Abstract
Rapeseed/canola (Brassica napus L.) is considered amongst the “big four” oilseed crops with varying degrees of cold tolerance. Differential protein expression of cold acclimated young leaves of two canola genotypes, Sari Gul (spring type cold-sensitive) and Zarfam (winter type cold-tolerant), were determined via two dimensional polyacrylamide gel electrophoresis. Seedling leaves were cold acclimated by temperature regime and collected before and after cold treatment at 4 and − 4 °C after 24 h, proteins were isolated and separated on 2-DE. Gel analysis of 651 protein spots revealed that 19 protein spots were significantly different between the two conditions in response to early cold acclimation. Following nanoflow liquid chromatography–tandem mass spectrometry, 19 protein sequences were identified in gel spots, which were reported for the first time in response to early cold acclimation in B. napus and nearly half of them were associated with various aspects of chloroplast physiology; suggesting that the cold stress response of B. napus is achieved, at least partly, by regulation of chloroplast function. Our work has provided novel insights into the plant response to cold stress and should pave the way for future studies towards functional analysis of candidate genes in cold response.
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Abdel-Ghany SE, Müller-Moulé P, Niyogi KK, Pilon M, Shikanai T (2005) Two P-type ATPases are required for copper delivery in Arabidopsis thaliana chloroplasts. Plant Cell 17:1233–1251
Agarwal M, Hao Y, Kapoor A, Dong CH, Fujii H, Zheng X, Zhu JK (2006) A R2R3 type MYB transcription factor is involved in the cold regulation of CBF genes and in acquired freezing tolerance. J Biol Chem 281:37636–37645
Ali A, Goswami S, Kumar R, Singh K, Singh JP, Kumar A, Kumari A, Sakhrey AK, Rai G, Praveen S (2018) Wheat oxygen evolving enhancer protein: identification and characterization of Mn-binding metalloprotein of photosynthetic pathway involved in regulating photosytem II integrity and network of antioxidant enzymes under heat stress. Int J of Curr Microbiol App Sci 7:177–199
Amme S, Matros A, Schlesier B, Mock H-P (2006) Proteome analysis of cold stress response in Arabidopsis thaliana using DIGE-technology. J Exp Bot 57:1537–1546
An F, Li G, Li QX, Kaimian L, Carvalho LJCB, Ou W, Chen S (2016) The comparatively proteomic analysis in response to cold stress in cassava plantlets. Plant Mol Biol Rep 34:1095–1110
Andeme Ondzighi C, Christopher DA, Cho EJ, Chang SC, Staehelin LA (2008) Arabidopsis protein disulfide isomerase-5 inhibits cysteine proteases during trafficking to vacuoles before programmed cell death of the endothelium in developing seeds. Plant Cell 20:2205–2220
Arora R, Wisniewski ME (1995) Ultrastructural and protein changes in cell suspension cultures of peach associated with low temperature-induced cold acclimation and abscisic acid treatment. Plant Cell Tissue Org Cult 40:17–24
Balbuena TS, Salas JJ, Martínez-Force E, Garces R, Thelen JJ (2011) Proteome analysis of cold acclimation in sunflower. J Proteome Res 10:2330–2346
Benjamins R, Barbez E, Ortbauer M, Terpstra I, Lucyshyn D, Moulinier-Anzola J, Khan M, Leitner J, Malenica N, Butt H, Korbei B, Scheres B, Kleine-Vehn J, Luschnig C (2016) PPP1, a plant-specific regulator of transcription controls Arabidopsis development and PIN expression. Sci Reports 6:32196
Bertolde FZ, Almeida AA, Pirovani CP (2014) Analysis of gene expression and proteomic profiles of clonal genotypes from Theobroma cacao subjected to soil flooding. PLoS One 7:e108705
Bocian A, Kosmala A, Rapacz M, Jurczyk B, Marczak L, Zwierzykowski Z (2011) Differences in leaf proteome response to cold acclimation between Lolium perenne plants with distinct levels of frost tolerance. J. Plant Physiol 168:1271–1279
Bradford MM (1976) A rapid and sensitive method for the quantification of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254
