Abstract
How to enhance fruit tolerance to cold stress is an important biological interest. In this paper, we found that mango (Mangifera indica L.) fruit treated with 10 μM brassinolide (BL) showed a higher tolerance to cold temperature of 5 °C. Further, we compared the changes in expression profiles of plasma membrane (PM) proteins and the corresponding gene expressions between BL-treated and control fruit. Fourteen differential proteins were positively identified by mass spectrometry, and were categorized into four groups, including transport, cellular biogenesis, defense and stress response, and unknown function. Among them, four proteins (remorin, abscisic stress ripening-like protein, type II SK2 dehydrin, and temperature-induced lipocalin) and genes encoding these proteins were up-regulated in BL treatment under cold stress. Moreover, we found that PM lipids in BL-treated fruit showed lower phase transition temperature and higher unsaturation degree, leading to higher fluidity under low temperature. These findings ascertain that PM proteins and lipids are involved in BL-mediated responses to cold stress in mango fruit, and provide novel evidence that BL plays an important role in regulating cold stress tolerance in fruit.
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Abbreviations
- 2-DE:
-
Two-dimensional gel electrophoresis
- BL:
-
Brassinolide
- BRs:
-
Brassinosteroids
- CI:
-
Chilling injury
- CBB:
-
Coomassie brilliant blue
- DBI:
-
Double bond index
- DSC:
-
Differential scanning calorimetry
- EPR:
-
Electron paramagnetic resonance
- FAs:
-
Fatty acids
- IEF:
-
Isoelectric focusing
- PM:
-
Plasma membrane
- UFAs:
-
Unsaturated fatty acids
References
Allagulova ChR, Gimalov FR, Shakirova FM, Vakhitov VA (2003) The plant dehydrins: structure and putative functions. Biochemistry 68:945–951
Bajguz A, Hayat S (2009) Effects of brassinosteroids on the plant responses to environmental stresses. Plant Physiol Biochem 47:1–8
Bajguz A, Tretyn A (2003) The chemical characteristic and distribution of brassinosteroids in plants. Phytochemistry 62:1027–1046
Bariola PA, Retelska D, Stasiak A, Kammerer RA, Fleming A, Hijri M, Franks S, Farmer EE (2004) Remorins form a novel family of coiled coil-forming oligomeric and filamentous proteins associated with apical, vascular and embryonic tissues in plants. Plant Mol Biol 55:579–594
Belkhadir Y, Chory J (2006) Brassinosteroid signaling: a paradigm for steroid hormone signaling from the cell surface. Science 314:1410–1411
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
Chan ZL, Qin GZ, Xu XB, Li BQ, Tian SP (2007) Proteome approach to characterize proteins induced by antagonist yeast and salicylic acid in peach fruit. J Proteome Res 6:1677–1688
Charron JBF, Breton G, Badawi M, Sarhan F (2002) Molecular and structural analyses of a novel temperature stress-induced lipocalin from wheat and Arabidopsis. FEBS Lett 517:129–132
Charron JBF, Ouellet F, Pelletier M, Danyluk J, Chauve C, Sarhan F (2005) Identification, expression, and evolutionary analyses of plant lipocalins. Plant Physiol 139:2017–2028
Chinnusamy V, Zhu JH, Zhu JK (2007) Cold stress regulation of gene expression in plants. Trends Plant Sci 12:444–451
Close TJ (1996) Dehydrins: emergence of a biochemical role of a family of plant dehydration proteins. Physiol Plant 97:795–803
Clouse SD, Sasse JM (1998) Brassinosteroids: essential regulators of plant growth and development. Annu Rev Plant Physiol Plant Mol Biol 49:427–451
Ding ZS, Tian SP, Zheng XL, Zhou ZW, Xu Y (2007) Responses of reactive oxygen metabolism and quality in mango fruit to exogenous oxalic acid or salicylic acid under chilling temperature stress. Physiol Plant 130:112–121
Divi UK, Rahman T, Krishna P (2010) Brassinosteroid-mediated stress tolerance in Arabidopsis shows interactions with abscisic acid, ethylene and salicylic acid pathways. BMC Plant Biol 10:151
Ephritikhine G, Ferro M, Rolland N (2004) Plant membrane proteomics. Plant Physiol Biochem 42:943–962
Han J, Tian SP, Meng XH, Ding ZS (2006) Response of physiologic metabolism and cell structures in mango fruit to exogenous methyl salicylate under low-temperature stress. Physiol Plant 128:125–133
Hazel JR, Williams EE (1990) The role of alterations in membrane lipid composition in enabling physiological adaptation of organisms to their physical environment. Prog Lipid Res 29:167–227
Kalifa Y, Gilad A, Konrad Z, Zaccai M, Scolnik PA, Bar-Zvi D (2004) The water- and salt-stress-regulated Asr1 (abscisic acid stress ripening) gene encodes a zinc-dependent DNA-binding protein. Biochem J 381:373–378
Krishna P (2003) Brassinosteroid-mediated stress responses. J Plant Growth Regul 22:289–297
Laloi M, Perret AM, Chatre L, Melser S, Cantrel C, Vaultier MN, Zachowski A, Bathany K, Schmitter JM, Vallet M, Lessire R, Hartmann MA, Moreau P (2007) Insights into the role of specific lipids in the formation and delivery of lipid microdomains to the plasma membrane of plant cells. Plant Physiol 143:461–472
Lefebvre B, Furt F, Hartmann MA, Michaelson LV, Carde JP, Sargueil-Boiron F, Rossignol M, Napier JA, Cullimore J, Bessoule JJ, Mongrand S (2007) Characterization of lipid rafts from Medicago truncatula root plasma membranes: a proteomic study reveals the presence of a raft-associated redox system. Plant Physiol 144:402–418
