Effects of Toxic Gases, Ozone, Carbon Dioxide, and Wastes on Plant Secondary Metabolism

  • Vinay Kumar
  • Tushar Khare
  • Sagar Arya
  • Varsha Shriram
  • Shabir H. Wani


Various kinds of human activities along with environmental interactions or changes are occasioning the addition and accumulation of hazardous entities in the environment. The subsequent result of this is negative effects of these factors on living systems including plants. Factors such as heavy metals, toxic gases, ozone, and carbon dioxide have a major impact on plant growth and secondary metabolism of the plants. Secondary metabolites are the key players in plant adaptation to these environmental stresses and play a role in mitigating the negative effects of these stresses. Both primary and secondary metabolisms are altered under these stress environments, however, plants have evolved to endure these conditions through inducing several regulating mechanisms such as evapotranspiration of available water, controlled openings and closings of stomata as per the availability of water, over accumulation of various osmoprotectants and osmoregulators, induction of antioxidant machinery and fine tuning of transcriptional and post-transcriptional regulations of gene expressions. In most of the plants, the ultimate result of these defensive adaptations is regulated production of the secondary metabolites. In this chapter, we have discussed the effects of toxic gases, ozone, carbon dioxide as well as other wastes including the nanoparticles-wastes on plant secondary metabolites.


Toxic gases Secondary metabolism Secondary metabolites Ozone Carbon dioxide Heavy metals Nanoparticles Wastes 



Plant Secondary Metabolites


Carbon Dioxide




Sulfur Dioxide


Hydrogen Sulfide














Naphthalene acetic acid


Non-structural Carbohydrates



The research support through the Science and Engineering Research Board (SERB), Department of Science and Technology (DST), Government of India funds (grant number SR/FT/LS-93/2011 and EMR/2016/003896) to VK’s lab is gratefully acknowledged. SHW is grateful to University Grants Commission, New Delhi India for providing Raman Post-Doctoral Fellowship.


