(5):4367–4382

    CAS  Google Scholar 

  • Singh AA, Agrawal SB, Shahi JP, Agrawal M (2014) Investigating the response of tropical maize (Zea mays L.) cultivars against elevated levels of O3 at two developmental stages. Ecotoxicology 23(8):1447–1463

    CAS  Google Scholar 

  • Singh AA, Ghosh A, Pandey B, Agrawal M, Agrawal SB (2023) Unravelling the ozone toxicity in Zea mays L.(C4 plant) under the elevated level of CO2 fertilization. Tropical Ecology:1–17

  • Singh AA, Singh S, Agrawal M, Agrawal SB (2015) Assessment of ethylene diurea-induced protection in plants against ozone phytotoxicity. Rev Environ Contam Toxicol 233:129–184

    CAS  Google Scholar 

  • Singh NB, Khare S, Singh A, Yadav V, Yadav RK (2021) Salicylic acid and Indole acetic acid synergistically ameliorates ferulic acid toxicity in Brassica juncea L. seedlings. Plant Physiology Reports 26(4):729–740

    Google Scholar 

  • Sirikantaramas S, Yamazaki M, Saito K (2008) Mechanisms of resistance to self-produced toxic secondary metabolites in plants. Phytochemistry Reviews 7(3):467–477

    CAS  Google Scholar 

  • Smallegange RC, Van Loon JJA, Blatt SE, Harvey JA, Agerbirk N, Dicke M (2007) Flower vs. leaf feeding by Pieris brassicae: glucosinolate-rich flower tissues are preferred and sustain higher growth rate. J Chem Ecol 33(10):1831–1844

    CAS  Google Scholar 

  • Smith CG, Rodgers MW, Zimmerlin A, Ferdinando D, Bolwell GP (1994) Tissue and subcellular immunolocalisation of enzymes of lignin synthesis in differentiating and wounded hypocotyl tissue of French bean (Phaseolus vulgaris L.). Planta 192(2):155–164

    CAS  Google Scholar 

  • Smith LM, Reynolds HL (2014) Light, allelopathy, and post-mortem invasive impact on native forest understory species. Biol Invasions 16(5):1131–1144

    Google Scholar 

  • Stafford HA (1988) Proanthocyanidins and the lignin connection. Phytochemistry 27(1):1–6

    CAS  Google Scholar 

  • Steppuhn A, Gase K, Krock B, Halitschke R, Baldwin IT (2004) Nicotine’s defensive function in nature. PLoS Biol 2(8):e217

    Google Scholar 

  • Subramanian S, Graham MY, Yu O, Graham TL (2005) RNA interference of soybean isoflavone synthase genes leads to silencing in tissues distal to the transformation site and to enhanced susceptibility to Phytophthora sojae. Plant Physiol 137(4):1345–1353

    CAS  Google Scholar 

  • Sugai T, Okamoto S, Agathokleous E, Masui N, Satoh F, Koike T (2020) Leaf defense capacity of Japanese elm (Ulmus davidiana var. japonica) seedlings subjected to a nitrogen loading and insect herbivore dynamics in a free air ozone-enriched environment. Environ Sci Pollut Res 27(3):3350–3360

    CAS  Google Scholar 

  • Sun L, Su H, Zhu Y, Xu M (2012) Involvement of abscisic acid in ozone-induced puerarin production of Pueraria thomsnii Benth. suspension cell cultures. Plant Cell Rep 31(1):179–185

    CAS  Google Scholar 

  • Tabashnik BE (1987) Plant secondary compounds as oviposition deterrents for cabbage butterfly, Pieris rapae (Lepidoptera: Pieridae). J Chem Ecol 13(2):309–316

    CAS  Google Scholar 

  • Takshak S, Agrawal SB (2016) Ultraviolet-B radiation: a potent elicitor of phenylpropanoid pathway compounds. J Sci Res 60:79–96

    Google Scholar 

  • Tamaoki M, Nakajima N, Kubo A, Aono M, Matsuyama T, Saji H (2003) Transcriptome analysis of O3-exposed Arabidopsis reveals that multiple signal pathways act mutually antagonistically to induce gene expression. Plant Mol Biol 53(4):443–456

