Proteomic changes in the grains of foxtail millet (Setaria italica (L.) Beau) under drought stress
Abstract
Drought has become a serious problem that threatens global food security. Foxtail millet (Setaria italica) can be used as a model crop for drought-resistant research because of its excellent performance in drought tolerance. In this study, the typical drought-tolerant foxtail millet landrace ‘Huangjinmiao’ was grown in a field under control and drought stress conditions to investigate its response to drought stress. The proteins in the harvested grains were analysed through two-dimensional electrophoresis (2-DE) coupled with matrix-assisted laser desorption/ionization-tandem time-of-flight (MALDI-TOF/TOF) analysis to characterize the response of foxtail millet under drought stress at a proteomic level. A total of 104 differentially abundant protein spots (DAPs) were identified; among them, 57 were up-regulated and 47 were down-regulated under drought treatment. The identified proteins were involved in an extensive range of biological processes, including storage proteins, protein folding, starch and sucrose metabolism, glycolysis/gluconeogenesis, biosynthesis of amino acids, detoxification and defense, protein degradation, tricarboxylic acid (TCA) cycle, protein synthesis, energy metabolism, transporter, pentose phosphate pathway, and signal transduction. Post-translational protein modifications might also occur. Moreover, the albumin content greatly decreased under drought stress, whereas the gliadin content considerably increased (p<0.01). In conclusion, this study provides new information on the proteomic changes in foxtail millet under drought stress and a framework for further studies on the function of these identified proteins.Downloads
References
Abedi T, Pakniyat H, 2010. Antioxidant enzyme changes in response to drought stress in ten cultivars of oilseed rape (Brassica napus L.). Czech J Genet Plant Breed 46 (1): 27-34. https://doi.org/10.17221/67/2009-CJGPB
Agboola S, Ng D, Mills D, 2005. Characterisation and functional properties of Australian rice protein isolates. J Cereal Sci 41 (3): 283-290. https://doi.org/10.1016/j.jcs.2004.10.007
Alley RB, Berntsen T, Bindoff NL, Chen Z, Chidthaisong A, Friedlingstein P, Gregory JM, Hegerl GC, Heimann M, Hewitson B, 2007. IPCC, 2007: Summary for policymakers. Cambridge University Press.
Begcy K, Walia H, 2015. Drought stress delays endosperm development and misregulates genes associated with cytoskeleton organization and grain quality proteins in developing wheat seeds. Plant Sci 240: 109-119. https://doi.org/10.1016/j.plantsci.2015.08.024
Bettinger RL, Barton L, Morgan C, 2010. The origins of food production in north China: A different kind of agricultural revolution. Evol Anthropol 19 (1): 9-21. https://doi.org/10.1002/evan.20236
Bing Y, Li J, Jin K, Dufresne C, Na Y, Qi S, Zhang Y, Ma C, Duong BV, Chen S, 2016. Quantitative proteomics and phosphoproteomics of sugar beet monosomic addition line M14 in response to salt stress. J Proteom 143: 286-297. https://doi.org/10.1016/j.jprot.2016.04.011
Callis J, Vierstra RD, 2000. Protein degradation in signaling. Curr Opin Plant Biol 3 (5): 381-386. https://doi.org/10.1016/S1369-5266(00)00100-X
Candiano G, Bruschi M, Musante L, Santucci L, Ghiggeri GM, Carnemolla B, Orecchia P, Zardi L, Righetti PG, 2004. Blue silver: a very sensitive colloidal Coomassie G-250 staining for proteome analysis. Electrophoresis 25 (9): 1327-1333. https://doi.org/10.1002/elps.200305844
Candogan BN, Sincik M, Buyukcangaz H, Demirtas C, Goksoy AT, Yazgan S, 2013. Yield, quality and crop water stress index relationships for deficit-irrigated soybean [Glycine max (L.) Merr.] in sub-humid climatic conditions Agr Water Manage 118: 113-121. https://doi.org/10.1016/j.agwat.2012.11.021
Cao Y, Luo Q, Tian Y, Meng F, 2017. Physiological and proteomic analyses of the drought stress response in Amygdalus Mira (Koehne) Yu et Lu roots. BMC Plant Biol 17 (1): 53. https://doi.org/10.1186/s12870-017-1000-z
Chastain CJ, Gu XY, 2006. Posttranslational regulation of pyruvate, orthophosphate dikinase in developing rice (Oryza sativa) seeds. Planta 224 (4): 924-934. https://doi.org/10.1007/s00425-006-0259-3
Chmielewska K, Rodziewicz P, Swarcewicz B, Sawikowska A, Krajewski P, Marczak L, Ciesiolka D, Kuczynska A, Mikolajczak K, Ogrodowicz P, et al., 2016. Analysis of drought-induced proteomic and metabolomic changes in barley (Hordeum vulgare L.) leaves and roots unravels some aspects of biochemical mechanisms involved in drought tolerance. Front Plant Sci 7: 1108. https://doi.org/10.3389/fpls.2016.01108
Cho EK, Hong CB, 2004. Molecular cloning and expression pattern analyses of heat shock protein 70 genes from Nicotiana tabacum. J Plant Biol 47 (2): 149-159. https://doi.org/10.1007/BF03030646
Criqui MC, De AEJ, Camasses A, Capron A, Parmentier Y, Inzé D, Genschik P, 2002. Molecular characterization of plant ubiquitin-conjugating enzymes belonging to the UbcP4/E2-C/UBCx/UbcH10 gene family. Plant Physiol 130 (3): 1230. https://doi.org/10.1104/pp.011353
Cui S, Huang F, Wang J, Ma X, Cheng Y, Liu J, 2005. A proteomic analysis of cold stress responses in rice seedlings. Proteomics 5 (12): 3162-3172. https://doi.org/10.1002/pmic.200401148
Cui Y, 2012. Analysis of differential proteins of cotton leaves under salt stress. Mol Plant Breed 13 (4): 455.
