Abstract
In a changing climate, drought stress accounts for significant crop yield loss. To test the hypothesis that proteins play an important role in plant drought tolerance, we conducted physiological and proteomic analyses to investigate the stress responses of two sugar beet (Beta vulgaris L.) cultivars with contrasting tolerance to drought stress. Under drought, the tolerant cultivar had higher relative water content, root length, dry weight, and root system area than the drought-sensitive cultivar. In addition, the tolerant cultivar had higher antioxidant enzyme activities than the sensitive cultivar to prevent ROS damage under drought stress conditions. Proteomic analysis resulted in identification of 23 and 27 drought-responsive proteins in the sensitive and tolerant cultivars, respectively. Based on their functions, these proteins were classified into nine categories. Many proteins in several different biological processes showed different abundance patterns between the genotypes (for example, oxygen-evolving enhancer proteins, choline monooxygenase, and malate dehydrogenase). Although some proteins changed similarly in trend between the two genotypes, they showed different levels of changes (for example, S-adenosylmethionine synthase). Furthermore, the poor correlation between transcription and protein levels was confirmed in this study. Our findings would lead to an improved understanding of the integrated physiology and proteome responses of the different sugar beet genotypes under drought stress.
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References
Aebi H (1984) Catalase in vitro. Method Enzymol 105:121–126
Alvarez S, Roy Choudhury S, Pandey S (2014) Comparative quantitative proteomics analysis of the ABA response of roots of drought-sensitive an drought-tolerant wheat varieties identifies proteomic signatures of drought adaptability. J Proteom Res 13:1688–1701. doi:10.1021/pr401165b
Apel K, Hirt H (2004) Reactive oxygen species: metabolism, oxidative stress, and signal transduction. Annu Rev Plant Biol 55:373–399. doi:10.1146/annurev.arplant.55.031903.141701
Asada K (1997) The role of ascorbate peroxidase and monodehydroascorbate reductase in H2O2 scavenging in plants. Cold Spring Harb Monogr Arch 34: 715–735. doi:10.1101/087969502.34.715
Begara-Morales JC, Sánchez-Calvo B, Chaki M, Valderrama R, Mata-Pérez C, López-Jaramillo J, Padilla MN, Carreras A, Corpas FJ, Barroso JB (2014) Dual regulation of cytosolic ascorbate peroxidase (APX) by tyrosine nitration and S-nitrosylation. J Exp Bot 65:527–538. doi:10.1093/jxb/ert396
Biswas DK, Jiang GM (2011) Differential drought-induced modulation of ozone tolerance in winter wheat species. J Exp Bot 62:4153–4162. doi:10.1093/jxb/err104
Bota J, Medrano H, Flexas J (2004) Is photosynthesis limited by decreased Rubisco activity and RuBP content under progressive water stress? New Phytol 162:671–681. doi:10.1111/j.1469-8137.2004.01056.x
Büyük İ, Inal B, Ilhan E, Tanriseven M, Aras S, Erayman M (2016) Genome-wide identification of salinity responsive HSP70s in common bean. Mol Biol Rep 43:1251–1266. doi:10.1007/s11033-016-4057-0
Chen TH, Murata N (2008) Glycine betaine: an effective protectant against abiotic stress in plants. Trends Plant Sci 13:499–505. doi:10.1016/j.tplants.2008.06.007
Chołuj D, Karwowska R, Jasi´nska M, Haber G (2004) Growth and dry matter partitioning in sugar beet plants (Beta vulgaris L.) under moderate drought. Plant Soil Environ 50:265–272
Chołuj D, Karwowska R, Ciszewska A, Jasi´nska M (2008) Influence of long-term drought stress on osmolyte accumulation in sugar beet (Beta vulgaris L.) plants. Acta Physol Plant 30:679–687. doi:10.1007/s11738-008-0166-2
Davis DG, Swanson HR (1984) Activity of stress-related enzymes in the perennial weed leafy spurge (Euphorbia esula L.). Environ Exp Bot 46:95–108
Faghani E, Gharechahi J, Komatsu S, Mirzaei M, Khavarinejad RA, Najafi F, Farsad LK, Salekdeh GH (2015) Comparative physiology and proteomic analysis of two wheat genotypes contrasting in drought tolerance. J Proteom 114:1–15. doi:10.1016/j.jprot.2014.10.018