Cai H, Zhou Y, Xiao J, Li X, Zhang Q, Lian X (2009) Overexpressed glutamine synthetase gene modifies nitrogen metabolism and abiotic stress responses in rice. Plant Cell Rep 28:527–537
Carpaneto A, Ivashikina N, Levchenko V, Krol E, Jeworutzki E, Zhu JK, Hedrich R (2007) Cold transiently activates calcium-permeable channels in Arabidopsis mesophyll cells. Plant Physiol 143:487–494
Chen Y, Wang XM, Zhou L, He Y, Wang D, Qi YH, Jiang DA (2015) Rubisco activase is also a multiple responder to abiotic stresses in rice. PLoS One 10(10):e0140934
Chevallet M, Luche S, Rabilloud T (2006) Silver staining of proteins in polyacrylamide gels. Nat Protoc 1:1852–1858
Chou IT, Gasser CS (1997) Characterization of the cyclophilin gene family of Arabidopsis thaliana and phylogenetic analysis of known cyclophilin proteins. Plant Mol Biol 35:873–892
Chow CN, Zheng HQ, Wu NY, Chien CH, Huang HD, Lee TY, Chiang-Hsieh YF, Hou PF, Yang TY, Chang WC (2015) PlantPAN 2.0: an update of plant promoter analysis navigator for reconstructing transcriptional regulatory networks in plants. Nucleic Acids Res 1:10–35
Ciftci-Yilmaz S, Mittler R (2008) The zinc finger network of plants. Cell Mol Life Sci 65:1150–1160
Ciftci-Yilmaz S, Morsy MR, Song L, Coutu A, Krizek BA, Lewis MW, Warren D, Cushman J, Connolly EL, Mittler R (2007) The EAR-motif of the Cys2/His2-type zinc finger protein Zat7 plays a key role in the defense response of Arabidopsis to salinity stress. J Biol Chem 282:9260–9268
Cominelli E, Galbiati M, Vavasseur A, Conti L, Sala T, Vuylsteke M, Leonhardt N, Dellaporta SL, Tonelli C (2005) A guard-cell-specific MYB transcription factor regulates stomatal movements and plant drought tolerance. Curr Biol 15:1196–1200
Cui S, Wang F, Ma X, Cheng Y, Liu J (2005) A proteomic analysis of cold stress responses in rice seedlings. Proteomics 5:3162–3172
Černý M, Kuklová A, Hoehenwarter W, Fragner L, Novák O, Rotková G, Jedelsky PL, Žáková K, Šmehilová M, Strnad M, Weckwerth W, Brzobohaty B (2013) Proteome and metabolome profiling of cytokinin action in Arabidopsis identifying both distinct and similar responses to cytokinin down- and up-regulation. J Exp Bot 64:4193–4206
Davletova S, Rizhsky L, Liang H, Shengqiang Z, Oliver DJ, Coutu J, Shulaev V, Schlauch K, Mittler R (2005) Cytosolic ascorbate peroxidase 1 is a central component of the reactive oxygen gene network of Arabidopsis. Plant Cell 17:268–281
Ding JP, Pickard BG (1993) Modulation of mechanosensitive calcium-selective cation channels by temperature. Plant J 3:713–720
Do H, Kim IS, Jeon BW, Lee CW, Park AK, Wi AR, Shin SC, Park H, Kim YS, Yoon HS, Kim HW, Lee JH (2016) Structural understanding of the recycling of oxidized ascorbate by dehydroascorbate reductase (OsDHAR) from Oryza sativa L. japonica. Sci Rep 6:194–198
Dumont E, Bahrman N, Goulas E, Valot B, Sellier H, Hilbert JL, Vuylsteker C, Lejeune-Hénaut I, Delbreil B (2011) A proteomic approach to decipher chilling response from cold acclimation in pea (Pisum sativum L.). Plant Sci 180:86–98
Edrisi Maryan K, Samizadeh Lahiji H, Farrokhi N, Hasani Komeleh H (2019) Analysis of Brassica napus dehydrins and their co-expression regulatory networks in relation to cold stress. Gene Expr Patterns 31:7–17
Fanucchi F, Alpi E, Olivieri S, Cannistraci CV, Bachi A, Alpi A, Alession M (2012) Acclimation increases freezing stress response of Arabidopsis thaliana at proteome level. Biochim Biophys Acta 1824:813–825
FAOSTAT (2010) Brassica napus. Available at https://faostat.fao.org. Accessed 02/10/2019
Fiebelkorn D, Rahman M (2016) Development of a protocol for frost-tolerance evaluation in rapeseed/canola (Brassica napus L.). The Crop J 4:147–152
Fischer G, Schmid FX (1999) Peptidyl prolyl cis/trans isomerases. In: Bakau B (ed) Molecular chaperones and folding catalysts: regulation, cellular function and mechanism. Harwood Academic Publishers, Amsterdam, pp 461–489
