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| Wheat PROTON GRADIENT REGULATION 5 is Involved in Tolerance to Photoinhibition |
| WANG Yuan-ge, HE Xue, MA Wen-ying, ZHAO Xue-qiang, LI Bin , TONG Yi-ping |
| The State Key Laboratory for Plant Cell and Chromosome Engineering, Institute of Genetics and Developmental Biology, Chinese Academy of Sciences, Beijing 100101, P.R.China |
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摘要 Wheat (Triticum aestivum L.) often experiences photoinhibition due to strong light during the grain filling stage. As such, increasing the tolerance of wheat to photoinhibition is very desirable in breeding efforts focused on increasing grain yields. Previous reports have suggested that PROTON GRADIENT REGULATION 5 (PGR5) plays a central role in the generation of a proton gradient across the thylakoid membrane (DpH) and in acclimation to high light intensity conditions. Three PGR5 homoeologues were isolated from wheat, and mapped onto chromosomes 7A, 7B and 7D, respectively. The TaPGR5s shared highly similar genomic sequences and gene structures. The transcripts of TaPGR5s were found to be abundantly expressed in the flag leaves, and were transiently up-regulated by treatment with high light. High light treatment inhibited the net photosynthetic rate (Pn) and the maximal quantum yield of photosystem II (Fv/Fm). Further, these inhibitions were more evident in the leaves with reduced expression of TaPGR5s achieved using virus-induced gene silencing methods. Moreover, reducing TaPGR5 expression impaired the induction of non-photochemical quenching (NPQ), which caused more severe cell membrane damage and lipid peroxidation in high light. Additionally, we observed that TaPGR5s transcripts were more abundantly expressed in the wheat genotypes with higher ms-delayed light emission (ms-DLE), a value reflecting transthylakoid DpH. These results suggested that TaPGR5s play important roles in the tolerance of wheat to photoinhibition.
Abstract Wheat (Triticum aestivum L.) often experiences photoinhibition due to strong light during the grain filling stage. As such, increasing the tolerance of wheat to photoinhibition is very desirable in breeding efforts focused on increasing grain yields. Previous reports have suggested that PROTON GRADIENT REGULATION 5 (PGR5) plays a central role in the generation of a proton gradient across the thylakoid membrane (DpH) and in acclimation to high light intensity conditions. Three PGR5 homoeologues were isolated from wheat, and mapped onto chromosomes 7A, 7B and 7D, respectively. The TaPGR5s shared highly similar genomic sequences and gene structures. The transcripts of TaPGR5s were found to be abundantly expressed in the flag leaves, and were transiently up-regulated by treatment with high light. High light treatment inhibited the net photosynthetic rate (Pn) and the maximal quantum yield of photosystem II (Fv/Fm). Further, these inhibitions were more evident in the leaves with reduced expression of TaPGR5s achieved using virus-induced gene silencing methods. Moreover, reducing TaPGR5 expression impaired the induction of non-photochemical quenching (NPQ), which caused more severe cell membrane damage and lipid peroxidation in high light. Additionally, we observed that TaPGR5s transcripts were more abundantly expressed in the wheat genotypes with higher ms-delayed light emission (ms-DLE), a value reflecting transthylakoid DpH. These results suggested that TaPGR5s play important roles in the tolerance of wheat to photoinhibition.
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Received: 09 April 2013
Accepted:
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| Fund: This research was supported by the National Basic Research Program of China (2009CB118302 and 2011CB100304). |
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Corresponding Authors:
TONG Yi-ping, Tel: +86-10-64806556, Fax: +86-10-64807609, E-mail: yptong@genetics.ac.cn
E-mail: yptong@genetics.ac.cn
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Cite this article:
WANG Yuan-ge, HE Xue, MA Wen-ying, ZHAO Xue-qiang, LI Bin , TONG Yi-ping.
2014.
Wheat PROTON GRADIENT REGULATION 5 is Involved in Tolerance to Photoinhibition. Journal of Integrative Agriculture, 13(6): 1206-1215.