Feller U, Anders I, Mae T (2008) Rubiscolytics: fate of rubisco after its enzymatic function in a cell is terminated. J Exp Bot 59:1615–1624. doi:10.1093/jxb/erm242
Gazanchian A, Hajheidari M, Sima NK, Salekdeh GH (2007) Proteome response of Elymus elongatum to severe water stress and recovery. J Exp Bot 58:291–300. doi:10.1093/jxb/erl226
Hajheidari M, Abdollahian-Noghabi M, Askari H, Heidari M, Sadeghian SY, Ober ES, Salekdeh GH (2005) Proteome analysis of sugar beet leaves under drought stress. Proteomics 5:950–960. doi:10.1002/pmic.200401101
Harb A, Krishnan A, Ambavaram MM, Pereira A (2010) Molecular and physiological analysis of drought stress inArabidopsis reveals early responses leading to acclimation in plant growth. Plant Physiol 154:1254–1271. doi:10.1104/pp.110.161752
Kang G, Li G, Xu W, Peng X, Han Q, Zhu Y, Guo T (2012) Proteomics reveals the effects of salicylicacid on growth and tolerance to subsequent drought stress in wheat. J Proteom Res 11:6066–6079. doi:10.1021/pr300728y
Kaur N, Dhawan M, Sharma I, Pati PK (2016) Interdependency of Reactive Oxygen Species generating and scavenging system in salt sensitive and salt tolerant cultivars of rice. BMC Plant Biol 16:131. doi:10.1186/s12870-016-0824-2
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 Proteom Res 14:3068–3081. doi:10.1021/pr501323d
Köllner TG, Lenk C, Zhao N, Seidl-Adams I, Gershenzon J, Chen F, Degenhardt J (2010) Herbivore-induced. SABATH methyltransferases of maize that methylate anthranilic acid using s-adenosyl-L-methionine. Plant Physiol 153:1795–1807. doi:10.1104/pp.110.158360
Komatsu S, Makino T, Yasue H (2013) Proteomic and biochemical analyses of the cotyledon and root of flooding-stressed soybean plants. PLoS ONE 8:e65301. doi:10.1371/journal.pone.0065301
Leng L, Liang Q, Jiang J, Zhang C, Hao Y, Wang X, Su W (2017) A subclass of HSP70s regulate development and abiotic stress responses in Arabidopsis thaliana. J Plant Res 130:349–363. doi:10.1007/s10265-016-0900-6
Li H, Cao H, Wang Y, Pang Q, Ma C, Chen S (2009) Proteomic analysis of sugar beet apomictic monosomic addition line M14. J Proteom 73:297–308. doi:10.1016/j.jprot.2009.09.012
Li H, Pan Y, Zhang Y, Wu C, Ma C, Yu B, Zhu N, Koh J, Chen S (2015) Salt stress response of membrane proteome of sugar beet monosomic addition line M14. J Proteom 127:18–33. doi:10.1016/j.jprot.2015.03.025
Luo D, Niu X, Yu J, Yan J, Gou X, Lu BR, Liu Y (2012) Rice choline monooxygenase (OsCMO) protein functions in enhancing glycine betaine biosynthesis in transgenic tobacco but does not accumulate in rice (Oryza sativa L. ssp. japonica). Plant Cell Rep 31:1625–1635. doi:10.1007/s00299-012-1276-2
Ma H, Song L, Shu Y, Wang S, Niu J, Wang Z, Yu T, Gu W, Ma H (2012) Comparative proteomic analysis of seedling leaves of different salt tolerant soybean genotypes. J Proteom 75:1529–1546. doi:10.1016/j.jprot.2011.11.026
Mohammadi PP, Moieni A, Hiraga S, Komatsu S (2012) Organ-specific proteomic analysis of drought-stressed soybean seedlings. J Proteom 75:1906–1923. doi:10.1016/j.jprot.2011.12.041
Nakano Y, Asada K (1981) Hydrogen peroxide is scavenged by ascorbate-specific peroxidase in spinach chloroplasts. Plant Cell Physiol 22:867–880
Pidgeon JD, Werker AR, Jaggard KW, Richter GM, Lister DH, Jones PD (2001) Climatic impact on the productivity of sugar beet in Europe, 1961–1995. Field Crop Res 109:27–37. doi:10.1016/S0168-1923(01)00254-4
Pitzschke A, Forzani C, Hirt H (2006) Reactive oxygen species signaling in plants. Antioxid Redox Signal 8:1757–1764. doi:10.1089/ars.2006.8.1757
Rajabi A, Ranji Z, Griffiths Z, Ober ES (2007) A preliminary study on genotypic differences in transcript abundance of drought responsive genes in sugar beet. Pak J Biol Sci 10:3599–3605. doi:10.3923/pjbs.2007.3599.3605
Roje S (2006) S-Adenosyl-L-methionine: beyond the universal methyl group donor. Phytochemistry 67:1686–1698. doi:10.1016/j.phytochem.2006.04.019
