Identification of Drought-Responsive Proteins of Sensitive and Tolerant Tea (Camellia sinensis L) Clones under Normal and Drought Stress Conditions

Author(s): Mehdi Rahimi*, Mojtaba Kordrostami, Mojtaba Mortezavi, Sanam SafaeiChaeikar.

Journal Name: Current Proteomics

Volume 17 , Issue 3 , 2020

Become EABM
Become Reviewer

Graphical Abstract:


Abstract:

Background: Tea is one of the most popular calming drinks. Drought is a major environmental factor that limited the growth and development of plants.

Objective: Therefore, the identification of proteins under the drought stress conditions in tea can have an essential role in the breeding programs and tea production.

Methods: For this purpose, 14 tea clones were studied under normal and drought stress conditions in two separate experiments, and the leaves of the clones were stored at −80°C. After the identification of two clones (100 and 278) as tolerant and sensitive clones, respectively, the proteomics approach was used to compare the leaf protein profile changes under both conditions.

Results: The results of proteomics showed about 500 detectable protein spots, of which 250 spots were repeatable. Among the 250 reproducible spots, 16 spots responded to the drought stress, which showed the highest amount of variation among the treatments. Thioredoxin, peroxidase, superoxide dismutase, ribosomal protein, and hsp70 were mentioned among the identified proteins. These proteins were involved in various cellular functions.

Conclusion: Identified proteins also had a crucial role in regulating carbohydrate and nitrogen metabolism and the scavenging of the Reactive Oxygen Species (ROS). Upregulation of proteins involved in protein processing (ribosomal protein), oxygen species scavenging, and defense (Superoxide dismutase, Peroxidase, and thioredoxin) may increase plant adaptation to drought stress. This study was the first report that showed ribosomal protein L32 was significantly changed in tea against drought stress response. Therefore, these proteins can protect the plant against drought stress. This study partially identified the drought stress proteins in the tea plant.

Keywords: Mass spectrometry, tea, drought tolerance, protein, spot, ribosome, clones.