  1. Aghajanzadeh T, Kopriva S, Hawkesford MJ, Koprivova A, De Kok LJ (2015) Atmospheric H2S and SO2 as sulfur source for Brassica juncea and Brassica rapa: impact on the glucosinolate composition. Front Plant Sci 6:924. doi: 10.3389/fpls.2015.00924CrossRefPubMedPubMedCentralGoogle Scholar
  2. Ali M, Hahn E, Paek K (2005) CO2-induced total phenolics in suspension cultures of Panax ginseng C. A. Mayer roots: role of antioxidants and enzymes. Plant Physiol Biochem 43:449–457CrossRefGoogle Scholar
  3. Bortolin R, Caregnato F et al (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 129:16–24CrossRefGoogle Scholar
  4. Cao H, Jiang Y, Chen J, Zhang H, Huang W, Li L, Zhang W (2009) Arsenic accumulation in Scutellaria baicalensis Georgi and its effects on plant growth and pharmaceutical components. J Hazard Mater 171:508–513. doi: 10.1016/j.jhazmat.2009.06.022CrossRefPubMedGoogle Scholar
  5. Chang Y, Seo E, Gyllenhaal C et al (2003) Panax ginseng: a role in cancer therapy? Integr Cancer Ther 2:13–33CrossRefGoogle Scholar
  6. Chen X, Chen Q, Zhang X, Li R, Jia Y, Ef AA, Jia A, Hu L, Hu X (2016) Hydrogen sulfide mediates nicotine biosynthesis in tobacco (Nicotiana tabacum) under high temperature conditions. Plant Physiol Biochem 104:174–179. doi: 10.1016/j.plaphy.2016.02.033CrossRefPubMedGoogle Scholar
  7. Chung CY, Chung PL, Liao SW (2011) Carbon fixation efficiency of plants influenced by sulfur dioxide. Environ Monit Assess 173:701–707CrossRefGoogle Scholar
  8. Ezuruike U, Prieto JM (2014) The use of plants in the traditional management of diabetes in Nigeria: pharmacological and toxicological considerations. J Ethnopharmacol 155:857–924CrossRefGoogle Scholar
  9. Falk KL, Tokuhisa JG, Gershenzon J (2007) The effect of sulfur nutrition on plant glucosinolate content: physiology and molecular mechanisms. Plant Biol 9:573–581. doi: 10.1055/s-2007-965431CrossRefPubMedPubMedCentralGoogle Scholar
  10. Fazal H, Abbasi BH, Ahmad N, Ali M (2016) Elicitation of medicinally important antioxidant secondary metabolites with silver and gold nanoparticles in Callus cultures of Prunella vulgaris L. Appl Biochem Biotechnol 180:1076–1092. doi: 10.1007/s12010-016-2153-1CrossRefPubMedGoogle Scholar
  11. Garcia-Sanchez S, Bernales I, Cristobal S (2015) Early response to nanoparticles in the Arabidopsis transcriptome compromises plant defence and root-hair development through salicylic acid signalling. BMC Genom 16:341. doi: 10.1186/s12864-015-1530-4CrossRefGoogle Scholar
  12. Ghasemzadeh A, Jaafar HZ (2011) Effect of CO2 enrichment on synthesis of some primary and secondary metabolites in ginger (Zingiber officinale Roscoe). Int J Mol Sci 12:1101–1114Google Scholar
  13. Ghasemzadeh A, Jaafar H, Rahmat A (2010) Elevated carbon dioxide increases contents of flavonoids and phenolic compounds, and antioxidant activities in Malaysian young ginger (Zingiber officinale Roscoe.) varieties. Molecules 15(7907):7922Google Scholar
  14. Giraud E, Ivanova A, Gordon CS, Whelan J, Considine MJ (2012) Sulphur dioxide evokes a large scale reprogramming of the grape berry transcriptome associated with oxidative signaling and biotic defense responses. Plant, Cell Environ 35:405–417. doi: 10.1111/j.1365-3040.2011.02379.xCrossRefGoogle Scholar
  15. Gosal SS, Wani SH, Kang MS (2009) Biotechnology and drought tolerance. J Crop Improv 23(1):19–54CrossRefGoogle Scholar
  16. Haworth M, Elliott-Kingston C, Gallagher A, Fitzgerald A, McElwain JC (2012) Sulphur dioxide fumigation effects on stomatal density and index of non-resistant plants: implications for the stomatal palaeo-[CO2] proxy method. Rev Palaeobot Palynol 182:44–54Google Scholar
  17. He XY, Huang W, Chen W, Dong T, Liu CB, Chen ZJ, Xu S, Ruan YN (2009) Changes of main secondary metabolites in leaves of Ginkgo biloba in response to ozone fumigation. J Environ Sci 21:199–203CrossRefGoogle Scholar
  18. Heyworth C, Iason G, Temperton V (1998) The effect of elevated CO2 concentration and nutrient supply on carbon-based plant secondary metabolites in Pinus sylvestris L. Oncologia 115:344–350Google Scholar
  19. Huang W, He X, Liu C et al (2010) Effects of elevated carbon dioxide and ozone on foliar flavonoids of Ginkgo biloba. Adv Mat Res 113:165–169Google Scholar
