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Analysis of thylakoid membrane protein and photosynthesis-related key enzymes in super high-yield hybrid rice LYPJ grown in field condition during senescence stage

Abstract

A proteomic analysis combining photosynthesis-related key enzymes measurement and mRNA level analysis was used to investigate the variations of proteins involved in the photosynthetic apparatus in flag leaves of high-yield rice LYPJ during senescence under field conditions. The stability of chlorophyll-protein complexes of thylakoid membranes was measured by BN-PAGE system. Our findings revealed that the LHCII complexes were more stable than F0F1-ATPase and Cyb 6 /f complexes. Thylakoid membranes proteins during the senescence stage were separated by two-dimensional gel electrophoresis. We identified 13 photosynthesis-related proteins (a fivefold or greater variation), including electron transport, Calvin–Benson cycle and chloroplast protease during senescence of flag leaves. Moreover, our data showed that Ca2+-ATPase was more stable during senescence of flag leaves in rice, compared to Mg2+-ATPase. In enzymes activities analyses, it was observed that a little increment of C4 photosynthetic enzymes activities at the beginning of flag leaves senescence might compensate, to some degree, for the larger reductions in Rubisco activity, confirmed by quantitative RT-PCR analysis.

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References

  • Bate NJ, Rothstein SJ, Thompson JE (1991) Expression of nuclear and chloroplast photosynthesis specific genes during leaf senescence. J Exp Bot 42:801–811

    Article  CAS  Google Scholar 

  • Bertamini M, Nedunchezhian N (2002) Leaf age effects on chlorophyll, Rubisco, photosynthetic electron transport activities and thylakoid membrane protein in field grown grapevine leaves. J Plant Physiol 159:799–803

    Article  CAS  Google Scholar 

  • Bradford MM (1976) A rapid and sensitive method for the quantization of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254

    Article  CAS  PubMed  Google Scholar 

  • Brady CJ (1981) A coordinated decline in the synthesis of subunits of Ribulosebisphosphate carboxylase in aging wheat leaves. I. Analysis of isolated protein, subunits and ribosomes. Aust J Plant Physiol 8:591–602

    Article  CAS  Google Scholar 

  • Crafts-Brandner SJ, Salvucci ME, Egli DB (1990) Changes in ribulosebisphosphate carboxylase/oxygenase and ribulosebisphosphate 5-phosphate kinase abundances and photosynthetic capacity during leaf senescence. Photosynth Res 23:223–230

    Article  CAS  PubMed  Google Scholar 

  • Crecelius F, Streb P, Feierabend J (2003) Malate metabolism and reactions of oxidoreduction in cold-hardened winter rye (Secale cereale L.) leaves. J Exp Bot 54:1075–1083

    Article  CAS  PubMed  Google Scholar 

  • Doubnerová V, Ryšlavá H (2011) What can enzymes of C4 photosynthesis do for C3 plants under stress? Plant Sci 180:575–583

    Article  PubMed  Google Scholar 

  • Doubnerová V, Jirásková A, Janosková M, Müller K, Bat’ková P, Synková H, Cerovská N, Ryslavá H (2007) The activity and isoforms of NADP-malic enzyme in Nicotiana benthamiana plants under biotic stress. Gen Physiol Biophys 26:281–289

    PubMed  Google Scholar 

  • Doubnerová V, Miedzińska L, Dobrá J, Vankova R, Ryšlavá H (2014) Phosphoenolpyruvate carboxylase, NADP-malic enzyme, and pyruvate, phosphate dikinase are involved in the acclimation of Nicotiana tabacum L. to drought stress. J Plant Physiol 171:19–25

    Article  Google Scholar 

  • Evans IM, Rus AM, Belanger EM, Kimoto M, Brusslan JA (2010) Dismantling of Arabidopsis thaliana mesophyll cell chloroplasts during natural leaf senescence. Plant Biol 12:1–12

    Article  CAS  PubMed  Google Scholar 

  • Ferguson DL, Al-khatib K, Guikema JA, Paulsen GM (1993) Degradation of proteins from thylakoid membranes in senescing wheat leaves at high temperature. Plant Cell Environ 16:421–428

    Article  CAS  Google Scholar 

  • Ghosh S, Mahoney SR, Penterman JN, Peirson D, Dumbroff EB (2001) Ultrastructural and biochemical changes in chloroplasts during Brassica napus senescence. Plant Physiol Biochem 39:777–784

