PSI becomes more tolerant to fluoranthene through the initiation of cyclic electron flow
Rupal Singh Tomar A and Anjana Jajoo A B
+ Author Affiliations
- Author Affiliations
A School of Life Science, Devi Ahilya University, Indore 452017, M.P. India.
B Corresponding author. Email: anjanajajoo@hotmail.com
Functional Plant Biology 44(10) 978-984 https://doi.org/10.1071/FP17121
Submitted: 26 April 2017 Accepted: 9 June 2017 Published: 14 July 2017
Abstract
Environmental pollution by organic compounds such as polycyclic aromatic hydrocarbons (PAHs) poses a potential ecological risk to photosynthetic organisms. In the present study, the toxic effects of fluoranthene (FLT) on the energy conversion of PSI and PSII in wheat (Triticum aestivum L.) plants were studied. By evaluating the performance of both PSI and PSII, which act as an internal environmental sensor, it was revealed that activity of both photosystems was negatively affected by FLT treatment. However, the quantum yield of PSII, Y(II), was reduced at 5 µM FLT, whereas the quantum yield of PSI, Y(I), significantly decreased at 25 µM FLT. The decline in Y(II) was accompanied by an increase in nonregulated energy dissipation, Y(NO). The decrease in Y(I) induced by FLT was caused by donor-side, and acceptor side limitation of PSI. Cyclic electron flow (CEF) was activated only at higher concentrations and was associated with the inhibition of linear electron flow (LEF) after exposure to a higher concentration of FLT. The inhibition of LEF and induction of CEF seems to be essential for the tolerance of PSI to FLT toxicity.
Additional keywords: polycyclic aromatic hydrocarbons, PSII, Triticum aestivum, wheat.
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 | 1:CAS:528:DC%2BC28XltlSqtL4%3D&md5=2ebf581a5ef861f79e84a40fcb484d19CAS |
Aina R, Palin L, Citterio S (2006) Molecular evidence for benzo[a]pyrene and naphthalene genotoxicity in Trifolium repens L. Chemosphere 65, 666–673.
| Molecular evidence for benzo[a]pyrene and naphthalene genotoxicity in Trifolium repens L.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD28XovVWrsbg%3D&md5=c739fde4169f30625682f31729e6d716CAS |
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 | 1:CAS:528:DC%2BD1cXhtlylurbO&md5=861fd2a6cc525d119c80380d52f9edf3CAS |
Essemine J, Xiao Y, Qu M, Mi H, Zhu X-G (2017) Cyclic electron flow may provide some protection against PSII photoinhibition in rice (Oryza sativa L.) leaves under heat stress. Journal of Plant Physiology 211, 138–146.
| Cyclic electron flow may provide some protection against PSII photoinhibition in rice (Oryza sativa L.) leaves under heat stress.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2sXis1Sisrk%3D&md5=741e2176491d47a39927ea29b78d304eCAS |
Evans AD, Nipper EM (2008) The influence of biomass on the toxicity of hydrophobic organic contaminants. Archives of Environmental Contamination and Toxicology 54, 219–225.
| The influence of biomass on the toxicity of hydrophobic organic contaminants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXosVyquw%3D%3D&md5=4fb47d93730124781e3bdaf52cafe709CAS |
Huang W, Zhang S-B, Cao K-F (2010) Stimulation of cyclic electron flow during recovery after chilling-induced photoinhibition of PSII. Plant & Cell Physiology 51, 1922–1928.
| Stimulation of cyclic electron flow during recovery after chilling-induced photoinhibition of PSII.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhsVekt7jL&md5=76b17d0671459a23d6666bd8c29e0b94CAS |
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 | 1:CAS:528:DC%2BD28XpsFKnsb8%3D&md5=7960957264833e7a94b8696a584f5addCAS |
Jajoo A, Makala NR, Tomar RS, Grieco M, Tikkanen M, Aro E-M (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 | 1:CAS:528:DC%2BC2cXntFygtbY%3D&md5=79e5f1c9354f52f33dcaf49822d3f6a9CAS |
Johnson GN (2011) Physiology of PSI cyclic electron transport in higher plants. Biochimica et Biophysica Acta 1807, 384–389.