  20. Ibrahim M, Jaafar H (2012) Impact of elevated carbon dioxide on primary, secondary metabolites and antioxidant responses of Eleais guineensis Jacq. (Oil Palm) seedlings. Molecules 17:5195–5211. doi: 10.3390/molecules17055195CrossRefPubMedGoogle Scholar
  21. Ibrahim M, Jaafar H, Karimi E et al (2014) Allocation of secondary metabolites, photosynthetic capacity, and antioxidant activity of Kacip Fatimah (Labisia pumila Benth) in response to CO2 and light intensity. Sci World J. doi: 10.1155/2014/360290CrossRefGoogle Scholar
  22. Idso S, Kimball B, Pettit G et al (2000) Effects of atmospheric CO2 enrichment on the growth and development of Hymenocallis littoralis (amaryllidaceae) and the concentrations of several antineoplastic and antiviral constituents of its bulbs. Am J Bot 87(6):769–773CrossRefGoogle Scholar
  23. IPCC (2014) Summary for policymakers: synthesis report. Available from
  24. Jasim B, Thomas R, Mathew J, Radhakrishnan EK (2017) Plant growth and diosgenin enhancement effect of silver nanoparticles in Fenugreek (Trigonella foenum-graecum L.). Saudi Pharm J 25:443–447. doi: 10.1016/j.jsps.2016.09.012CrossRefPubMedGoogle Scholar
  25. Jordan D, Green T, Chappelka A (1991) Response of total tannins and phenolics on Loblolly pine foliage exposed to ozone and acid rain. J Chem Ecol 17:505–513CrossRefGoogle Scholar
  26. Khare T, Kumar V, Kavi Kishor PB (2015) Na+ and Cl ions show additive effects under NaCl stress on induction of oxidative stress and the responsive antioxidative defense in rice. Protoplasma 252:1149–1165. doi: 10.1007/s00709-014-0749-2CrossRefPubMedGoogle Scholar
  27. Kováčik J, Grúz J, Bačkor M, Tomko J, Strnad M, Repčák M (2008) Phenolic compounds composition and physiological attributes of Matricaria chamomilla grown in copper excess. Environ Exp Bot 62:145–152. doi: 10.1016/j.envexpbot.2007.07.012CrossRefGoogle Scholar
  28. Kumar V, Khare T (2015) Individual and additive effects of Na+ and Cl ions on rice under salinity stress. Arch Agron Soil Sci 61:381–395. doi: 10.1080/03650340.2014.936400CrossRefGoogle Scholar
  29. Kumar V, Khare T (2016) Differential growth and yield responses of salt-tolerant and susceptible rice cultivars to individual (Na+ and Cl) and additive stress effects of NaCl. Acta Physiol Plant 38(7):170. doi: 10.1007/s11738-016-2191-xCrossRefGoogle Scholar
  30. Kumar V, Shriram V, Kavi Kishor PB, Jawali N, Shitole MG (2010) Enhanced proline accumulation and salt stress tolerance of transgenic indica rice by over expressing P5CSF129A gene. Plant Biotechnol Rep 4(1):37–48. doi: 10.1007/S11816-009-0118-3CrossRefGoogle Scholar
  31. Lavola A, Julkunen-Tiitto R, Pakkonen E (1994) Does ozone stress change the primary or secondary metabolites of Birch (Betula pendul Roth.)? New Phytol 126:637–642CrossRefGoogle Scholar
  32. Mahn A, Reyes A (2012) An overview of health-promoting compounds of broccoli (Brassica oleracea var. italica) and the effect of processing. Food Sci Technol Int 18:503–514CrossRefGoogle Scholar
  33. Mapara N, Sharma M, Shriram V, Bharadwaj R, Mohite KC, Kumar V (2015) Antimicrobial potentials of Helicteres isora silver nanoparticles against extensively drug resistant (XDR) clinical isolates of Pseudomonas aeruginosa. Appl Microbiol Biotechnol 99:10655–10667. doi: 10.1007/s00253-015-6938-xCrossRefPubMedGoogle Scholar
  34. Marslin G, Sheeba CJ, Franklin G (2017) Nanoparticles alter secondary metabolism in plants via ROS burst. Front Plant Sci 8:832. doi: 10.3389/fpls.2017.00832CrossRefPubMedPubMedCentralGoogle Scholar
  35. Mishra T (2016) Climate change and production of secondary metabolites in medicinal plants: a review. Int J Herb Med 4:27–30Google Scholar
  36. Montesinos-Pereira D, Barrameda-Medina Y, Baenas N, Moreno DA, Sanchez-Rodriguez E, Blasco B, Ruiz JM (2016) Evaluation of hydrogen sulfide supply to biostimulate the nutritive and phytochemical quality and the antioxidant capacity of Cabbage (Brassica oleracea L.‘Bronco’). J Appl Bot Food Qual 89. doi: 10.5073/JABFQ.2016.089.038
  37. Mosaleeyanon K, Zobayed SMA, Afreen F, Kozai T (2005) Relationships between net photosynthetic rate and secondary metabolite contents in St. John’s wort. Plant Sci 169:523–531Google Scholar
  38. Murch SJ, Saxena PK (2002) Mammalian neurohormones: potential significance in reproductive physiology of St. John’s wort (Hypericum perforatum L.)? Naturwissenschaften 89:555–560Google Scholar
