Photosynthetica 2013, 51(1):33-44 | DOI: 10.1007/s11099-012-0081-z
The effects of enhanced UV-B radiation on photosynthetic and biochemical activities in super-high-yield hybrid rice Liangyoupeijiu at the reproductive stage
- 1 College of Life Sciences, Nanjing Normal University, Nanjing, Jiangsu, China
- 2 Institute of Food & Crops, Jiangsu Academy of Agricultural Sciences, Nanjing, Jiangsu, China
- 3 Shandong Provincial Forest Germplasm Resources Center, Jinan, Shandong, China
- 4 Center of Research & Development, Shenzhen Techand Ecology & Environment Co., LTD., Shenzhen, Guangdong, China
We investigated the light reactions, CO2 assimilation, but also the chloroplast ultrastructure in the upper three functional leaves (flag, 2nd, and 3rd leaves) of the Chinese super-high-yield hybrid rice (Oryza sativa L.) Liangyoupeijiu (LYPJ) with ultraviolet-B (UV-B) treatment during reproductive development. Photosynthetic parameters showed that the upper 3 functional leaves of LYPJ entered into senescence approximately 15 days after flag leaf emergence (DAE). Leaves in UV-B treatment exhibited greater efficiency in absorbing and utilizing light energy of photosystem II (PSII), characterized by higher chlorophyll (Chl) content and the whole chain electron transport rate (ETR). However, UV-B radiation reduced activities of Ca2+-ATPase and photophosphorylation. The significantly decreased activity of ribulose-1,5-bisphosphate carboxylase/oxygenase (Rubisco) was greatly associated with the decline in photosynthetic efficiency. The net photosynthetic rate (P N) and stomatal conductance (g s) suffered strong reductions before 25 DAE, and afterwards showed no significant difference between control and treatment. UV-B treatment delayed chloroplasts development of flag leaves. Chloroplast membranes later swelled and disintegrated, and more stromal thylakoids were parallel to each other and were arranged in neat rows, which might be responsible for better performance of the primary light reaction. It is likely that accumulation of starch and an increase in the number of lipid droplet and translucent plastoglobuli were results of an inhibition of carbohydrate transport. Our results suggest that long-term exposure to enhanced UV-B radiation was unlikely to have detrimental effects on the absorption flux of photons and the transport of electrons, but it resulted in the decrease of photophosphorylation and Rubisco activation of LYPJ. The extent of the damage to the chloroplast ultrastructure was consistent with the degree of the inhibition of photosynthesis.
Keywords: chloroplast ultrastructure; gas exchange; light reaction; photosynthesis; Rubisco; UV-B radiation.
Received: October 12, 2011; Accepted: September 24, 2012; Published: March 1, 2013Show citation
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References
- Albert, K.R., Mikkelsen, T.N., Ro-Poulsen, H.: Effects of ambient versus reduced UV-B radiation on high arctic Salix arctica assessed by measurements and calculations of chlorophyll a fluorescence parameters from fluorescence transients. - Plant Physiol. 124: 208-226, 2005. Go to original source...
- Allen, D.J., Nogués, S., Morison, J.I.L. et al.: A thirty percent increase in UV-B has no impact on photosynthesis in well watered and droughted pea plants in the field. - Global Change Biol. 5: 235-244, 1999. Go to original source...
- Ambasht, N.K., Agrawal, M.: Influence of supplemental UV-B radiation on photosynthetic characteristics of rice plants. - Photosynthetica 34: 401-408, 1997. Go to original source...
- Appenroth, K.J., Stöckel, J., Srivastava, A., Strasser, R.J.: Multiple effects of chromate on the photosynthetic apparatus of Spirodela polyrhiza as probed by O-J-I-P chlorophyll a fluorescence measurements. - Environ. Pollut. 115: 49-64, 2001. Go to original source...
- Arnon, D.I.: Copper enzymes in isolated chloroplasts, polyphenol oxidase in Beta vulgaris. - Plant Physiol. 24: 1-15, 1949. Go to original source...
- Ashida, H., Danchin, A., Yokota, A.: Was photosynthetic Rubisco recruited by acquisitive evolution from Rubisco like proteins involved in sulfur metabolism? - Res. Microbiol. 156: 611-618, 2005. Go to original source...
