Secondary Metabolite Production in Plants: History
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Zubair Altaf Reshi
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Waquar Ahmad
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Alexander S. Lukatkin
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Saad Bin Javed

Plants, being sessile organisms, face potential threats from environmental or pathogenic stressors. These stresses can lead to osmotic imbalances, physiological and biochemical changes, and cellular dehydration, ultimately resulting in the death of the affected plant. To defend themselves, plants have evolved three different response mechanisms. Ephemeral desert plants respond by avoiding stress by regulating their life cycle, as the fragile plants lack effective mechanisms to survive stress, while resistant plants respond with efficient defensive mechanisms to counter various stresses. This defensive system is modulated by plants through alterations and modifications in membrane structure, cell cycle and division remodelling, changes in photosynthetic activity, conductance, and transpiration rates, which collectively affect growth, metabolic activity, and the physiology of metabolic compounds.

  • plant tissue culture
  • environmental stress
  • defence action
  • industrial use
  • sustainable production

1. Salt Stress

Salt stress exerts a negative impact on plant growth and productivity [1]. Plants respond to salt stress by undergoing changes in their metabolic activity to counteract the toxicity induced by excessive salt levels [1]. Salinity often causes osmotic imbalance and ionic toxicity in plants, leading to membrane disruption and cellular dehydration in the cytoplasm [2]. These changes in ionic and osmotic components can result in either an increase or decrease in the accumulation of plant secondary metabolites. In vitro studies have revealed a decline in anthocyanin accumulation in salt-sensitive species [3], while the decrease in phenolic, anthocyanin, and flavonoid content under salt stress conditions was less pronounced in salt-tolerant clones [4]. Proline, which regulates stress signals and serves as an osmotic buffer, energy sink, and protector of membranes and proteins, shows increased accumulation in the roots of Alfalfa under salt stress [5]. Various studies have observed the accumulation of polyphenols and flavonoids under salinity stress in plants like Hordeum vulgare and Cakile maritma [6][7]. Transcription factors GmCAM4 and GmERFo57 play crucial roles in providing resistance to salinity stress in Glycine max [8]. Spinacia oleracea demonstrates resistance against saline soil by enhancing the production of 20-Hydroxyecdysone (20E) [9]. Furthermore, alkaloids such as vincristine and reserpine in Catharanthus roseus and Rauvolfia tetraphylla, respectively, increase under saline conditions [10].

2. Drought Stress

Drought severely impacts plants’ biochemical and physiological processes, causing disruptions in the electron transport chain and leading to the production of reactive oxygen species (ROS) like H2O2, OH−, and O2−. These ROS inflict oxidative damage on lipids, nucleic acids, and proteins, and also disrupt the photosynthetic mechanism of plants. Drought severity varies among plant species and is often accompanied by increased solar radiation and temperature [11]. The stress disturbs plant metabolism, reduces cell turgidity and signalling, and impairs energy storage, plasma membrane structure, and resource allocation [12].
To cope with drought stress, plants have developed response mechanisms that involve the accumulation of secondary metabolites such as phenolics, terpenes, and alkaloids. These secondary metabolites help regulate ionic balance and enzyme activity, repair oxidative damage, and maintain the connection between the phenotype and genotype of plants [13][14]. However, increased production of these metabolites can lead to reduced biomass in some plant species [15]. For instance, under drought stress, plants like Artemisia annua and Catharanthus roseus increase secondary metabolite production by several times [16]. Drought stress induces elevated expression of PAL genes, responsible for flavonoid synthesis, in roots of Scutellaria baicalensis [17]. In Chenopodium quinoa, the accumulation of saponin changes under different drought stress conditions [18]. Drought stress also affects the carotenoid and chlorophyll ratio in plants. Notably, Bellis perennis and Ophiorrhiza mungos show enhanced production of camptothecin, alkaloids, and phenolic compounds, respectively, under drought conditions [19][20].
Drought stress has varying effects on the concentrations of secondary metabolites in the roots and leaves of Bupleurum chinensis plants. For example, saikosaponin concentrations in the roots increase during vegetative and reproductive growth, while leaf rutin concentrations decrease significantly during these stages [21].
These studies underscore the intricate interplay between abiotic stresses and plant physiological responses, leading to diverse responses of secondary metabolites against drought stress.

