PSI-driven cyclic electron flow partially alleviates the peroxidation of red alga <i>Gelidium amansii</i> (Gelidiaceae) caused by temporary high temperature -- Journal of Oceanology and Limnology,2022,40(1):206-215

	Cite this paper:
	Yongfu LI, Jianguo LIU, Litao ZHANG. PSI-driven cyclic electron flow partially alleviates the peroxidation of red alga Gelidium amansii (Gelidiaceae) caused by temporary high temperature[J]. Journal of Oceanology and Limnology, 2022, 40(1): 206-215

PSI-driven cyclic electron flow partially alleviates the peroxidation of red alga Gelidium amansii (Gelidiaceae) caused by temporary high temperature

Yongfu LI^1,2, Jianguo LIU^1,2, Litao ZHANG^1,2

1 CAS and Shandong Province Key Laboratory of Experimental Marine Biology, Center for Ocean Mega-Science, Institute of Oceanology, Chinese Academy of Sciences, Qingdao 266071, China;
2 Marine Biology and Biotechnology Laboratory, Pilot National Laboratory for Marine Science and Technology (Qingdao), Qingdao 266237, China

Abstract:

PSI-driven cyclic electron flow (CEF-I) helps higher plants avoid severe heat damage. Gelidium amansii, a red seaweed used in the production of agar, inhabits subtidal rocks but can be found in the intertidal zone. The biological role of CEF-I is still unclear in this organism. Wild G. amansii was exposed to 30 ℃ heat stress for 12 h with continuous lighting. The results showed that treatment at 30 ℃ gradually decreased maximal PSII photochemical efficiency (F_v/F_m), linear electron transfer rate, and activity of photosynthetic reaction center. Both the maximal photochemical efficiency under light (F_v'/F_m') and maximum quantum yield of light-adapted PSII (Φ_PSII) were maintained at a relatively stable level during the initial 6 h and then significantly decreased at 12 h. The up-regulated CEF-I helps to enhance proton gradient transfer across thylakoid membrane to protect oxygen-evolving complex against heat damage. Following the addition of a CEF-I inhibitor to plants, the F_v/F_m greatly decreased, suggesting that the CEF-I alleviates degree of photoinhibition caused by strong light. The results of measurement of antioxidant enzymes, including superoxide dismutase (SOD), ascorbate peroxidase (APX) and catalase (CAT), and the contents of H₂O₂ and malonaldehyde (MDA) provided additional evidence that CEF-I plays a protective role to a certain extent for G. amansii to manage stress at 30 ℃. Therefore, it can be concluded that CEF-I enables G. amansii to survive in intertidal zones by protecting it from the heat damage caused by high temperature stress.

Received: 2020-11-23 Revised:

Tools

PDF (543 KB) Free

Print this page

Add to favorites

Email this article to others

Authors

Articles by Yongfu LI

Articles by Jianguo LIU

Articles by Litao ZHANG

References:
Agrawal D, Allakhverdiev S I, Jajoo A. 2016. Cyclic electron flow plays an important role in protection of spinach leaves under high temperature stress. Russian Journal of Plant Physiology, 63(2): 210-215.
Aihara Y, Takahashi S, Minagawa J. 2016. Heat induction of cyclic electron flow around photosystem I in the symbiotic dinoflagellate Symbiodinium. Plant Physiology, 171(1): 522-529.
Alemu S T. 2020. Photosynthesis limiting stresses under climate change scenarios and role of chlorophyll fluorescence: a review article. Cogent Food & Agriculture, 6(1): 1785136.
Baker N R. 2008. Chlorophyll fluorescence: a probe of photosynthesis in vivo. Annual Review of Plant Biology, 59: 89-113.
Blouin N A, Brodie J A, Grossman A C, Xu P, Brawley S H. 2011. Porphyra: a marine crop shaped by stress. Trends in Plant Science, 16(1): 29-37.
Brestic M, Zivcak M, Hauptvogel P, Misheva S, Kocheva K, Yang X H, Li X N, Allakhverdiev S I. 2018. Wheat plant selection for high yields entailed improvement of leaf anatomical and biochemical traits including tolerance to non-optimal temperature conditions. Photosynthesis Research, 136(2): 245-255.
Burrows P A, Sazanov L A, Svab Z, Maliga P, Nixon P J. 1998. Identification of a functional respiratory complex in chloroplasts through analysis of tobacco mutants containing disrupted plastid ndh genes. The EMBO Journal, 17(4): 868-876.
Davison I R, Pearson G A. 1996. Stress tolerance in intertidal seaweeds. Journal of Phycology, 32(2): 197-211.
De Ronde J A D, Cress W A, Kruger G H J, Strasser R J, Staden J V. 2004. Photosynthetic response of transgenic soybean plants, containing an Arabidopsis P5CR gene, during heat and drought stress. Journal of Plant Physiology, 161(11): 1211-1224.
Dou H O, Xv K P, Meng Q W, Li G, Yang X H. 2014. Potato plants ectopically expressing Arabidopsis thaliana CBF3 exhibit enhanced tolerance to high-temperature stress. Plant, Cell & Environment, 38(1): 61-72.
Eggert A, Wiencke C. 2000. Adaptation and acclimation of growth and photosynthesis of five Antarctic red algae to low temperatures. Polar Biology, 23: 609-618.
Eggert A. 2012. Seaweed responses to temperature. In: Wiencke C, Bischof K eds. Seaweed Biology: Novel Insights into Ecophysiology, Ecology and Utilization. Springer, Berlin, Heidelberg. p.47-66.
Endo T, Mil H, Shikanai T, Asada K. 1997. Donation of electrons to Plastoquinone by NAD(P)H dehydrogenase and by Ferredoxin-Quinone reductase in Spinach chloroplasts. Plant and Cell Physiology, 38(11): 1 272-1 277.
Gao S, Huan L, Lu X P, Jin W H, Wang X L, Wu M J, Wang G C. 2016. Photosynthetic responses of the low intertidal macroalga Sargassum fusiforme (Sargassaceae) to saline stress. Photosynthetica, 54(3): 430-437.
Gao S, Shen S D, Wang G C, Niu J F, Lin A P, Pan G H. 2011. PSI-driven cyclic electron flow allows intertidal macroalgae Ulva sp. (Chlorophyta) to survive in desiccated conditions. Plant and Cell Physiology, 52(5): 885-893.
Gao S, Wang G C. 2012. The enhancement of cyclic electron flow around photosystem I improves the recovery of severely desiccated Porphyra yezoensis (Bangiales, Rhodophyta). Journal of Experimental Botany, 63(12): 4 349-4 358.
González-Mendoza D, Gil F F Y, Escoboza-Garcia F, Santamaría J M, Zapata-Perez O. 2013. Copper stress on photosynthesis of black mangle (Avicennia germinans). Anais Da Academia Brasileira de Ciências, 85(2): 665-670.
Guo Y P, Zhou H F, Zhang L C. 2006. Photosynthetic characteristics and protective mechanisms against photooxidation during high temperature stress in two citrus species. Scientia Horticulturae, 108(3): 260-267.
Huan L, Xie X J, Zheng Z B, Sun F F, Wu S C, Li M Y, Gao S, Gu W H, Wang G C. 2014. Positive correlation between PSI response and oxidative pentose phosphate pathway activity during salt stress in an intertidal macroalga. Plant and Cell Physiology, 55(8): 1 395-1 403.
Huang L J. 2010. Artificial Culture of Gelidium amansii (Lamx.). 2^nd edn. China Ocean Press, Beijing. p.7-123.
Huang W, Hu H. 2015. Effect of growth temperature on the activity of cyclic electron flow in tobacco leaves. Plant Diversity and Resources, 37(3): 283-292. (in Chinese with English abstract)
Huang W, Yang Y J, Hu H, Zhang S B. 2015. Different roles of cyclic electron flow around photosystem I under sub-saturating and saturating light intensities in tobacco leaves. Frontiers in Plant Science, 6: 923.
