Comparative proteomics analysis of two maize hybrids revealed drought-stress tolerance mechanisms

References

• Wang N, Liang LI, Gao WW, et al. Transcriptomes of early developing tassels under drought stress reveal differential expression of genes related to drought tolerance in maize. J Integr Agric. 2018;17(6):1276–1288.
   Web of Science ®Google Scholar
• Gong F, Yang L, Tai F, et al. “Omics” of maize stress response for sustainable food production: opportunities and challenges. OMICS. 2014;18(12):714–732.
   PubMed Web of Science ®Google Scholar
• Li GK, Gao J, Peng H, et al. Proteomic changes in maize as a response to heavy metal (lead) stress revealed by iTRAQ quantitative proteomics. Genet Mol Res. 2016;15(1).
   Web of Science ®Google Scholar
• Shikha M, Pooja B, Mallikarjuna MG, et al. Structural, functional, and evolutionary characterization of major drought transcription factors families in maize. Front Chem. 2018;6:177.
   PubMed Web of Science ®Google Scholar
• Liu Y, Zhou M, Gao Z, et al. RNA-seq analysis reveals mapkkk family members related to drought tolerance in maize. PLoS One. 2015;10(11):e0143128.
   PubMed Web of Science ®Google Scholar
• Du CY, Duan ZY, Wang JX, et al. Drought resistance of eight maize varieties at seedling stage in Yunnan Province. Plant Dis Pests. 2015;6:28–34.
   Google Scholar
• Alam I, Sharmin SA, Kim KH, et al. Proteome analysis of soybean roots subjected to short-term drought stress. Plant Soil. 2010;333(1–2):491–505.
   Web of Science ®Google Scholar
• Gao ZY, Liu H, Wang HL, et al. Generation of the genetic mutant population for the screening and characterization of the mutants in response to drought in maize. Chin Sci Bull. 2014;59(8):766–775.
   Google Scholar
• Yang LM, Jiang TB, Fountain JC, et al. Protein profiles reveal diverse responsive signaling pathways in kernels of two maize inbred lines with contrasting drought sensitivity. Int J Mol Sci. 2014;15(10):18892–18918.
   PubMed Web of Science ®Google Scholar
• Zheng J, Fu J, Gou M, et al. Genome-wide transcriptome analysis of two maize inbred lines under drought stress. Plant Mol Biol. 2010;72(4–5):407–421.
   PubMed Web of Science ®Google Scholar
• Budak H, Hussain B, Khan Z, et al. From genetics to functional genomics: improvement in drought signaling and tolerance in wheat. Front Plant Sci. 2015;6:1012.
   PubMed Web of Science ®Google Scholar
• Zong N, Li X-J, Wang L, et al. Maize ABP2 enhances tolerance to drought and salt stress in transgenic arabidopsis. J Integr Agric. 2018;17(11):2379–2393.
   Web of Science ®Google Scholar
• Cui LM, Wang XX, Xuan HD, et al. Changes in several physiological and biochemical indices of maize seedling roots caused by drought stress. Plant Dis Pests. 2015;6:35–37.
   Google Scholar
• Hoque MIU, Nesar Uddin M, Fakir Rasel MSA, et al. Drought and salinity affect leaf and root anatomical structures in three maize genotypes. J Bangladesh Agric Univ. 2018;16(1):47–55.
   Google Scholar
• Westgate ME. Water status and development of the maize endosperm and embryo during drought. Crop Sci. 1994;34(1):76–83.
   Web of Science ®Google Scholar
• Tahmasebi S, Heidari B, Pakniyat H, et al. Independent and combined effects of heat and drought stress in the Seri M82 × Babax bread wheat population. Plant Breed. 2014;133(6):702–711.
   Web of Science ®Google Scholar
• Bin Z, Li W, Chang X, et al. Effects of favorable alleles for water-soluble carbohydrates at grain filling on grain weight under drought and heat stresses in wheat. PLoS One. 2014;9(7):e102917.