3. Temperature Stress

Elevated temperatures lead to reduced development and early leaf senescence in plants. The impact of temperature on the production of secondary metabolites varies among different plant species [22][23]. Heat treatments can cause enzyme inactivation, and lipid and protein denaturation negatively affect membrane integrity. Under temperature stress, carotenoid and β-carotene accumulation in Brassicaceae are reduced [22]. Acidic pH combined with a high temperature in hairy root culture promotes the accumulation of flavonolignans in Silybum marianum [24]. Some plants, like Melastoma malabathricum, show increased anthocyanin and biomass production at lower temperatures compared to higher temperatures [25]. Daucus carota responds to heat shock by increasing terpene accumulation, while the production levels of α-terpinolene decrease at the same temperature. Short-term temperature treatment enhances isoprene production synthesized through the nonmevalonate pathway (MEP), which is believed to counteract the negative effects of heat shock [26][27]. Different temperature ranges can significantly affect the level of secondary metabolites in plants, as observed in Amaranthus cruentus [28]. Salicylic acid and phenolic content in flowering plants [29] and phenolic compounds in gymnosperms [30] were found to decrease with increasing temperature. In tea plants, the concentration of catechin levels increases when treated with higher temperatures [31].

4. Light, UV, and Ionization Radiation

Light plays a critical role in plant metabolism and the production of secondary metabolites. Stable light intensity regulates photosynthesis and dry matter accumulation. However, abnormal irradiation can lead to photodamage and negatively affect photosynthetic reaction centres, causing photoinhibition, which limits plant survival, growth, and development [32]. The production and accumulation of secondary metabolites from various precursor elements depend on light intensity and the lengths of the photoperiod [33][34]. Different plant species respond differently to the quality, intensity, and length of photoperiod (day length) [35]. Appropriate light intensity regulates the accumulation and quality of flavonoids, alkaloids, spermine, and hexadecanoic acid [34][36]. For example, Melastoma malabathricum cell cultures exposed to different light intensities and full irradiance or complete darkness showed varying anthocyanin yield and biomass accumulation [25]. In vitro cultured seedlings of Hyptid marrubiodes exhibited increased production of flavonoids in red light, while rutin accumulation increased in white and blue light [37]. UV light treatment generally has a positive effect on the synthesis of secondary metabolites; however, at higher irradiation doses of UV-C and UV-B, some plants may react with decreased growth, abnormal metabolic activity, and photosynthesis [38].
Exposure of Asparagus officinalis to UV-B results in higher activity of peroxidase and phenylalanine ammonia-lyase, which ultimately enhances the accumulation of quercetin-4′-O-monoglucoside [39]. In Catharanthus roseus, UV-B light exposure significantly influences the production of vinblastine and vincristine, both used in treating leukemia and lymphoma [40]. Moreover, a combination of UV light (280–320 nm) with red light stimulates anthocyanin production in Malus domestica [41], while UV irradiation on Fagopyrum esculentum increases the content of quercetin [42]. Several studies have shown that UV light treatment is associated with increased phenolic compounds and ROS scavenging systems [43].
Additionally, the duration of light exposure plays a role in affecting secondary metabolite concentration. For example, light intensity and wavelength had a considerable effect on the accumulation of secondary metabolites in the leaves of Flourensia cernua [44]. Similarly, Ipomea batatus demonstrated differential effects on the concentration of phenolic compounds and flavonoids with enhanced levels observed upon exposure to longer light duration [45]. In green algae, Dunaliella baradawil, the accumulation of indoleamines like melatonin and serotonin increased under different photoperiod treatments [46].

