Abstract
This study was aimed to investigate how exogenous manganese (Mn) would limit damage in the oxygen-evolving complex (OEC) and photosynthetic apparatus of maize seedlings caused during seawater vulnerability. In this study, seawater was applied in 2-week-old maize (Zea mays L.) seedling, and the degree of damage of photosynthetic pigment pool, the OEC, and net electron transport rate were observed. Mn supplement was also added in maize seedlings to limit the damage of the OEC and photosynthetic apparatus caused during salinity. Leaf relative water content (RWC), fresh weight (FW), and photosynthetic pigment pool (chlorophyll a, chlorophyll b, and carotenoids) sharply declined after 7 days of treatment; however, Mn supplement increased these values. Chlorophyll fluorescence induction (OJIP) transients showed low Fv/Fo, an additional K step, enhanced variable fluorescence (VK) and degree of damage to the OEC (WK) during salinity, and indicates damage of OEC at electron donor side of photosystem II (PSII). The OEC intact within PSII was a primary damage center during salinity which inhibited electron transport process that resulted in a huge loss of maximum quantum yield of PSII (Fv/Fm), but a significant recovery in photosynthetic apparatus was observed after exogenous application of manganese. Structural and functional integrity of the photosynthetic apparatus was recovered up to a certain extent after exogenous application of Mn. Findings from this study should help to understand the basic knowledge of photosynthetic apparatus efficiency in response to damage caused by exposure to seawater. Outcomes of this study will be used to mitigate salinity problem with Mn supplement for growth and development of crops.
Similar content being viewed by others
References
Arnon DI (1949) Copper enzymes in isolated chloroplasts. Polyphenoloxidase in Beta vulgaris. Plant Physiol 24:1–15
Barrs HD, Weatherley PE (1962) A re-examination of the relative turgidity technique for estimating water deficits in leaves. Aust J Biol Sci 15:413–428
Cao, P., Xie, Y., Li, M., Pan, X., Zhang, H., Zhao, X., 2015. Crystal structure analysis of extrinsic PsbP protein of photosystem II reveals a manganese induced conformational change. Mol Plant 8, 664–666. doi: :https://doi.org/10.1016/j.molp. 2015.01.002
Chaves M.M., Flexas J., Pinheiro C. 2009: Photosynthesis under drought and salt stress: regulation mechanisms from whole plant to cell. – Annals of Botany-London 103: 551-560
Cramer GR, Nowak RS (1992) Supplemental manganese improves the relative growth, net assimilation and photosynthetic rates of salt-stressed barley. Physiol Plant 84:600–605
Demetriou G, Neonaki C, Navakoudis E, Kotzabasis K (2007) Salt stress impact on the molecular structure and function of the photosynthetic apparatus—the protective role of polyamines. Biochimica et Biophysica Acta (BBA) – Bioenergetics 1767(4):272–280
FAO (1997) Soil map of the world. Revised Legend. World Soil Resources Report, FAO, Rome
Foley JA, Ramankutty N, Brauman KA, Cassidy ES, Gerber JS, Johnston M, Mueller ND, O’Connell C, Ray DK, West PC, Balzer C, Bennett EM, Carpenter SR, Hill J, Monfreda C, Polasky S, Rockstrom J, Sheehan J, Siebert S, Tilman D, Zaks DP (2011) Solutions for a cultivated planet. Nature. 478:337–342
Force L, Critchley C, van Rensen JJS (2003) New fluorescence parameters for monitoring photosynthesis in plants. 1. The effect of illumination on the fluorescence parameters of the JIP-test. Photosynth Res 78:17–33