[1]
De Costa, W.; Mohotti, A.J.; Wijeratne, M.A. Ecophysiology of tea. Braz. J. Plant Physiol., 2007, 19(4), 299-332.
[http://dx.doi.org/10.1590/S1677-04202007000400005]
[2]
Panda, H. The complete book on cultivation and manufacture of tea; Asia Pacific Business Press Incorporated: New Dehli, India, 2011, p. 592.
[3]
Hajiboland, R. Environmental and nutritional requirements for tea cultivation. Folia Hortic., 2017, 29(2), 199-220.
[http://dx.doi.org/10.1515/fhort-2017-0019]
[4]
Farooq, M.; Wahid, A.; Kobayashi, N.; Fujita, D.; Basra, S. Plant drought stress: effects, mechanisms and management. Agron. Sustain. Dev., 2009, 29(1), 185-212.
[http://dx.doi.org/10.1051/agro:2008021]
[5]
Anjum, S.A.; Xie, X.Y.; Wang, L.C.; Saleem, M.F.; Man, C.; Lei, W. Morphological, physiological and biochemical responses of plants to drought stress. Afr. J. Agric. Res., 2011, 6(9), 2026-2032.
[6]
Kwon, S.J.; Kwon, S.I.; Bae, M.S.; Cho, E.J.; Park, O.K. Role of the methionine sulfoxide reductase MsrB3 in cold acclimation in Arabidopsis. Plant Cell Physiol., 2007, 48(12), 1713-1723.
[http://dx.doi.org/10.1093/pcp/pcm143] [PMID: 17956860]
[7]
Hajheidari, M.; Abdollahian-Noghabi, M.; Askari, H.; Heidari, M.; Sadeghian, S.Y.; Ober, E.S.; Salekdeh, G.H. Proteome analysis of sugar beet leaves under drought stress. Proteomics, 2005, 5(4), 950-960.
[http://dx.doi.org/10.1002/pmic.200401101] [PMID: 15712235]
[8]
Munns, R. Genes and salt tolerance: bringing them together. New Phytol., 2005, 167(3), 645-663.
[http://dx.doi.org/10.1111/j.1469-8137.2005.01487.x] [PMID: 16101905]
[9]
Seki, M.; Narusaka, M.; Ishida, J.; Nanjo, T.; Fujita, M.; Oono, Y.; Kamiya, A.; Nakajima, M.; Enju, A.; Sakurai, T.; Satou, M.; Akiyama, K.; Taji, T.; Yamaguchi-Shinozaki, K.; Carninci, P.; Kawai, J.; Hayashizaki, Y.; Shinozaki, K. Monitoring the expression profiles of 7000 Arabidopsis genes under drought, cold and high-salinity stresses using a full-length cDNA microarray. Plant J., 2002, 31(3), 279-292.
[http://dx.doi.org/10.1046/j.1365-313X.2002.01359.x] [PMID: 12164808]
[10]
Vinocur, B.; Altman, A. Recent advances in engineering plant tolerance to abiotic stress: achievements and limitations. Curr. Opin. Biotechnol., 2005, 16(2), 123-132.
[http://dx.doi.org/10.1016/j.copbio.2005.02.001] [PMID: 15831376]
[11]
Gygi, S.P.; Rist, B.; Aebersold, R. Measuring gene expression by quantitative proteome analysis. Curr. Opin. Biotechnol., 2000, 11(4), 396-401.
[http://dx.doi.org/10.1016/S0958-1669(00)00116-6] [PMID: 10975460]
[12]
Zivy, M.; de Vienne, D. Proteomics: a link between genomics, genetics and physiology. Plant Mol. Biol., 2000, 44(5), 575-580.
[http://dx.doi.org/10.1023/A:1026525406953] [PMID: 11198419]
[13]
Kosová, K.; Vítámvás, P.; Urban, M.O.; Prášil, I.T.; Renaut, J. Plant abiotic stress proteomics: the major factors determining alterations in cellular proteome. Front. Plant Sci., 2018, 9, 22.
[14]
Michaletti, A.; Naghavi, M.R.; Toorchi, M.; Zolla, L.; Rinalducci, S. Metabolomics and proteomics reveal drought-stress responses of leaf tissues from spring-wheat. Sci. Rep., 2018, 8, 18.
[http://dx.doi.org/10.1038/s41598-018-24012-y]
[15]
Nazari, M.; Moosavi, S.S.; Maleki, M. Morpho-physiological and proteomic responses of Aegilops tauschii to imposed moisture stress. Plant Physiol. Biochem., 2018, 132, 445-452.
[http://dx.doi.org/10.1016/j.plaphy.2018.09.031] [PMID: 30292161]
[16]
Prinsi, B.; Negri, A.S.; Failla, O.; Scienza, A.; Espen, L. Root proteomic and metabolic analyses reveal specific responses to drought stress in differently tolerant grapevine rootstocks. BMC Plant Biol., 2018, 18(1), 28.
[http://dx.doi.org/10.1186/s12870-018-1343-0]
[17]
Rezaee, F.; Lahouti, M.; Maleki, M.; Ganjeali, A. Comparative proteomics analysis of white top (Lepidium draba L.) seedlings in response to exogenous glucose. Int. J. Biol. Macromol., 2018, 120(Pt B), 2458-2465.
