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Journal of Integrative Agriculture  2016, Vol. 15 Issue (05): 1005-1016    DOI: 10.1016/S2095-3119(15)61163-7
Physiology·Biochemistry·Cultivation·Tillage Advanced Online Publication | Current Issue | Archive | Adv Search |
Comparative proteomic analysis provides new insights into ear leaf senescence of summer maize (Zea mays L.) under fild condition
WEI Shan-shan*, WANG Xiang-yu*, LIU Peng, ZHANG Ji-wang, ZHAO Bin, DONG Shu-ting  
State Key Laboratory of Crop Biology/National Engineering Laboratory for Efficient Utilization of Soil and Fertilizer Resources/ College of Agronomy, Shandong Agricultural University, Tai’an 271018, P.R.China
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Abstract  As the most important organ in plant photosynthesis, the leaf plays an important role in plant growth and development. Leaf senescence is associated with fundamental changes in the proteome. To research the molecular mechanisms of leaf senescence, protein expression in senescing maize ear leaves grown under field conditions was analyzed using two-dimensional gel electrophoresis and matrix-assisted laser desorption/ionisation time-of-flight/time-of-flight mass spectrometry (MALDI-TOF/TOF MS). A total of 60 senescence-associated proteins were identified. The identified proteins are involved in many biological processes, especially energy, metabolism and protein synthesis. Several of the identified proteins have not been previously reported as senescence-associated, including glycine-rich RNA-binding protein.
Keywords:  maize (Zea mays L.)        ear leaf        proteomics       senescence  
Received: 07 May 2015   Accepted: 03 May 2016

We acknowledge financial supports from the National Natural Science Foundation of China (31171497), the National Basic Research Program of China (973 Program, 2011CB100105), the Corn Industry Technology System, Ministry of Agriculture, China (CARS-02) and the Special Fund for Agro-scientific Research in the Public Interest, China (201203096, 201203100).

Corresponding Authors:  DONG Shu-ting, Tel/Fax: +86-538-8245838, E-mail:    
About author:  WEI Shan-shan, E-mail:; WANG Xiang-yu, E-mail: * These authors contributed equally to this study

Cite this article: 

WEI Shan-shan, WANG Xiang-yu, LIU Peng, ZHANG Ji-wang, ZHAO Bin, DONG Shu-ting. 2016. Comparative proteomic analysis provides new insights into ear leaf senescence of summer maize (Zea mays L.) under fild condition. Journal of Integrative Agriculture, 15(05): 1005-1016.

Amiour N, Imbaud S, Clément G, Agier N, Zivy M, Valot B, Balliau T, Armengaud P, Quilleré I, Caňas R, Tercet-Laforgue T, Hirel B. 2012. The use of metabolomics integrated with transcriptomic and proteomic studies for identifying key steps involved in the control of nitrogen metabolism in crops such as maize. Journal of Experimental Botany, 63, 5017–5033.

Amunts A, Toporik H, Borovikova A, Nelson N. 2010. Structure determination and improved model of plant photosystem I. Journal of Biological Chemistry, 285, 3478–3486.

Andersson A, Keskitalo J, Sjödin A, Bhalerao R, Sterky F, Wissel K, Tandre K, Aspeborg H, Moyle R, Ohmiya Y, Bhalerao R, Brunner A, Gustafsson P, Karlsson J, Lundeberg J, Nilsson O, Sandberg G, Strauss S, Sundberg B, Uhlen M, et al. 2004. A transcriptional timetable of autumn senescence. Genome Biology, 5, R24.

Besseau S, Li J, Palva E T. 2012. WRKY54 and WRKY70 co-operate as negative regulators of leaf senescence in Arabidopsis thaliana. Journal of Experimental Botany, 63, 2667–2679.

Bhalerao R, Keskitalo J, Sterky F, Erlandsson R, Björkbacka H, Birve S J, Karlsson J, Gardeström P, Gustafsson P, Lundeberg J, Jansson S. 2003. Gene expression in autumn leaves. Plant Physiology, 131, 430–442.