Fricke W, Peters WS (2002) The biophysics of leaf growth in salt-stressed barley. A study at the cell level. Plant Physiol 129:374–388
Godfray HC, Pretty J, Thomas SM, Warham EJ, Beddington JR (2011) Global food supply: linking policy on climate and food. Science 331:1013–1014
Goussi R, Manaa A, Derbali W, Cantamessa S, Abdelly C, Barbato R (2018) Comparative analysis of salt stress, duration and intensity, on the chloroplast ultrastructure and photosynthetic apparatus in Thellungiella salsuginea. J Photochem Photobiol B 183:275–287
Guo Y, Tan J (2015) Recent advances in the application of chlorophyll a fluorescence from photosystem II. Photochem Photobiol 91:1–14. https://doi.org/10.1111/php.12362
Gupta R (2019) Tissue specific disruption of photosynthetic electron transport rate in pigeonpea (Cajanuscajan L.) under elevated temperature. Plant Signal Behav. https://doi.org/10.1080/15592324.2019.1601952
Hasanuzzaman M, Hossain MA, Fujita M (2011a) Nitric oxide modulates antioxidant defense and the methylglyoxal detoxification system and reduces salinity-induced damage of wheat seedlings. Plant Biotechnology Report 5:353–365
Hasanuzzaman M, Hossain MA, Fujita M (2011b) Selenium-induced up-regulation of the antioxidant defense and methylglyoxal detoxification system reduces salinity-induced damage in rapeseed seedlings. Biol Trace Elem Res 143:1704–1721
Hasegawa PM, Bressan RA, Z, J.K. & B, H.J (2000) Plant cellular and molecular responses to high salinity. Annu Rev Plant Physiol Plant Mol Biol 51:463–499
Järvi S, Gollan PJ, Aro EM (2013) Understanding the roles of the thylakoid lumen in photosynthesis regulation. Front Plant Sci 4:434. https://doi.org/10.3389/fpls.2013.00434
Kalaji HM, Govindjee Bosa K, Kościelniak J, Żuk-Gołaszewska K (2011) Effects of salt stress on photosystem II efficiency and CO2 assimilation of two Syrian barley landraces. Environ Exp Bot 73:64–72
Kirk JTO, Allen RL (1965) Dependence of chloroplast pigments synthesis on protein synthetic effects on actilione. Biochemistry Biophysics Research Journal Canada 27:523–530
Krieger-Liszkay A, Krupinska K, Shimakawa G (2019) The impact of photosynthesis on initiation of leaf senescence. Physiol Plant 166:148–164. https://doi.org/10.1111/ppl.12921
Lidon FC, Barreiro M, Ramalho J (2004) Manganese accumulation in rice: implications for photosynthetic functioning. J Plant Physiol 161:1235–1244
Mahajan S, Tuteja N (2005) Cold, salinity and drought stresses: an overview. Achf Biochem Biophysics 444:139–158. https://doi.org/10.1016/j.abb.2005.10.018
Manaa A, Goussi R, Derbali W, Cantamessa S, Abdelly C, Barbato R (2019) Salinity tolerance of quinoa (Chenopodium quinoa Willd) as assessed by chloroplast ultrastructure and photosynthetic performance. Environ Exp Bot 162:103–114
Mehta P., Jajoo A., Mathur 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
Millaleo R, Reyes-Diaz M, Ivanov AG, Mora ML, Alberdi M (2010) Manganese as essential and toxic element for plants: transport, accumulation and resistance mechanisms. J Soil Sci Plant Nutr 10:476–494
Misra A.N. Srivastava A., Strasser R.J.: Utilization of fast chlorophyll a fluorescence technique in assessing the salt/ion sensitivity of mung bean and Brassica seedlings – Journal Plant Physiol 158: 1173–1181, 2001
Misra AN, Latowski D, Strzalka K (2006) The xanthophyll cycle activity in kidney bean and cabbage leaves under salinity stress. Russ J Plant Physiol 53:102–109
Munns R (2011) Plant adaptations to salt and water stress: differences and commonalities. Adv Bot Res 57:1–32