[http://dx.doi.org/10.1016/j.ijbiomac.2018.09.016] [PMID: 30193920]
[18]
Li, Q.; Li, J.; Liu, S.; Huang, J.; Lin, H.; Wang, K.; Cheng, X.; Liu, Z. A comparative proteomic analysis of the buds and the young expanding leaves of the tea plant (Camellia sinensis L.). Int. J. Mol. Sci., 2015, 16(6), 14007-14038.
[http://dx.doi.org/10.3390/ijms160614007] [PMID: 26096006]
[19]
Liu, S.; Gao, J.; Chen, Z.; Qiao, X.; Huang, H.; Cui, B.; Zhu, Q.; Dai, Z.; Wu, H.; Pan, Y.; Yang, C.; Liu, J. Comparative proteomics reveals the physiological differences between winter tender shoots and spring tender shoots of a novel tea (Camellia sinensis L.) cultivar ever growing in winter. BMC Plant Biol., 2017, 17(1), 12.
[http://dx.doi.org/10.1186/s12870-017-1144-x.]
[20]
Wu, L-Y.; Fang, Z-T.; Lin, J-K.; Sun, Y.; Du, Z-Z.; Guo, Y-L.; Liu, J-H.; Liang, Y-R.; Ye, J-H. Complementary iTRAQ proteomic and transcriptomic analyses of leaves in tea plant (Camellia sinensis L.) with different maturity and regulatory network of flavonoid biosynthesis. J. Proteome Res., 2019, 18(1), 252-264.
[PMID: 30427694]
[21]
Xu, Q.; Wang, Y.; Ding, Z.; Fan, K.; Ma, D.; Zhang, Y.; Yin, Q. Aluminum induced physiological and proteomic responses in tea (Camellia sinensis) roots and leaves. Plant Physiol. Biochem., 2017, 115, 141-151.
[http://dx.doi.org/10.1016/j.plaphy.2017.03.017] [PMID: 28364710]
[22]
Yongguang, H.; Yongzong, L.; Jian, L. Comparative proteomics analysis of tea leaves exposed to subzero temperature: Molecular mechanism of freeze injury. Int. J. Agric. Biol. Eng., 2013, 6(4), 27-34.
[23]
Zhou, Q.; Chen, Z.; Lee, J.; Li, X.; Sun, W. Proteomic analysis of tea plants (Camellia sinensis) with purple young shoots during leaf development. PLoS One, 2017, 12(5), 18.
[24]
Zhou, L.; Xu, H.; Mischke, S.; Meinhardt, L.W.; Zhang, D.; Zhu, X.; Li, X.; Fang, W. Exogenous abscisic acid significantly affects proteome in tea plant (Camellia sinensis) exposed to drought stress. Hortic. Res., 2014, 1, 9.
[25]
Rahimi, M.; Kordrostami, M.; Mortezavi, M. Evaluation of tea (Camellia sinensis L.) biochemical traits in normal and drought stress conditions to identify drought tolerant clones. Physiol. Mol. Biol. Plants, 2019, 25(1), 59-69.
[http://dx.doi.org/10.1007/s12298-018-0564-x] [PMID: 30804630]
[26]
Hurkman, W.J.; Tanaka, C.K. Solubilization of plant membrane proteins for analysis by two-dimensional gel electrophoresis. Plant Physiol., 1986, 81(3), 802-806.
[http://dx.doi.org/10.1104/pp.81.3.802] [PMID: 16664906]
[27]
Ó’Fágáin, C. Lyophilization of proteins.Protein Purification Protocols; Cutler, P., Ed.; Humana Press: USA, 2004, pp. 309-321.
[28]
Bradford, M.M. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem., 1976, 72(1-2), 248-254.
[http://dx.doi.org/10.1016/0003-2697(76)90527-3] [PMID: 942051]
[29]
Blum, H.; Beier, H.; Gross, H.J. Improved silver staining of plant proteins, RNA and DNA in polyacrylamide gels. Electrophoresis, 1987, 8, 93-99.
[http://dx.doi.org/10.1002/elps.1150080203]
[30]
Melanie-9.1.1-software Melanie 2D gel analysis software for protein expression profiling; SIB Swiss Institute of Bioinformatics: Switzerland, 2018.
[31]
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.
[http://dx.doi.org/10.1146/annurev.arplant.57.032905.105444] [PMID: 16669782]
[32]
Hadiarto, T.; Tran, L-S.P. Progress studies of drought-responsive genes in rice. Plant Cell Rep., 2011, 30(3), 297-310.
[http://dx.doi.org/10.1007/s00299-010-0956-z] [PMID: 21132431]
[33]
Jogaiah, S.; Govind, S.R.; Tran, L.S.P. Systems biology-based approaches toward understanding drought tolerance in food crops. Crit. Rev. Biotechnol., 2013, 33(1), 23-39.
[http://dx.doi.org/10.3109/07388551.2012.659174] [PMID: 22364373]
[34]
Tran, L-S.P.; Urao, T.; Qin, F.; Maruyama, K.; Kakimoto, T.; Shinozaki, K.; Yamaguchi-Shinozaki, K. Functional analysis of AHK1/ATHK1 and cytokinin receptor histidine kinases in response to abscisic acid, drought, and salt stress in Arabidopsis. Proc. Natl. Acad. Sci. USA, 2007, 104(51), 20623-20628.