- Babu, T.S., Jansen, M.A.K., Greenberg, B.M. et al.: Amplified degradation of photosystem II D1 and D2 proteins under a mixture of photosynthetically active radiation and UV-B radiation: dependence on redox status of photosystem II. - Photochem. Photobiol. 69: 553-559, 1999. Go to original source...
- Chen, G.-X., Liu, S.-H., Zhang, C.J., Lu, C.G.: Effects of drought on photosynthetic characteristics of flag leaves of a newly-developed super-high-yield rice hybrid. - Photosynthetica 42: 573-578, 2004. Go to original source...
- Coombs, J., Hind, G., Leegood, R.C.: Photosynthetic energy conversion. - In Coombs, J., Hall, D.O., Long, S.P., Scurlock, J.M.O. (ed.): Techniques in Bioproductivity and Photosynthesis. Pp. 136-137. Pergamon Press Publishing, New York 1985.
- Desimone, M., Henke, A., Wagner, E.: Oxidative stress induces partial degradation of the large subunit of ribulose-1,5-bisphosphate carboxylase/oxygenase in isolated chloroplasts of barley. - Plant Physiol. 111: 789-796, 1996. Go to original source...
- Desimone, M., Wagner, E., Johanningmeier, U.: Degradation of active-oxygen-modified ribulose-1,5-bisphosphate carboxylase/oxygenase by chloroplastic proteases requires ATPhydrolysis. - Planta 205: 459-466, 1998. Go to original source...
- Dunahay, T.G., Staehelin, L.A., Seibert, M.: Structural, biochemical and biophysical characterization of four oxygen evolving photosystem II preparations from spinach. - Biochim. Biophys. Acta 764: 179-193, 1984. Go to original source...
- Erickson, D.J., Zepp, R.G., Atlas, E.: Ozone depletion and the air sea exchange of greenhouse and chemically reactive trace gases. - Chemosphere: Global Change Sci. 2: 137-149, 2000. Go to original source...
- Famiani, F., Walker, R.P., Tecsi, L., Chen, Z.H., Proietti, P., Leegood, R.C.: An immunohistochemical study of the compartmentation of metabolism during the development of grape (Vitis vinifera L.) berries. - J. Exp. Bot. 51: 675-683, 2000.
- Fedina, I., Hidema, J., Velitchkova, M. et al.: UV-B induced stress responses in three rice cultivars. - Biol. Plant. 54: 571-574, 2010. Go to original source...
- Flint, S.D., Caldwell, M.M.: A biological spectral weighting function for ozone depletion research with higher plants. - Plant Physiol. 117: 137-144, 2003. Go to original source...
- Gerhardt, K.E., Wilson, M.I., Greenberge, B.M.: Tryptophan photolysis leads to a UV-B induced 66kDa photoproduct of ribulose-1, 5-bisphosphate carboxylase/oxygenase (Rubisco) in vitro and in vivo. - Photochem. Photobiol. 70: 49-56, 1999.
- Guidi, L.D.E., Soldatini, G.F.: Assimilation of CO2, enzyme activation and photosynthetic electron transport in bean leaves, as affected by high light and ozone. - New Phytol. 156: 377-388, 2002. Go to original source...
- Hada, H., Hidema, J., Maekawa, M., Kumagai, T.: Higher amounts of anthocyanins and UV-absorbing compounds effectively lowered CPD photorepair in purple rice (Oryza sativa L.). - Plant Cell Environ. 26: 1691-1701, 2003. Go to original source...
- Hidema, J., Kumagai, T.: Sensitivity of Rice to Ultraviolet-B Radiation. - Ann. Bot. 97: 933-942, 2006. Go to original source...
- Hidema, J., Zhang, W.-.H., Yamamoto, M., Sato, T., Kumagai, T. Changes in grain size and grain storage protein of rice (Oryza sativa L.) in response to elevated UV-B radiation under outdoor conditions. - J. Radiat. Res. 46: 143-149, 2005. Go to original source...
- Hirouchi, T., Nakajima, S., Najrana, T., Tanaka, M., Matsunaga, T., Hidema, J., Teranishi, M., Fujino, T., Kumagai, T., Yamamoto, K.: A gene for a Class II DNA photolyase from Oryza sativa: cloning of the cDNA by dilution-amplification. - Mol. Genet. Genomics 269: 508-516, 2003. Go to original source...