   PubMed Web of Science ®Google Scholar
• Wang Z, Jiang J, Liao Y, et al. Risk assessment of maize drought hazard in the middle region of farming-pastoral ecotone in northern china. Nat Hazards. 2015;76(3):1515–1534.
   Web of Science ®Google Scholar
• Lei L, Shi J, Chen J, et al. Ribosome profiling reveals dynamic translational landscape in maize seedlings under drought stress. Plant J. 2015;84(6):1206–1218.
   PubMed Web of Science ®Google Scholar
• Liu XD, Xh L, Wh L, et al. Analysis on difference for drought responses of maize breeds at seedling stage. J Maize Sci. 2004;3:63–65.
   Google Scholar
• Bin WU, Li XH, Mu JX, et al. Genetic variation in fifty-three maize breeds in relation to drought tolerance at seedling stage. Sci Agric Sin. 2007;4:665–676.
   Google Scholar
• Jurgens SK, Johnson RR, Boyer JS. Dry matter production and translocation in maize subjected to drought during grain fill. Agron J. 1978;70(4):678–682.
   Web of Science ®Google Scholar
• Lu DL, Cai XM, Lu WP. Effects of water deficit during grain filling on the physicochemical properties of waxy maize starch. Starch. 2015;67(7–8):692–700.
   Web of Science ®Google Scholar
• Jin XN, Fu ZY, Ding D, et al. Proteomic identification of genes associated with maize grain-filling rate. PLoS One. 2013;8(3):e59353.
   PubMed Web of Science ®Google Scholar
• Zhilan X, Han K, Gu L, et al. Transcriptome analysis of heterosis in maize (Zea mays L.) hybrid longping 206. J Agric Biotechnol. 2017;25:709–721.
   Google Scholar
• Li G, Gao HY, Zhao B, et al. Effects of drought stress on activity of photosystems in leaves of maize at grain filling stage. Acta Agronom Sin. 2009;35(10):1916–1922.
   Google Scholar
• Mu XH, Chen QW, Chen FJ, et al. Within-leaf nitrogen allocation in adaptation to low nitrogen supply in maize during grain-filling stage. Front Plant Sci. 2016;7:699.
   PubMed Web of Science ®Google Scholar
• Geng LI, Hui-Yuan G, Peng L, et al. Effects of nitrogen fertilization on photosynthetic performance in maize leaf at grain filling stage. Plant Nutr Fertil Sci. 2010;16:536–542.
   Google Scholar
• Kosová K, Vítámvás P, Prášil IT, et al. Plant proteome changes under abiotic stress—contribution of proteomics studies to understanding plant stress response. J Proteomics. 2011;74(8):1301–1322.
   PubMed Web of Science ®Google Scholar
• Si W, Fen N, Qinbin Z, et al. Enhancing omics research of crop responses to drought under field conditions. Front Plant Sci. 2017;8:174.
   PubMed Web of Science ®Google Scholar
• Pérez-Clemente RM, Vives V, Zandalinas SI, et al. Biotechnological approaches to study plant responses to stress. Biomed Res Int. 2013;2013:654120.
   PubMed Web of Science ®Google Scholar
• Shuzhen W, Wenyue C, Wenfei X, et al. Differential proteomic analysis using itraq reveals alterations in hull development in rice (Oryza sativa L.). PLoS One. 2015;10(7):e0133696.
   PubMed Web of Science ®Google Scholar
• Ma C, Zhou J, Chen G, et al. iTRAQ-based quantitative proteome and phosphoprotein characterization reveals the central metabolism changes involved in wheat grain development. BMC Genomics. 2014;15:1029.
   PubMed Web of Science ®Google Scholar
• Jin HY, Liu ST, Zenda T, et al. Maize leaves drought-responsive genes revealed by comparative transcriptome of two cultivars during the filling stage. PLoS One. 2019;14(10):e0223786.
   PubMed Web of Science ®Google Scholar
• Hsiao TC. Plant responces to water stress. Annu Rev Plant Physiol. 1973;24(1):519–570.