5. Heavy Metal Stress

Plants respond differently to metal toxicity, resulting in variations in the accumulation and production of secondary metabolites due to the differential mobility of heavy metals that alter plant components, leading to reduced biosynthesis of plant defence compounds [47]. The adaptation and tolerance of plants against heavy metal stress are associated with the signalling molecules responsible for the synthesis and accumulation of secondary metabolites [48]. For example, Hypericum perforatum showed decreased accumulation of hypericin and pseudohypericin when exposed to nickel stress [49]. Nickel can either increase or inhibit the synthesis and accumulation of anthocyanin content in different plant species [50][51]. Brassica juncea treated with Fe, Mn, and Cr showed increased plant oil content [52]. Toxicity under high copper chloride (CuCl2) conditions activates the defence mechanism in Viburnum ichangense, leading to the accumulation and biosynthesis of ichangoside and phenolic diglycoside [53]. Salix purpurea exhibits an increased accumulation of phenolic compounds and salicylic acid under Cu- and Ni-stress conditions [54].

This entry is adapted from the peer-reviewed paper 10.3390/metabo13080895

References

  1. Zhao, S.; Zhang, Q.; Liu, M.; Zhou, H.; Ma, C.; Wang, P. Regulation of Plant Responses to Salt Stress. Int. J. Mol. Sci. 2021, 22, 4609.
  2. Haider, M.Z.; Ashraf, M.A.; Rasheed, R.; Hussain, I.; Riaz, M.; Qureshi, F.F.; Hafeez, A. Impact of Salinity Stress on Medicinal Plants. In Medicinal Plants: Their Response to Abiotic Stress; Springer: Singapore, 2023; pp. 199–239.
  3. Daneshmand, F.; Arvin, M.J.; Kalantari, K.M. Physiological Responses to NaCl Stress in Three Wild Species of Potato in Vitro. Acta Physiol. Plant. 2010, 32, 91–101.
  4. Parmar, R.D.; Mali, S.C.; Patel, A.I.; Patel, P.K. In Vitro Response of Promising Sugarcane Varieties for Salinity Tolerance through Callus Culture. Int. J. Chem. Stud. 2017, 5, 1180–1186.
  5. Alagoz, S.M.; Lajayer, B.A.; Ghorbanpour, M. Proline and Soluble Carbohydrates Biosynthesis and Their Roles in Plants under Abiotic Stresses. In Plant Stress Mitigators; Academic Press: Cambridge, MA, USA, 2023; pp. 169–185.
  6. Ali, R.M.; Abbas, H.M. Response of Salt Stressed Barley Seedlings to Phenylurea. Plant Soil Environ. 2003, 49, 158–162.
  7. Ksouri, R.; Megdiche, W.; Debez, A.; Falleh, H.; Grignon, C.; Abdelly, C. Salinity Effects on Polyphenol Content and Antioxidant Activities in Leaves of the Halophyte Cakile maritima. Plant Physiol. Biochem. 2007, 45, 244–249.
  8. Rao, S.S.; El-Habbak, M.H.; Havens, W.M.; Singh, A.; Zheng, D.; Vaughn, L.; Haudenshield, J.S.; Hartman, G.L.; Korban, S.S.; Ghabrial, S.A. Overexpression of GmCaM4 in Soybean Enhances Resistance to Pathogens and Tolerance to Salt Stress. Mol. Plant Pathol. 2014, 15, 145–160.
  9. Muchate, N.S.; Rajurkar, N.S.; Suprasanna, P.; Nikam, T.D. Evaluation of Spinacia oleracea (L.) for Phytodesalination and Augmented Production of Bioactive Metabolite, 20-Hydroxyecdysone. Int. J. Phytoremediation 2018, 20, 981–994.
  10. Ahl, S.A.; Omer, E.A. Medicinal and Aromatic Plants Production under Salt Stress. A Review. Herba Pol. 2011, 57, 2.