Meng XH, Han J, Wang Q, Tian SP (2009) Changes in physiology and quality of peach fruit treated by methyl jasmonate under low temperature stress. Food Chem 106:501–508
Moellering ER, Muthan B, Benning C (2010) Freezing tolerance in plants requires lipid remodeling at the outer chloroplast membrane. Science 330:227–230
Moore S, Payton P, Wright M, Tanksley S, Giovannoni J (2005) Utilization of tomato microarrays for comparative gene expression analysis in the Solanaceae. J Exp Bot 56:2885–2895
Quartacci MF, Cosi E, Navari-Izzo F (2001) Lipids and NADPH-dependent superoxide production in plasma membrane vesicles from roots of wheat grown under copper deficiency or excess. J Exp Bot 52:77–84
Raison JK, Orr GR (1986) Phase transitions in thylakoid polar lipids of chilling sensitive plants. A comparison of detection methods. Plant Physiol 80:638–645
Raison JK, Wright LC (1983) Thermal phase transitions in the polar lipids of plant membranes. Their induction by disaturated phospholipids and their possible relation to chilling injury. Biochim Biophys Acta 731:69–78
Sasse JM (2003) Physiological actions of brassinosteroids: an update. J Plant Growth Regul 22:276–288
Spencer WE, Christensen MJ (1999) Multiplex relative RT-PCR method for verification of differential gene expression. Biotechniques 27:1044–1052
Steponkus PL, Uemura M, Balsamo RA, Arvinte T, Lynch DV (1988) Transformation of the cryobehavior of rye protoplasts by modification of the plasma membrane lipid composition. Proc Natl Acad Sci USA 85:9026–9030
Thomashow MF (1999) Plant cold acclimation: freezing tolerance genes and regulatory mechanisms. Annu Rev Plant Physiol Plant Mol Biol 50:571–599
Tian SP, Liu J, Zhang CF, Meng XH (2010) Quality properties of harvested mango fruits and regulating technologies. In: Sivakumar D (ed) New trends in postharvest management of fresh produce II. Fresh Produce 4 (Special issue 1), Global Science Books, Kagawa ken, Japan, pp 49–54
Tunnacliffe A, Wise MJ (2007) The continuing conundrum of the LEA proteins. Naturwissenschaften 94:791–812
Uemura M, Tominaga Y, Nakagawara C, Shigematsu S, Minami A, Kawamura Y (2006) Responses of the plasma membrane to low temperatures. Physiol Plant 126:81–89
Valluru R, Lammens W, Claupein W, Van den Ende W (2008) Freezing tolerance by vesicle-mediated fructan transport. Trends Plant Sci 13:409–414
Wada H, Gombos Z, Murata N (1990) Enhancement of chilling tolerance of a cyanobacterium by genetic manipulation of fatty acid desaturation. Nature 347:200–203
Wang ZY, Seto H, Fujioka S, Yoshida S, Chory J (2001) BRI1 is a critical component of a plasma-membrane receptor for plant steroids. Nature 410:380–383
Yamaguchi-Shinozaki K, Shinozaki K (2005) Organization of cis-acting regulatory elements in osmotic- and cold-stress responsive promoters. Trends Plant Sci 10:88–94
Yin ZM, Rorat T, Szabala BM, Ziolkowska A, Malepszy S (2006) Expression of a Solanum sogarandinum SK3-type dehydrin enhances cold tolerance in transgenic cucumber seedlings. Plant Sci 170:1164–1172
Zaharah SS, Singh Z (2011) Postharvest nitric oxide fumigation alleviates chilling injury, delays fruit ripening and maintains quality in cold-stored ‘Kensington Pride’ mango. Postharvest Biol Technol 60:202–210
Zaharah SS, Singh Z, Symons GM, Reid JB (2012) Role of brassinosteroids, ethylene, abscisic acid, and indole-3-acetic acid in mango fruit ripening. J Plant Growth Regul. doi:10.1007/s00344-011-9245-5
Zhang CF, Tian SP (2009) Crucial contribution of membrane lipids’ unsaturation to acquisition of chilling-tolerance in peach fruit stored at 0 °C. Food Chem 115:405–411
Zhang CF, Tian SP (2010) Peach fruit acquired tolerance to low temperature stress by accumulation of linolenic acid and N-acylphosphatidylethanolamine in plasma membrane. Food Chem 120:864–872
Zhang CF, Ding ZS, Xu XB, Wang Q, Qin GZ, Tian SP (2010) Crucial roles of membrane stability and its related proteins in the tolerance of peach fruit to chilling injury. Amino Acids 39:181–194
Zhu Z, Zhang ZQ, Qin GZ, Tian SP (2010) Effects of brassinosteroids on postharvest disease and senescence of jujube fruit in storage. Postharvest Biol Technol 56:50–55
Acknowledgments
This study was supported by the National Natural Science Foundation of China (Grant No. 31030051) and the National Basic Research Program of China (973 Program, Grant No. 2011CB100604), and the CAS/SAFEA International Partnership Program for Creative Research Teams (Grant No. 20090491019).
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The authors have declared that no competing interests exist.
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B. Li and C. Zhang contributed equally to this work.
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Li, B., Zhang, C., Cao, B. et al. Brassinolide enhances cold stress tolerance of fruit by regulating plasma membrane proteins and lipids. Amino Acids 43, 2469–2480 (2012). https://doi.org/10.1007/s00726-012-1327-6
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DOI: https://doi.org/10.1007/s00726-012-1327-6