   Google Scholar
• Swägger H. Tricine-SDS-PAGE. Nat Protoc. 2006;1:16–22.
   PubMed Web of Science ®Google Scholar
• Liu XD, Xie L, Wei Y, et al. Abiotic stress resistance, a novel moonlighting function of ribosomal protein rpl44 in the halophilic fungus aspergillus glaucus. Appl Environ Microbiol. 2014;80(14):4294–4300.
   PubMed Web of Science ®Google Scholar
• Cui D, Wu D, Liu J, et al. Proteomic analysis of seedling roots of two maize inbred lines that differ significantly in the salt stress response. PLoS One. 2015;10(2):e0116697.
   PubMed Web of Science ®Google Scholar
• Tai FJ, Yuan ZL, Wu XL, et al. Identification of membrane proteins in maize leaves, altered in expression under drought stress through polyethylene glycol treatment. Report. Plant Omics. 2011;4:250–256.
   Web of Science ®Google Scholar
• Benešová M, Holá D, Fischer L, et al. The physiology and proteomics of drought tolerance in maize: early stomatal closure as a cause of lower tolerance to short-term dehydration? PLoS One. 2012;7(6):e38017.
   PubMed Web of Science ®Google Scholar
• Shu LB, Ding W, Wu JH, et al. Proteomic analysis of rice leaves shows the different regulations to osmotic stress and stress signals. J Integr Plant Biol. 2010;52(11):981–995.
   PubMed Web of Science ®Google Scholar
• Mazzucotelli E, Mastrangelo AM, Crosatti C, et al. Abiotic stress response in plants: when post-transcriptional and post-translational regulations control transcription. Plant Sci. 2008;174(4):420–431.
   Web of Science ®Google Scholar
• Yamaguchi-Shinozaki K, Shinozaki K. Transcriptional regulatory networks in cellular responses and tolerance to dehydration and cold stresses. Annu Rev Plant Biol. 2006;57:781–803.
   PubMed Web of Science ®Google Scholar
• Rushton PJ, Somssich IE. Transcriptional control of plant genes responsive to pathogens. Curr Opin Plant Biol. 1998;1(4):311–315.
   PubMed Web of Science ®Google Scholar
• Mesbah K, Camus A, Babinet C, et al. Mutation in the Trapalpha/Ssr1 gene, encoding translocon-associated protein alpha, results in outflow tract morphogenetic defects. Mol Cell Biol. 2006;26(20):7760–7771.
   PubMed Web of Science ®Google Scholar
• Fons RD, Bogert BA, Hegde RS. Substrate-specific function of the translocon-associated protein complex during translocation across the ER membrane. J Cell Biol. 2003;160(4):529–539.
   PubMed Web of Science ®Google Scholar
• Kang Y, Udvardi M. Global regulation of reactive oxygen species scavenging genes in alfalfa root and shoot under gradual drought stress and recovery. Plant Signal Behav. 2012;7(5):539–543.
   PubMedGoogle Scholar
• Farooq M, Wahid A, Kobayashi N, et al. Plant drought stress: effects, mechanisms and management. Agronom Sustain Agric. 2009;29:185–212.
   Web of Science ®Google Scholar
• Nakano R, Matsumura T, Sakakibara H, et al. Cloning of maize ferredoxin iii gene: presence of a unique repetitive nucleotide sequence within an intron found in the 5'-untranslated region. Plant Cell Physiol. 1997;38(10):1167–1170.
   PubMed Web of Science ®Google Scholar
• Alam J, Whitaker RA, Krogmann DW, et al. Isolation and sequence of the gene for ferredoxin i from the cyanobacterium anabaena sp. strain pcc 7120. J Bacteriol. 1986;168(3):1265–1271.
   PubMed Web of Science ®Google Scholar
• Sofo A, Dichio B, Xiloyannis C, et al. Antioxidant defences in olive trees during drought stress: changes in activity of some antioxidant enzymes. Funct Plant Biol. 2005;32(1):45–53.