    CAS  Google Scholar 

  • Tanou G, Fotopoulos V, Molassiotis A (2012) Priming against environmental challenges and proteomics in plants: update and agricultural perspectives. Front Plant Sci 3:216

    Google Scholar 

  • Tattini M, Matteini P, Saracini E, Traversi ML, Giordano C, Agati G (2007) Morphology and biochemistry of non-glandular trichomes in Cistus salvifolius L. leaves growing in extreme habitats of the Mediterranean basin. Plant Biology 9(03):411–419

    CAS  Google Scholar 

  • Tiwari S, Agrawal M (2018) Tropospheric ozone and its impacts on crop plants. Springer International Publishing AG, Berlin

    Google Scholar 

  • Tonelli M, Pellegrini E, D’Angiolillo F, Petersen M, Nali C, Pistelli L, Lorenzini G (2015) Ozone-elicited secondary metabolites in shoot cultures of Melissa officinalis L. Plant Cell, Tissue and Organ Culture (PCTOC) 120(2):617–629

    CAS  Google Scholar 

  • Tosti N, Pasqualini S, Borgogni A, Ederli L, Falistocco E, Crispi S, Paolocci F (2006) Gene expression profiles of O3-treated Arabidopsis plants. Plant Cell Environ 29(9):1686–1702

    CAS  Google Scholar 

  • Treutter D (2005) Significance of flavonoids in plant resistance and enhancement of their biosynthesis. Plant biology 7(06):581–591

    CAS  Google Scholar 

  • Treutter D (2006) Significance of flavonoids in plant resistance: a review. Environ Chem Lett 4(3):147–157

    CAS  Google Scholar 

  • Trowbridge AM, Bowers MD, Monson RK (2016) Conifer monoterpene chemistry during an outbreak enhances consumption and immune response of an eruptive folivore. J Chem Ecol 42(12):1281–1292

    CAS  Google Scholar 

  • Uddling J, Hall M, Wallin G, Karlsson PE (2005) Measuring and modelling stomatal conductance and photosynthesis in mature birch in Sweden. Agric For Meteorol 132(1-2):115–131

    Google Scholar 

  • Valkama E, Koricheva J, Oksanen E (2007) Effects of elevated O3, alone and in combination with elevated CO2, on tree leaf chemistry and insect herbivore performance: a meta-analysis. Glob Chang Biol 13(1):184–201

    Google Scholar 

  • van Mölken T, Kuzina V, Munk KR, Olsen CE, Sundelin T, van Dam NM, Hauser TP (2014) Consequences of combined herbivore feeding and pathogen infection for fitness of Barbarea vulgaris plants. Oecologia 175(2):589–600

    Google Scholar 

  • Verma P, Mathur AK, Srivastava A, Mathur A (2012) Emerging trends in research on spatial and temporal organization of terpenoid indole alkaloid pathway in Catharanthus roseus: a literature update. Protoplasma 249(2):255–268

    CAS  Google Scholar 

  • Vives-Peris V, de Ollas C, Gómez-Cadenas A, Pérez-Clemente RM (2020) Root exudates: from plant to rhizosphere and beyond. Plant Cell Rep 39(1):3–17

    CAS  Google Scholar 

  • Vives-Peris V, Molina L, Segura A, Gómez-Cadenas A, Pérez-Clemente RM (2018) Root exudates from citrus plants subjected to abiotic stress conditions have a positive effect on rhizobacteria. J Plant Physiol 228:208–217

    CAS  Google Scholar 

  • Wallis C, Eyles A, Chorbadjian R, McSpadden Gardener B, Hansen R, Cipollini D, Herms DA, Bonello P (2008) Systemic induction of phloem secondary metabolism and its relationship to resistance to a canker pathogen in Austrian pine. New Phytol 177(3):767–778

    CAS  Google Scholar 

  • Wang J, Zhu J, Zeng Q, Liu G (2014) Phenolic compounds and antioxidant ability responses to experimental free-air ozone exposure in two wheat cultivars. Bull Environ Contam Toxicol 93:625–631

  • Wang P, Marsh EL, Ainsworth EA, Leakey AD, Sheflin AM, Schachtman DP (2017) Shifts in microbial communities in soil, rhizosphere and roots of two major crop systems under elevated CO2 and O3. Sci Rep 7(1):1–12