  11. Marchin, R.M.; Backes, D.; Ossola, A.; Leishman, M.R.; Tjoelker, M.G.; Ellsworth, D.S. Extreme heat increases stomatal conductance and drought-induced mortality risk in vulnerable plant species. Glob. Chang. Biol. 2022, 28, 1133–1146.
  12. Obata, T.; Fernie, A.R. The Use of Metabolomics to Dissect Plant Responses to Abiotic Stresses. Cell. Mol. Life Sci. 2012, 69, 3225–3243.
  13. Salvi, P.; Manna, M.; Kaur, H.; Thakur, T.; Gandass, N.; Bhatt, D.; Muthamilarasan, M. Phytohormone signaling and crosstalk in regulating drought stress response in plants. Plant Cell Rep. 2021, 40, 1305–1329.
  14. Suhre, K.; Gieger, C. Genetic Variation in Metabolic Phenotypes: Study Designs and Applications. Nat. Rev. Genet. 2012, 13, 759–769.
  15. Isah, T. Stress and Defense Responses in Plant Secondary Metabolites Production. Biol. Res. 2019, 52, 39.
  16. Katz, L.; Baltz, R.H. Natural Product Discovery: Past, Present, and Future. J. Ind. Microbiol. Biotechnol. 2016, 43, 155–176.
  17. Yuan, Y.; Liu, Y.; Wu, C.; Chen, S.; Wang, Z.; Yang, Z.; Qin, S.; Huang, L. Water Deficit Affected Flavonoid Accumulation by Regulating Hormone Metabolism in Scutellaria baicalensis Georgi Roots. PLoS ONE 2012, 7, e42946.
  18. Solíz-Guerrero, J.B.; De Rodriguez, D.J.; Rodríguez-García, R.; Angulo-Sánchez, J.L.; Méndez-Padilla, G. Quinoa Saponins: Concentration and Composition Analysis. In Trends New Crop. New Uses; Janick, J., Whipkey, A., Eds.; ASHS Press: Alexandria, VA, USA, 2002; pp. 110–114.
  19. Cingöz, G.; Pehlivan Karakaş, F. The Effects of Nutrient and Macronutrient Stress on Certain Secondary Metabolite Accumulations and Redox Regulation in Callus Cultures of Bellis perennis L. Turk. J. Biol. 2016, 40, 1328–1335.
  20. Deepthi, S.; Satheeshkumar, K. Effects of Major Nutrients, Growth Regulators and Inoculum Size on Enhanced Growth and Camptothecin Production in Adventitious Root Cultures of Ophiorrhiza mungos L. Biochem. Eng. J. 2017, 117, 198–209.
  21. Yang, L.-L.; Yang, L.; Yang, X.; Zhang, T.; Lan, Y.-M.; Zhao, Y.; Han, M.; Yang, L.-M. Drought Stress Induces Biosynthesis of Flavonoids in Leaves and Saikosaponins in Roots of Bupleurum chinense DC. Phytochemistry 2020, 177, 112434.
  22. Li, Y.; Kong, D.; Fu, Y.; Sussman, M.R.; Wu, H. The effect of developmental and environmental factors on secondary metabolites in medicinal plants. Plant Physiol. Biochem. 2020, 148, 80–89.
  23. Jamloki, A.; Bhattacharyya, M.; Nautiyal, M.C.; Patni, B. Elucidating the relevance of high temperature and elevated CO2 in plant secondary metabolites (PSMs) production. Heliyon 2021, 7, e07975.
  24. Rahimi, S.; Hasanloo, T. The Effect of Temperature and pH on Biomass and Bioactive Compounds Production in Silybum marianum Hairy Root Cultures. Res. J. Pharmacogn. 2016, 3, 53–59.
  25. Chan, L.K.; Koay, S.S.; Boey, P.L.; Bhatt, A. Effects of Abiotic Stress on Biomass and Anthocyanin Production in Cell Cultures of Melastoma malabathricum. Biol. Res. 2010, 43, 127–135.
