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Journal of Integrative Agriculture  2019, Vol. 18 Issue (10): 2193-2204    DOI: 10.1016/S2095-3119(18)62140-9
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Dynamic changes of root proteome reveal diverse responsive proteins in maize subjected to cadmium stress
REN Wen1, 2, LIU Ya2, ZHOU Miao-yi2, SHI Zi2, WANG Tian-yu1, ZHAO Jiu-ran2, LI Yu
1 Institute of Crop Sciences, Chinese Academy of Agricultural Sciences, Beijing 100081, P.R.China
2 Maize Research Center, Beijing Academy of Agriculture & Forestry Sciences/Beijing Key Laboratory of Maize DNA Fingerprinting and Molecular Breeding, Beijing 100097, P.R.China
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Toxic symptoms and tolerance mechanisms of heavy metal in maize are well documented.  However, limited information is available regarding the changes in the proteome of maize seedling roots in response to cadmium (Cd) stress.  Here, we employed an iTRAQ-based quantitative proteomic approach to characterize the dynamic alterations in the root proteome during early developmental in maize seedling.  We conducted our proteomic experiments in three-day seedling subjected to Cd stress, using roots in four time points.  We identified a total of 733, 307, 499, and 576 differentially abundant proteins after 12, 24, 48, or 72 h of treatment, respectively.  These proteins displayed different functions, such as ribosomal synthesis, reactive oxygen species homeostasis, cell wall organization, cellular metabolism, and carbohydrate and energy metabolism.  Of the 166 and 177 proteins with higher and lower abundance identified in at least two time points, 14 were common for three time points.  We selected nine proteins to verify their expression using quantitative real-time PCR.  Proteins involved in the ribosome pathway were especially responsive to Cd stress.  Functional characterization of the proteins and the pathways identified in this study could help our understanding of the complicated molecular mechanism involved in Cd stress responses and create a list of candidate gene responsible for Cd tolerance in maize seeding roots.
Keywords:  cadmium stress        iTRAQ proteomics        maize seedling roots  
Received: 08 June 2018   Accepted:
Fund: This work was supported by the Foundation for Young Scientist of Beijing Academy of Agriculture & Forestry Sciences, China (QNJJ201505) and the National Key Research and Development Program of China (SQ2016ZY03002163).
Corresponding Authors:  Correspondence LI Yu, Tel: +86-10-62131196, E-mail:; ZHAO Jiu-ran, Tel: +86-10-51503936, Fax: +86-10-51503404, E-mail:    

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REN Wen, LIU Ya, ZHOU Miao-yi, SHI Zi, WANG Tian-yu, ZHAO Jiu-ran, LI Yu. 2019. Dynamic changes of root proteome reveal diverse responsive proteins in maize subjected to cadmium stress. Journal of Integrative Agriculture, 18(10): 2193-2204.

Ahsan N, Renaut J, Komatsu S. 2009. Recent developments in the application of proteomics to the analysis of plant responses to heavy metals. Proteomics, 9, 2602–2621.
Barber D J W, Thomas J K. 1978. Reactions of radicals with lecithin bilayers. Radiation Research, 74, 51–65.
Benavides M, Gallego M S, Tomaro M L. 2005. Cadmium toxicity in plants. Brazilian Journal of Plant Physiology, 17, 1.
Benešová M, Holá D, Fischer L, Jedelský P L, Hnili?ka F, Wilhelmová N, Rothová O, Ko?ová M, Procházková D, Honnerová J. 2012. The physiology and proteomics of drought tolerance in maize: Early stomatal closure as a cause of lower tolerance to short-term dehydration? PLoS ONE, 7, e38017.
Chao D Y, Silva A, Baxter I, Huang Y S, Nordborg M, Danku J, Lahner B, Yakubova E, Salt D E. 2012. Genome-wide association studies identify heavy metal ATPase3 as the primary determinant of natural variation in leaf cadmium in Arabidopsis thaliana. PLoS Genetics, 8, e1002923.