Folgado R, Panis B, Sergeant K, Renaut J, Swennen R, Hausman JF (2013) Differential protein expression in response to abiotic stress in two potato species: Solanum commersonii dun and Solanum tuberosum L. Int J Mol Sci 14:4912–4933
Forde BG, Lea PJ (2007) Glutamate in plants: metabolism, regulation, and signaling. J Exp Bot 58:2339–2358
Fu J, Momčilović J, Prasad PV (2012) Roles of protein synthesis elongation factor EF-Tu in heat tolerance. J. Botany 2012: 1-8. https://doi.org/10.1155/2012/835836
Fukao Y, Ferjani A, Fujiwara M, Nishimori Y, Ohtsu I (2009) Identification of zinc-responsive proteins in the roots of Arabidopsis thaliana using a highly improved method of two-dimensional electrophoresis. Plant Cell Physiol 50:2234–2239
Gao F, Zhou Y, Zhu W, Xiaofeng L, Fan L, Zhang G (2009) Proteomic analysis of cold stress-responsive proteins in Thellungiella rosette leaves. Planta 230:1033–1046
Gao SQ, Chen M, Xu ZS, Zhao CP, Li L, Xu HJ, Tang YM, Zhao X, Ma YZ (2011) The soybean GmbZIP1 transcription factor enhances multiple abiotic stress tolerances in transgenic plants. Plant Mol Biol 75:537–553
Gharechahi J, Alizadeh H, Naghavi MR, Sharifi G (2014) A proteomic analysis to identify cold acclimation associated proteins in wild wheat (Triticum urartu L.). Mol Biol Rep 41:3897–3905
Ghelis T, Bolbach G, Clodic G, Habricot Y, Miginiac E, Sotta B, Jeannette E (2008) Protein tyrosine kinases and protein tyrosine phosphatases are involved in abscisic acid-dependent processes in Arabidopsis seeds and suspension cells. Plant Physiol 148:1668–1680
Godoy AV, Lazzaro AS, Casalongue CA, Sengundo BS (2000) Expression of a Solanum tuberosum cyclophilin gene is regulated by fungal infection and abiotic stress conditions. Plant Sci 152:123–134
Goulas E, Schubert M, Kieselbach T, Kleczkowski LA, Gardeström P, Schröder W, Hurry V (2006) The chloroplast lumen and stromal proteomes of Arabidopsis thaliana show differential sensitivity to short-and long-term exposure to low temperature. Plant J 47:720–734
Grimaud F, Renaut J, Dumont E, Sergeant K, Lucau-Danila A, Blervacq AS, Sellier H, Bahrman N, Lejeune-Hénaut I, Delbreil B, Goulas E (2013) Exploring chloroplastic changes related to chilling and freezing tolerance during cold acclimation of pea (Pisum sativum L.). J Proteome 80:145–159
Guy C (1990) Cold acclimation and freezing stress tolerance: role of protein metabolism. Ann Rev Plant Physiol Plant Mol Biol 41:187–223
Guy C, Kaplan F, Kopka J, Selbig J, Hincha DK (2008) Metabolomics of temperature stress. Physiol Plant 132:220–235
Han F, Chen H, Li XJ, Yang MF, Liu GS, Shen SH (2009) A comparative proteomic analysis of rice seedlings under various high-temperature stresses. Biochim Biophys Acta 1794:1625–1634
Han Q, Kang G, Guo T (2013) Proteomic analysis of spring freeze-stress responsive proteins in leaves of bread wheat (Triticum aestivum L.). Plant Physiol Biochem 63:236–244
Hare PD, Cress WA, van Staden J (1998) Dissecting the roles of osmolyte accumulation during stress. Plant Cell Environ 21:535–553
Hashimoto M, Komatsu S (2007) Proteomic analysis of rice during cold stress. Proteomics 7:1293–1302
He WD, Gao J, Dou TX, Shao XH, Bi FC, Sheng O, Deng GM, Li CYY, Hu CH, Zhang S, Yang QS, Yi GJ (2018a) Early cold-induced peroxidases and aquaporins are associated with high cold tolerance in Dajiao (Musa spp. ‘Dajiao’). Front Plant Sci 9:282
He H, Yang Q, Shen B, Zhang S, Peng X (2018b) OsNOA1 functions in a threshold-dependent manner to regulate chloroplast proteins in rice at lower temperatures. BMC Plant Biol 18:44
Hoagland DR, Arnon DI (1950) The water culture method for growing plant without soil. California Agricultural Experiment Station 347. University of California Berkley Press, CA, p 347
Hoshida H, Tanaka Y, Hibino T, Hayashi Y, Tanaka A, Takabe T, Takabe T (2000) Enhanced tolerance to salt stress in transgenic rice that overexpresses chloroplast glutamine synthetase. Plant Mol Biol 43:103–111