[http://dx.doi.org/10.1073/pnas.0706547105] [PMID: 18077346]
[35]
Valliyodan, B.; Nguyen, H.T. Understanding regulatory networks and engineering for enhanced drought tolerance in plants. Curr. Opin. Plant Biol., 2006, 9(2), 189-195.
[http://dx.doi.org/10.1016/j.pbi.2006.01.019] [PMID: 16483835]
[36]
Yang, S.; Vanderbeld, B.; Wan, J.; Huang, Y. Narrowing down the targets: towards successful genetic engineering of drought-tolerant crops. Mol. Plant, 2010, 3(3), 469-490.
[http://dx.doi.org/10.1093/mp/ssq016] [PMID: 20507936]
[37]
Mok, D.W.; Mok, M.C. Cytokinin metabolism and action. Annu. Rev. Plant Physiol. Plant Mol. Biol., 2001, 52(1), 89-118.
[http://dx.doi.org/10.1146/annurev.arplant.52.1.89] [PMID: 11337393]
[38]
Kakimoto, T. Identification of plant cytokinin biosynthetic enzymes as dimethylallyl diphosphate: ATP/ADP isopentenyltransferases. Plant Cell Physiol., 2001, 42(7), 677-685.
[http://dx.doi.org/10.1093/pcp/pce112] [PMID: 11479373]
[39]
Takei, K.; Sakakibara, H.; Sugiyama, T. Identification of genes encoding adenylate isopentenyltransferase, a cytokinin biosynthesis enzyme, in Arabidopsis thaliana. J. Biol. Chem., 2001, 276(28), 26405-26410.
[http://dx.doi.org/10.1074/jbc.M102130200] [PMID: 11313355]
[40]
Sakakibara, H. Nitrate-specific and cytokinin-mediated nitrogen signaling pathways in plants. J. Plant Res., 2003, 116(3), 253-257.
[http://dx.doi.org/10.1007/s10265-003-0097-3] [PMID: 12836045]
[41]
Sun, J.; Niu, Q-W.; Tarkowski, P.; Zheng, B.; Tarkowska, D.; Sandberg, G.; Chua, N-H.; Zuo, J. The Arabidopsis AtIPT8/PGA22 gene encodes an isopentenyl transferase that is involved in de novo cytokinin biosynthesis. Plant Physiol., 2003, 131(1), 167-176.
[http://dx.doi.org/10.1104/pp.011494] [PMID: 12529525]
[42]
Werner, T.; Schmülling, T. Cytokinin action in plant development. Curr. Opin. Plant Biol., 2009, 12(5), 527-538.
[http://dx.doi.org/10.1016/j.pbi.2009.07.002] [PMID: 19740698]
[43]
Davies, W.J.; Zhang, J. Root signals and the regulation of growth and development of plants in drying soil. Annu. Rev. Plant Biol., 1991, 42(1), 55-76.
[http://dx.doi.org/10.1146/annurev.pp.42.060191.000415]
[44]
Gan, S.; Amasino, R.M. Inhibition of leaf senescence by auto regulated production of cytokinin. Science, 1995, 270(5244), 1986-1988.
[http://dx.doi.org/10.1126/science.270.5244.1986] [PMID: 8592746]
[45]
Kim, H.J.; Ryu, H.; Hong, S.H.; Woo, H.R.; Lim, P.O.; Lee, I.C.; Sheen, J.; Nam, H.G.; Hwang, I. Cytokinin-mediated control of leaf longevity by AHK3 through phosphorylation of ARR2 in Arabidopsis. Proc. Natl. Acad. Sci. USA, 2006, 103(3), 814-819.
[http://dx.doi.org/10.1073/pnas.0505150103] [PMID: 16407152]
[46]
Riefler, M.; Novak, O.; Strnad, M.; Schmülling, T. Arabidopsis cytokinin receptor mutants reveal functions in shoot growth, leaf senescence, seed size, germination, root development, and cytokinin metabolism. Plant Cell, 2006, 18(1), 40-54.
[http://dx.doi.org/10.1105/tpc.105.037796] [PMID: 16361392]
[47]
Ha, S.; Vankova, R.; Yamaguchi-Shinozaki, K.; Shinozaki, K.; Tran, L-S.P. Cytokinins: metabolism and function in plant adaptation to environmental stresses. Trends Plant Sci., 2012, 17(3), 172-179.
[http://dx.doi.org/10.1016/j.tplants.2011.12.005] [PMID: 22236698]
[48]
Ma, Q-H. Genetic engineering of cytokinins and their application to agriculture. Crit. Rev. Biotechnol., 2008, 28(3), 213-232.
[http://dx.doi.org/10.1080/07388550802262205] [PMID: 18855152]
[49]
Peleg, Z.; Apse, M.P.; Blumwald, E. Engineering salinity and water-stress tolerance in crop plants: getting closer to the field.Adv. Botanical Res; Turkan, I., Ed.; Elsevier: CA, USA, 2011, pp. 405-443.
[50]