Borrás L, Slafer G A, Otegui M E. 2004. Seed dry weight response to source-sink manipulations in wheat, maize and soybean: A quantitative reappraisal. Field Crops Research, 86, 131–146.

Bradford M M. 1976. A rapid and sensitive method for the quantization of microgram quantities of protein utilizing the principle of protein-dye binding. Analytical Biochemistry, 72, 248–254.

Buchanan-Wollaston V. 1997. The molecular biology of leaf senescence. Journal of Experimental Botany, 48, 181–199.

Buchanan-Wollaston V, Page T, Harrison E, Breeze E, Lim P O, Nam H G, Lin J F, Wu S H, Swidzinski J, Ishizaki K, Leaver C J. 2005. Comparative transcription analysis reveals significant differences in gene expression and signaling pathways between development and dark/starvation-induced senescence in Arabidopsis. The Plant Journal, 42, 567–585.

Dong M H, Gu J R, Zhang L, Chen P F, Liu T F, Deng J H, Lu H Q, Han L Y, Zhao B H. 2014. Comparative proteomics analysis of superior and inferior spikelets in hybrid rice during grain filling and response of inferior spikelets to drought stress using isobaric tags for relative and absolute quantification. Journal of Proteomics, 109, 382–399.

Doubnerova V, Janoskova M, Synkova H, Subr Z, Cerovska N, Ryslava H. 2007. Effect of Potato virus Y on the activities of antioxidant and anaplerotic enzymes in Nicotiana tabacum L. transgenic plants transformed with the gene for P3 protein. General and Applied Plant Physiology, 33, 123–140.

Edwards G E, Nakamoto H, Burnell J N, Hatch M D. 1985. Pyruvate, Pidikinase and NADP-malate dehydrogenase in C4 photosynthesis: Properties and mechanism of light/dark regulation. Annual Review of Plant Physiology, 36, 255–286.

Fadeel A A. 1962. Location and property of chloroplasts and pigment determination in roots. Plant Physiology, 15, 130–147.

Fernie A R, Carrari F, Sweetlove L J. 2004. Respiratory metabolism: Glycolysis, the TCA cycle and mitochondrial electron transport. Current Opinion in Plant Biology, 7, 254–261.

Gepstein S, Sabehi G, Carp M J, Hajouj T, Nesher M F, Yariv I, Dor C, Bassani M. 2003. Large-scale identification of leaf senescence-associated genes. The Plant Journal, 36, 629–642.

Gomez J, Sanchez-Martinez D, Stiefel V, Rigau J, Puigdomenech P, Pages M. 1988. A gene induced by the plant hormone abscisic acid in response to water stress encodes a glycine-rich protein. Nature, 334, 262–264.

Gulati A, Jaiwal P K. 1996. Effect of NaCl on nitrate reductitase, glutamate dehydrogenase and glutamate in Vigna radiata Calli. Plant Biology, 38, 177–183.

Guo Y, Cai Z, Gan S. 2004. Transcriptome of Arabidopsis leaf senescence. Plant Cell Environment, 27, 521–549.

He Y, Tang W, Swain J D, Green A L, Jack T P, Gan S. 2001. Networking senescence-regulating pathways by using Arabidopsis enhancer trap lines. Plant Physiology, 126, 707–716.

Hebeler R, Oeljeklaus S, Reidegeld K A, Eisenacher M, Stephan C, Sitek B, Stühler K, Meyer H E, Sturre M J G, Dijkwel P P, Warscheid B. 2007. Study of early leaf senescence in Arabidopsis thaliana by quantitative proteomics using reciprocal 14N/15N labeling and difference gel electrophoresis. Molecular & Cellular Proteomics, 7, 108–120.