Hsu CC, Zhu Y, Arrington JV, Paez JS, Wang P, Zhu P, Chen I-H, Zhu JK, Tao WA (2018) Universal plant phosphoproteomics workflow and its application to tomato signaling in response to cold stress. Mol Cell Protemics 17:2068–2080
Huang J, Sun S, Xu D, Lan H, Sun H, Wang Z, Bao Y, Wang J, Tang H, Zhang H (2012) A TFIIIA-type zinc finger protein confers multiple abiotic stress tolerances in transgenic rice (Oryza sativa L.). plant Mol. Biol 80:337–350
Huo C, Zhang B, Wang H, Wang F, Liu M, Gao Y, Zhang W, Deng Z, Sun D, Tang W (2016) Comparative study of early cold-regulated proteins by two-dimensional difference gel electrophoresis reveals a key role for phospholipase Dα1 in mediating cold acclimation signaling pathway in rice. Mol Cell Protemics 15:1397–1411
Janska A, Marsik P, Zelenkova S, Ovesna J (2010) Cold stress and acclimation - what is important for metabolic adjustment? Plant Biol 12:395–405
Jesperson D, Huang B (2015) Proteins associated with heat-induced leaf senescence in creeping bentgrass as affected by foliar application of nitrogen, cytokinins, and an ethylene inhibitor. Proteomics 15:798–812
Ji L, Zhou P, Zhu Y, Liu F, Li R, Qiu Y (2017) Proteomic analysis of rice seedlings under cold stress. Protein J 36:299–307
Jiang Y, Yang B, Harris NS, Deyholos MK (2007) Comparative proteomic analysis of NaCl stress-responsive proteins in Arabidopsis roots. J Exp Bot 58:3591–3607
Kamal AH, Cho K, Choi JS, Jin Y, Park CS, Lee JS, Woo SH (2013) Patterns of protein expression in water-stressed wheat chloroplasts. Biol Plant 57:305–331
Kan CC, Chung TY, Yan-An J, Hsieh HH (2015) Glutamine rapidly induces the expression of key transcription factor genes involved in nitrogen and stress responses in rice roots. BMC Genomics 16:731
Kanehisa M, Sato Y, Furumichi M, Morishima K, Tanabe M (2019) New approach for understanding genome variations in KEGG. Nucleic Acids Res 47:590–595
Kawamura Y, Uemura M (2003) Mass spectrometric approach for identifying putative plasma membrane proteins of Arabidopsis leaves associated with cold acclimation. Plant J 36:141–154
Kilian J, Peschke F, Berendzen KW, Harter K, Wanke D (2012) Prerequisites, performance and profits of transcriptional profiling the abiotic stress response. Biochim Biophys Acta 1819:166–175
Kliebenstein DJ, Monde RA, Last RL (1998) Superoxide dismutase in Arabidopsis: an eclectic enzyme family with disparate regulation and protein localization. Plant Physiol 118:637–650
Kosová K, Prasil IT, Vitamvas P, Dobrev P, Motyka V, Flokova K, Novak O, Turecková V, Rolcik J, Pesek B, Travnickova A, Gaudinova A, Galiba G, Janda T, Vlasakova E, Prasilova P, Vankova R (2012) Complex phytohormone responses during the cold acclimation of two wheat cultivars differing in cold tolerance, winter Samanta and spring Sandra. J Plant Physiol 169:567–576
Kosova K, Vitamvas P, Planchon S, Renaut J, Vankova R, Prasil IT (2013) Proteome analysis of cold response in spring and winter wheat (Triticum aestivum) crowns reveals similarities in stress adaptation and differences in regulatory processes between the growth habits. J Proteome Res 12:4830–4845
Kullertz G, Liebau A, Rucknagel A, Schierhorn A, Diettrich B, Fischer G, Luckner M (1999) Stress-induced expression of cyclophilins in proembryonic masses of Digitalis lanata does not protect against freezing/thawing stress. Planta 208:599–605
Kuo WY, Huang CH, Liu AC, Cheng CP, Li SH, Chang WC, Weiss C, Azem A, Jinn TL (2013) CHAPERONIN 20 mediates iron superoxide dismutase (FeSOD) activity independent of its co-chaperonin role in Arabidopsis chloroplasts. New Phytol 197:99–110
Laemmli UK (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227:680–685
Lardon A, Triboi-Blondel AM (1995) Cold and freeze stress at flowering effects on seed yield in winter rapeseed. Field Crops Res 44:95–101
Laxa M, König J, Dietz KJ, Kandlbinder A (2007) Role of the cysteine residues in Arabidopsis thaliana cyclophilin CYP20-3 in peptidyl-prolyl cis-trans isomerase and redox-related functions. Biochem J 401:287–297