Chinnusamy V, Gong Z Z, Zhu J K. 2008. Abscisic acid-mediated epigenetic processes in plant development and stress responses. Journal of Integrative Plant Biology, 50, 1187–1195.
Chinnusamy V, Zhu J K. 2009. Epigenetic regulation of stress responses in plants. Current Opinion in Plant Biology, 12, 133.
Dalcorso G, Farinati S, Furini A. 2010. Regulatory networks of cadmium stress in plants. Plant Signaling & Behavior, 5, 663.
Feng J, Jia W, Lv S, Bao H, Miao F, Zhang X, Wang J, Li J, Li D, Zhu C. 2018. Comparative transcriptome combined with morpho-physiological analyses revealed key factors for differential cadmium accumulation in two contrasting sweet sorghum genotypes. Plant Biotechnology Journal, 16, 558–571.
Foyer C H, Noctor G. 2005. Redox homeostasis and antioxidant signaling: A metabolic interface between stress perception and physiological responses. The Plant Cell, 17, 1866–1875.
Fukao Y, Ferjani A, Tomioka R, Nagasaki N, Kurata R, Nishimori Y, Fujiwara M, Maeshima M. 2011. iTRAQ analysis reveals mechanisms of growth defects due to excess zinc in Arabidopsis. Plant Physiology, 155, 1893–1907.
Gratão P L, Monteiro C C, Rossi M L, Martinelli A P, Peres L E P, Medici L O, Gratãoa P L, Monteiro C C, Rossi M L, Martinelli A P, Peres L E, Medici L O, Lea P J, Azevedo R A. 2009. Differential ultrastructural changes in tomato hormonal mutants exposed to cadmium. Environmental & Experimental Botany, 67, 387–394.
Haider S, Pal R. 2013. Integrated analysis of transcriptomic and proteomic data. Current Genomics, 14, 91–110.
Hinkson I, Elias J. 2017. The dynamic state of protein turnover: It’s about time. Trends in Cell Biology, 21, 293–303.
Hossain Z, Komatsu S. 2012. Contribution of proteomic studies towards understanding plant heavy metal stress response. Frontiers in Plant Science, 3, 43–48.
Hu X, Li N, Wu L, Li C, Li C, Zhang L T, Wang W. 2015a. Quantitative iTRAQ-based proteomic analysis of phosphoproteins and ABA-regulated phosphoproteins in maize leaves under osmotic stress. Scientific Reports, 5, 15626.
Hu X, Wu L, Zhao F, Zhang D, Li N, Zhu G, Li C, Wang W. 2015b. Phosphoproteomic analysis of the response of maize leaves to drought, heat and their combination stress. Frontiers in Plant Science, 6, 298.
Jamet E, Canut H, Boudart G, Pontlezica R F. 2006. Cell wall proteins: A new insight through proteomics. Trends in Plant Science, 11, 33–39.
Karp N A, Huber W, Sadowski P G, Charles P D, Hester S V, Lilley K S. 2010. Addressing accuracy and precision issues in iTRAQ quantitation. Molecular & Cellular Proteomics, 9, 1885–1897.
Kruger N J. 1998. The Bradford method for protein quantitation. Methods in Molecular Biology, 32, 9–15.
Li G K, Gao J, Peng H, Shen Y O, Ding H P, Zhang Z M, Pan G T, Lin H J. 2015. Proteomic changes in maize as a response to heavy metal (lead) stress revealed by iTRAQ quantitative proteomics. Genetics and Molecular Research, 15, gmr7254.
Liu Y, Yu X, Feng Y, Zhang C, Wang C, Zeng J, Huang Z, Kang H, Fan X, Sha L, Zhang H, Zhou Y, Gao S, Chen Q. 2017. Physiological and transcriptome response to cadmium in cosmos (Cosmos bipinnatus Cav.) seedlings. Scientific Reports, 7, 14691.
Livak K J, Schmittgen T D. 2001. Analysis of relative gene expression data using real-time quantitative PCR and the 2(–Delta Delta C(T)) method. Methods, 25, 402–408.