    Google Scholar 

  • Wang RL, Staehelin C, Peng SL, Wang WT, Xie XM, Lu HN (2010) Responses of Mikania micrantha, an invasive weed to elevated CO2: induction of β-caryophyllene synthase, changes in emission capability and allelopathic potential of β-caryophyllene. J Chem Ecol 36(10):1076–1082

    CAS  Google Scholar 

  • War AR, Paulraj MG, Ahmad T, Buhroo AA, Hussain B, Ignacimuthu S, Sharma HC (2012) Mechanisms of plant defense against insect herbivores. Plant Signal Behav 7(10):1306–1320

    Google Scholar 

  • Widhalm JR, Jaini R, Morgan JA, Dudareva N (2015) Rethinking how volatiles are released from plant cells. Trends Plant Sci 20(9):545–550

    CAS  Google Scholar 

  • Wink M (2018) Plant secondary metabolites modulate insect behavior-steps toward addiction? Front Physiol 9:364

    Google Scholar 

  • Wink M, Schimmer O (2010) Molecular modes of action of defensive secondary metabolites. In: Annual Plant Reviews Volume 39: Functions and Biotechnology of Plant Secondary Metabolites, vol 39, pp 21–161

    Google Scholar 

  • Xingyuan HE, Huang W, Wei CH, Tian DO, Changbing LI, Zhenju CH, Sheng XU, Yanan RU (2009) Changes of main secondary metabolites in leaves of Ginkgo biloba in response to ozone fumigation. J Environ Sci 21(2):199–203

    Google Scholar 

  • Xu C, Arancon RAD, Labidi J, Luque R (2014) Lignin depolymerisation strategies: towards valuable chemicals and fuels. Chem Soc Rev 2014(43):7485–7500

    Google Scholar 

  • Yadav DS, Rai R, Mishra AK, Chaudhary N, Mukherjee A, Agrawal SB, Agrawal M (2019) ROS production and its detoxification in early and late sown cultivars of wheat under future O3 concentration. Sci Total Environ 659:200–210

    CAS  Google Scholar 

  • Yalpani N, Enyedi AJ, León J, Raskin I (1994) Ultraviolet light and ozone stimulate accumulation of salicylic acid, pathogenesis-related proteins and virus resistance in tobacco. Planta 193(3):372–376

    CAS  Google Scholar 

  • Yamamoto K, Takahashi K, Caputi L, Mizuno H, Rodriguez‐Lopez CE, Iwasaki T, Ishizaki K, Fukaki H, Ohnishi M, Yamazaki M, Masujima T (2019) The complexity of intercellular localisation of alkaloids revealed by single-cell metabolomics. New Phytol 224(2):848–859

    CAS  Google Scholar 

  • Yan H, Guo H, Yuan E, Sun Y, Ge F (2018) Elevated CO2 and O3 alter the feeding efficiency of Acyrthosiphon pisum and Aphis craccivora via changes in foliar secondary metabolites. Sci Rep 8(1):1–13

    Google Scholar 

  • Yeshi K, Crayn D, Ritmejerytė E, Wangchuk P (2022) Plant secondary metabolites produced in response to abiotic stresses has potential application in pharmaceutical product development. Molecules 27(1):313

    CAS  Google Scholar 

  • Yu F, Luca VD (2014) Transport of monoterpenoid indole alkaloids in Catharanthus roseus. Plant ABC Transporters:63–75

  • Yuan X, Shang B, Xu Y, Xin Y, Tian Y, Feng Z, Paoletti E (2017) No significant interactions between nitrogen stimulation and ozone inhibition of isoprene emission in Cathay poplar. Sci Total Environ 601:222–229

    Google Scholar 

  • Zebelo SA, Matsui K, Ozawa R, Maffei ME (2012) Plasma membrane potential depolarization and cytosolic calcium flux are early events involved in tomato (Solanum lycopersicon) plant-to-plant communication. Plant Sci 196:93–100

    CAS  Google Scholar 

  • Zhang J, Tang H, Zhu J, Lin X, Feng Y (2019) Effects of elevated ground-level ozone on paddy soil bacterial community and assembly mechanisms across four years. Sci Total Environ 654:505–513