| Physiology of PSI cyclic electron transport in higher plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhsFynsrw%3D&md5=7220cd4c8c841922e1e48d0fffa9af38CAS |
Kalaji MH, Schansker G, Ladle RJ, Goltsev V, Bosa K, Allakhverdiev SI, Brestic M, Bussotti F, Calatayud A, Dąbrowski P, et al (2014) Frequently asked questions about in vivo chlorophyll fluorescence: practical issues. Photosynthesis Research
| Frequently asked questions about in vivo chlorophyll fluorescence: practical issues.Crossref | GoogleScholarGoogle Scholar |
Kalaji HM, Jajoo A, Oukarroum A, Brestic M, Zivcak M, Samborska A, Cetner MD, Łukasik I, Goltsev V, Ladle RJ (2016) Chlorophyll “a” fluorescence as a tool to monitor physiological status of plants under abiotic stress conditions. Acta Physiologiae Plantarum 38, 102
| Chlorophyll “a” fluorescence as a tool to monitor physiological status of plants under abiotic stress conditions.Crossref | GoogleScholarGoogle Scholar |
Kalaji HM, Schansker G, Brestic M, Bussotti F, Calatayud A, Ferroni L, Goltsev V, Guidi L, Jajoo A, Li P, et al (2017) Frequently asked questions about chlorophyll fluorescence, the sequel. Photosynthesis Research
| Frequently asked questions about chlorophyll fluorescence, the sequel.Crossref | GoogleScholarGoogle Scholar |
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 | 1:CAS:528:DyaK2cXnt1OjtA%3D%3D&md5=e401d2d4e84541a9cb1a1179dab7121bCAS |
Kramer DM, Avenson TJ, Kanazawa A, Cruz JA, Ivanov B, Edwards GE (2004) The relationship between photosynthetic electron transfer and its regulation. In ‘Chlorophyll a fluorescence: a signature of photosynthesis’. (Eds Papageorgiou GC, Govindjee) pp. 251–78 (Springer: Dordrecht).
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 | 1:CAS:528:DC%2BC2cXksVWns7c%3D&md5=4399c8000bb44e030375d1c4c46dd310CAS |
Kummerova M, Vanova L (2007) Chlorophyll fluorescence as an indicator of fluoranthene phototoxicity. Plant, Soil and Environment 53, 430–436.
Kummerová M, Krulová J, Zezulka S, Tríska J (2006) Evaluation of fluoranthene phytotoxicity in pea plants by Hill reaction and chlorophyll fluorescence. Chemosphere 65, 489–496.
| Evaluation of fluoranthene phytotoxicity in pea plants by Hill reaction and chlorophyll fluorescence.Crossref | GoogleScholarGoogle Scholar |
Mathur S, Jajoo A, Mehta P, Bharti S (2011) Analysis of elevated temperature-induced inhibition of photosystem II using chlorophyll a fluorescence induction kinetics in wheat leaves (Triticum aestivum). Plant Biology 13, 1–6.
| Analysis of elevated temperature-induced inhibition of photosystem II using chlorophyll a fluorescence induction kinetics in wheat leaves (Triticum aestivum).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3MXhsFKqurc%3D&md5=a2fba89dca513acc146866e3f300c2b8CAS |
Mathur S, Kalaji HM, Jajoo A (2016) Investigation of deleterious effect of chromium phytotoxicity and photosynthesis in wheat plants. Photosynthetica 54, 185–192.
| Investigation of deleterious effect of chromium phytotoxicity and photosynthesis in wheat plants.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC28XhsVyktbY%3D&md5=3ed7883d8eabcbe8a7239d3a5ac1789cCAS |
Mehta P, Jajoo A, Mathur S, Bharti S (2010) Chlorophyll a fluorescence study revealing effects of high salt stress on photosystem II in wheat leaves. Plant Physiology and Biochemistry 48, 16–20.
| Chlorophyll a fluorescence study revealing effects of high salt stress on photosystem II in wheat leaves.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1MXhs1Wlu7nM&md5=cccee6ae2d9a9319626e05d6836907ceCAS |
Oguntimehin I, Nakatani N, Sakugawa H (2008) Phytotoxicities of fluoranthene and phenanthrene deposited on needle surfaces of the evergreen conifer, Japanese red pine (Pinus densiflora Sieb. et Zucc.). Environmental Pollution 154, 264–271.
| Phytotoxicities of fluoranthene and phenanthrene deposited on needle surfaces of the evergreen conifer, Japanese red pine (Pinus densiflora Sieb. et Zucc.).Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BD1cXmvFeqsb4%3D&md5=9797ff3949f79b37c550139307b7dacaCAS |
Pfündel E, Klughammer C, Schreiber U (2008) Monitoring the effects of reduced PS II antenna size on quantum yields of photosystems I and II using the Dual-PAM-100 measuring system. PAM Application Notes 1, 21–24.