Luo M, Zhao Y, Wang Y, Shi Z, Zhang P, Zhang Y, Song W, Zhao J. 2017. Comparative proteomics of contrasting maize genotypes provides insights into salt-stress tolerance mechanisms. Journal of Proteome Research, 17, 141–153.
Martinoia E, Maeshima M, Neuhaus H E. 2007. Vacuolar transporters and their essential role in plant metabolism. Journal of Experimental Botany, 58, 83–102.
Mota R, Pereira S B, Meazzini M, Rui F, Santos A, Evans C A, Philippis R D, Wright P C, Tamagnini P. 2015. Effects of heavy metals on Cyanothece sp. CCY 0110 growth, extracellular polymeric substances (EPS) production, ultrastructure and protein profiles. Journal of Proteomics, 120, 75–94.
Nocito F F, Pirovano L, Cocucci M, Sacchi G A. 2002. Cadmium-induced sulfate uptake in maize roots. Plant Physiology, 129, 1872–1879.
Pál M, Horváth E, Janda T, Páldi E, Szalai G. 2005. Cadmium stimulates the accumulation of salicylic acid and its putative precursors in maize (Zea mays) plants. Physiologia Plantarum, 125, 356–364.
Peng H, He X, Gao J, Ma H, Zhang Z, Shen Y, Pan G, Lin H. 2015. Transcriptomic changes during maize roots development responsive to cadmium (Cd) pollution using comparative RNAseq-based approach. Biochemical & Biophysical Research Communications, 464, 1040–1047.
Polle A, Schützendübel A. 2003. Heavy metal signalling in plants: linking cellular and organismic responses. In: Hirt H, Shinozaki K, eds., Plant Responses to Abiotic Stress. Springer-Verlag, Berlin-Heidelberg. pp. 187–215.
Rascio N, Vecchia F D, Ferretti M, Merlo L, Ghisi R. 1993. Some effects of cadmium on maize plants. Archives of Environmental Contamination and Toxicology, 25, 244–249.
Rogers R S, Dharsee M, Ackloo S, Sivak J M, Flanagan J G. 2012. Proteomics analyses of human optic nerve head astrocytes following biomechanical strain. Molecular & Cellular Proteomics, 11, M111.012302.
Sandberg A, Lindell G, Källström B N, Branca R M, Danielsson K G, Dahlberg M, Larson B, Forshed J, Lehtiö J. 2012. Tumor proteomics by multivariate analysis on individual pathway data for characterization of vulvar cancer phenotypes. Molecular & Cellular Proteomics, 11, M112.016998.
Sang T, Shan X, Li B, Shu S, Sun J, Guo S. 2016. Comparative proteomic analysis reveals the positive effect of exogenous spermidine on photosynthesis and salinity tolerance in cucumber seedlings. Plant Cell Reports, 35, 1769–1782.
Shen Y, Zhang Y, Chen J, Lin H, Zhao M, Peng H L, Yuan G, Zhang S, Zhang Z. 2013. Genome expression profile analysis reveals important transcripts in maize roots responding to the stress of heavy metal Pb. Physiologia Plantarum, 147, 270–282.
Su A, Song W, Xing J, Zhao Y, Zhang R, Li C, Duan M, Luo M, Shi Z, Zhao J. 2016. Identification of genes potentially associated with the fertility instability of S-type cytoplasmic male sterility in maize via bulked segregant RNA-seq. PLoS ONE, 11, e0163489.
Tuomainen M H, Nunan N, Lehesranta S J, Tervahauta A I, Hassinen V H, Schat H, Koistinen K M, Auriola S, Mcnicol J, Kärenlampi S O. 2006. Multivariate analysis of protein profiles of metal hyperaccumulator Thlaspi caerulescens accessions. Proteomics, 6, 3696–3706.
Visioli G, Marmiroli N. 2013. The proteomics of heavy metal hyperaccumulation by plants. Journal of Proteomics, 79, 133–145.
Wang M, Zou J, Duan X, Jiang W D. 2007. Cadmium accumulation and its effects on metal uptake in maize (Zea mays L.). Bioresource Technology, 98, 82–88.