- Hofmann, R.W., Campbell, B.D., Fountain, D.W. et al.: Multivariate analysis of intraspecific responses to UV-B radiation in white clover (Trifolium repens L.). - Plant Cell Environ. 24: 917-927, 2001. Go to original source...
- Huang, L.-K., He, J., Chow, W. S. et al.: Responses of detached rice leaves to moderate supplementary ultraviolet-B radiation allow early screening for relative sensitivity to ultraviolet-B irradiation. - Aust. J. Plant Physiol. 20: 285-297, 1993. Go to original source...
- Jordan, B.R., He, J., Chow, W.S.: Changes in mRNA levels and polypeptide subunits of ribulose-1,5-bisphosphate carboxylase in response to supplementary UV-B radiation. - Plant Cell Environ. 15: 91-98, 1992. Go to original source...
- Jiang, Z.-X., Huang, Z.-Q., Meng, Y.-H.: Quantitative relationship between the quality of big seedlings and the source and sink of population at seed setting stages in middle hybrid rice. - Acta Agron. Sin. 28: 65-68, 2002. [In Chin.]
- Kakani, V.G., Reddy, K.R., Zhao, D. Sailaja, K.: Field crop responses to ultraviolet-B radiation: a review. - Agric. For. Meteorol. 120: 191-218, 2003. Go to original source...
- Ketcham, S.R., Davenport, J.W., Warncke, K.: Role of the γ subunit of Chloroplast coupling factor 1 in the lightdependent activation of phosphosphorylation and ATPase activity by dithiothreitol. - J. Biol. Chem. 259: 7286-7293, 1984.
- Kim, H.Y., Kobayashi, K., Nouchi, I., Yoneyama, T.: Enhanced UV-B radiation has little effects on growth, delta 13C values and pigments of pot-grown rice (Oryza sativa) in the field. - Plant Physiol. 96: 1-5, 1996. Go to original source...
- Kolb, C.A., Käser, M.A., Kopecký, J. et al.: Effects of natural intensities of visible and ultraviolet radiation on epidermal ultraviolet screening and photosynthesis in grape leaves. - Plant Physiol. 127: 863-875, 2001. Go to original source...
- Kumagai, T., Hidema, J., Kang, H.S., Sato, T.: Effects of supplemental UV-B radiation on the growth and yield of two cultivars of Japanese lowland rice (Oryza sativa L.) under the field in a cool rice-growing region of Japan. - Agr. Ecosyst. Environ. 83: 201-208, 2001. Go to original source...
- Ladygin, V.G.: Photosystem damage and spatial architecture of thylakoids in chloroplasts of pea chlorophyll mutants. - Biol. Bull. 31: 268-76, 2004. Go to original source...
- Lidon, F.C., Ramalho, J. C.: Impact of UV-B irradiation on photosynthetic performance and chloroplast membrane components in Oryza sativa L. - J. Photochem. Photobiol. B 104: 457-466, 2011. Go to original source...
- Li, P.-M., Gao, H.-Y., Strasser, R.J.: Application of the fast chlorophyll fluorescence induction dynamics analysis in photosynthesis study. - J. Plant Physiol. Mol. Biol. 31: 559-566, 2005.
- Liu, M., Li, R.-G, Fan, H., Du, G.-C.: Effects of enhanced UV-B radiation on photosynthetic pigments and some enzymes in tobacco. - Acta Bot. Bor-Occid. Sin. 27: 291-296, 2007. [In Chin.]
- Makino, A., Mae, T., Ohira, K.: Photosynthesis and ribulose- 1,5-bisphosphate carboxylase/oxygenase in rice leaves from emergence through senescence. Quantitative analysis by carboxylation/oxygenation and regeneration of ribulose-1,5-bisphosphate. - Planta 166: 414-420, 1985. Go to original source...
- Mazza, C.A., Battista, D., Zima, A.M., Szwarcberg-Bracchitta M., Giordano, C.V., Acevedo, A., Scopel, A.L., Ballare, C.L.: The effects of solar ultraviolet-B radiation on the growth and yield of barley are accompanied by increased DNA damage and antioxidant responses. - Plant Cell Environ. 22: 61-70, 1999. Go to original source...
