Photosynthetic response in wheat plants caused by the phototoxicity of fluoranthene
Rupal S. Tomar A and Anjana Jajoo
B C
+ Author Affiliations
- Author Affiliations
A School of Life Science, Devi Ahilya University, Indore 452017, India.
B School of Biotechnology, Devi Ahilya University, Indore 452017, India.
C Corresponding author. Email: anjanajajoo@hotmail.com
Functional Plant Biology 46(8) 725-731 https://doi.org/10.1071/FP18328
Submitted: 27 December 2018 Accepted: 19 March 2019 Published: 26 April 2019
Abstract
Environmental organic pollutants such as polycyclic aromatic hydrocarbons (PAHs) affect photosynthetic performance in plants. The photooxidation of PAHs in natural sunlight, especially UV radiation, enhances the toxicity of PAHs. However, it is unclear as how these compounds and their photoproducts affect the photosynthetic apparatus. In this study, measurements of PSI and PSII were simultaneously performed in wheat (Triticum aestivum L.) plants treated with fluoranthene (FLT) and photomodified fluoranthene (PFLT). The study aimed to investigate whether the phototoxicity of FLT has a different mechanism of toxicity on the two photosystems. With regard to PSII, FLT and PFLT produced a significant decrease in the quantum yield of PSII and a pronounced increase in the yield of nonregulated energy dissipation. A significant reduction was observed in the yield of nonphotochemical quenching. The toxic effects of the PFLT treatment on PSII’s performance were more pronounced. Likewise, we noted severe disruption in the electron transport rate in PSII and a decline in Fm caused by FLT phototoxicity. A decline in the quantum yield of PSI and an increase in donor and acceptor side limitation were observed concomitantly. The impact of PFLT was more evident than that of FLT. The data demonstrated that PSI is more tolerant of FLT but for PFLT, particularly at higher concentrations, a pronounced inhibition was observed in the oxidation–reduction kinetics of P700. All these data suggest that increased cyclic electron flow can confer greater protection from FLT toxicity but not from toxicity induced by higher concentrations of PFLT.
Additional keywords: cyclic electron flow, polycyclic aromatic hydrocarbons, PSI, PSII.
References
Agrawal D, Allakhverdiev SI, Jajoo A (2016) Cyclic electron flow plays an important role in protection of spinach leaves (Spinacia oleracia) under high temperature stress. Russian Journal of Plant Physiology: a Comprehensive Russian Journal on Modern Phytophysiology 63, 210–215.| Cyclic electron flow plays an important role in protection of spinach leaves (Spinacia oleracia) under high temperature stress.Crossref | GoogleScholarGoogle Scholar |
Aksmann A, Tukaj Z (2008) Intact anthracene inhibits photosynthesis in algal cells: a fluorescence induction study on Chlamydomonas reinhardtii cw92 strain. Chemosphere 74, 26–32.
| Intact anthracene inhibits photosynthesis in algal cells: a fluorescence induction study on Chlamydomonas reinhardtii cw92 strain.Crossref | GoogleScholarGoogle Scholar | 18980775PubMed |
Deng C-N, Zhang D-Y, Pan X-L (2014) Toxic effects of erythromycin on Photosystem I and II in Microcystis aeruginosa. Photosynthetica 52, 574–580.
| Toxic effects of erythromycin on Photosystem I and II in Microcystis aeruginosa.Crossref | GoogleScholarGoogle Scholar |
Essemine J, Govindachary S, Ammar S, Bouzid S, Carpentier R (2012) Enhanced sensitivity of the photosynthetic apparatus to heat stress in digalactosyl-diacylglycerol deficient Arabidopsis. Environmental and Experimental Botany 80, 16–26.
| Enhanced sensitivity of the photosynthetic apparatus to heat stress in digalactosyl-diacylglycerol deficient Arabidopsis.Crossref | GoogleScholarGoogle Scholar |
Hideg E, Kos PE, Schreiber U (2008) Imaging of NPQ and ROS formation in tobacco leaves: heat inactivation of the water–water cycle prevents down-regulation of PS II. Plant & Cell Physiology 49, 1879–1886.
| Imaging of NPQ and ROS formation in tobacco leaves: heat inactivation of the water–water cycle prevents down-regulation of PS II.Crossref | GoogleScholarGoogle Scholar |
Huang XD, Dixon DG, Greenberg BM (1993) Impacts of UV radiation and photomodification on the toxicity of PAHs to the higher plant Lemna gibba (duckweed). Environmental and Experimental Botany 12, 1067–1077.