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| Aro E M, Suorsa M, Rokka A, Allahverdiyeva Y, Paakkarinen V, Saleem A, Battchikova N, Rintamäki E. 2005. Dynamics of photosystem II: A proteomic approach to thylakoid protein complexes. Journal of Experimental Botany, 56, 347-356 Aro E M, Virgin I, Andersson B. 1993. Photoinhibition of photosystem II: inactivation, protein damage and turnover. Biochimica et Biophysica Acta, 1143, 113-134 Cheng J F, Ma W M, Chen G Y, Hu M J, Shen Y G, Li Z S, Tong Y P, Li B, Li H W. 2009. Dynamic changes of photosynthetic characteristics in Xiaoyan 54, Jing 411, and the stable selected superior strains of their hybrid progenies. Acta Agronomica Sinica, 35, 1051-1058 (in Chinese) Fang J J, Ma W Y, Zhao X Q, He X, Li B, Tong Y P, Li Z S. 2012. Lower canopy temperature is associated with higher cytokinin concentration in the flag leaf of wheat. Crop Science, 52, 2743-2756Field T S, Lee D W, Holbrook N M 2001. Why leaves turn red in autumn? The role of anthocyanins in senescing leaves of red-osier dogwood. Plant Physiology, 127, 566-574 Gould K S, Markham K R, Smith R H, Goris J J 2000. Functional role of anthocyanins in the leaves of Quintinia serrata A. Cunn. Journal of Experimental Botany, 51, 1107-1115 Hakala M, Tuominen I, Keränen M, Tyystjärvi T, Tyystjärvi E. 2005. Evidence for the role of the oxygen-evolving manganese complex in photoinhibition of photosystem II. Biochimica et Biophysica Acta, 1706, 68-80 Kasahara M, Kagawa T, Oikawa K, Suetsugu N, Miyao M, Wada M. 2002. Chloroplast avoidance movementreduces photodamage in plants. Nature, 420, 829-832 Krause G H, Weis E. 1991. Chlorophyll fluorescence and photosynthesis: The basics. Annual Review of Plant Physiology and Plant Molecular Biology, 42, 313-349 Levitt J. 1980. Responses of Plants to Environmental Stresses: Water, Radiation, Salt and Other Stresses. Academic Press, New York. Li X P, Zhao X Q, He X, Zhao G Y, Liu D C, Zhang A M, Zhang X Y, Tong Y P, Li Z S. 2011. Haplotype analysis of the genes encoding glutamine synthetase plastic isoforms and their association with nitrogen-use-and yield-related traits in bread wheat. New Phytologist, 189, 449-458 Livak K J, Schmittgen T D. 2001. Analysis of relative gene expression data using real-time quantitative PCR and the 2-DDCT method. Methods, 25, 402-408 Long T A, Okegawa Y, Shikanai T, Schmidt G W, Covert S F. 2008. Conserved role of PROTON GRADIENT REGULATION 5 in the regulation of PSI cyclic electron transport. Planta, 228, 907-918 Mattoo A K, Edelman M. 1987. Intransmbrane translocation and post-translational palmitoylation of the chloroplast 32-kDa herbicide-binding protein. Proceedings of the National Academy of Sciences of the United States of America, 84, 1497-1501 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, 361-371 Munekage Y N, Genty B, Peltier G. 2008. Effect of PGR5 impairment on photosynthesis and growth in Arabidopsis thaliana. Plant and Cell Physiology, 49, 1688-1698 Murata N, Takahashi S, Nishiyama Y, Allakhverdiev S I. 2007. Photoinhibition of photosystem II under environmental stress. Biochimica et Biophysica Acta, 1767, 414-421 Müller P, Li X P, Niyogi K K. 2001. Non-photochemical quenching. A response to excess light energy. Plant Physiology, 125, 1558-1566 Nishiyama Y, Allakhverdiev S I, Murata N. 2006. A new paradigm for the action of reactive oxygen species in the photoinhibition of photosystem II. Biochimica et Biophysica Acta, 1757, 742-749 Nishiyama Y, Yamamoto H, Allakhverdiev S I, Inaba M, Yokota A, Murata N. 2001. Oxidative stress inhibits the repair of photodamage to the photosynthetic machinery. EMBO Journal, 20, 5587-5594Nishikawa Y, Yamamoto H, Okegawa Y, Wada S, Sato N, Taira Y, Sugimoto K, Makino A, Shikanai T. 2012. PGR5- dependent cyclic electron transport around PSI contributes to the redox homeostasis in chloroplasts rather than CO2 fixation and biomass production in rice. Plant and Cell Physiology, 53, 2117-2126 Niyogi K K. Photoprotection revisited: Genetic and molecular approaches. 