Schroda M, Vallon O, Wollman FA, Beck CF (1999) A chloroplast-targeted heat shock protein 70 (HSP70) contributes to the photoprotection and repair of photosystem II during and after Photoinhibition. Plant Cell 11:1165–1678. doi:10.1105/tpc.11.6.1165
Shi H, Ye T, Chan Z (2013) Comparative proteomic and physiological analyse sreveal the protective effect of exogenous polyamines in the Bermuda grass (Cynodon dactylon) response to salt and drought stresses. J Proteom Res 12:4951–4964. doi:10.1021/pr400479k
Stewart RR, Bewley JD (1980) Lipid peroxidation associated with accelerated aging of soybean axes. Plant Physiol 65:245–248
Taheri F, Nematzadeh G, Zamharir MG, Nekouei MK, Naghavi M, Mardi M, Salekdeh GH (2011) Proteomic analysis of the Mexican lime tree response to “Candidatus Phytoplasma aurantifolia” infection. Mol Biosyst 7:3028–3035. doi:10.1039/c1mb05268c
Torabi S, Wissuwa M, Heidari M, Naghavi MR, Gilany K, Hajirezaei MR, Omidi M, Yazdi-Sa Omidi M, Yazdi-Samadi B, Ismail AM, Salekdeh GH (2009) A comparative proteome approach to decipher the mechanism of rice adaptation to phosphorous deficiency. Proteomics 9:159–170. doi:10.1002/pmic.200800350
Wang QJ, Sun H, Dong QL, Sun TY, Jin ZX, Hao YJ, Yao YX (2016) The enhancement of tolerance to salt and cold stresses by modifying the redox state and salicylic acid content via the cytosolic malate dehydrogenase gene in transgenic apple plants. Plant Biotechnol J 14:1986–1997. doi:10.1111/pbi.12556
Yamada N, Takahashi H, Kitou K, Sahashi K, Tamagake H, Tanaka Y, Takabe T (2015) Suppressed expression of choline monooxygenase in sugar beet on the accumulation of glycinebetaine. Plant Physiol Biochem 96:217–221. doi:10.1016/j.plaphy.2015.06.014
Yao YX, Dong QL, Zhai H, You CX, Hao YJ (2011) The functions of an apple cytosolic malate dehydrogenase gene in growth and tolerance to cold and salt stresses. Plant Physiol Biochem 49:257–264. doi:10.1016/j.plaphy.2010.12.009
Yi X, McChargue M, aborde S, Frankel LK, Bricker TM (2005) The manganese-stabilizing protein is required for photosystem II assembly/stability and photoautotrophyin higher plants. J Biol Chem 280:16170–16174. doi:10.1074/jbc.M501550200
Zadražnik T, Hollung K, Egge-Jacobsen W, Meglič V, Šuštar-Vozlič J (2013) Differential proteomic analysis of drought stress response in leaves of common bean (Phaseolus vulgaris L.). J Proteom 78:254–272. doi:10.1016/j.jprot.2012.09.021
Zhao Y, Du H, Wang Z, Huang B (2011) Identification of proteins associated with water-deficit tolerance inC4 perennial grass species, Cynodondactylon × Cynodon transvaalensis and Cynodon dactylon. Physiol Plant 141:40–55. doi:10.1111/j.1399-3054.2010.01419.x
Zhu JK (2002) Salt and drought stress signal transduction in plants. Annu Rev Plant Biol 253:247–273. doi:10.1146/annurev.arplant.53.091401.143329
Acknowledgements
Lisa David from University of Florida is acknowledged for critical reading of the manuscript. This work was supported by the International Cooperation Project (Project No. 2010DFAN31530: Drought resistance, salt tolerance breeding, and cultivation for energy beet); Project of National Natural Science Foundation of China (Project No. 31271779: Excavation of germplasm resources of higher salt tolerance and osmotic regulation mechanism in sugar beet); Project of National Natural Science Foundation of Heilongjiang province (Project No. C2016048: A preliminary study on the molecular drought tolerance mechanism of T510 strain of sugar beet); and Youth Science Funds of Heilongjiang University (Project No. QL201511: A preliminary study on salt tolerance mechanism of T510 strains of sugar beet).
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Wang, Y., Peng, C., Zhan, Y. et al. Comparative Proteomic Analysis of Two Sugar Beet Cultivars with Contrasting Drought Tolerance. J Plant Growth Regul 36, 537–549 (2017). https://doi.org/10.1007/s00344-017-9703-9
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DOI: https://doi.org/10.1007/s00344-017-9703-9