Qin, H.; Gu, Q.; Zhang, J.; Sun, L.; Kuppu, S.; Zhang, Y.; Burow, M.; Payton, P.; Blumwald, E.; Zhang, H. Regulated expression of an isopentenyltransferase gene (IPT) in peanut significantly improves drought tolerance and increases yield under field conditions. Plant Cell Physiol., 2011, 52(11), 1904-1914.
[http://dx.doi.org/10.1093/pcp/pcr125] [PMID: 21920877]
[51]
Rivero, R.M.; Kojima, M.; Gepstein, A.; Sakakibara, H.; Mittler, R.; Gepstein, S.; Blumwald, E. Delayed leaf senescence induces extreme drought tolerance in a flowering plant. Proc. Natl. Acad. Sci. USA, 2007, 104(49), 19631-19636.
[http://dx.doi.org/10.1073/pnas.0709453104] [PMID: 18048328]
[52]
Rivero, R.M.; Shulaev, V.; Blumwald, E. Cytokinin-dependent photorespiration and the protection of photosynthesis during water deficit. Plant Physiol., 2009, 150(3), 1530-1540.
[http://dx.doi.org/10.1104/pp.109.139378] [PMID: 19411371]
[53]
Igamberdiev, A.U.; Kleczkowski, L.A. Optimization of ATP synthase function in mitochondria and chloroplasts via the adenylate kinase equilibrium. Front. Plant Sci., 2015, 6, 10.
[http://dx.doi.org/10.3389/fpls.2015.00010]
[54]
Hahn, A.; Parey, K.; Bublitz, M.; Mills, D.J.; Zickermann, V.; Vonck, J.; Kühlbrandt, W.; Meier, T. Structure of a complete ATP synthase dimer reveals the molecular basis of inner mitochondrial membrane morphology. Mol. Cell, 2016, 63(3), 445-456.
[http://dx.doi.org/10.1016/j.molcel.2016.05.037] [PMID: 27373333]
[55]
Shi, H.; Ye, T.; Chan, Z. Comparative proteomic responses of two bermudagrass (Cynodon dactylon (L). Pers.) varieties contrasting in drought stress resistance. Plant Physiol. Biochem., 2014, 82, 218-228.
[http://dx.doi.org/10.1016/j.plaphy.2014.06.006] [PMID: 24992888]
[56]
Lee, R.S.; Pagan, J.; Wilke-Mounts, S.; Senior, A.E. Characterization of Escherichia coli ATP synthase beta-subunit mutations using a chromosomal deletion strain. Biochemistry, 1991, 30(28), 6842-6847.
[http://dx.doi.org/10.1021/bi00242a006] [PMID: 1829962]
[57]
Kottapalli, K.R.; Rakwal, R.; Shibato, J.; Burow, G.; Tissue, D.; Burke, J.; Puppala, N.; Burow, M.; Payton, P. Physiology and proteomics of the water-deficit stress response in three contrasting peanut genotypes. Plant Cell Environ., 2009, 32(4), 380-407.
[http://dx.doi.org/10.1111/j.1365-3040.2009.01933.x] [PMID: 19143990]
[58]
Zhou, S.; Li, M.; Guan, Q.; Liu, F.; Zhang, S.; Chen, W.; Yin, L.; Qin, Y.; Ma, F. Physiological and proteome analysis suggest critical roles for the photosynthetic system for high water-use efficiency under drought stress in Malus. Plant Sci., 2015, 236, 44-60.
[http://dx.doi.org/10.1016/j.plantsci.2015.03.017] [PMID: 26025520]
[59]
Valero-Galván, J.; González-Fernández, R.; Navarro-Cerrillo, R.M.; Gil-Pelegrín, E.; Jorrín-Novo, J.V. Physiological and proteomic analyses of drought stress response in Holm oak provenances. J. Proteome Res., 2013, 12(11), 5110-5123.
[http://dx.doi.org/10.1021/pr400591n] [PMID: 24088139]
[60]
Tezara, W.; Mitchell, V.; Driscoll, S.; Lawlor, D. Water stress inhibits plant photosynthesis by decreasing coupling factor and ATP. Nature, 1999, 401(6756), 914.
[http://dx.doi.org/10.1038/44842]
[61]
Cao, Y.; Luo, Q.; Tian, Y.; Meng, F. Physiological and proteomic analyses of the drought stress response in Amygdalus Mira (Koehne) Yü et Lu roots. BMC Plant Biol., 2017, 17(1), 16.
[62]
Ban, N.; Nissen, P.; Hansen, J.; Moore, P.B.; Steitz, T.A. The complete atomic structure of the large ribosomal subunit at 2.4 A resolution. Science, 2000, 289(5481), 905-920.
[http://dx.doi.org/10.1126/science.289.5481.905] [PMID: 10937989]
[63]
Barakat, A.; Szick-Miranda, K.; Chang, I.F.; Guyot, R.; Blanc, G.; Cooke, R.; Delseny, M.; Bailey-Serres, J. The organization of cytoplasmic ribosomal protein genes in the Arabidopsis genome. Plant Physiol., 2001, 127(2), 398-415.
[http://dx.doi.org/10.1104/pp.010265] [PMID: 11598216]
[64]
Hanson, C.L.; Videler, H.; Santos, C.; Ballesta, J.P.; Robinson, C.V. Mass spectrometry of ribosomes from Saccharomyces cerevisiae: implications for assembly of the stalk complex. J. Biol. Chem., 2004, 279(41), 42750-42757.