Munns R, Tester M (2008) Mechanisms of salinity tolerance. Annu Rev Plant Biol 59:651–681
Munns R, Passioura JB, Colmer TD, Byrt CS (2019) Osmotic adjustment and energy limitations to plant growth in saline soil. New Phytol. https://doi.org/10.1111/nph.15862
Murata N., Allakhverdiev S.I., Nishiyama Y. (2012). The mechanism of photoinhibition in vivo: re-evaluation of the roles of catalase, α-tocopherol, non-photochemical quenching, and electron transport. – BBA-Bioenergetics 1817: 1127-1133
Nahar K, Hasanuzzaman M, Alam MM, Fujita M (2015) Roles of exogenous glutathione in antioxidant defense system and methylglyoxal detoxification during salt stress in mung bean. Biol Plant 59:745–756
Nishiyama Y Allakhverdiev S.I., Murata N. (2011). Protein synthesis is the primary target of reactive oxygen species in the photoinhibition of photosystem II. – Physiol. Plantarum 142: 35–46
Oliveira KS, de Mello Prado R, de Farias Guedes VH (2020) Leaf spraying of manganese with silicon addition is agronomically viable for corn and sorghum plants. J Soil Sci Plant Nutr:1–9. https://doi.org/10.1007/s42729-020-00173-6
Ozfidan-Konakci C, Yildiztugay E, Kucukoduk M (2015) Protective roles of exogenously applied gallic acid in Oryza sativa subjected to salt and osmotic stresses: effects on the total antioxidant capacity. Plant Growth Regul 75:219–234
Pandya DH, Mer RK, Prajith PK, Pandey AN (2004) Effect of salt stress and manganese supply on growth of barley seedlings. J Plant Nutr 27:1361–1379
Parmoon G, Ebadi A, Jahanbakhsh S, Hashemi M, Moosavi SA (2019) Assessing photosynthetic performance of fennel (Foeniculum vulgare mill) influenced by plant growth regulators and drought stress imposed at vegetative and reproductive stages. Ital J Agron 14(2):93–100
Rahman A, Hossain MS, Mahmud JA, Nahare K, Hasanuzzaman M, Fujita M (2016) Manganese-induced salt stress tolerance in rice seedlings: regulation of ion homeostasis, antioxidant defense and glyoxalase systems. Physiol Mol Biol Plants 22:291–306. https://doi.org/10.1007/s12298-016-0371-1
Rochaix JD (2011) Regulation of photosynthetic electron transport. Biochimica et Biophysica Acta (BBA) – Bioenergetics 1807:375–383. https://doi.org/10.1016/j.bbabio.2010.11.010
Safdar H, Amin A, Shafiq Y, Ali A, Yasin R, Shoukat A, Hussan MU, Sarwar MI (2019) A review: impact of salinity on plant growth. Nat Sci 17(1):34–40
Saha P, Chatterjee P, Biswas AK (2010) NaCl pretreatment alleviates salt stress by enhancement of antioxidant defense system and osmolyte accumulation in mungbean (Vigna radiat L. Wilczek). Indian J Exp Biol 48:593–600
Schmidt SB, Powikrowska M, Krogholm KS, Naumann-Busch B, Schjoerring JK, Husted S, Jensen PE, Pedas PR (2016) Photosystem II functionality in barley responds dynamically to changes in leaf manganese status. Front Plant Sci 7:1772
Sebastian A, Prasad MNV (2015) Iron-and manganese-assisted cadmium tolerance in Oryza sativa L.: lowering of rhizotoxicity next to functional photosynthesis. Planta 241:1519–1528
Shannon MC (1998) Adaptation of plants to salinity. Adv Agron 60:75–119
Stefanov D, Petkova V, Denev ID (2011) Screening for heat tolerance in common bean (Phaseolus vulgaris L.) lines and cultivars using JIP-test. Sci Hortic 128(1):1–6
Strasser R.J., Tsimilli-Michael M., Srivastava A. (2000) The fluorescence transient as a tool to characterize and screen photosynthetic samples. – In: Yunus M., Pathre U., Mohanty P. (ed.): Probing Photosynthesis: Mechanisms, Regulation and Adaptation. Taylor & Francis, London 443–480 pp.