   PubMed Web of Science ®Google Scholar
• Hunter T. Protein kinases and phosphatases: the yin and yang of protein phosphorylation and signaling. Cell. 1995;80(2):225–236.
   PubMed Web of Science ®Google Scholar
• Ding X, Cao Y, Huang L, et al. Activation of the indole-3-acetic acid-amido synthetase gh3-8 suppresses expansin expression and promotes salicylate- and jasmonate-independent basal immunity in rice. Plant Cell. 2008;20(1):228–240.
   PubMed Web of Science ®Google Scholar
• Peat TS, Bottcher C, Newman J, et al. Crystal structure of an indole-3-acetic acid amido synthetase from grapevine involved in auxin homeostasis. Plant Cell. 2012;24(11):4525–4538.
   PubMed Web of Science ®Google Scholar
• Fatmi MQ, Chang CEA, Mozzarelli A. The role of oligomerization and cooperative regulation in protein function: the case of tryptophan synthase. PLoS Comput Biol. 2010;6(11):e1000994.
   PubMed Web of Science ®Google Scholar
• Hinchman SK, Henikoff S, Schuster SM. A relationship between asparagine synthetase A and aspartyl tRNA synthetase. J Biol Chem. 1992;267(1):144–149.
   PubMed Web of Science ®Google Scholar
• Pickart CM, Rose IA. Mechanism of ubiquitin carboxyl-terminal hydrolase. borohydride and hydroxylamine inactivate in the presence of ubiquitin. J Biol Chem. 1986;261(22):10210–10217.
   PubMed Web of Science ®Google Scholar
• Pickart CM, Rose IA. Ubiquitin carboxyl-terminal hydrolase acts on ubiquitin carboxyl-terminal amides. J Biol Chem. 1985;260(13):7903–7910.
   PubMed Web of Science ®Google Scholar
• Zhang Z, Li J, Liu H, et al. Roles of ubiquitination-mediated protein degradation in plant responses to abiotic stresses. Environ Exp Bot. 2015;114:92–103.
   Web of Science ®Google Scholar
• Pace HC, Brenner C. The nitrilase superfamily: classification, structure and function. Genome Biol. 2001;2(1):REVIEWS0001.
   PubMed Web of Science ®Google Scholar
• Brenner C. Catalysis in the nitrilase superfamily. Curr Opin Struct Biol. 2002;12(6):775–782.
   PubMed Web of Science ®Google Scholar
• Rincón-Limas DE, Krueger DA, Patel PI. Functional characterization of the human hypoxanthine phosphoribosyltransferase gene promoter: evidence for a negative regulatory element. Mol Cell Biol. 1991;11(8):4157–4164.
   PubMed Web of Science ®Google Scholar
• Ding H, Yue LJ, Yang CL. Progress in the study of hypoxanthine guanine phosphoribtransferase. Genetics. 2013;35:948–954.
   Google Scholar
• Francone OL, Gurakar A, Fielding C. Distribution and functions of lecithin:cholesterol acyltransferase and cholesteryl ester transfer protein in plasma lipoproteins. Evidence for a functional unit containing these activities together with apolipoproteins A-I and D that catalyzes the esterif. The J Biol Chem. 1989;264:7066–7072.
   PubMed Web of Science ®Google Scholar
• Persson O, Valadi A, Thomas N, et al. Metabolic control of the Escherichia coli universal stress protein response through fructose-6-phosphate. Mol Microbiol. 2007;65(4):968–978.
   PubMed Web of Science ®Google Scholar
• Isokpehi RD, Simmons SS, Cohly Ekunwe SIN, et al. Identification of drought-responsive universal stress proteins in viridiplantae. Bioinform Biol Insights. 2011;5:41–58.
   PubMedGoogle Scholar
• Tkaczuk KLA, Shumilin I, Chruszcz M, et al. Structural and functional insight into the universal stress protein family. Evol Appl. 2013;6(3):434–449.