    Article  CAS  Google Scholar 

  • Gregersen PL, Holm PB, Krupinska K (2008) Leaf senescence and nutrient remobilisation in barley and wheat. Plant Biol 10:37–49

    Article  CAS  PubMed  Google Scholar 

  • Guha A, Sengupta D, Reddy AR (2013) Polyphasic chlorophyll a fluorescence kinetics and leaf protein analyses to track dynamics of photosynthetic performance in mulberry during progressive drought. J Photochem Photobiol B 119:71–83

    Article  CAS  PubMed  Google Scholar 

  • Hao L, Wang Y, Zhang J, Xie Y, Zhang M, Duan L, Li Z (2013) Coronatine enhances drought tolerance via improving antioxidative capacity to maintaining higher photosynthetic performance in soybean. Plant Sci 210:1–9

    Article  CAS  PubMed  Google Scholar 

  • Hojka M, Thiele W, Tóth SZ, Lein W, Bock R, Schöttler MA (2014) Inducible repression of nuclear-encoded subunits of the cytochrome b6f complex in tobacco reveals an extraordinarily long lifetime of the complex. Plant Physiol 165:1632–1646

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Humbeck K, Krupinska K (2003) The abundance of minor chlorophyll a/b-binding proteins CP29 and LHCI of barley (Hordeum vulgare L.) during leaf senescence is controlled by light. J Exp Bot 54:375–383

    Article  CAS  PubMed  Google Scholar 

  • Humbeck K, Quast S, Krupinska K (1996) Functional and molecular changes in the photosynthetic apparatus during senescence of flag leaves from field-grown barley plants. Plant Cell Environ 19:337–344

    Article  CAS  Google Scholar 

  • Johnson HS, Hatch MD (1970) Properties and regulation of leaf NADP malate dehydrogenase and malic enzyme in plants with C4-carboxylic pathway of photosynthesis. Biochem J 119:273–280

    PubMed Central  CAS  PubMed  Google Scholar 

  • Kang K, Kim YS, Park S, Back K (2009) Evaluation of light-harvesting complex proteins as senescence-related protein markers in detached rice leaves. Photosynthetica 47:638–640

    Article  CAS  Google Scholar 

  • Komenda J, Knoppová J, Krynická V, Nixon PJ, Tichý M (2010) Role of FtsH2 in the repair of Photosystem II in mutants of the cyanobacterium Synechocystis PCC 6803 with impaired assembly or stability of the Ca Mn (4) cluster. Biochim Biophys Acta 1797:566–575

    Article  CAS  PubMed  Google Scholar 

  • Krupinska K, Mulisch M, Hollmann J, Tokarz K, Zschiesche W, Kage H, Humbeck K, Bilger W (2012) An alternative strategy of dismantling of the chloroplasts during leaf senescence observed in a high-yield variety of barley. Physiol Plant 144:189–200

    Article  CAS  PubMed  Google Scholar 

  • Kügler M, Jänsch L, Kruft V, Schmitz UK, Braun HP (1997) Analysis of the chloroplast protein complexes by blue-native polyacrylamide gel electrophoresis (BN-PAGE). Photosynthesis Res 53:35–44

    Article  Google Scholar 

  • Lu QT, Lu CM, Zhang JH, Kuang TY (2002) Photosynthesis and chlorophyll a fluorescence during flag leaf senescence of field-grown wheat plants. J Plant Physiol 159:1173–1178

    Article  CAS  Google Scholar 

  • Lu QT, Wen XG, Lu CM, Zhang QD, Kuang TY (2003) Photoinhibition and photoprotection in senescent leaves of field-grown wheat plants. Plant Physiol Biochem 41:749–754

    Article  CAS  Google Scholar 

  • Martínez DE, Costa ML, Guiamet JJ (2008) Senescence-associated degradation of chloroplast proteins inside and outside the organelle. Plant Biol 10:15–22

    Article  PubMed  Google Scholar 

  • Nilo-Poyanco R, Olivares D, Orellana A, Hinrichsen P, Pinto M (2013) Proteomic analysis of grapevine (Vitis vinifera L.) leaf changes induced by transition to autotrophy and exposure to high light irradiance. J Proteomics 91:309–330

    Article  CAS  PubMed  Google Scholar 

  • Roberts DR, Thompson JE, Dumbroff EB, Gepstein S, Mattoo AK (1987) Differential changes in the synthesis and steady-state levels of thylakoid proteins during bean leaf senescence. Plant Mol Biol 9:343–353