Herbinger K, Then C, Haberer K, Alexou M, Löw M, Remele K, Rennenberg H, Matyssek R, Grill D, Wieser G, Tausz M. 2007. Gas exchange and antioxidative compounds in young beech trees under free-air ozone exposure and comparisons to adult trees. Plant Biology, 9, 288–297.

Hortensteiner S, Feller U. 2002. Nitrogen metabolism and remobilization during senescence. Journal of Experimental Botany, 53, 927–937.

Ishikawa K, Matsui I, Payan F, Cambillau C, Ishida H, Kawarabayasi Y, Kikuchi H, Roussel A. 2002. A hyperthermostable D-ribose-5-phosphate isomerase from Pyrococcus horikoshii characterization and three-dimensional structure. Structure, 10, 877–886.

Kerner R, Delgado-Eckert E, Ernst D, Dupuy J W, Grams T E E, Winkler J B, Lindermayr C, Müller-Starck G. 2014. Large-scale protein analysis of European beech trees following four vegetation periods of twice ambient to zone exposure. Journal of Proteomics, 109, 417–435.

Lim P O, Kim H J, Nam H G. 2006. Leaf senescence. Annual Review of Plant Physiology, 58, 115–136.

Lim P O, Woo H R, Nam H G. 2003. Molecular genetics of leaf senescence in Arabidopsis. Trends Plant Science, 8, 272–278.

Lin J F, Wu S H. 2004. Molecular events in senescing Arabidopsis leaves. The Plant Journal, 39, 612–628.

Liu T N, Gu L M, Dong S T, Zhang J W, Liu P, Zhao B. 2015. Optimum leaf removal increases canopy apparent photosynthesis, 13C-photosynthate distribution and grain yield of maize crops grown at high density. Field Crops Research, 170, 32–39.

Liu X P, Grams T E E, Matyssek R, Rennenberg H. 2005. Effects of elevated pCO2 and/or pO3 on C-, N-, and S-metabolites in the leaves of juvenile beech and spruce differ between trees grown in monoculture and mixed culture. Plant Physiology and Biochemistry, 43, 147–154.

Lu K X, Cao B H, Feng X P, He Y, Jiang D A. 2009. Photosynthetic response of salt-tolerant and sensitive soybean varieties. Photosynthetica, 47, 381–387.

Malkin R, Niyogi K. 2000. Photosynthesis. In: Buchanan B, Gruissem W, Jones R, eds., Biochemistry and Molecular Biology of Plants. American Society of Plant Physiologists Rockville, USA. pp. 568–628.

Nagy Z, Németh E, Guóth A, Bona L, Wodala B, Pécsváradi A. 2013. Metabolic indicators of drought stress tolerance in wheat, Glutamine synthetase isoenzymes and Rubisco. Plant Physiology and Biochemistry, 67, 48–54.

Neuhoff V, Arnold N, Taube D, Erhardt W. 1988. Improved staining of proteins in polyacrylamide gels including isoelectric focusing gels with clear background at nanogram sensitivity using Coomassie brilliant blue G-250 and R-250. Electrophoresis, 9, 255–262.

Nomata T, Kabeya Y, Sato N. 2000. Cloning and characterization of glycine-rich RNA-binding protein cDNAs in the moss Physcomitrella patens. Plant Cell Physiology, 45, 48–56.

Parker R, Flowers T J, Moore A L, Harpham NV. 2006. An accurate and reproducible method for proteome profiling of the effectsof salt stress in the rice leaf lamina. Journal of Experimental Botany, 57, 1109–1118.

Pécsváradi A, Nagy Z, Varga A, Vashegyi A, Labádi I, Galbács G, Zsoldos F. 2009. Chloroplastic glutamine synthetase is activated by direct binding of aluminium. Plant Physiology, 135, 43–50.

Ramakrishnan Y, White S W. 1998. Ribosomal protein structures, insights into the architecture, machinery and evolution of the ribosome. Trends in Biochemical Sciences, 23, 208–212.