Lee H, Guo Y, Ohta M, Xiong L, Stevenson B, Zhu JK (2002) LOS2, a genetic locus required foe cold-responsive gene transcription encodes a bi-functional enolase. EMBO J 21:2692–2702
Lei Y, Shah T, Yong C, Lu Y, Xue-Kun Z, Xi-Ling Z (2019) Physiological and molecular responses to cold stress in rapeseed (Brassica napus L.). J Integrative Agriculture 18:2742–2752
Leonardo A, Zepada M, Baudo MM, Palva ET, Heino P (1998) Isolation and characterization of a cDNA corresponding to a stress-activated cyclophilin gene in Solanum commersonii. J Exp Bot 49:1451–1452
Lescot M, Dehais P, Thijs G, Marchal K, Moreau Y, Peer YV, Rouze P, Rombauts S (2002) PlantCARE, a database of plant cis-acting regulatory elements and a portal to tools for in silico analysis of promoter sequences. Nucleic Acids Res 30:325–327
Lim EM, Ehrlich SC, Maguin E (2000) Identification of stress-inducible proteins in Lactobacillus delbrueckii subsp. Bulgaricus. Electrophoresis 21:2557–2561
Liu Z, Taub CC, McClung CR (1996) Identification of an Arabidopsis thaliana ribulose-1,5-bisphosphate carboxylase/oxygenase activase (RCA) minimal promoter regulated by light and the circadian clock. Plant Physiol 112:43–51
Liu Q, Kasuga M, Sakuma Y, Abe H, Miura S, Yamaguchi-Shinozaki K, Shinozaki K (1998) Two transcription factors, DREB1 and DREB2, with an EREBP/AP2 DNA binding domain separate two cellular signal transduction pathways in drought- and low-temperature responsive gene expression, respectively, in Arabidopsis. Plant Cell 10:1391–1406
Liu S, Gao J, Chen Z, Qiao X, Huang H, Cui B, Zhu Q, Dai Z, Wu H, Pan Y, Yang C, Li J (2007) 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 17:206
Liu XG, Xu H, Zhang JY, Liang GW, Liu YT, Guo AG (2012) Effect of low temperature on chlorophyll biosynthesis in albinism line of wheat (Triticum aestivum) FA85. Physiol Plant 145:384–394
Liu X, Liu B, Xue S, Cai Y, Qi W, Jian C, Xu S, Wang T, Ren H (2016) Cucumber (Cucumis sativus L.) nitric oxide synthase associated gene1 (CsNOA1) plays a role in chilling stress. Front Plant Sci 7:1652
Lyons JM (1973) Chilling injury in plants. Ann Rev Plant Physiol 24:445–466
Ma L, Coulter JA, Liu L, Zhao Y, Chang Y, Pu Y, Zeng X, Xu Y, Wu J, Fang Y, Bai J, Sun W (2019) Transcriptome analysis reveals key cold-stress-responsive genes in winter rapeseed (Brassica rapa L.). Int J Molec Sci 20(5):1071
Manavski N, Torabi S, Lezhneva L, Arif MA, Frank W, Meurer J (2015) High chlorophyll fluorescence 145 binds to and stabilizes the psaA 5' UTR via a newly defined repeat motif in embryophyta. Plant Cell 27(9):2600–2615
Marivet J, Frendo P, Burkard G (1992) Effects of abiotic stresses on cyclophilin gene expression in maize and bean and sequence analysis of bean cyclophilin cDNA. Plant Sci 84:171–178
Marri L, Sparla F, Pupillo P, Trost P (2005) Co-ordinated gene expression of photosynthetic glyceraldehyde-3-phosphate dehydrogenase, phosphoribulokinase, and CP12 in Arabidopsis thaliana. J Exp Bot 56:73–80
Maršálová L, Vítámvás P, Hynek R, Prášil IT, Kosová K (2016) Proteomic response of Hordeum vulgare cv. Tadmor and Hordeum marinum to salinity stress: similarities and differences between a glycophyte and a halophyte. Front Plant Sci 7:1154
Messing SAJ, Gabelli SB, Echeverria I, Vogel JT, Guan JC, Tan BC, Klee HJ, McCarty DR, Amzel LM (2010) Structural insights into maize Viviparous14, a key enzyme in the biosynthesis of the phytohormone abscisic acid. Plant Cell 22:2970–2980
Mi H, Huang X, Muruganujan A, Tang H, Mills C, Kang D, Thomas PD (2016) PANTHER version 11: expanded annotation data from gene ontology and reactome pathways, and data analysis tool enhancements. Nucleic Acids Res 45:183–189
Mirzaei M, Soltani N, Sarhadi E, George IS, Neilson KA, Pascovici D, Shahbazian S, Haynes PA, Atwell BJ, Salekdeh GH (2013) Manipulating root water supply elicits major shifts in the shoot proteome. J Proteome Res 13:517–526
Mizoi J, Shinozaki K, Yamaguchi-Shinozaki K (2012) AP2/ERF family transcription factors in plant abiotic stress responses. Biochim Biophys Acta 1819:86–96