    Article  CAS  PubMed  Google Scholar 

  • Ryslava H, Muller K, Semoradova S, Synkova H, Cerovska N (2003) Photosynthesis and activity of phosphoenolpyruvate carboxylase in Nicotiana tabacum L. leaves infected by Potato virus A and Potato virus Y. Photosynthetica 41:357–363

    Article  CAS  Google Scholar 

  • Sayeed SA, Behera BK, Mohanty P (1985) Interaction of light quality and benzimidazole on pigment contents and on photochemical activity of chloroplasts isolated from detached senescing wheat (Triticum aestivum) leaves. Physiol Plant 64:383–388

    Article  CAS  Google Scholar 

  • Schiltz S, Gallardo K, Huart M, Negroni L, Sommerer N, Burstin J (2004) Proteome reference maps of vegetative tissues in pea. An investigation of nitrogen mobilization from leaves during seed filling. Plant Physiol 135:2241–2260

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Shao J, Zhang Y, Yu J, Guo L, Ding Y (2011) Isolation of thylakoid membrane complexes from rice by a new double-strip BN/SDS-PAGE and bioinformatics prediction of stromal ridge subunits interaction. PLoS One 6:e20342

    Article  PubMed Central  CAS  PubMed  Google Scholar 

  • Smeets K, Cuypers A, Lambrechts A, Semane B, Hoet P, Van Laere A, Vangronsveld J (2005) Induction of oxidative stress and antioxidative mechanisms in Phaseolus vulgaris after Cd application. Plant Physiol Biochem 43:437–444

    Article  CAS  PubMed  Google Scholar 

  • Sobhanian H, Aghaei K, Komatsu S (2011) Changes in the plant proteome resulting form salt stress: toward the creation of salt-tolerant crops? J Proteomics 74:1323–1337

    Article  CAS  PubMed  Google Scholar 

  • Soussi M, Ocana A, Lluch C (1998) Effects of salt stress on growth, photosynthesis and nitrogen fixation in chick-pea (Cicer arietinum L.). J Exp Bot 49:1329–1337

    Article  CAS  Google Scholar 

  • Tang YL, Wen XG, Lu CM (2005) Differential changes in degradation of chlorophyll-protein complexes of photosystem I and photosystem II during flag leaf senescence of rice. Plant Physiol Biochem 43:193–201

    Article  CAS  PubMed  Google Scholar 

  • Wu XY, Kuai BK, Jia JZ, Jing HC (2012) Regulation of leaf senescence and crop genetic improvement. J Integr Plant Biol 54:936–952

    Article  CAS  PubMed  Google Scholar 

  • Yang XH, Chen XY, Ge QY, Li B, Tong YP, Li ZS, Kuang TY, Lu CM (2007) Characterization of photosynthesis of flag leaves in a wheat hybrid and its parents grown under field conditions. J Plant Physiol 164:318–326

    Article  CAS  PubMed  Google Scholar 

  • Zhang A, Lu Q, Yin Y, Ding S, Wen X, Lu C (2010) Comparative proteomic analysis provides new insights into the regulation of carbon metabolism during leaf senescence of rice grown under field conditions. J Plant Physiol 167:1380–1389

    Article  CAS  PubMed  Google Scholar 

  • Zheng CF, Jiang D, Liu FL, Dai TB, Jing Q, Cao WX (2009) Effects of salt and waterlogging stresses and their combination on leaf photosynthesis, chloroplast ATP synthesis, and antioxidant capacity in wheat. Plant Sci 176:575–582

    Article  CAS  Google Scholar 

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Acknowledgments

This research was supported by the National Natural Science Foundation of China (No. 31271621), Natural Science Foundation of Jiangsu Province, China (No. 11KJA180001), the Priority Academic Program Development of Jiangsu Higher Education Institutions (PAPD) and NSFC for Talents Training in Basic Science (J1103507, J1210025).

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Correspondence to Guoxiang Chen.

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Communicated by J. Gao.

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Wang, Y., Yu, J., Jiang, X. et al. Analysis of thylakoid membrane protein and photosynthesis-related key enzymes in super high-yield hybrid rice LYPJ grown in field condition during senescence stage. Acta Physiol Plant 37, 1 (2015). https://doi.org/10.1007/s11738-014-1746-y

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  • DOI: https://doi.org/10.1007/s11738-014-1746-y

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