  39. Nasim SA, Dhir B (2010) Heavy Metals alter the potency of medicinal plants, In: Whitacre DM (ed) Reviews of environmental contamination and toxicology, reviews of environmental contamination and toxicology 203, doi: 10.1007/978-1-4419-1352-4_5
  40. Pellegrini E, Carucci G, Campanella A et al (2011) Ozone stress in Melissa officinalis plants assessed by photosynthetic function. Environ Exp Bot 73:94–101CrossRefGoogle Scholar
  41. Pellegrini E, Francini A, Lorenzini G et al (2015) Ecophysiological and antioxidant traits of Salvia officinalis under ozone stress. Environ Sci Pollu Res 22:13083–13093CrossRefGoogle Scholar
  42. Rahimtoola S (2004) Digitalis therapy for patients in clinical heart failure. Circulation 109:2942–2946. doi: 10.1161/01.CIR.0000132477.32438.03CrossRefPubMedGoogle Scholar
  43. Rai V, Khatoon S, Bisht SS, Mehrotra S (2005) Effect of cadmium on growth, ultramorphology of leaf and secondary metabolites of Phyllanthus amarus Schum. and Thonn. Chemosphere 61:1644–1650. doi: 10.1016/j.chemosphere.2005.04.052CrossRefPubMedPubMedCentralGoogle Scholar
  44. Rai V, Mehrotra S (2008) Chromium-induced changes in ultramorphology and secondary metabolites of Phyllanthus amarus Schum & Thonn.—an hepatoprotective plant. Environ Monit Assess 147:307–315. doi: 10.1007/s10661-007-0122-4CrossRefPubMedGoogle Scholar
  45. Rai V, Vaypayee P, Singh SN, Mehrotra S (2004) Effect of chromium accumulation on photosynthetic pigments, oxidative stress defense system, nitrate reduction, proline level and eugenol content of Ocimum tenuiflorum L. Plant Sci 167:1159–1169. doi: 10.1016/j.plantsci.2004.06.016CrossRefGoogle Scholar
  46. 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 27:1049–1062Google Scholar
  47. Sanghera GS, Wani SH, Hussain W, Singh NB (2011) Engineering cold stress tolerance in crop plants. Curr Genomics 12(1):30CrossRefGoogle Scholar
  48. Saravanan S, Karthi S (2014) effect of elevated CO2 on growth and biochemical changes in Catharanthus roseus—an valuable medicinal herb. World J Pharm Pharmaceuti Sci 3:411–422Google Scholar
  49. Schonhof I, Klaring H, Krumbein A et al (2007) Interaction between atmospheric CO2 and Glucosinolates in Broccoli. J Chem Ecol 33:105–114. Doi: 10.1007/s10886-006-9202-0CrossRefGoogle Scholar
  50. Shakeri A, Sahebkar A, Javadi B (2016) Melissa officinalis L.—a review of its traditional uses, phytochemistry and pharmacology. J Ethnopharmacol. doi: 10.1016/j.jep.2016.05.010
  51. Shriram V, Kumar V, Devarumath RM, Khare T, Wani SH (2016) MicroRNAs as potent targets for abiotic stress tolerance in plants. Front Plant Sci 7:817. doi: 10.3389/fpls.2016.00817CrossRefPubMedPubMedCentralGoogle Scholar
  52. Silva LC, Araujo TO, Martinez CA, Lobo F, Azevedo AA, Oliva MA (2015) Differential responses of C3 and CAM native Brazilian plant species to a SO2− and SPMFe− contaminated Restinga. Environ Sci Pollut Res Int 22:140007–140017. doi: 10.1007/s11356-015-4391-0CrossRefGoogle Scholar
  53. Singh A, Agrawal M (2015) Effects of ambient and elevated CO2 on growth, chlorophyll fluorescence, photosynthetic pigments, antioxidants, and secondary metabolites of Catharanthus roseus (L.) G Don. grown under three different soil N levels. Environ Sci Pollut Res 22:3936–3946CrossRefGoogle Scholar
  54. Snow M, Bard R, Olszyk D et al (2003) Monoterpenes levels in needles of Douglas fir exposed to elevated CO2 and temperature. Physiol Plant 117:352–358CrossRefGoogle Scholar
  55. Stiling P, Cornelissen T (2007) How does elevated carbon dioxide (CO2) affect plant–herbivore interactions? a field experiment and meta-analysis of CO2− mediated changes on plant chemistry and herbivore performance. Glob Change Biol 13:1823–1842. doi: 10.1111/j.1365-2486.2007.01392.xCrossRefGoogle Scholar
  56. Stuhlfauth T, Fock H (1990) Effect of whole season CO2 enrichment on the cultivation of a medicinal plant, Digitalis lanata. J Agro Crop Sci 164: 168–173CrossRefGoogle Scholar
  57. Stuhlfauth T, Klug K, Fock H (1987) The production of secondary metabolites by Digitalis lanata during CO2 enrichment and water stress. Phytochemistry 26(10):2735–2739CrossRefGoogle Scholar
  58. Sun L, Su H, Zhu Y et al (2012) Involvement of abscisic acid in ozone-induced puerarin production of Pueraria thomsnii Benth. suspension cell cultures. Plant Cell Rep 31:179–185CrossRefGoogle Scholar