Huang W, Yang Y J, Zhang S B, Liu T. 2018. Cyclic electron flow around photosystem i promotes ATP synthesis possibly helping the rapid repair of photodamaged photosystem ii at low light. Frontiers in Plant Science, 9: 239.
Huang W, Zhang S B, Cao K F. 2012. Physiological role of cyclic electron flow in higher plants. Plant Science Journal, 30(1): 100-106. (in Chinese with English abstract)
Ibrahim M H, Jaafar H Z E. 2012. Reduced photoinhibition under low irradiance enhanced Kacip Fatimah (Labisia pumila Benth) secondary metabolites, Phenyl alanine lyase and antioxidant activity. International Journal of Molecular Sciences, 13(5): 5 290-5 306.
Johnson G N. 2011. Reprint of: physiology of PSI cyclic electron transport in higher plants. Biochimica et Biophysica Acta (BBA)-Bioenergetics, 1807(8): 906-911.
Kofer W, Koop H U, Wanner G, Steinmüller K. 1998. Mutagenesis of the genes encoding subunits A, C, H, I, J and K of the plastid NAD(P)H-plastoquinone-oxidoreductase in tobacco by polyethylene glycolmediated plastome transformation. Molecular and General Genetics MGG, 258(1-2): 166-173.
Kula M, Kalaji H M, Skoczowski A. 2017. Culture density influence on the photosynthetic efficiency of microalgae growing under different spectral compositions of light. Journal of Photochemistry and Photobiology B: Biology, 167: 290-298.
Kumar Y N, Poong S W, Gachon C, Brodie J, Sade A, Lim P E. 2020. Impact of elevated temperature on the physiological and biochemical responses of Kappaphycus alvarezii (Rhodophyta). PLoS One, 15(9): e0239097.
Kuznetsov V V, Radyukina N L, Shevyakova N I. 2006. Polyamines and stress: biological role, metabolism, and regulation. Russian Journal of Plant Physiology, 53(5): 583.
Larkum A W D, Szabó M, Fitzpatrick D, Raven J A. 2017. Cyclic electron flow in cyanobacteria and eukaryotic algae. In: Barber J, Ruban A V eds. Photosynthesis and Bioenergetics. World Scientific Publishing, Singapore. p.305-343.
Lee T M, Shiu C T. 2009. Implications of mycosporine-like amino acid and antioxidant defenses in UV-B radiation tolerance for the algae species Ptercladiella capillacea and Gelidium amansii. Marine Environmental Research, 67(1): 8-16.
Li H, Liu J G, Zhang L T, Pang T. 2016a. Effects of low temperature stress on the antioxidant system and photosynthetic apparatus of Kappaphycus alvarezii (Rhodophyta, Solieriaceae). Marine Biology Research, 12(10): 1 064-1 077.
Li H, Liu J G, Zhang L T, Pang T. 2016b. Antioxidant responses and photosynthetic behaviors of Kappaphycus alvarezii and Kappaphycus striatum (Rhodophyta, Solieriaceae) during low temperature stress. Botanical Studies, 57: 21.
Li Y F, Liu J G, Zhang L T, Pang T, Qin R Y. 2019. Effects of temperature on the photosynthetic performance in mature thalli of the red alga Gelidium amansii (Gelidiaceae). Aquaculture, 512: 734320.
Li Y F, Liu J G, Zhang L T, Pang T. 2016c. Changes of photosynthetic performances in mature thalli of the red alga Gelidium amansii (Gelidiaceae) exposed to different salinities. Marine Biology Research, 12(6): 631-639.
Mathur S, Agrawal D, Jajoo A. 2014. Photosynthesis: response to high temperature stress. Journal of Photochemistry and Photobiology B: Biology, 137: 116-126.
Mathur S, Allakhverdiev S I, Jajoo A. 2011a. Analysis of high temperature stress on the dynamics of antenna size and reducing side heterogeneity of photosystem II in wheat leaves (Triticum aestivum). Biochimica et Biophysica Acta, 1807(1): 22-29.
Mathur S, Jajoo A, Mehta P, Bharti S. 2011b. Analysis of elevated temperature-induced inhibition of photosystem II using chlorophyll a fluorescence induction kinetics in wheat leaves (Triticum aestivum). Plant Biology, 13(1): 1-6.
Mittler R. 2002. Oxidative stress, antioxidants and stress tolerance. Trends in Plant Science, 7(9): 405-410.
Munekage Y, Hojo M, Meurer J, Endo T, Tasaka M, Shikanai T. 2002. PGR5 is involved in cyclic electron flow around photosystem I and is essential for photoprotection in Arabidopsis. Cell, 110(3): 361-371.
Muraoka R, Okuda K, Kobayashi Y, Shikanai T. 2006. A eukaryotic factor required for accumulation of the chloroplast NAD(P)H dehydrogenase complex in Arabidopsis. Plant Physiology, 142(4): 1 683-1 689.
Naeem M, Traub J R, Athar H U R, Loescher W. 2020. Exogenous calcium mitigates heat stress effects in common bean: a coordinated impact of photoprotection of PSII, up-regulating antioxidants, and carbohydrate metabolism. Acta Physiologiae Plantarum, 42(12): 180.