Huang W, Zhang SB, Cao KF (2010) The different effects of chilling stress under moderate illumination on Photosystem II compared with Photosystem I and subsequent recovery in tropical tree species. Photosynthesis Research 103, 175–182.
| The different effects of chilling stress under moderate illumination on Photosystem II compared with Photosystem I and subsequent recovery in tropical tree species.Crossref | GoogleScholarGoogle Scholar | 20221850PubMed |
Ivanov AG, Hendrickson L, Krol M, Selstam E, Oquist G, Hurry V, Huner NPA (2006) Digalactosyl-diacylglycerol deficiency impairs the capacity for photosynthetic intersystem electron transport and state transitions in Arabidopsis thaliana due to Photosystem I acceptor-side limitations. Plant & Cell Physiology 47, 1146–1157.
| Digalactosyl-diacylglycerol deficiency impairs the capacity for photosynthetic intersystem electron transport and state transitions in Arabidopsis thaliana due to Photosystem I acceptor-side limitations.Crossref | GoogleScholarGoogle Scholar |
Jajoo A, Mekala NR, Tomar RS, Grieco M, Tikkanen M, Aro EM (2014) Inhibitory effects of polycyclic aromatic hydrocarbons (PAHs) on photosynthetic performance are not related to their aromaticity. Journal of Photochemistry and Photobiology. B, Biology 137, 151–155.
| Inhibitory effects of polycyclic aromatic hydrocarbons (PAHs) on photosynthetic performance are not related to their aromaticity.Crossref | GoogleScholarGoogle Scholar | 24793324PubMed |
Kan X, Ren J, Tingting C, Min C, Chenliu L, Ronghua Z, Yu Z, Huanhuan L, Dexiang D, Zhitong Y (2017) Effects of salinity on photosynthesis in maize probed by prompt fluorescence, delayed fluorescence and P700 signals. Environmental and Experimental Botany 140, 56–64.
| Effects of salinity on photosynthesis in maize probed by prompt fluorescence, delayed fluorescence and P700 signals.Crossref | GoogleScholarGoogle Scholar |
Khpalwak W, Abdel-dayem MS, Sakugawa H (2018) Individual and combined effects of fluoranthene, phenanthrene, mannitol and sulfuric acid on marigold (Calendula officinalis). Ecotoxicology and Environmental Safety 148, 834–841.
| Individual and combined effects of fluoranthene, phenanthrene, mannitol and sulfuric acid on marigold (Calendula officinalis).Crossref | GoogleScholarGoogle Scholar | 29197798PubMed |
Klughammer C, Schreiber U (1994) An improved method, using saturating light pulses, for the determination of Photosystem-I quantum yield via P700+ absorbance changes at 830 nm. Planta 192, 261–268.
| An improved method, using saturating light pulses, for the determination of Photosystem-I quantum yield via P700+ absorbance changes at 830 nm.Crossref | GoogleScholarGoogle Scholar |
Kmentova E (2003). Response of plant to fluoranthene in environment. Ph.D Thesis, Masaryk University, Brno, Czech Republic.
Kreslavski VD, Lankin AV, Vasilyeva GK, Luybimov VY, Semenova GN, Schmitt FJ, Friedrich T, Allakhverdiev SI (2014) Effects of polyaromatic hydrocarbons on Photosystem II activity in pea leaves. Plant Physiology and Biochemistry 81, 135–142.
| Effects of polyaromatic hydrocarbons on Photosystem II activity in pea leaves.Crossref | GoogleScholarGoogle Scholar | 24637130PubMed |
Kreslavski VD, Brestic M, Zharmukhamedov SK, Lyubimov VY, Lankin AV, Jajoo A, Allakhverdiev SI (2017) Mechanisms of inhibitory effects of polycyclic aromatic hydrocarbons in photosynthetic primary processes in pea leaves and thylakoid preparations. Plant Biology 19, 683–688.
| Mechanisms of inhibitory effects of polycyclic aromatic hydrocarbons in photosynthetic primary processes in pea leaves and thylakoid preparations.Crossref | GoogleScholarGoogle Scholar | 28646629PubMed |
Kummerová M, Vanova L (2007) Chlorophyll fluorescence as an indicator of fluoranthene phototoxicity. Plant, Soil and Environment 53, 430–436.
| Chlorophyll fluorescence as an indicator of fluoranthene phototoxicity.Crossref | GoogleScholarGoogle Scholar |
Lampi MA, Gurska J, McDonald KI, Xie F, Huang X, Dixon DG, Greenberg BM (2006) Photoinduced toxicity of polycyclic aromatic hydrocarbons to Daphnia magna: ultraviolet-mediated effects and the toxicity of polycyclic aromatic hydrocarbon photoproducts. Environmental Toxicology and Chemistry 25, 1079–1087.
| Photoinduced toxicity of polycyclic aromatic hydrocarbons to Daphnia magna: ultraviolet-mediated effects and the toxicity of polycyclic aromatic hydrocarbon photoproducts.Crossref | GoogleScholarGoogle Scholar | 16629147PubMed |
Marzooghi S, Toro DMDI (2017) A critical review of polycyclic aromatic hydrocarbon phototoxicity models. Environmental Toxicology and Chemistry 36, 1138–1148.