- Normile, D.: Agriculture: Variety spices up Chinese rice yields. - Science 289: 1122-1123, 2000. Go to original source...
- Ranjbarfordoei, A., Samson, R., and Damme, P.V.: Photosynthesis performance in sweet almond [Prunus dulcis (Mill) D. Webb] exposed to supplemental UV-B radiation. - Photosynthetica 49: 107-111, 2011. Go to original source...
- Rech, M., Mouget, J.L., Morant-Manceau, A., Rosa, P., Tremblin, G.: Long-term acclimation to UV radiation: effects on growth, photosynthesis and carbonic anhydrase activity in marine diatoms. - Bot. Mar. 48: 407-420, 2005. Go to original source...
- Ren, J., Yao, Y.-A., Yang, Y.-Q, Korpelaninen, H., Junttila, O., Li, C.-Y.: Growth and physiological responses to supplemental UV-B radiation of two contrasting poplar species. - Tree Physiol. 26: 665-672, 2006. Go to original source...
- Ruggaber, A., Dlugi, R., Nakajima, T.: Modelling of radiation quantities and photolysis frequencies in the troposphere. - J. Atmos. Chem. 18:171-210, 1994. Go to original source...
- Ruhland, C.T., Xiong, F.S, Clark, W.D., Day, T.A.: The influence of ultraviolet-B radiation on growth, hydroxycinnamic acids and flavonoids of Deschampsia antarctica during springtime ozone depletion in Antarctica. - Photochem. Photobiol. 81: 1086-1093, 2005. Go to original source...
- Sato, T., Kang, H.-S., Kumagai, T.: Genetic study of resistance to inhibitory effects of UV radiation in rice (Oryza sativa L.). - Physiol. Plant. 91: 234-238, 1994. Go to original source...
- Sato, T., Ueda, T., Fukuta, Y., Kumagai, T., Yano, M.: Mapping of quantitative trait loci associated with ultraviolet-B resistance in rice (Oryza sativa L.). - Theor. Appl. Genet. 107: 1003-1008, 2003. Go to original source...
- Sayre, R.T., Kennedy, R,A.: Photosynthetic enzyme activities and localization in Mollugo veticillata populations differing in the levels of C3 and C4 cycle operation. - Plant Physiol. 64: 293-299, 1979. Go to original source...
- Strasser, R.J., Srivastava, A., Tsimilli-Michael, M.: The fluorescence transient as a tool to characterize and screen photosynthetic samples. - In: Yunus, M., Pathre, U., Mohanty, P. (ed.): Probing Photosynthesis: Mechanism, Regulation and Adaptation. Pp. 445-483. Taylor & Francis Press Publishing, London 2000.
- Strasser, R.J., Tsimill-Michael, M., Srivastava, A.: Analysis of the chlorophyll a fluorescence transient. - In: Papageorgiou, G.C., Govindjee (ed.): Advances in Photosynthesis and Respiration. Pp.1-47. KAP Press Publishing, Dordrecht 2004. Go to original source...
- Takeuchi, A., Yamaguchi, T., Hidema, J., Strid, A., Kumagai, T.: Changes in synthesis and degradation of Rubisco and LHCII with leaf age in rice (Oryza sativa L.) growing under supplementary UV-B radiation. - Plant Cell Environ. 25: 695-706, 2002. Go to original source...
- Teramura, A. H., Ziska, L. H., Sztein, A. E.: Changes in growth and photosynthetic capacity of rice with increased UV-B radiation. - Plant Physiol. 83: 373-380, 1991. Go to original source...
- Teranishi, M., Iwamatsu, Y., Hidema, J., Kumagai, T.: Ultraviolet-B sensitivities in Japanese lowland rice cultivars: cyclobutane pyrimidine dimer photolyase activity and gene mutation. - Plant Cell Physiol. 45: 1845-1856, 2004.
- UNEP, Executive Summary. Final of UNEP/WMO scientific assessment of ozone depletion: 2002. Prepared by scientific assessment panel of the montreal protocol on substances that deplete the ozone layer (Released by WMO/UNEP on 23 August 2002).