[http://dx.doi.org/10.1074/jbc.M405718200] [PMID: 15294894]
[65]
Fromont-Racine, M.; Senger, B.; Saveanu, C.; Fasiolo, F. Ribosome assembly in eukaryotes. Gene, 2003, 313, 17-42.
[http://dx.doi.org/10.1016/S0378-1119(03)00629-2] [PMID: 12957375]
[66]
Casati, P.; Walbot, V. Gene expression profiling in response to ultraviolet radiation in maize genotypes with varying flavonoid content. Plant Physiol., 2003, 132(4), 1739-1754.
[http://dx.doi.org/10.1104/pp.103.022871] [PMID: 12913132]
[67]
Ferreyra, M.L.F.; Pezza, A.; Biarc, J.; Burlingame, A.L.; Casati, P. Plant L10 ribosomal proteins have different roles during development and translation under UV-B stress. Plant Physiol., 2010, 110.
[68]
Mukhopadhyay, P.; Reddy, M.K.; Singla-Pareek, S.L.; Sopory, S.K. Transcriptional downregulation of rice rpL32 gene under abiotic stress is associated with removal of transcription factors within the promoter region. PLoS One, 2011, 6(11)e28058
[http://dx.doi.org/10.1371/journal.pone.0028058] [PMID: 22132208]
[69]
Moin, M.; Bakshi, A.; Madhav, M.S.; Kirti, P.B. Expression profiling of ribosomal protein gene family in dehydration stress responses and characterization of transgenic rice plants overexpressing RPL23A for water-use efficiency and tolerance to drought and salt stresses. Front Chem., 2017, 5, 97.
[http://dx.doi.org/10.3389/fchem.2017.00097] [PMID: 29184886]
[70]
Kachroo, A.; Kachroo, P. Fatty Acid-derived signals in plant defense. Annu. Rev. Phytopathol., 2009, 47, 153-176.
[http://dx.doi.org/10.1146/annurev-phyto-080508-081820] [PMID: 19400642]
[71]
Browse, J.; Somerville, C. Glycerolipid synthesis: biochemistry and regulation. Annu. Rev. Plant Biol., 1991, 42(1), 467-506.
[http://dx.doi.org/10.1146/annurev.pp.42.060191.002343]
[72]
Wallis, J.G.; Browse, J. Mutants of Arabidopsis reveal many roles for membrane lipids. Prog. Lipid Res., 2002, 41(3), 254-278.
[http://dx.doi.org/10.1016/S0163-7827(01)00027-3] [PMID: 11814526]
[73]
Zhang, M.; Barg, R.; Yin, M.; Gueta-Dahan, Y.; Leikin-Frenkel, A.; Salts, Y.; Shabtai, S.; Ben-Hayyim, G. Modulated fatty acid desaturation via overexpression of two distinct ω-3 desaturases differentially alters tolerance to various abiotic stresses in transgenic tobacco cells and plants. Plant J., 2005, 44(3), 361-371.
[http://dx.doi.org/10.1111/j.1365-313X.2005.02536.x] [PMID: 16236147]
[74]
Chi, X.; Zhang, Z.; Chen, N.; Zhang, X.; Wang, M.; Chen, M.; Wang, T.; Pan, L.; Chen, J.; Yang, Z. Isolation and functional analysis of fatty acid desaturase genes from peanut (Arachis hypogaea L.). PLoS One, 2017, 12(12), 28.
[75]
Cascella, K.; Jollivet, D.; Papot, C.; Léger, N.; Corre, E.; Ravaux, J.; Clark, M.S.; Toullec, J-Y. Diversification, evolution and sub-functionalization of 70kDa heat-shock proteins in two sister species of Antarctic krill: differences in thermal habitats, responses and implications under climate change. PLoS One, 2015, 10(4), 23.
[76]
Marček, T.; Tkalec, M.; Vidaković-Cifrek, Ž.; Ježić, M.; Ćurković-Perica, M. Expression of dehydrins, HSP70, Cu/Zn SOD, and RuBisCO in leaves of tobacco (Nicotiana tabacum L.) dihaploids under salt stress. In Vitro Cell. Dev. Biol. Plant, 2016, 52(3), 233-240.
[http://dx.doi.org/10.1007/s11627-016-9752-y]
[77]
Popović, Ž.D.; Subotić, A.; Nikolić, T.V.; Radojičić, R.; Blagojević, D.P.; Grubor-Lajšić, G.; Koštál, V. Expression of stress-related genes in diapause of European corn borer (Ostrinia nubilalis Hbn.). Comp. Biochem. Physiol. B Biochem. Mol. Biol., 2015, 186, 1-7.
[http://dx.doi.org/10.1016/j.cbpb.2015.04.004] [PMID: 25882225]
[78]
Yer, E.N.; Baloglu, M.C.; Ziplar, U.T.; Ayan, S.; Unver, T. Drought-responsive Hsp70 gene analysis in Populus at genome-wide level. Plant Mol. Biol. Report., 2016, 34(2), 483-500.
[http://dx.doi.org/10.1007/s11105-015-0933-3]
[79]