1999. Annual Review of Plant Physiology and Plant Molecular Biology, 50, 333-359 Ohad I, Kyle D J, Arntzen C J. 1984. Membrane protein damage and repair: removal and replacement of inactivated 32-kilodalton polypeptides in chloroplast membranes. The Journal of Cell Biology, 99, 481-485 Ohnishi N, Allakhverdiev S I, Takahashi S, Higashi S, Watanabe M, Nishiyama Y, Murata N. 2005. Two-step mechanism of photodamage to photosystem II: Step one occurs at the oxygen-evolving complex and step two occurs at the photochemical reaction center. Biochemistry, 44, 8494-8499 Okegawa Y, Long T A, Iwano M, Takayama S, Kobayashi Y, Covert S F, Shikanai T. 2007. A balanced PGR5 level is required for chloroplast development and optimum operation of cyclic electron transport around photosystem I. Plant and Cell Physiology, 48, 1462-1471 Reynolds M, Foulkes J, Furbank R, Griffiths S, King J, Murchie E, Parry M, Slafer G. 2012. Achieving yield gains in wheat. Plant, Cell and Environment, 35, 1799-1823 Sairam R K. 1994. Effect of moisture stress on physiological activities of two contrasting wheat genotypes. Indian Journal of Experimental Biology, 32, 594-593 Smillie R M, Hetherington S E. 1999. Photoabatement by anthocyanin shields photosynthetic systems from light stress. Photosynthetica, 36, 451-463 Steyn W J, Wand S J E, Holcroft D M, Jacobs G. 2002. Anthocyanins in vegetative tissues: A proposed unified function in photoprotection. New Phytologist, 155, 349- 361. Suorsa M, Järvi S, Grieco M, Nurmi M, Pietrzykowska M, Rantala M, Kangasjärvi S, Paakkarinen V, Tikkanen M, Jansson S, Aro E M. 2012. PROTON GRADIENT REGULATION5 is essential for proper acclimation of Arabidopsis photosystem I to naturally and artificially fluctuating light conditions. The Plant Cell, 24, 2934-2948Takahashi S, Bauwe H, Badger M. 2007. Impairment of the photorespiratory pathway accelerates photoinhibition of photosystem II by suppression of repair process and not acceleration of damage process in Arabidopsis. Plant Physiology, 144, 487-494Takahashi S, Milward S E, Fan D Y, Chow W S, Badger M R. 2009. How does cyclic electron flow alleviate photoinhibitionin Arabidopsis? Plant Physiology, 149, 1560-1567Takahashi S, Murata N. 2008. How do environmental stresses accelerate photoinhibition? Trends in Plant Science, 13, 178-182Tyystjärvi E. 2008. Photoinhibition of photosystem II and photodamage of the oxygen evolving manganese cluster. Coordination Chemistry Reviews, 252, 361-376Wang 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, 465-474 Wang S W, Xu C C, Bai K Z, Zhang Q D, Li L B, Kuang T Y, Li J Y, Li Z S. 2000. Comparative study on photoinhibition between two wheat genotypes. Acta Botanica Sinica, 42, 1300-1303 (in Chinese) Wraight C A, Crofts A R. 1971. Delayed light emission and high energy state of chloroplasts. European Journal of Biochemistry, 19, 386-397 Yang X H, Chen X Y, Ge Q Y, Li B, Tong Y P, Zhang A M, Li Z S, Kuang T Y, Lu C M. 2006. Tolerance of photosynthesis to photoinhibition, high temperature and drought stress in flag leaves of wheat: A comparison between a hybridization line and its parents grown under field conditions. Plant Science, 171, 389-397 Yu F, Tang C Q, Xin Y Y, Peng D C, Li L B, Kuang T Y, Li Z S. 2001. Comparative spectroscopic studies oil the photoinhibition process in photosystem I complex from two wheat cultivars. Acta Botanica Sinica, 43, 1243-1249 (in Chinese) Zhao H B, Guo H J, Zhao L S, Gu J Y, Zhao S R, Li J H, Liu L X. 2011. Agronomic traits and photosynthetic characteristics of chlorophyll-deficient wheat mutant induced by spaceflight environment. Acta Agronomica Sinica, 37, 119-126 (in Chinese) Zhou H B, Li S F, Deng Z Y, Wang X P, Chen T, Zhang J S, Chen S Y, Ling H Q, Zhang A M, Wang D W, Zhang X Q. 2007. Molecular analysis of three new receptor-like kinase genes from hexaploid wheat and evidence for their participation in wheat hypersensitive response to stripe rust fungus infection. The Plant Journal, 52, 420-434 |
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