Strasser RJ, Tsimilli-Michael M, Srivastava A (2004) Analysis of the chlorophyll a fluorescence transient. – In: Papageorgiou G.C., Govindjee (ed.): Chlorophyll a Fluorescence: A Signature of photosynthesis, Advances in Photosynthesis and Respiration, Springer, Dordrecht 19.. 321–362 pp.
Takahashi S, Badger MR (2011) Photoprotection in plants: a new light on photosystem II damage. Trends Plant Sci 16:5359
Tóth SZ, Schansker G, Strasser RJ (2007) A non-invasive assayof the plastoquinone pool redox state based on the OJIP-transient. Photosynth Res 93:193–203
Tsimilli-Michael M, Strasser RJ (2008) In vivo assessment of plants’ vitality: applications in detecting and evaluating the impact of mycorrhization on host plants. In: Varma A. editor. Mycorrhiza: State of the Art. Genetics and Molecular Biology, Eco-Function, Biotechnology, Eco-Physiology, Structure and Systematics, 3rd ed. 2008 Dordrecht, Netherland. Springer. 679-703 pp.
Tuncturk M, Tuncturk R, Yasar F (2008) Changes in micronutrients, dry weight and plant growth of soybean (Glycine max L. Merrill) cultivars under salt stress. Afr J Biotechnol 7:1650–1654
Vass I (2011) Role of charge recombination processes in photodamage and photoprotection of the photosystem II complex. – Physiol. Plantarum 142:6–16
Vogt L, Vinyard DJ, Khan S, Brudvig GW (2015) Oxygen-evolving complex of photosystem II: an analysis of second-shell residues and hydrogen-bonding networks. Curr Opin Chem Biol 25:152–158
Wu F, Guclu H (2013) Global maize trade and food security: implications from a social network model. Risk Anal 33(12). https://doi.org/10.1111/risa.120642013
Yang Y-J, Liu T, Zhang S-B, Huang W (2019) Special issue in honour of Prof. Reto J. StrasserPhotoinhibition of oxygen-evolving complex and photosystem II at chilling stress in the tropical tree species Dalbergia odorifera. Photosynthetica. https://doi.org/10.32615/ps.2019.138
Yanykin DV, Khorobrykh AA, Khorobrykh SA, Klimov VV (2010) Photoconsumption of molecular oxygen on both donor and acceptor sides of photosystem II in Mn-depleted subchloroplast membrane fragments. Biochimica et Biophysica Acta (BBA) – Bioenergetics 1797:516–523
Zavafer A, Koinuma W, Chow WS et al (2017) Mechanism of photodamage of the oxygen evolving Mn cluster of photosystem II by excessive light energy. Sci Rep-UK 7:7604
Zhang H, Liu N, Zhao J, Ge F, Xu Y, Chen Y (2019) Disturbance of photosystem II-oxygen evolution complex induced the oxidative damage in Chlorella vulgaris under the stress of cetyltrimethylammonium chloride. Chemosphere 223:659–667
Zushi K, Matsuzoe N (2017) Using of chlorophyll a fluorescence OJIP transients for sensing salt stress in the leaves and fruits of tomato. Sci Hortic 219:216–221
Acknowledgments
I thank Mr. Mahendra Singh, Department of Language and Literature, for the editing and proofreading, and Ms. Adimaitoga and Ms. Sujeshni for the assistance during experimentation. Special thanks to Mr. Monish, Mr. Nitesh, Mr. Sarwan, and Ms. Jimaima, Vatukoula Gold Mines PLC, Fiji, for the manganese (Mn) analysis.
Author Contribution Statement
RG designed the research, conducted the experiments, and wrote the manuscript.
Funding
The work was supported by Fiji National University.
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Conflict of Interest
The author declares that he has no conflict of interest.
Additional information
Publisher’s Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Gupta, R. Manganese Repairs the Oxygen-Evolving Complex (OEC) in Maize (Zea mays L.) Damage During Seawater Vulnerability. J Soil Sci Plant Nutr 20, 1387–1396 (2020). https://doi.org/10.1007/s42729-020-00220-2
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s42729-020-00220-2