- Vallejos, R.H., Arana, J.L., Ravizzini, R.A.: Changes in activity and structure of the chloroplast proton ATPase induced by illumination of spinach leaves. - J. Biol. Chem. 258: 7317-7321, 1983.
- Van Heerden, P.D.R., Strasser, R.J., Krüger, G.H.J.: Reduction of dark chilling stress in N2-fixing soybean by nitrate as indicated by chlorophyll a fluorescence kinetics. - Plant Physiol. 121: 239-249, 2004. Go to original source...
- Wang, Q., Zhang, Q.-D, Lu, C.-M. et al.: Pigments content, net photosynthesis rate and water use efficiency of super highyield rice hybrids at different developmental stages. - Chin. J. Plant Ecol. 26: 647-651, 2002. [In Chin.] Go to original source...
- Wei, J.-M., Wang, D.-F., Shi, X.-B., Shen, Y.-G.: Structure and function of ATP synthase. - In: Kuang, T.-Y. (ed.): Mechanism and Regulation of Primary Energy Conversion Process in Photosynthesis. Pp.330-357. Jiangsu Sci. Technol. Press Publishing, Nanjing 2003. [In Chin.]
- Wilson, M.I., Greenberg, B.M.: Protection of the D1 photosystem II reaction center protein from degradation in ultraviolet radiation following adaptation of Brassica napus L. to growth in ultraviolet-B. - Photochem. Photobiol. 57: 556-563, 1993. Go to original source...
- Wu, X.-C., Fang, C.-X., Chen, J.-Y. et al.: A proteomic analysis of leaf responses to enhanced ultraviolet-B radiation in two rice (Oryza sativa L.) cultivars differing in UV sensitivity. - J. Plant Biol. 54: 251-261, 2011. Go to original source...
- Xiong, F.-S., Day, T.-A.: Effect of solar ultraviolet-B radiation during springtime ozone depletion on photosynthesis and biomass production of Antarctic vascular plants. - Plant Physiol. 125: 738-751, 2001. Go to original source...
- Xu, K., Qiu, B.-S.: Responses of super-high-yield hybrid rice Liangyoupeijiu to enhancement of ultraviolet-B radiation. - Plant Sci. 172: 139-149, 2007. Go to original source...
- Xu, Y., Yin, H., Mao, X.-Y.: Studies on the effects of enhanced UV-B radiation on growth and production of rice. - Chin. Agr. Sci. Bull. 22: 411-414, 2006. [In Chin.]
- Yang, C.-W., Lin, G.-Z., Peng, C.-L. et al.: Changes in the activities of C4 pathway enzymes and stable carbon isotope discrimination in flag leaves of super-high-yield hybrid rice. - Acta Bot. Sin. 45: 1261-1265, 2003. [In Chin.]
- Yoshida, S.: Physiological analysis of rice yield. - In: Yoshida, S. (ed.): Fundamentals of rice crop science. Pp. 231-251. Int. Rice Res. Inst. Publishing, Wallingford 1981.
- Yu, G.-H., Chen, G.-X., Jiang, Y.-Z. et al.: Light Reaction Characteristics in functional leaves of Liangyoupeijiu in the reproductive growth stage. - Acta Agron. Sin. 36: 1959-1966, 2010. [In Chin.]
- Zhang, C.-J., Chu, C.-J., Chen, G.-X. et al.: Photosynthetic and biochemical activities in flag leaves of a newly developed super-high-yield hybrid rice (Oryza sativa) and its parents during the reproductive stage. - J. Plant Res. 120: 209-217, 2007. Go to original source...
- Zhang, F.-C., He, Y.-H., Zheng, Y.-F., Wang, C.-H.: Effect of enhanced UV-B radiation on wheat. - J. Nanjing Inst. Meteorol. 26: 545-551, 2003. [In Chin.]
- Zhang, M.-P., Zhang, C.-J., Yu, G.-H. et al.: Changes in chloroplast ultrastructure, fatty acid components of thylakoid membrane and chlorophyll a fluorescence transient in flag leaves of a super-high-yield hybrid rice and its parents during the reproductive stage. - J. Plant Physiol. 167: 277-285, 2010. Go to original source...