   PubMed Web of Science ®Google Scholar
• Loukehaich R, Wang T, Ouyang BZ, et al. SpUSP, an annexin-interacting universal stress protein, enhances drought tolerance in tomato. J Exp Bot. 2012;63(15):5593–5606.
   PubMed Web of Science ®Google Scholar
• Sridhar VV, Kapoor A, Zhang K, et al. Control of DNA methylation and heterochromatic silencing by histone H2B deubiquitination. Nature. 2007;447(7145):735–738.
   PubMed Web of Science ®Google Scholar
• Liu X, Luo M, Zhang W, et al. Histone acetyltransferases in rice (Oryza sativa L.): phylogenetic analysis, subcellular localization and expression. BMC Plant Biol. 2012;12:145.
   PubMed Web of Science ®Google Scholar
• Chinnusamy V, Zhu J-K. Epigenetic regulation of stress responses in plants. Curr Opin Plant Biol. 2009;12(2):133–139.
   PubMed Web of Science ®Google Scholar
• Pan LN. [Epigenetic regulation of abiotic stress response in plants to improve the stress tolerance]. Yi Chuan. 2013;35(6):745–751.
   PubMedGoogle Scholar
• Tariq M, Saze H, Probst AV, et al. Erasure of cpg methylation in arabidopsis alters patterns of histone h3 methylation in heterochromatin. Proc Natl Acad Sci USA. 2003;100(15):8823–8827.
   PubMed Web of Science ®Google Scholar
• Sokol A, Kwiatkowska A, Jerzmanowski A, et al. Up-regulation of stress-inducible genes in tobacco and arabidopsis cells in response to abiotic stresses and aba treatment correlates with dynamic changes in histone h3 and h4 modifications. Planta. 2007;227(1):245–254.,
   PubMed Web of Science ®Google Scholar
• Sun ZW, Allis CD. Ubiquitination of histone H2B regulates H3 methylation and gene silencing in yeast. Nature. 2002;418(6893):104–108.
   PubMed Web of Science ®Google Scholar
• Ng HH, Xu RM, Zhang Y, et al. Ubiquitination of histone H2B by Rad6 is required for efficient Dot1-mediated methylation of histone H3 lysine 79. J Biol Chem. 2002;277(38):34655–34657.
   PubMed Web of Science ®Google Scholar
• Ohki I, Shimotake N, Fujita N, et al. Solution structure of the methyl-CpG-binding domain of the methylation-dependent transcriptional repressor MBD1. EMBO (European Molecular Biology Organization). EMBO J. 1999;18(23):6653–6661.
   PubMed Web of Science ®Google Scholar
• Roloff TC, Ropers HH, Nuber UA. Comparative study of methyl-CpG-binding domain proteins. BMC Genomics. 2003;4(1):1.
   PubMed Web of Science ®Google Scholar
• Du Q, Luu PL, Stirzaker C, et al. Methyl-CpG-binding domain proteins: readers of the epigenome. Epigenomics. 2015;7(6):1051–1073.
   PubMed Web of Science ®Google Scholar
• Callahan MA, Handley MA, Lee YH, et al. Functional interaction of human immunodeficiency virus type 1 Vpu and Gag with a novel member of the tetratricopeptide repeat protein family. J Virol. 1998;72(6):5189–5197.
   PubMed Web of Science ®Google Scholar
• Wang H, Shen H, Wang Y, et al. Overexpression of small glutamine-rich tpr-containing protein promotes apoptosis in 7721 cells. FEBS Lett. 2005;579(5):1279–1284.
   PubMed Web of Science ®Google Scholar
• Allan RK, Ratajczak T. Versatile TPR domains accommodate different modes of target protein recognition and function. Cell Stress Chaperones. 2011;16(4):353–367.
   PubMed Web of Science ®Google Scholar
• Bennett-Lovsey R, Hart SE, Shirai H, et al. The SWIB and the MDM2 domains are homologous and share a common fold. Bioinformatics. 2002;18(4):626–630.