| A critical review of polycyclic aromatic hydrocarbon phototoxicity models.Crossref | GoogleScholarGoogle Scholar | 28012186PubMed |
Oukarroum A, Schansker G, Strasser RJ (2009) Drought stress effects on Photosystem I content and Photosystem II thermotolerance analyzed using Chl a fluorescence kinetics in barley varieties differing in their drought tolerance. Physiologia Plantarum 137, 188–199.
| Drought stress effects on Photosystem I content and Photosystem II thermotolerance analyzed using Chl a fluorescence kinetics in barley varieties differing in their drought tolerance.Crossref | GoogleScholarGoogle Scholar | 19719481PubMed |
Ralph PJ, Gademann R (2005) Rapid light curves: a powerful tool to assess photosynthetic activity. Aquatic Botany 82, 222–237.
| Rapid light curves: a powerful tool to assess photosynthetic activity.Crossref | GoogleScholarGoogle Scholar |
Schansker G., Srivastava A., Govindjee , Strasser RJ (2003) Characterization of the 820-nm transmission signal paralleling the chlorophyll a fluorescence rise (OJIP) in pea leaves. Functional Plant Biology 30, 785–796.
| Characterization of the 820-nm transmission signal paralleling the chlorophyll a fluorescence rise (OJIP) in pea leaves.Crossref | GoogleScholarGoogle Scholar |
Schreiber U, Klughammer C (2008) New accessory for the Dual-PAM-100: the P515/535 module and examples of its application. PAM Application Notes 1, 1–10.
Shikanai T (2007) Cyclic electron transport around Photosystem I: genetic approaches. Annual Review of Plant Biology 58, 199–217.
| Cyclic electron transport around Photosystem I: genetic approaches.Crossref | GoogleScholarGoogle Scholar | 17201689PubMed |
Suzuki K, Ohmori Y, Ratel E (2011) High root temperature blocks both linear and cyclic electron transport in the dark during chilling of the leaves of rice seedlings. Plant & Cell Physiology 52, 1697–1707.
| High root temperature blocks both linear and cyclic electron transport in the dark during chilling of the leaves of rice seedlings.Crossref | GoogleScholarGoogle Scholar |
Tikkanen M, Mekala NR, Aro EM (2014) Photosystem II photoinhibition–repair cycle protects Photosystem I from irreversible damage Biochimica et Biophysica Acta 1837, 210–215.
| Photosystem II photoinhibition–repair cycle protects Photosystem I from irreversible damageCrossref | GoogleScholarGoogle Scholar | 24161359PubMed |
Tomar RS, Jajoo A (2014) Fluoranthene, a polycyclic aromatic hydrocarbon, inhibits light as well as dark reactions of photosynthesis in wheat (Triticum aestivum). Ecotoxicology and Environmental Safety 109, 110–115.
| Fluoranthene, a polycyclic aromatic hydrocarbon, inhibits light as well as dark reactions of photosynthesis in wheat (Triticum aestivum).Crossref | GoogleScholarGoogle Scholar | 25173746PubMed |
Tomar RS, Jajoo A (2015) Photomodified fluoranthene exerts more harmful effects as compared to intact fluoranthene by inhibiting growth and photosynthetic processes. Ecotoxicology and Environmental Safety 122, 31–36.
| Photomodified fluoranthene exerts more harmful effects as compared to intact fluoranthene by inhibiting growth and photosynthetic processes.Crossref | GoogleScholarGoogle Scholar | 26186727PubMed |
Tomar RS, Jajoo A (2017) Photosystem I (PSI) becomes more tolerant to fluoranthene due to initiation of cyclic electron flow (CEF). Functional Plant Biology 44, 978–984.
| Photosystem I (PSI) becomes more tolerant to fluoranthene due to initiation of cyclic electron flow (CEF).Crossref | GoogleScholarGoogle Scholar |
Tomar RS, Sharma A, Jajoo A (2015) Assessment of phytotoxicity of anthracene in soybean (Glycine max) with a quick method of chlorophyll fluorescence. Plant Biology 17, 870–876.
| Assessment of phytotoxicity of anthracene in soybean (Glycine max) with a quick method of chlorophyll fluorescence.Crossref | GoogleScholarGoogle Scholar | 25565351PubMed |
Wang S, Pan X, Zhang D (2015) PSI showed higher tolerance to Sb(V) than PSII due to stimulation of cyclic electron flow around PSI. Current Microbiology 70, 27–34.
| PSI showed higher tolerance to Sb(V) than PSII due to stimulation of cyclic electron flow around PSI.Crossref | GoogleScholarGoogle Scholar | 25141964PubMed |
Zezulka S, Kummerova M, Babulab P, Vanovaa L (2013) Lemna minor exposed to fluoranthene: growth, biochemical, physiological and histochemical changes. Aquatic Toxicology (Amsterdam, Netherlands) 140, 37–47.
| Lemna minor exposed to fluoranthene: growth, biochemical, physiological and histochemical changes.Crossref | GoogleScholarGoogle Scholar |