Dai TB, Zhao H, Jing Q, Jiang D, Cao WX, 2006. Effects of high temperature and water stress during grain filling on grain protein and starch formation in winter wheat. Acta Ecologica Sinica 26 (11): 3670-3676.
Duran-Encalada JA, Paucar-Caceres A, Bandala ER, Wright GH, 2017. The impact of global climate change on water quantity and quality: A system dynamics approach to the US-Mexican transborder region. Eur J Oper Res 256 (2): 567-581. https://doi.org/10.1016/j.ejor.2016.06.016
Ganeshan S, Drinkwater JM, Repellin A, Chibbar RN, 2010. Selected carbohydrate metabolism genes show coincident expression peaks in grains of in vitro-cultured immature spikes of wheat (Triticum aestivum L.). J Agric Food Chem 58 (7): 4193-4201. https://doi.org/10.1021/jf903861q
Gao Y, Wu QY, 2009. Identification of the proteomic changes in Synechocystis sp. PCC 6803 following prolonged UV-B irradiation. J Exp Bot 60 (4): 1141. https://doi.org/10.1093/jxb/ern356
Ge P, Ma C, Wang S, Gao L, Li X, Guo G, Ma W, Yan Y, 2012. Comparative proteomic analysis of grain development in two spring wheat varieties under drought stress. Anal Bioanal Chem 402 (3): 1297-1313. https://doi.org/10.1007/s00216-011-5532-z
Guo G, Ge P, Ma C, Li X, Lv D, Wang S, Ma W, Yan Y, 2012. Comparative proteomic analysis of salt response proteins in seedling roots of two wheat varieties. J Proteomics 75 (6): 1867. https://doi.org/10.1016/j.jprot.2011.12.032
Hashiguchi A, Komatsu S, 2016. Impact of post-translational modifications of crop proteins under abiotic stress. Proteomes 4 (4): 42. https://doi.org/10.3390/proteomes4040042
Holmes‐Davis R, Tanaka CK, Vensel WH, Hurkman WJ, Mccormick S, 2005. Proteome mapping of mature pollen of Arabidopsis thaliana. Proteomics 5 (18): 4864-4884. https://doi.org/10.1002/pmic.200402011
Hubbard MJ, Mchugh NJ, 1996. Mitochondrial ATP synthase F1-beta-subunit is a calcium-binding protein. Febs Letters 391 (3): 323. https://doi.org/10.1016/0014-5793(96)00767-3
Ishikawa T, Yoshimura K, Tamoi M, Takeda T, Shigeoka S, 1997. Alternative mRNA splicing of 3'-terminal exons generates ascorbate peroxidase isoenzymes in spinach (Spinacia oleracea) chloroplasts. Biochem J 328 (3): 795-800. https://doi.org/10.1042/bj3280795
Kilic H, Yağbasanlar T, 2010. The effect of drought stress on grain yield, yield components and some quality traits of durum wheat (Triticum turgidum ssp. durum) cultivars. Notulae Botanicae Horti Agrobotanici Cluj-Napoca 38: 164-170.
Koh J, Chen G, Yoo MJ, Zhu N, Dufresne D, Erickson JE, Shao H, Chen S, 2015. Comparative proteomic analysis of Brassica napus in response to drought stress. J Proteome Res 14 (8): 3068-3081. https://doi.org/10.1021/pr501323d
Kottapalli KR, Rakwal R, Shibato J, Burow G, Tissue D, Burke J, Puppala N, Burow M, Payton P, 2009. Physiology and proteomics of the water-deficit stress response in three contrasting peanut genotypes. Plant Cell Environ 32 (4): 380-407. https://doi.org/10.1111/j.1365-3040.2009.01933.x
Kregel K, 2002. Heat shock proteins: modifying factors in physiological stress responses and acquired thermotolerance. J Appl Physiol 92(5): 2177-2186. https://doi.org/10.1152/japplphysiol.01267.2001
Lan T, Jiang D, Xie ZJ, Dai TB, Jing Q, Cao WX, 2004. Effects of post-anthesis drought and waterlogging on grain quality traits in different specialty wheat varieties. J Soil Water Conserv 18 (1): 193-196.