Ruan S L, Ma H S, Wang S H, Fu Y P, Xin Y, Liu W Z, Wang F, Tong J X, Wang S Z, Chen H Z. 2011. Proteomic identification of OsCYP2, a rice cyclophilin that confers salt tolerance in rice (Oryza sativa L.) seedlings when overexpressed. BMC Plant Biology, 11, 34–48.

Ruepp A, Zollner A, Maier D, Albermann K, Hani J, Mokrejs M, Tetko I, Güldener U, Mannhaupt G, Münsterkötter M, Mewes H W. 2004. The FunCat, a functional annotation scheme for systematic classification of proteins from whole genomes. Nucleic Acids Research, 32, 5539–5545.

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.

Sachetto-Martins G, Franco L O, Oliveira D E. 2000. Plant glycine-rich proteins, a family or just proteins with a common motif? Biochimica et Biophysica Acta, 1492, 1–14.

Sanan-Mishra N A, Tuteja N, Sopory S K. 2002. Salinity and ABA induced up-regulation and light mediated modulation of mRNA encoding glycine rich RNA binding protein from Sorghum bicolour. Biochemical and Biophysical Research Communications, 296, 1063–1068.

Sauer M, Jakob A, Nordheim A, Hochholdinger F. 2006. Proteomic analysis of shoot-borne root initiation in maize (Zea mays L.). Proteomics, 6, 2530–2541.

Sharabi-Schwager M, Lers A, Samach A, Guy C L, Porat R. 2010. Overexpression of the CBF2 transcriptional activator in Arabidopsis delays leaf senescence and extends plantlongevity. Journal of Experimental Botany, 61, 261–273.

Smart C M. 1994. Gene-expression during leaf senescence. New Phytologist, 126, 419–448.

Suzuki N, Koussevitzky S, Mittler R, Miller G. 2012. ROS and redox signalling in the response of plants to abiotic stress. Plant Cell Environmet, 35, 259–270.

Wardlaw I F. 1990. The control of carbon partitioning in plants. New Phytologist, 116, 341–381.

Wilson K A, McManus M T, Gordon M E, Jordan T W. 2002. The proteomics of senescence in leaves of white clover, Trifolium repens (L). Proteomics, 2, 1114–1122.

Wu L J, Han Z P, Wang S X, Wang X T, Sun A G, Zu X F, Chen Y H. 2013. Comparative proteomic analysis of the plant-virus interaction in resistant and susceptible ecotypes of maize infected with sugarcane mosaic virus. Journal of Proteomics, 89, 124–140.

Yang J, Zhang J, Wang Z, Zhu Q, Liu L. 2002. Abscisic acid and cytokinins in the root exudates and leaves and their relationship to senescence and remobilization of carbon reserves in rice subjected to water stress during grain filling. Planta, 215, 645–652.

Yao Y, Ni Z, Du J, Wang X, Wu H, Sun Q. 2006. Isolation and characterization of 15 genes encoding ribosomal proteins in wheat (Triticum aestivum L.). Plant Science, 170, 579–586.

Yoshida S. 1981. Physiological analysis of rice yield. In: Yoshida S, ed., Fundamentals of Rice Crop Science. The International Rice Research Institute, Los Bańos, The Philippines. pp. 231–251.

Zhang A H, Lu Q T, Yin Y, Ding S H, Wen X G, Lu C M. 2010. Comparative proteomic analysis provides new insights into the regulation of carbon metabolism during leaf senescence of rice grown under field conditions. Journal of Plant Physiology, 167, 1380–1389.

Zhang C J, Chen L, Shi D W, Chen G X, Lu C G, Wang P, Wang J, Chu H, Zhou Q C, Zuo M, Sun L. 2007. Characteristics of ribulose-1,5-bisphosphate carboxylase and C4 pathway key enzymes in flag leaves of a super-high-yield hybrid rice and its parents during the reproductive stage. South African Journal of Botany, 73, 22–28.
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