  26. Okereke, C.N.; Kaurilind, E.; Liu, B.; Kanagendran, A.; Pazouki, L.; Niinemets, Ü. Impact of heat stress of varying severity on papaya (Carica papaya) leaves: Major changes in stress volatile signatures, but surprisingly small enhancements of total emissions. Environ. Exp. Bot. 2022, 195, 104777.
  27. Singsaas, E.L. Terpenes and the Thermotolerance of Photosynthesis. New Phytol. 2000, 146, 1–2.
  28. Cawood, M.E.; Allemann, I.; Allemann, J. Impact of Temperature Stress on Secondary Metabolite Profile and Phytotoxicity of Amaranthus cruentus L. Leaf Extracts. Acta Agric. Slov. 2018, 111, 609–620.
  29. Sivadasan, U.; Chenhao, C.; Nissinen, K.; Randriamanana, T.; Nybakken, L.; Julkunen-Tiitto, R. Growth and Defence of Aspen (Populus tremula) after Three Seasons under Elevated Temperature and Ultraviolet-B Radiation. Can. J. For. Res. 2018, 48, 629–641.
  30. Zhang, Y.; Virjamo, V.; Du, W.; Yin, Y.; Nissinen, K.; Nybakken, L.; Guo, H.; Julkunen-Tiitto, R. Effects of Soil Pyrene Contamination on Growth and Phenolics in Norway Spruce (Picea abies) Are Modified by Elevated Temperature and CO2. Environ. Sci. Pollut. Res. 2018, 25, 12788–12799.
  31. Yao, L.; Caffin, N.; D’Arcy, B.; Jiang, Y.; Shi, J.; Singanusong, R.; Liu, X.; Datta, N.; Kakuda, Y.; Xu, Y. Seasonal Variations of Phenolic Compounds in Australia-Grown Tea (Camellia sinensis). J. Agric. Food Chem. 2005, 53, 6477–6483.
  32. Szymańska, R.; Ślesak, I.; Orzechowska, A.; Kruk, J. Physiological and Biochemical Responses to High Light and Temperature Stress in Plants. Environ. Exp. Bot. 2017, 139, 165–177.
  33. Verma, N.; Shukla, S. Impact of Various Factors Responsible for Fluctuation in Plant Secondary Metabolites. J. Appl. Res. Med. Aromat. Plants 2015, 2, 105–113.
  34. Kong, D.X.; Li, Y.Q.; Wang, M.L.; Bai, M.; Zou, R.; Tang, H.; Wu, H. Effects of Light Intensity on Leaf Photosynthetic Characteristics, Chloroplast Structure, and Alkaloid Content of Mahonia bodinieri (Gagnep.) Laferr. Acta Physiol. Plant. 2016, 38, 120.
  35. Givnish, T.J. Adaptation to Sun and Shade: A Whole-Plant Perspective. Aust. J. Plant Physiol. 1988, 15, 63–92.
  36. Li, Y.; Kong, D.; Liang, H.L.; Wu, H. Alkaloid Content and Essential Oil Composition of Mahonia breviracema Cultivated under Different Light Environments. J. Appl. Bot. Food Qual. 2018, 91, 171–179.
  37. Pedroso, R.C.N.; Branquinho, N.A.A.; Hara, A.C.B.A.M.; Costa, A.C.; Silva, F.G.; Pimenta, L.P.; Silva, M.L.A.; Cunha, W.R.; Pauletti, P.M.; Januario, A.H. Impact of Light Quality on Flavonoid Production and Growth of Hyptis marrubioides Seedlings Cultivated in Vitro. Rev. Bras. Farmacogn. 2017, 27, 466–470.
  38. Katerova, Z.; Todorova, D.; Sergiev, I. Plant Secondary Metabolites and Some Plant Growth Regulators Elicited by UV Irradiation, Light and/or Shade. In Medicinal Plants and Environmental Challenges; Springer: Berlin/Heidelberg, Germany, 2017; pp. 97–121.
  39. Eichholz, I.; Rohn, S.; Gamm, A.; Beesk, N.; Herppich, W.B.; Kroh, L.W.; Ulrichs, C.; Huyskens-Keil, S. UV-B-Mediated Flavonoid Synthesis in White Asparagus (Asparagus officinalis L.). Food Res. Int. 2012, 48, 196–201.
  40. Binder, B.Y.K.; Peebles, C.A.M.; Shanks, J.V.; San, K.Y. The Effects of UV-Stress on the Production of Terpenoid Indole Alkaloids in Catharanthus roseus Hairy Roots. Biotechnol. Prog. 2009, 25, 861–865.