Motohashi K, Koyama F, Nakanishi Y, Ueoka-Nakanishi H, Hisabori T (2003) Chloroplast cyclophilin is a target protein of thioredoxin. J Biol Chem 278:31848–31852
Mukherjee AK, Carp MJ, Zuchman R, Ziv T, Horwitz BA, Gepstein S (2010) Proteomics of the response of Arabidopsis thaliana to infection with Alternaria brassicicola. J Proteome 73:709–720
Nakashima K, Shinwari ZK, Sakuma Y, Seki M, Miura S, Shinozak K, Yamaguchi-Shinozaki K (2000) Organization and expression of two Arabidopsis DREB2 genes encoding DRE-binding proteins involved in dehydration- and high-salinity-responsive gene expression. Plant Mol Biol 42:657–665
Neuhoff V, Stamm R, Eibl H (1985) Clear background and highly sensitive protein staining with Coomassie blue dyes in polyacrylamide gels: a systematic analysis. Electrophoresis 6:427–448
Nouri MZ, Moumeni A, Komatsu S (2015) Abiotic stresses: insight into gene regulation and protein expression in photosynthetic pathways of plants. Int J Mol Sci 16:20392–20416
Obayashi T, Aoki Y, Tadaka S, Kagaya Y, Kinoshita K (2018) ATTED-II in 2018: a plant coexpression database based on investigation of statistical property of the mutual rank index. Plant Cell Physiol 59:3
Peleg Z, Blumwald E (2011) Hormone balance and abiotic stress tolerance in crop plants. Current Opinion Plant Biology 14:290–295
Pu Y, Liu L, Wu J, Zhao Y, Bai J, Ma L, Yue J, Jin J, Niu Z, Fang Y, Sun W (2019) Transcriptome profile analysis of winter rapeseed (Brassica napus L.) in response to freezing stress, reveal potentially connected events to freezing stress. Int J Molec Sci 20(11):2771
Raman K (2010) Construction and analysis of protein-protein interaction networks. Autom Express 2:2
Rocco M, Arena S, Renzone G, Scippa GS, Lomaglia T, Verrillo F, Scaloni A, Marra M (2013) Proteomic analysis of temperature stress-responsive proteins in Arabidopsis thaliana rosette leaves. Mol BioSyst 9:1257–1267
Roxas VP, Smith RK, Allen ER, Allen RD (1997) Overexpression of glutathione S-transferase/glutathioneperoxidase enhances the growth of transgenic tobacco seedlings during stress. Nat Biotechnol 15:988–991
Safari S, Mehrabi AA, Safari Z (2013) Efficiency of RAPD and ISSR markers in assessment of genetic diversity in Brassica napus genotypes. Int J Agric Crop Sci 5-3:273–279
Santner A, Estelle M (2009) Recent advances and emerging trends in plant hormone signaling. Nature 459:1071–1078
Sarry JE, Kuhn L, Ducruix C, Lafaye A, Junot C, Hugouvieux V, Jourdain A, Bastien O, Fievet JB, Vailhen D, Amekraz B, Moulin C, Ezan E, Garin J, Bourguignon J (2006) The early responses of Arabidopsis thaliana cells to cadmium exposure explored by protein and metabolite profiling analyses. Proteomics 6:2180–2198
Semane B, Dupae J, Cuypers A, Noben JP, Tuomainen M, Tervahauta A, Kärenlampi S, Van Belleghem F, Smeets K, Vangronsveld J (2010) Leaf proteome responses of Arabidopsis thaliana exposed to mild cadmium stress. J Plant Physiol 167:247–254
Shan X, Wang J, Chua L, Jiang D, Peng W, Xie D (2011) The role of Arabidopsis rubisco activase in jasmonate-induced leaf senescence. Plant Physiol 155:751–764
Shannon P, Markiel A, Ozier O, Baliga NS, Wang JT, Ramage D, Amin N, Schwikowski B, Ideker T (2003) Cytoscape: a software environment for integrated models of biomolecular interaction networks. Genome Res 13:2498–2504
Sharma AD, Wajapeyee N, Yadav V, Singh P (2003) Stress- induced changes in peptidyl-prolyl cis-trans isomerase activity of Sorghum bicolor seedlings. Biol Plant 47:367–371
Shin SY, Kim IS, Kim YH, Park HM, Lee JY, Kang HG, Yoon HS (2008) Scavenging reactive oxygen species by rice dehydroascorbate reductase alleviates oxidative stresses in Escherichia coli. Mol Cells 26:616–620
Sovero M (1993) Rapeseed, a new oilseed crop for the United States. In: Janick J, Simon JE (eds) New crops. Wiley, New York, pp 302–307