Heckathorn, S.A.; Ryan, S.L.; Baylis, J.A.; Wang, D.; Hamilton, E.W., III; Cundiff, L.; Luthe, D.S. In vivo evidence from an Agrostis stolonifera selection genotype that chloroplast small heat-shock proteins can protect photosystem II during heat stress. Funct. Plant Biol., 2002, 29(8), 935-946.
[http://dx.doi.org/10.1071/PP01191]
[80]
Wang, W.; Vinocur, B.; Shoseyov, O.; Altman, A. Role of plant heat-shock proteins and molecular chaperones in the abiotic stress response. Trends Plant Sci., 2004, 9(5), 244-252.
[http://dx.doi.org/10.1016/j.tplants.2004.03.006] [PMID: 15130550]
[81]
Sarkar, N.K.; Kim, Y.K.; Grover, A. Rice sHsp genes: genomic organization and expression profiling under stress and development. BMC Genomics, 2009, 10(1), 393.
[http://dx.doi.org/10.1186/1471-2164-10-393] [PMID: 19703271]
[82]
Sun, W.; Van Montagu, M.; Verbruggen, N. Small heat shock proteins and stress tolerance in plants. Biochim. Biophys. Acta, 2002, 1577(1), 1-9.
[http://dx.doi.org/10.1016/S0167-4781(02)00417-7] [PMID: 12151089]
[83]
Zou, J.; Liu, A.; Chen, X.; Zhou, X.; Gao, G.; Wang, W.; Zhang, X. Expression analysis of nine rice heat shock protein genes under abiotic stresses and ABA treatment. J. Plant Physiol., 2009, 166(8), 851-861.
[http://dx.doi.org/10.1016/j.jplph.2008.11.007] [PMID: 19135278]
[84]
Sato, Y.; Yokoya, S. Enhanced tolerance to drought stress in transgenic rice plants overexpressing a small heat-shock protein, sHSP17.7. Plant Cell Rep., 2008, 27(2), 329-334.
[http://dx.doi.org/10.1007/s00299-007-0470-0] [PMID: 17968552]
[85]
Bross, C.D.; Howes, T.R.; Abolhassani Rad, S.; Kljakic, O.; Kohalmi, S.E. Subcellular localization of Arabidopsis arogenate dehydratases suggests novel and non-enzymatic roles. J. Exp. Bot., 2017, 68(7), 1425-1440.
[http://dx.doi.org/10.1093/jxb/erx024] [PMID: 28338876]
[86]
Ehlting, J.; Mattheus, N.; Aeschliman, D.S.; Li, E.; Hamberger, B.; Cullis, I.F.; Zhuang, J.; Kaneda, M.; Mansfield, S.D.; Samuels, L.; Ritland, K.; Ellis, B.E.; Bohlmann, J.; Douglas, C.J. Global transcript profiling of primary stems from Arabidopsis thaliana identifies candidate genes for missing links in lignin biosynthesis and transcriptional regulators of fiber differentiation. Plant J., 2005, 42(5), 618-640.
[http://dx.doi.org/10.1111/j.1365-313X.2005.02403.x] [PMID: 15918878]
[87]
Cho, M-H.; Corea, O.R.; Yang, H.; Bedgar, D.L.; Laskar, D.D.; Anterola, A.M.; Moog-Anterola, F.A.; Hood, R.L.; Kohalmi, S.E.; Bernards, M.A.; Kang, C.; Davin, L.B.; Lewis, N.G. Phenylalanine biosynthesis in Arabidopsis thaliana. Identification and characterization of arogenate dehydratases. J. Biol. Chem., 2007, 282(42), 30827-30835.
[http://dx.doi.org/10.1074/jbc.M702662200] [PMID: 17726025]
[88]
Fraser, C.M.; Chapple, C. The phenylpropanoid pathway in Arabidopsis. The Arabidopsis Book, 2011, 9e0152
[http://dx.doi.org/10.1199/tab.0152]
[89]
Hanson, M.R.; Sattarzadeh, A. Trafficking of proteins through plastid stromules. Plant Cell, 2013, 25(8), 2774-2782.
[http://dx.doi.org/10.1105/tpc.113.112870] [PMID: 23983219]
[90]
Agati, G.; Biricolti, S.; Guidi, L.; Ferrini, F.; Fini, A.; Tattini, M. The biosynthesis of flavonoids is enhanced similarly by UV radiation and root zone salinity in L. vulgare leaves. J. Plant Physiol., 2011, 168(3), 204-212.
[http://dx.doi.org/10.1016/j.jplph.2010.07.016] [PMID: 20850892]
[91]
Mewis, I.; Khan, M.A.; Glawischnig, E.; Schreiner, M.; Ulrichs, C. Water stress and aphid feeding differentially influence metabolite composition in Arabidopsis thaliana (L.). J. Plant Physiol., 2012, 7(11), 15.
[92]
Nita, M.; Grzybowski, A. The role of the reactive oxygen species and oxidative stress in the pathomechanism of the age-related ocular diseases and other pathologies of the anterior and posterior eye segments in adults. Oxidat. Med. Cellular Longevity, 2016, pp. 23. Article ID: 3164734.
[http://dx.doi.org/10.1155/2016/3164734]
[93]