  41. Arakawa, O.; Hori, Y.; Ogata, R. Relative Effectiveness and Interaction of Ultraviolet-B, Red and Blue Light in Anthocyanin Synthesis of Apple Fruit. Physiol. Plant. 1985, 64, 323–327.
  42. Regvar, M.; Bukovnik, U.; Likar, M.; Kreft, I. UV-B Radiation Affects Flavonoids and Fungal Colonisation in Fagopyrum esculentum and F. tataricum. Cent. Eur. J. Biol. 2012, 7, 275–283.
  43. Spitaler, R.; Schlorhaufer, P.D.; Ellmerer, E.P.; Merfort, I.; Bortenschlager, S.; Stuppner, H.; Zidorn, C. Altitudinal Variation of Secondary Metabolite Profiles in Flowering Heads of Arnica montana cv. ARBO. Phytochemistry 2006, 67, 409–417.
  44. Estell, R.E.; Fredrickson, E.L.; James, D.K. Effect of Light Intensity and Wavelength on Concentration of Plant Secondary Metabolites in the Leaves of Flourensia cernua. Biochem. Syst. Ecol. 2016, 65, 108–114.
  45. Carvalho, I.S.; Cavaco, T.; Carvalho, L.M.; Duque, P. Effect of Photoperiod on Flavonoid Pathway Activity in Sweet Potato (Ipomoea batatas (L.) Lam.) Leaves. Food Chem. 2010, 118, 384–390.
  46. Ramakrishna, A.; Dayananda, C.; Giridhar, P.; Rajasekaran, T.; Ravishankar, G.A. Photoperiod Influences Endogenous Indoleamines in Cultured Green Alga Dunaliella bardawil. Indian J. Exp. Biol. 2011, 49, 234–240.
  47. Yaashikaa, P.R.; Kumar, P.S.; Jeevanantham, S.; Saravanan, R. A review on bioremediation approach for heavy metal detoxification and accumulation in plants. Environ. Pollut. 2022, 301, 119035.
  48. Jan, R.; Asaf, S.; Numan, M.; Lubna Kim, K.M. Plant secondary metabolite biosynthesis and transcriptional regulation in response to biotic and abiotic stress conditions. Agronomy. 2021, 11, 968.
  49. Murch, S.J.; Haq, K.; Rupasinghe, H.P.V.; Saxena, P.K. Nickel contamination affects growth and secondary metabolite composition of St. John’s wort (Hypericum perforatum L.). Environ. Exp. Bot. 2003, 49, 251–257.
  50. dos Reis, A.R.; de Queiroz Barcelos, J.P.; de Souza Osório, C.R.W.; Santos, E.F.; Lisboa, L.A.M.; Santini, J.M.K.; dos Santos, M.J.D.; Junior, E.F.; Campos, M.; de Figueiredo, P.A.M.; et al. A Glimpse into the Physiological, Biochemical and Nutritional Status of Soybean Plants under Ni-Stress Conditions. Environ. Exp. Bot. 2017, 144, 76–87.
  51. Merlot, S. Understanding Nickel Responses in Plants: More than Just an Interaction with Iron Homeostasis. Plant Cell Physiol. 2020, 61, 443–444.
  52. Singh, S.; Sinha, S. Accumulation of metals and its effects in Brassica juncea (L.) Czern. (cv. Rohini) grown on various amendments of tannery waste. Ecotoxicol. Environ. Saf. 2005, 62, 118–127.
  53. Wu, B.; Wang, K.; Wu, X. A new phenolic diglycoside produced in response to copper toxicity and a new flavan dimer from the leaves of Viburnum ichangense (Hemsl.). Rehd. Helv. Chim. Acta 2011, 94, 1677–1684.
  54. Drzewiecka, K.; Mleczek, M.; Gąsecka, M.; Magdziak, Z.; Budka, A.; Chadzinikolau, T.; Kaczmarek, Z.; Goliński, P. Copper and Nickel Co-Treatment Alters Metal Uptake and Stress Parameters of Salix purpurea × viminalis. J. Plant Physiol. 2017, 216, 125–134.
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