Lata C, Gupta S, Prasad M, 2013. Foxtail millet: a model crop for genetic and genomic studies in bioenergy grasses. Crit Rev Biotechnol 33 (3): 328-343. https://doi.org/10.3109/07388551.2012.716809
Li C, Yue J, Wu X, Xu C, Yu J, 2014. An ABA-responsive DRE-binding protein gene from Setaria italica, SiARDP, the target gene of SiAREB, plays a critical role under drought stress. J Exp Bot 65 (18): 5415-5427. https://doi.org/10.1093/jxb/eru302
Li P, Chen J, Wu P, 2011. Agronomic characteristics and grain yield of 30 spring wheat genotypes under drought stress and nonstress conditions. Agron J 103: 1619-1628. https://doi.org/10.2134/agronj2011.0013
Liu J, Zhang Y, Liu Y, Zhang A, Zhao W, Li S, 2014. Analysis of protein components in foxtail millet. Food & Machinery 6: 39-42. (in Chinese).
Liu K, Qi S, Li D, Jin C, Gao C, Duan S, Feng B, Chen M, 2017. TRANSPARENT TESTA GLABRA 1 ubiquitously regulates plant growth and development from Arabidopsis to foxtail millet (Setaria italica). Plant Sci 254: 60-69. https://doi.org/10.1016/j.plantsci.2016.10.010
Lu D, Lu W, 2013. Effects of heat stress during grain filling on the functional properties of flour from fresh waxy maize. Cereal Chem 90: 65-69. https://doi.org/10.1094/CCHEM-03-12-0035-R
Lu X, 2012. Effects of water stress on protein component of rice grain. Food & Machinery 28 (5): 63-65. (in Chinese).
Ma Z, Huang G, Gan W, 2005. Multi-scale temporal characteristics of the dryness/wetness over northern China during the last century. Chinese Journal of Atmospheric Sciences 29 (5): 671-682. (in Chinese).
Mann M, Jensen ON, 2003. Proteomic analysis of post-translational modifications. Nature Biotechnol 21 (3): 255. https://doi.org/10.1038/nbt0303-255
Parker R, Flowers T, Moore A, Harpham N, 2006. An accurate and reproducible method for proteome profiling of the effects of salt stress in the rice leaf lamina. J Exp Bot 57 (5): 1109. https://doi.org/10.1093/jxb/erj134
Pierre CS, Peterson CJ, Ross AS, Ohm J, Verhoeven MC, Larson M, Hoefer B, 2007. Change in grain protein composition of winter wheat cultivars under different levels of N and water stress. In: Wheat production in stressed environments. Springer, Dordrecht, pp: 535-542. https://doi.org/10.1007/1-4020-5497-1_65
Saint Pierre C, Peterson CJ, Ross AS, Ohm JB, Verhoeven MC, Larson M, Hoefer B, 2008. Winter wheat genotypes under different levels of nitrogen and water stress: Changes in grain protein composition. J Cereal Sci 47: 407-416. https://doi.org/10.1016/j.jcs.2007.05.007
Samarah NH, Alqudah AM, Amayreh JA, McAndrews GM, 2009. The effect of late-terminal drought stress on yield components of four barley cultivars. J Agron Crop Sci 195: 427-441. https://doi.org/10.1111/j.1439-037X.2009.00387.x
Shen YX, Guo WS, Zhou Y, Zhu XK, Feng CN, Peng YX, 2006. Effects of salinity stress on the dynamic changes in the accumulation of grain protein and its components in wheat. Journal of Triticeae Crops 26 (6): 100-103. (in Chinese).