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 | 1:CAS:528:DC%2BD3sXntV2ms7g%3D&md5=86ef818e660f34b188035824a1e5e3d9CAS |
Seyyedneja SM, Niknejad M, Koochak H (2011) A review of some different effects of air pollution on plants. Research Journal of Environmental Sciences 5, 302–309.
| A review of some different effects of air pollution on plants.Crossref | GoogleScholarGoogle Scholar |
Shikanai T (2014) Central role of cyclic electron transport around photosystem I in the regulation of photosynthesis. Current Opinion in Biotechnology 26, 25–30.
| Central role of cyclic electron transport around photosystem I in the regulation of photosynthesis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2cXlt1Cns7g%3D&md5=004484526aa3b7fe2f2f28131cdc7fdcCAS |
Sun Y, Geng Q, Du Y, Yang X, Zhai H (2017) Induction of cyclic flow around photosystem I during heat stress in grape leaves. Plant Science 256, 65–71.
| Induction of cyclic flow around photosystem I during heat stress in grape leaves.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC28XitFOhsLrI&md5=bcb6f6d395fd3916356ff33d57cee90eCAS |
Tomar RS, Jajoo A (2013a) Alteration in PSII heterogeneity under the influence of polycyclic aromatic hydrocarbon (fluoranthene) in wheat leaves (Triticum aestivum). Plant Science 209, 58–63.
| Alteration in PSII heterogeneity under the influence of polycyclic aromatic hydrocarbon (fluoranthene) in wheat leaves (Triticum aestivum).Crossref | GoogleScholarGoogle Scholar |
Tomar RS, Jajoo A (2013b) A quick investigation of the detrimental effects of environmental pollutant polycyclic aromatic hydrocarbon fluoranthene on the photosynthetic processes. Ecotoxicology 22, 1313–1318.
| A quick investigation of the detrimental effects of environmental pollutant polycyclic aromatic hydrocarbon fluoranthene on the photosynthetic processes.Crossref | GoogleScholarGoogle Scholar |
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 | 1:CAS:528:DC%2BC2cXhsVaktb7E&md5=5f9c17ef1d3971f93e02944ba3e15bebCAS |
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 | 1:CAS:528:DC%2BC2MXhtFOksb%2FK&md5=c778a1a04e50710b76d6ee9512fa04b0CAS |
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 | 1:CAS:528:DC%2BC2MXhtVOmsrzO&md5=2ea1cadd4a623cb2f0c842dc2d30629bCAS |
Wilhelm C, Selmar D (2011) Energy dissipation is an essential mechanism to sustain the viability of plants: the physiological limits of improved photosynthesis. Journal of Plant Physiology 168, 79–87.
| Energy dissipation is an essential mechanism to sustain the viability of plants: the physiological limits of improved photosynthesis.Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC3cXhsF2jurjO&md5=a3080285276fe60183a89e11a69a92f8CAS |
Zezulka S, Kummerova M, Babula P, Vanova L (2013) Lemna minor exposed to fluoranthene: growth, biochemical, physiological and histochemical changes. Aquatic Toxicology (Amsterdam, Netherlands) 140–141, 37–47.
| Lemna minor exposed to fluoranthene: growth, biochemical, physiological and histochemical changes.Crossref | GoogleScholarGoogle Scholar |
Zivcak M, Brestic M, Kunderlikova K, Olsovska K, Allakhverdiev S (2015) Effect of photosystem I inactivation on chlorophyll a fluorescence induction in wheat leaves: does activity of photosystem I play any role in OJIP rise? Journal of Photochemistry and Photobiology. B, Biology 152, 318–324.
| Effect of photosystem I inactivation on chlorophyll a fluorescence induction in wheat leaves: does activity of photosystem I play any role in OJIP rise?Crossref | GoogleScholarGoogle Scholar | 1:CAS:528:DC%2BC2MXhsVKhu7rL&md5=18fc71586cafeaba257dd84ac453cbe9CAS |