Wang J, Li H, Zou D, Zhao J, Fan L, Wu T. 2017. Transcriptome profile analysis of cadmium tolerance in chinese flowering cabbage. Horticulture Environment & Biotechnology, 58, 56–65.
Wang X, Shan X, Wu Y, Su S, Li S H, Han J, Xue C, Yuan Y. 2016. iTRAQ-based quantitative proteomic analysis reveals new metabolic pathways responding to chilling stress in maize seedlings. Journal of Proteomics, 146, 14–24.
Wang Y, Xu L, Tang M, Jiang H, Chen W, Zhang W, Wang R L. 2016. Functional and integrative analysis of the proteomic profile of radish root under Pb exposure. Frontiers in Plant Science, 7, 1871.
Wang Z, Wang Z, Shi L, Wang L, Xu F. 2010. Proteomic alterations of Brassica napus root in response to boron deficiency. Plant Molecular Biology, 74, 265–278.
Wang Z Q, Xu X Y, Gong Q Q, Xie C, Fan W, Yang J L, Lin Q S, Zheng S J. 2014. Root proteome of rice studied by iTRAQ provides integrated insight into aluminum stress tolerance mechanisms in plants. Journal of Proteomics, 98, 189.
Washburn M P, Koller A, Oshiro G, Ulaszek R R, Plouffe D, Deciu C, Winzeler E, Yates J R. 2003. Protein pathway and complex clustering of correlated mRNA and protein expression analyses in Saccharomyces cerevisiae. Proceedings of the National Academy of Sciences of the United States of America, 100, 3107–3112.
Xie C, Mao X, Huang J, Ding Y, Wu J, Dong S, Kong L, Gao G, Li CY, Wei L. 2011. KOBAS 2.0: A web server for annotation and identification of enriched pathways and diseases. Nucleic Acids Research, 39, 316–322.
Xu D, Sun L, S, Zhang L, Yang H. 2016. Understanding the heat shock response in the sea cucumber Apostichopus japonicus, using iTRAQ-based proteomics. International Journal of Molecular Sciences, 17, 150.
Xu L, Wang Y W, Wang J, Zhu X, Zhang K, Yu R, Wang R, Xie Y, Zhang W. 2015. De novo sequencing of root transcriptome reveals complex cadmium-responsive regulatory networks in radish (Raphanus sativus L.). Plant Science, 236, 313.
Yang L, Ji J, Harris-Shultz K R, Hui W, Wang H, Abd-Allah E F, Luo Y, Hu X. 2016. The dynamic changes of the plasma membrane proteins and the protective roles of nitric oxide in rice subjected to heavy metal cadmium stress. Frontiers in Plant Science, 7, 190.
Yang L T, Qi Y P, Lu Y B, Guo P, Sang W, Feng H, Zhang H X, Chen L S. 2013. iTRAQ protein profile analysis of Citrus sinensis roots in response to long-term boron-deficiency. Journal of Proteomics, 93, 179–206.
You X, Yang L T, Lu Y B, Li H, Zhang S Q, Chen L S. 2014. Proteomic changes of Citrus roots in response to long-term manganese toxicity. Trees, 28, 1383–1399.
Yu F, Han X, Geng C, Zhao Y, Zhang Z, Qiu F. 2014. Comparative proteomic analysis revealing the complex network associated with waterlogging stress in maize (Zea mays L.) seedling root cells. Proteomics, 15, 135–147.
Yu T, Li G, Dong S T, Liu P, Zhang J W, Zhao B. 2016. Proteomic analysis of maize grain development using iTRAQ reveals temporal programs of diverse metabolic processes. BMC Plant Biology, 16, 24.
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[2] LI Feng-tao, QI Jian-min, ZHANG Gao-yang, LIN Li-hui, FANG Ping-ping, TAO Ai-fen , XU Jian-tang. Effect of Cadmium Stress on the Growth, Antioxidative Enzymes and Lipid Peroxidation in Two Kenaf (Hibiscus cannabinus L.) Plant Seedlings[J]. >Journal of Integrative Agriculture, 2013, 12(4): 610-620.
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