Stefanowska M, Kuras M, Balska MK, Kacperska A (1999) Low temperature affects pattern of leaf growth and structure of cell walls in winter oilseed rape (Brassica napus L., var. oleifera L.). Ann Bot 84:313–319
Storozhenko S, De Pauw P, Van Montagu M, Inzé D, Kushnir S (1998) The heat-shock element is a functional component of the Arabidopsis APX1 gene promoter. Plant Physiol 118:1005–1014
Sung DY, Kaplan F, Lee KJ, Guy CL (2003) Acquired tolerance to temperature extremes. Trends Plant Sci 8:179–187
Sweetlove LJ, Heazlewood JL, Herald V, Holtzapffel R, Day DA, Leaver CJ, Millar AH (2002) The impact of oxidative stress on Arabidopsis mitochondria. Plant J 32:891–904
Szklarczyk D, Morris JH, Cook H, Kuhn M, Wyder S, Simonovic M, Santos A, Doncheva NT, Roth A, Bork P, Jensen LJ, von Mering C (2017) The STRING database in 2017: quality-controlled protein-protein association networks, made broadly accessible. Nucleic Acids Res 45:362–368
Taira M, Valtersson U, Burkhardt B, Ludwig RA (2004) Arabidopsis thaliana GLN2-encoded glutamine synthetase is dual targeted to leaf mitochondria and chloroplasts. Plant Cell 16:2048–2058
Takahashi D, Kawamura Y, Uemura M (2016) Cold acclimation is accompanied by complex responses of glycosyl phosphatidyl inositol (GPI)-anchored proteins in Arabidopsis. J Exp Botany 67:5203–5215
Takahashi D, Gorka M, Erban A, Graf A, KKopka J, Zuther E, Hincha DK (2019) Both cold and sub-zero acclimation induce cell wall modification and changes in the extracellular proteome in Arabidopsis thaliana. Sci Rep 9:2289
Taylor P, Nielsen PA, Trelle MB, Horning OB, Andersen MB, Vorm O, Moran MF, Kislinger T (2009) Automated 2D peptide separation on a 1D nano-LC-MS system. J Proteome Res 8:1610–1616
Terry DE, Umstot E, Desiderio DM (2004) Optimized sample-processing time and peptide recovery for the mass spectrometric analysis of protein digests. J Am Soc Mass Spectrom 15:784–794
Thomashow MF (1999) Plant cold acclimation: freezing tolerance genes and regulatory mechanisms. Annu Rev Plant Biol 50:571–599
Tian X, Liu Y, Huang Z, Duan H, Tong J, He X, Gu W, Ma H, Xiao L (2015) Comparative proteomic analysis of seedling leaves of cold-tolerant and – sensitive spring soybean cultivars. Mol Biol Rep 42:581–601
Uemura M, Joseph RA, Steponkus PL (1995) Cold acclimation of Arabidopsis thaliana (effect on plasma membrane lipid composition and freeze-induced lesions). Plant Physiol 109:15–30
Umezawa T, Nakashima K, Miyakawa T, Kuromori T, Tanokura M, Shinozaki K, Yamaguchi-Shinozaki K (2010) Molecular basis of the core regulatory network in ABA responses: sensing, signaling and transport. Plant Cell Physiol 51:1821–1839
Van Breusegem F, Slooten L, Stassart JM, Botterman J, Moens T, Van Montagu M, Inze D (1999) Effects of overproduction of tobacco MnSOD in maize chloroplasts on foliar tolerance to cold and oxidative stress. J Exp Bot 50:71–78
Wang L, Wang Z, Xu Y, Joo SH, Kim SK, Xue Z, Xu Z, Wang Z, Chong K (2009) OsGSR1 is involved in crosstalk between gibberellins and brassinosteroids in rice. The Plant J 57:498–510
Wang H, Wang S, Lu Y, Alvarez S, Hicks LM, Ge X, Xia Y (2012) Proteomic analysis of early-responsive redox-sensitive proteins in Arabidopsis. J Proteome Res 11:412–424
Wang J, Lan P, Gao H, Zheng L, Li W, Schmidt W (2013) Expression changes of ribosomal proteins in phosphate-and iron-deficient Arabidopsis roots predict stress-specific alterations in ribosome composition. BMC Genomics 14:783
Weiss W, Görg A (2007) Two-dimensional electrophoresis for plant proteomics. Methods Mol Biol 355:121–143
Welti R, Li W, Li M, Sang Y, Biesiada H, Zhou HE, Rajashekar CB, Williams TD, Wang X (2002) Profiling membrane lipids in plant stress responses, role of phospholipase D alpha in freezing-induced lipid changes in Arabidopsis. J Biol Chem 277:31994–32002
Wilson JM (1997) Mechanisms of chilling resistance in plants. In: Basra AS, Basra RK (eds) Mechanisms of environmental resistance in plants. Harwood Academic Publishers, Amsterdam, pp 111–122