Choudhury, F.K.; Rivero, R.M.; Blumwald, E.; Mittler, R. Reactive oxygen species, abiotic stress and stress combination. Plant J., 2017, 90(5), 856-867.
[http://dx.doi.org/10.1111/tpj.13299] [PMID: 27801967]
[94]
Karuppanapandian, T.; Moon, J.; Kim, C.; Manoharan, K.; Kim, W. Reactive oxygen species in plants: their generation, signal transduction, and scavenging mechanisms. Aust. J. Crop Sci., 2011, 5(6), 709-725.
[95]
Gill, S.S.; Anjum, N.A.; Gill, R.; Yadav, S.; Hasanuzzaman, M.; Fujita, M.; Mishra, P.; Sabat, S.C.; Tuteja, N. Superoxide dismutase--mentor of abiotic stress tolerance in crop plants. Environ. Sci. Pollut. Res. Int., 2015, 22(14), 10375-10394.
[http://dx.doi.org/10.1007/s11356-015-4532-5] [PMID: 25921757]
[96]
Luis, A.; Corpas, F.J.; López-Huertas, E.; Palma, J.M. Plant superoxide dismutases: function under abiotic stress conditions. Antioxidants and antioxidant enzymes in higher plants; Gupta, D.K.; Palma, J.M.; Corpas, F.J; Cham, S., Ed.; Switzerland, 2018, pp. 1-26.
[97]
Schreier, T.B.; Cléry, A.; Schläfli, M.; Galbier, F.; Stadler, M.; Demarsy, E.; Albertini, D.; Maier, B.A.; Kessler, F.; Hörtensteiner, S.; Zeeman, S.C.; Kötting, O. Plastidial NAD-dependent malate dehydrogenase: a moonlighting protein involved in early chloroplast development through its interaction with an FtsH12-FtsHi protease complex. Plant Cell, 2018, 30(8), 1745-1769.
[http://dx.doi.org/10.1105/tpc.18.00121] [PMID: 29934433]
[98]
Heyno, E.; Innocenti, G.; Lemaire, S.D.; Issakidis-Bourguet, E.; Krieger-Liszkay, A. Putative role of the malate valve enzyme NADP–malate dehydrogenase in H2O2 signalling in Arabidopsis. Philos. Trans. R. Soc. Lond. B Biol. Sci., 2014, 369, 8.
[99]
Babayev, H.; Mehvaliyeva, U.; Aliyeva, M.; Guliyev, N.; Feyziyev, Y. NADP-malate dehydrogenase isoforms of wheat leaves under drought: their localization, and some physicochemical and kinetic properties. J. Stress Physiol. Biochem., 2015, 11(3), 13-25.
[100]
Hebbelmann, I.; Selinski, J.; Wehmeyer, C.; Goss, T.; Voss, I.; Mulo, P.; Kangasjärvi, S.; Aro, E-M.; Oelze, M-L.; Dietz, K-J.; Nunes-Nesi, A.; Do, P.T.; Fernie, A.R.; Talla, S.K.; Raghavendra, A.S.; Linke, V.; Scheibe, R. Multiple strategies to prevent oxidative stress in Arabidopsis plants lacking the malate valve enzyme NADP-malate dehydrogenase. J. Exp. Bot., 2012, 63(3), 1445-1459.
[http://dx.doi.org/10.1093/jxb/err386] [PMID: 22140244]
[101]
Chmielewska, K.; Rodziewicz, P.; Swarcewicz, B.; Sawikowska, A.; Krajewski, P.; Marczak, Ł.; Ciesiołka, D.; Kuczyńska, A.; Mikołajczak, K.; Ogrodowicz, P. 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., 2016, 7, 14.
[102]
Holmgren, A. Thioredoxin. Annu. Rev. Biochem., 1985, 54(1), 237-271.
[http://dx.doi.org/10.1146/annurev.bi.54.070185.001321] [PMID: 3896121]
[103]
Atkin, O.K.; Macherel, D. The crucial role of plant mitochondria in orchestrating drought tolerance. Ann. Bot., 2009, 103(4), 581-597.
[http://dx.doi.org/10.1093/aob/mcn094] [PMID: 18552366]
[104]
Kneeshaw, S.; Gelineau, S.; Tada, Y.; Loake, G.J.; Spoel, S.H. Selective protein denitrosylation activity of Thioredoxin-h5 modulates plant Immunity. Mol. Cell, 2014, 56(1), 153-162.
[http://dx.doi.org/10.1016/j.molcel.2014.08.003] [PMID: 25201412]
[105]
Das, A.; Eldakak, M.; Paudel, B.; Kim, D-W.; Hemmati, H.; Basu, C.; Rohila, J.S. Leaf proteome analysis reveals prospective drought and heat stress response mechanisms in soybean. BioMed Res. Int., 2016, 20166021047
[http://dx.doi.org/10.1155/2016/6021047]
[106]
Pan, L.; Yang, Z.; Wang, J.; Wang, P.; Ma, X.; Zhou, M.; Li, J.; Gang, N.; Feng, G.; Zhao, J. Comparative proteomic analyses reveal the proteome response to short-term drought in Italian ryegrass (Lolium multiflorum). PLoS One, 2017, 12(9), 20.


Rights & PermissionsPrintExport Cite as


Article Details

VOLUME: 17
ISSUE: 3
Year: 2020
Page: [227 - 240]
Pages: 14
DOI: 10.2174/1570164617666191016094142
Price: $25

Article Metrics

PDF: 8