  59. Swanepoel JW, Kruger GHJ, Van Heerden PDR (2007) Effects of sulphur dioxide on photosynthesis in the succulent Augea capensis Thunb. J Arid Environ 70:208–221CrossRefGoogle Scholar
  60. 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 Organ Cult 120:617–629CrossRefGoogle Scholar
  61. Wang W, Zhao Y, Rayburn E et al (2007) In vitro anti-cancer activity and structure–activity relationships of natural products isolated from fruits of Panax ginseng. Cancer Chemother Pharmacol 59:589–601. doi: 10.1007/s00280-006-0300-zCrossRefPubMedGoogle Scholar
  62. Wani SH, Hossain MA (eds) (2015) Managing salt tolerance in plants: molecular and genomic perspectives. CRC Press, USAGoogle Scholar
  63. Wani SH, Sofi PA, Gosal SS, Singh NB (2010) In vitro screening of rice (Oryza sativa L) callus for drought tolerance. Commun Biometry Crop Sci 5(2):108–115Google Scholar
  64. Wani SH, Gosal SS (2011) Introduction of OsglyII gene into Oryza sativa for increasing salinity tolerance. Biol Plant 55(3):536–540CrossRefGoogle Scholar
  65. Wani SH, Singh NB, Haribhushan A, Mir JI (2013) Compatible solute engineering in plants for abiotic stress tolerance—role of Glycine Betaine. Curr Genomics 14(3):157–165CrossRefGoogle Scholar
  66. Wani SH, Gosal SS (2010) Genetic engineering for osmotic stress tolerance in plants–role of Proline. IUP J Genet Evol 3(4):14–25 Google Scholar
  67. Wani SH, Kumar V (2015) Plant stress tolerance: engineering ABA: a potent Phytohormone. Transcriptomics 3(2):1000113. doi: 10.4172/2329-8936.1000113CrossRefGoogle Scholar
  68. Wani SH, Kumar V, Shriram V, Sah SK (2016a) Phytohormones and their metabolic engineering for abiotic stress tolerance in crop plants. Crop J 4(3):162–176. doi: 10.1016/j.cj.2016.01.010
  69. Wani SH, Sah SK, Khare T, Shriram V, Kumar V (2016b) Engineering Phytohormones for abiotic stress tolerance in crop plants. In: Ahammed GJ, Yu J (eds) Plant hormones under challenging environmental factors. Springer Science+Business Media, Dordrecht. doi: 10.1007/978-94-0177758-2_10
  70. Wani SH, Dutta T, Neelapu NRR, Surekha C (2017) Transgenic approaches to enhance salt and drought tolerance in plants. Plant Gene. doi: 10.1016/j.plgene.2017.05.006CrossRefGoogle Scholar
  71. Weinmann S, Roll S, Schwarzbach C et al (2010) Effects of Ginkgo biloba in dementia: systematic review and meta-analysis. BMC Geriatrics 10:14. doi: 10.1186/1471-2318-10-14CrossRefPubMedPubMedCentralGoogle Scholar
  72. Xu M, Yang B, Dong J et al (2011) Enhancing hypericin production of Hypericum perforatum cell suspension culture by ozone exposure. Biotechnol Prog 27(4):1101–1106CrossRefGoogle Scholar
  73. Zhang B, Zheng LP, Yi Li W, Wen Wang J (2013) Stimulation of artemisinin production in Artemisia annua hairy roots by Ag–SiO2 core-shell nanoparticles. Curr Nanosci 9:363–370. doi: 10.2174/157341371130903001CrossRefGoogle Scholar
  74. Zhang H, Tan ZQ, Hu LY, Wang SH, Luo JP, Jones RL (2010) Hydrogen sulfide alleviates aluminum toxicity in germinating wheat seedlings. J Integr Plant Biol 52:556–567CrossRefGoogle Scholar
  75. Zhou L, Yang G, Sun H, Tang J, Yang J, Wang Y, Garran TA, Guo L (2016) Effects of different doses of cadmium on secondary metabolites and gene expression in Artemisia annua L. Front Med. doi: 10.1007/s11684-016-0486-3CrossRefPubMedGoogle Scholar
  76. Ziska L, Panicker S, Wojno H (2008) Recent and projected increases in atmospheric carbon dioxide and the potential impacts on growth and alkaloid production in wild poppy (Papaver setigerum DC.). Clim Change 91:395–403. doi: 10.1007/s10584-008-9418-9CrossRefGoogle Scholar
  77. Zobayed S, Saxena P (2004) Production of St. John’s wort plants under controlled environment for maximizing biomass and secondary metabolites. In Vitro Cell Dev Biol Plant 40:108–114CrossRefGoogle Scholar

Copyright information

© Springer International Publishing AG 2017

Authors and Affiliations

  1. 1.Department of BiotechnologyModern College (Savitribai Phule Pune University)PuneIndia
  2. 2.Department of Environmental SciencesSavitribai Phule Pune UniversityPuneIndia
  3. 3.Department of BotanyProf. Ramkrishna More College (Savitribai Phule Pune University)PuneIndia
  4. 4.Mountain Research Centre For Field CropsAnantnagIndia
  5. 5.Sher-e-Kashmir University of Agricultural Sciences and Technology of KashmirSrinagarIndia

Personalised recommendations