Xin H, Xianchao N, Pan X, Wei L, Min Y, Yu K, Lunwen Q, Wei H (2019) Comparative transcriptome analyses revealed conserved and novel responses to cold and freezing stress in Brassica napus L. G3: GENES, GENOMES, GENETICS 9(8):2723–2737
Xu T, Lee K, Gu L, Kim JI, Kang H (2013) Functional characterization of a plastid-specific ribosomal protein PSRP2 in Arabidopsis thaliana under abiotic stress conditions. Plant Physiol Biochem 73:405–411
Xu Y, Zeng X, Wu J, Zhang F, Li C, Jiang J, Wang Y, Sun W (2018) iTRAQ-based quantitative proteome revealed metabolic changes in winter turnip rape (Brassica rapa L.) under cold stress. Int J Molec Sci 19(11):3346
Yamasaki Y, Koehler G, Blacklock BJ, Randall SK (2013) Dehydrin expression in soybean. Plant Physiol Biochem 70:213–220
Yang A, Dai X, Zhang WH (2012) A R2R3-type MYB gene, OsMYB2, is involved in salt, cold, and dehydration tolerance in rice. J Exp Bot 63:2541–2556
Ye J, Fang L, Zheng H, Zhang Y, Chen J, Zhang Z, Wang J, Li S, Li R, Bolund L, Wang J (2006) WEGO: a web tool for plotting GO annotations. Nucleic Acids Res 34:293–297
Zhang Y, Wen Z, Washburn MP, Florens L (2009) Effect of dynamic exclusion duration on spectral count based quantitative proteomics. Anal Chem 81:6317–6326
Zhang XF, Jiang T, Wu Z, Du SY, Yu YT, Jiang SC, Lu K, Feng K, Wang XF, Zhang DP (2013) Cochaperonin CPN20 negatively regulates abscisic acid signaling in Arabidopsis. Plant Mol Biol 83:205–218
Zhang N, Huo W, Zhang L, Chen F, Cui D (2016a) Identification of winter-responsive proteins in bread wheat using proteomics analysis and virus-induced gene silencing (VIGS). Mol Cell Proteomics 15:2954–2969
Zhang W, Zhang H, Ning L, Li B, Bao M (2016b) Quantitative proteomic analysis provides novel insights into cold stress responses in petunia seedlings. Front Plant Sci 7:136
Acknowledgments
The authors thank Iran National Science Foundation (INSF) (grant number: 95814286) for financial support. We also would like to thank Mehdi Amini at Reproductive Biotechnology Research Center, Avicenna Research Institute, ACECR, Tehran, Iran, for being instrumental.
Funding
This work was supported by the Iran National Science Foundation (INSF) [Grant number: 95814286, 2017-2019.
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Khazar Edrisi Maryan carried out the plant culture, protein isolation, 2D-PAGE, spot analysis, and preparation of manuscript first draft. Habibollah Samizadeh Lahiji supervised Khazar Edrisi Maryan and designed the initial setup of the experiments. Naser Farrokhi supervised Khazar Edrisi Maryan on protein isolation, 2D-PAGE, bioinformatics analysis of the corresponding genes and promoters. Naser Farrokhi edited and commented on the draft and made it ready to be submitted to the journal. Protein identification by tandem mass spectrometry was carried out by Sara Hamzelou under the supervision of Paul A. Haynes. Hassan Hasani Komeleh advised Khazar Edrisi Maryan on plant culture and reviewed the manuscript.
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Key Message
• Cold acclimation is different between the cold tolerant vs cold sensitive genotypes that can be seen through changes of protein profiles.
• The highly affected cellular organelle in response to cold stress is chloroplast as reflected in expression changes that are reported in the corresponding proteins.
• Cold stress has pronounced effects on metabolic pathways.
• The expressions of corresponding genes to changed proteins appear to be in control of plant hormones, mainly methyl jasmonate and abscisic acid as determined via analysis of cis-elements within the promoters.
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Maryan, K.E., Lahiji, H.S., Farrokhi, N. et al. Comparative Leaf Proteomics of Brassica napus Genotypes with Distinctive Levels of Early Cold Acclimation. Plant Mol Biol Rep 39, 317–334 (2021). https://doi.org/10.1007/s11105-020-01249-4
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DOI: https://doi.org/10.1007/s11105-020-01249-4