   PubMed Web of Science ®Google Scholar
• Vieira WA, Coetzer Thérèsa L. Localization and interactions of Plasmodium falciparum SWIB/MDM2 homologues. Malar J. 2016;15:32.
   PubMed Web of Science ®Google Scholar
• Frum R, Ramamoorthy M, Mohanraj L, et al. MDM2 controls the timely expression of cyclin A to regulate the cell cycle. Mol Cancer Res. 2009;7(8):1253–1267.
   PubMed Web of Science ®Google Scholar
• Kushwaha HR, Singh AK, Sopory SK, et al. Genome wide expression analysis of CBS domain containing proteins in Arabidopsis thaliana (L.), Heynh and Oryza sativa L. reveals their developmental and stress regulation. BMC Genomics. 2009;10:200.
   PubMed Web of Science ®Google Scholar
• Zhu QL, Li MY, Liu GD, et al. Molecular characterization and functional prediction of novel leaf sag encoding a CBS-domain-containing protein from coleus blumei. Chin J Biochem Mol Biol. 2007;23:262–270.
   Google Scholar
• Singh AK, Kumar R, Pareek A, et al. Overexpression of rice cbs domain containing protein improves salinity, oxidative, and heavy metal tolerance in transgenic tobacco. Mol Biotechnol. 2012;52(3):205–216.
   PubMed Web of Science ®Google Scholar
• Salem AMH, Nakano T, Takuwa M, et al. Genetic analysis of repair and damage tolerance mechanisms for DNA-protein cross-links in escherichia coli. J Bacteriol. 2009;191(18):5657–5668.
   PubMed Web of Science ®Google Scholar
• Karran P, Bignami M. DNA damage tolerance, mismatch repair and genome instability. Bioessays. 1994;16(11):833–839.
   PubMed Web of Science ®Google Scholar
• Chen YH, Szakal B, Castellucci F, et al. DNA damage checkpoint and recombinational repair differentially affect the replication stress tolerance of Smc6 mutants. Mol Biol Cell. 2013;24(15):2431–2441.
   PubMed Web of Science ®Google Scholar
• Li X, Heyer W. Homologous recombination in DNA repair and DNA damage tolerance. Cell Res. 2008;18(1):99–113.
   PubMed Web of Science ®Google Scholar
• Roche Y, Zhang D, Segers-Nolten GMJ, et al. Fluorescence correlation spectroscopy of the binding of nucleotide excision repair protein XPC-hHr23B with DNA substrates. J Fluoresc. 2008;18(5):987–995.
   PubMed Web of Science ®Google Scholar
• Rodrigo G, Roumagnac S, Wold MS, et al. DNA replication but not nucleotide excision repair is required for uvc-induced replication protein a phosphorylation in mammalian cells. Mol Cell Biol. 2000;20(8):2696–2705.
   PubMed Web of Science ®Google Scholar
• Hoogstraten D, Bergink S, Verbiest VHM, et al. Versatile DNA damage detection by the global genome nucleotide excision repair protein XPC. J Cell Sci. 2008;121(Pt 17):2850–2859.
   PubMed Web of Science ®Google Scholar
• Min JH, Pavletich NP. Recognition of DNA damage by the Rad4 nucleotide excision repair protein. Nature. 2007;449(7162):570–575.
   PubMed Web of Science ®Google Scholar
• Jaciuk M, Nowak E, Skowronek K, et al. Structure of uvra nucleotide excision repair protein in complex with modified DNA. Nat Struct Mol Biol. 2011;18(2):191–197.
   PubMed Web of Science ®Google Scholar
• Zenda T, Liu S, Wang X, et al. Comparative proteomic and physiological analyses of two divergent maize inbred lines provide more insights into drought-stress tolerance mechanisms. IJMS. 2018;19(10):3225.
   Web of Science ®Google Scholar
• Wang X, Zenda T, Liu S, et al. Comparative proteomics and physiological analyses reveal important maize filling-kernel drought-responsive genes and metabolic pathways. IJMS. 2019;20(15):3743.
   Web of Science ®Google Scholar