Niu J F, Feng J H, Xie X J, Gao S, Wang G C. 2016. Involvement of cyclic electron flow in irradiance stress responding and its potential regulation of the mechanisms in Pyropia yezoensis. Chinese Journal of Oceanology and Limnology, 34(4): 730-739.
Price G D. 2011. Inorganic carbon transporters of the cyanobacterial CO₂ concentrating mechanism. Photosynthesis Research, 109(1-3): 47-57.
Sampath-Wiley P, Neefus C D, Jahnke L S. 2008. Seasonal effects of sun exposure and emersion on intertidal seaweed physiology: fluctuations in antioxidant contents, photosynthetic pigments and photosynthetic efficiency in the red alga Porphyra umbilicalis Kützing (Rhodophyta, Bangiales). Journal of Experimental Marine Biology and Ecology, 361(2): 83-91.
Sharkey T D, Schrader S M. 2006. High temperature stress. In: Rao K V M, Raghavendra A S, Reddy K J eds. Physiology and Molecular Biology of Stress Tolerance in Plants. Springer, Dordrecht. p.101-129.
Shikanai T. 2007. Cyclic electron transport around photosystem I: genetic approaches. Annual Review of Plant Biology, 58: 199-217.
Shikanai T. 2016. Regulatory network of proton motive force: contribution of cyclic electron transport around photosystem I. Photosynthesis Research, 129(3): 253-260.
Takahashi S, Milward S E, Fan D Y, Chow W S, Badger M R. 2009. How does cyclic electron flow alleviate photoinhibition in Arabidopsis? Plant Physiology, 149(3): 1 560-1 567.
Teng F, Fang G H, Xu X Q. 2017. Effects of internal tidal dissipation and self-attraction and loading on semidiurnal tides in the Bohai Sea, Yellow Sea and East China Sea: a numerical study. Chinese Journal of Oceanology and Limnology, 35(5): 987-1 001.
Várkonyi Z, Bajkán S, Váradi G, Lehoczki E. 2005. Light response of the chlorophyll fluorescence parameters and partitioning of absorbed light energy in wild type and npq4 mutant of Arabidopsis thaliana. Acta Biologica Szegediensis, 49(1-2): 229-232.
Wang C J, Yamamoto H, Shikanai T. 2015. Role of cyclic electron transport around photosystem I in regulating proton motive force. Biochimica et Biophysica Acta (BBA)-Bioenergetics, 1847(9): 931-938.
Wang P, Duan W, Takabayashi A, Endo T, Shikanai T, Ye J Y, Mi H L. 2006. Chloroplastic NAD(P)H dehydrogenase in tobacco leaves functions in alleviation of oxidative damage caused by temperature stress. Plant Physiology, 141(2): 465-474.
Wang W X, Vinocur B, Shoseyov O, Altman A. 2004. Role of plant heat-shock proteins and molecular chaperones in the abiotic stress response. Trends in Plant Science, 9(5): 244-252.
Xie E Y, Sun Q H. 2018. Cultivation of Gelidium. In: He P M, Zhang Z Y, Zhang X C, Ma J H eds. Seaweed Cultivation. Science Press, Beijing. p.355-380. (in Chinese)
Yamori W, Shikanai T. 2016. Physiological functions of cyclic electron transport around photosystem I in sustaining photosynthesis and plant growth. Annual Review of Plant Biology, 67: 81-106.
Yang X L, Xu H, Li T L, Wang R. 2017. Effects of exogenous melatonin on photosynthesis of tomato leaves under drought stress. Scientia Agricultura Sinica, 50(16): 3 186-3 195. (in Chinese with English abstract)
Yang Y F, Chai Z Y, Wang Q, Chen W Z, He Z L, Jiang S J. 2015. Cultivation of seaweed Gracilaria in Chinese coastal waters and its contribution to environmental improvements. Algal Research, 9: 236-244.
Yin Y, Li S M, Liao W Q, Lu Q T, Wen X G, Lu C M. 2010. Photosystem II photochemistry, photoinhibition, and the xanthophyll cycle in heat-stressed rice leaves. Journal of Plant Physiology, 167(12): 959-966.
Zaneveld J S. 1969. Factors controlling the delimitation of littoral benthic marine algal zonation. American Zoologist, 9(2): 367-391.
Zhang L T, He M L, Liu J G, Li L. 2015. Role of the mitochondrial alternative oxidase pathway in hydrogen photoproduction in Chlorella protothecoides. Planta, 241(4): 1 005-1 014.
Zhang L T, Liu J G. 2016. Effects of heat stress on photosynthetic electron transport in a marine cyanobacterium Arthrospira sp. Journal of Applied Phycology, 28(2): 757-763.
Zhang L T, Su F, Zhang C H, Gong F Y, Liu J G. 2017. Changes of photosynthetic behaviors and photoprotection during cell transformation and astaxanthin accumulation in Haematococcus pluvialis grown outdoors in tubular photobioreactors. International Journal of Molecular Sciences, 18(1): 33.
Zhang L T, Zhang Z S, Gao H Y, Xue Z C, Yang C, Meng X L, Meng Q W. 2011. Mitochondrial alternative oxidase pathway protects plants against photoinhibition by alleviating inhibition of the repair of photodamaged PSII through preventing formation of reactive oxygen species in Rumex K-1 leaves. Physiologia Plantarum, 143(4): 396-407.