Simon WJ, 2010. Identification of Arabidopsis salt and osmotic stress responsive proteins using two-dimensional difference gel electrophoresis and mass spectrometry. Proteomics 5 (16): 4185-4196. https://doi.org/10.1002/pmic.200401282
Sunilkumar BA, Tareke E, 2016. Identification of discrepancies in grain quality and grain protein composition through avenin proteins of oat after an effort to increase protein content. Agr Food Security 5: 7. https://doi.org/10.1186/s40066-016-0056-6
Suty L, Lequeu J, Lançon A, Etienne P, Petitot AS, Blein JP, 2003. Preferential induction of 20S proteasome subunits during elicitation of plant defense reactions: towards the characterization of "plant defense proteasomes". Int J Biochem Cell Biol 35 (5): 637-650. https://doi.org/10.1016/S1357-2725(02)00386-2
Taniguchi K, 2016. Future changes in precipitation and water resources for Kanto Region in Japan after application of pseudo global warming method and dynamical downscaling. J Hydrol: Reg Stud 8: 287-303. https://doi.org/10.1016/j.ejrh.2016.10.004
Veeranagamallaiah G, Jyothsnakumari G, Thippeswamy M, Chandra Obul Reddy P, Surabhi GK, Sriranganayakulu G, Mahesh Y, Rajasekhar B, Madhurarekha C, Sudhakar C, 2008. Proteomic analysis of salt stress responses in foxtail millet (Setaria italica L. cv. Prasad) seedlings. Plant Sci 175 (5): 631-641. https://doi.org/10.1016/j.plantsci.2008.06.017
Wang M, Li P, Li C, Pan Y, Jiang X, Zhu D, Zhao Q, Yu J, 2014. SiLEA14, a novel atypical LEA protein, confers abiotic stress resistance in foxtail millet. BMC Plant Biol 14 (1): 1-16. https://doi.org/10.1186/s12870-014-0290-7
Wang W, Vinocur B, Shoseyov O, Altman A, 2004. Role of plant heat-shock proteins and molecular chaperones in the abiotic stress response. Trends Plant Sci 9 (5): 244-252. https://doi.org/10.1016/j.tplants.2004.03.006
Wang X, Jun MA, Zhang GY, Xi-Huan LI, Wang XF, Zhi-Ying MA, 2007. Proteomic analysis of cotton leaf under Verticillium dahliae stress. Cotton Sci 19 (4): 273-278. (in Chinese).
Wang Y, Li L, Tang S, Liu J, Zhang H, Zhi H, Jia G, Diao X, 2016. Combined small RNA and degradome sequencing to identify miRNAs and their targets in response to drought in foxtail millet. BMC Genet 17: 57. https://doi.org/10.1186/s12863-016-0364-7
Wang Z, He F, Fang W, Liao Y, 2013. Assessment of physical vulnerability to agricultural drought in China. Natural Hazards 67 (2): 645-657. https://doi.org/10.1007/s11069-013-0594-1
Wu C, 1995. Heat shock transcription factors: structure and regulation. Ann Rev Cell Devel Biol 11 (11): 441. https://doi.org/10.1146/annurev.cb.11.110195.002301
Wu K, Liu H, Sultan MARF, Liu Xl, Zhang J, Yu F, Zhao Hx, 2015. Physiological and comparative proteomic analysis reveals different drought responses in roots and leaves of drought-tolerant wild wheat (Triticum boeoticum). PLoS One 10: e0121852. https://doi.org/10.1371/journal.pone.0121852
Wu Y, Mirzaei M, Pascovici D, Chick JM, Atwell BJ, Haynes PA, 2016. Quantitative proteomic analysis of two different rice varieties reveals that drought tolerance is correlated with reduced abundance of photosynthetic machinery and increased abundance of ClpD1 protease. J Proteomics 143: 73-82. https://doi.org/10.1016/j.jprot.2016.05.014
Yadav A, Khan Y, Prasad M, 2016. Dehydration-responsive miRNAs in foxtail millet: genome-wide identification, characterization and expression profiling. Planta 243 (3): 749-766. https://doi.org/10.1007/s00425-015-2437-7
Yi F, Chen J, Yu J, 2015. Global analysis of uncapped mRNA changes under drought stress and microRNA-dependent endonucleolytic cleavages in foxtail millet. BMC Plant Biol 15: 241. https://doi.org/10.1186/s12870-015-0632-0
Yu J, Ahmedna M, Goktepe I, 2007. Peanut protein concentrate: Production and functional properties as affected by processing. Food Chem 103: 121-129. https://doi.org/10.1016/j.foodchem.2006.08.012
Zadraznik T, Egge-Jacobsen W, Meglic V, Sustar-Vozlic J, 2017. Proteomic analysis of common bean stem under drought stress using in-gel stable isotope labeling. J Plant Physiol 209: 42-50. https://doi.org/10.1016/j.jplph.2016.10.015
Zhang M, Lv D, Ge P, Bian Y, Chen G, Zhu G, Li X, Yan Y, 2014. Phosphoproteome analysis reveals new drought response and defense mechanisms of seedling leaves in bread wheat (Triticum aestivum L.). J Proteomics 109: 290-308. https://doi.org/10.1016/j.jprot.2014.07.010
Zörb C, Schmitt S, Mühling KH, 2010. Proteomic changes in maize roots after short-term adjustment to saline growth conditions. Proteomics 10 (24): 4441. https://doi.org/10.1002/pmic.201000231
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