    CAS  Google Scholar 

  • Zhang J, Wang Y, Mao Z, Liu W, Ding L, Zhang X, Yang Y, Wu S, Chen X, Wang Y (2022) Transcription factor McWRKY71 induced by ozone stress regulates anthocyanin and proanthocyanidin biosynthesis in Malus crabapple. Ecotoxicol Environ Saf 232:113274

    CAS  Google Scholar 

  • Zhang L, Xu B, Wu T, Wen MX, Fan LX, Feng ZZ, Paoletti E (2017) Transcriptomic analysis of Pak Choi under acute ozone exposure revealed regulatory mechanism against ozone stress. BMC Plant Biol 17(1):1–15

    Google Scholar 

  • Zhang X, Zhang X, Wang T, Li C (2021) Metabolic response of soybean leaves induced by short-term exposure of ozone. Ecotoxicol Environ Saf 213:112033

    CAS  Google Scholar 

  • Zhang X, Zhang X, Zhang L, Zhang Y, Zhang D, Gu X, Zheng Y, Wang T, Li C (2020a) Metabolite profiling for model cultivars of wheat and rice under ozone pollution. Environ Exp Bot 179:104214

    CAS  Google Scholar 

  • Zhang X, Zhang X, Zhang Y, Zhang D, Gu X, Zheng Y, Zhang L, Wang T, Li C (2020b). Comparison of metabolite profiling among model cultivars of wheat, rice and soybean under elevated ozone. Authorea Preprints.

  • Zhang Z, Diao E, Shen X, Ma W, Ji N, Dong H (2014) Ozone-induced changes in phenols and antioxidant capacities of peanut skins. J Food Process Eng 37(5):506–514

    CAS  Google Scholar 

  • Zhao J, Davis LC, Verpoorte R (2005) Elicitor signal transduction leading to production of plant secondary metabolites. Biotechnol Adv 23(4):283–333

    CAS  Google Scholar 

  • Zhao T, Wang W, Tian R, Wang Y (2016) Effects of ozone stress on secondary metabolism and antioxidant capacity in soybean roots. In: International Conference on Biomedical and Biological Engineering. Atlantis Press, pp 421–427

    Google Scholar 

  • Zhu X, Skoneczny D, Weidenhamer JD, Mwendwa JM, Weston PA, Gurr GM, Callaway RM, Weston LA (2016) Identification and localization of bioactive naphthoquinones in the roots and rhizosphere of Paterson’s curse (Echium plantagineum), a noxious invader. J Exp Bot 67(12):3777–3788

    CAS  Google Scholar 

  • Zucker WV (1983) Tannins: does structure determine function? An ecological perspective. Am Nat 121(3):335–365

    CAS  Google Scholar 

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Acknowledgements

The authors are grateful to the Head of Department of Botany, and Co-ordinators, CAS in Botany, Banaras Hindu University, Varanasi, India. Aditya Abha Singh greatly acknowledges the University Grants Commission, Government of India for the financial support as UGC-BSR start-up grant no.F.30-578/2021(BSR). Aditya Abha Singh is also thankful to the Head of Department of Botany, University of Lucknow, Lucknow, India. The Council of Scientific and Industrial Research (CSIR), New Delhi is also being acknowledged for granting ‘Emeritus Scientist’ scheme to Prof. Shashi Bhushan Agrawal.

Funding

Author A has received research support from UGC-BSR start-up grant no.F.30-578/2021(BSR) and author D has received financial support from The Council of Scientific and Industrial Research (CSIR) in the form of ‘Emeritus Scientist’ Scheme.

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Aditya Abha Singh: material preparation, data collection, and writing original draft; Annesha Ghosh: material preparation, data collection, and writing original draft; Madhoolika Agrawal: writing review and editing; Shashi Bhushan Agrawal: conceptualization, writing—review and editing, and supervision. Aditya Abha Singh and Annesha Ghosh contributed to the study conception and design. All authors read and approved the final manuscript.

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Correspondence to Shashi Bhushan Agrawal.

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Singh, .A., Ghosh, A., Agrawal, M. et al. Secondary metabolites responses of plants exposed to ozone: an update. Environ Sci Pollut Res 30, 88281–88312 (2023). https://doi.org/10.1007/s11356-023-28634-2

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