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Tonoplast Lipid Composition and Proton Pump of Pineapple Fruit During Low-Temperature Storage and Blackheart Development

The Journal of Membrane Biology volume 247, pages 429–439 (2014)Cite this article

Abstract

Vacuole represents a major storage organelle playing vital roles in pH homoeostasis and cellular detoxification. The chemical and functional properties of tonoplast in response to chilling temperature and their roles in chilling injury are largely unknown. In the current study, lipid composition of tonoplast and the activities of two vacuolar proton pumps, H+-ATPase (V-ATPase) and H+-pyrophosphatase (V-PPase), were investigated in accordance with the development of blackheart, a form of chilling injury in pineapple fruit (Ananas comosus). Chilling temperature at 10 °C for 1 week induced irreversible blackheart injury in concurrence with a substantial decrease in V-ATPase activity. By contrast, the activity was increased after 1 week at 25 °C. The activity of V-PPase was not changed under both temperatures. Level of total phospholipids of tonoplast decreased at 10 °C, but increased at 25 °C. There was no change at the level of total glycolipids under both temperatures. Thus, low temperature increased the ratio of total glycolipids vs. total phospholipids of tonoplast. Phosphatidylcholine and phosphatidylethanolamine were the predominant phospholipids of tonoplast. Low temperature increased the relative level of phosphatidic acid but decreased the percentage of both phosphatidylcholine and phosphatidylethanolamine. Unsaturated fatty acids accounted for over 60 % of the total tonoplast fatty acids, with C18:1 and C18:2 being predominant. Low temperature significantly decreased the percentage of C18:3. Modification of membrane lipid composition and its effect on the functional property of tonoplast at low temperature were discussed in correlation with their roles in the development of chilling injury in pineapple fruit.

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References

  • Ames BN (1966) Assay of inorganic phosphate, total phosphate and phosphatases. Methods Enzymol 8:115–118

    CAS  Article  Google Scholar 

  • Bargmann BO, Munnik T (2006) The role of phospholipase D in plant stress responses. Curr Opin Plant Biol 9(5):515–522

    CAS  Article  PubMed  Google Scholar 

  • Behzadipour M, Ratajczak R, Faist K, Pawlitschek P, Trémolières A, Kluge M (1998) Phenotypic adaptation of tonoplast fluidity to growth temperature in the CAM plant Kalanchoë daigremontiana ham. et Per. is accompanied by changes in the membrane phospholipid and protein composition. J Membr Biol 166:61–70

    CAS  Article  PubMed  Google Scholar 

  • Berglund AH, Norberg P, Quartacci MF, Nilsson R, Liljenberg C (2001) Properties of plant plasma membrane lipid models – bilayer permeability and monolayer behaviour of glucosylceramide and phosphatidic acid in phospholipid mixtures. Physiologia Plantarum 109:117–122

    Article  Google Scholar 

  • Borsani J, Budde C, Porrini L, Lauxmann M, Lombardo V, Murray R, Andreo C, Drincovich M, Lara M (2009) Carbon metabolism of peach fruit after harvest: changes in enzymes involved in organic acid and sugar level modifications. J Exp Bot 60:1823–1837

    CAS  Article  PubMed  Google Scholar 

  • Bradford MM (1976) A rapid and sensitive method for the quantitative microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–252

    CAS  Article  PubMed  Google Scholar 

  • Dahler JM, Underhill SJR, Zhou Y, Giles J (2000) Blackheart and biochemical changes in pineapple fruit as affected by storage, maturity and cultivar. Acta Hortic 575:603–610

    Google Scholar 

  • Darley CP, Davies JM, Sanders D (1995) Chill-induced changes in the activity and abundance of the vacuolar proton-pumping pyrophosphatase from mung bean hypocotyls. Plant Physiol 109:659–665

    PubMed Central  CAS  PubMed  Google Scholar 

  • deOliveira LMN, Sobreira ACdM, Monteiro FdP, deMelo DF (2009) Chill-induced changes in fatty acid composition of tonoplast vesicles from hypocotyls of Vigna unguiculata (L.). Walp Braz J Plant Physiol 22:69–72

    Article  Google Scholar 

  • Devaiah SP, Pan X, Hong Y, Roth M, Welti R, Wang X (2007) Enhancing seed quality and viability by suppressing phospholipase D in Arabidopsis. Plant J 50:950–957

    CAS  Article  PubMed  Google Scholar 

  • Dietz KJ, Tavakoli N, Kluge C, Mimura T, Sharma SS, Harris GC, Chardonnens AN, Golldack D (2001) Significance of the V-type ATPase for the adaptation to stressful growth conditions and its regulation on the molecular and biochemical level. J Exp Bot 363:1969–1980

    Article  Google Scholar 

  • Domínguez T, Hernández ML, Pennycooke JC, Jiménez P, Martínez-Rivas JM, Sanz C, Stockinger EJ, Sánchez-Serrano JJ, Sanmartín M (2010) Increasing ω-3 desaturase expression in tomato results in altered aroma profile and enhanced resistance to cold stress. Plant Physiol 153:655–665

    PubMed Central  Article  PubMed  Google Scholar 

  • Dupont FM (1987) Variable effects of nitrate on ATP-dependent proton transport by barley root membranes. Plant Physiol 84:526–534

    PubMed Central  CAS  Article  PubMed  Google Scholar 

  • Etxeberria E, Gonzalez P (2004) Simultaneous isolation of tonoplast and plasmalemma from citrus juice cells: combination of sucrose gradient and two phase partitioning. HortScience 39:174–176

    Google Scholar 

  • Fan L, Zheng SQ, Wang XM (1997) Antisense suppression of phospholipase D alpha retards abscisic acid- and ethylene-promoted senescence of postharvest Arabidopsis leaves. Plant Cell 9:2183–2196

    PubMed Central  CAS  PubMed  Google Scholar 

  • Ferrol N, Bennett AB (1996) A single gene may encode differentially localized Ca2+-ATPases in tomato. Plant Cell 8:1159–1169

    PubMed Central  CAS  PubMed  Google Scholar 

  • Hodges TK, Leonard RT (1974) Purification of a plasma membrane-bound adenosine triphosphatase from plant roots. Methods Enzymol 32:392–406

    CAS  Article  PubMed  Google Scholar 

  • Hong K, Xu H, Wang J, Zhang L, Hu H, Jia Z, Gu H, He Q, Gong D (2013) Quality changes and internal browning developments of summer pineapple fruit during storage at different temperatures. Sci Hortic 151:68–74

    CAS  Article  Google Scholar 

  • Hu H, Li X, Dong C, Chen W (2011) Effects of wax treatment on quality and postharvest physiology of pineapple fruit in cold storage. Afr J Biotechnol 10(39):7592–7603

    CAS  Google Scholar 

  • Imbault AK, Marie-Alphonsine PA, Horry JP, Francois-Haugrin M, Romuald K, Soler A (2011) Polyphenol oxidase and peroxidase expression in four pineapple varieties (Ananas comosus L.) after a chilling injury. J Agric Food Chem 59:342–348

    Article  Google Scholar 

  • Kadohama N, Goh T, Ohnishi M, Fukaki H, Mimura T, Suzuki Y (2013) Sudden collapse of vacuoles in Saintpaulia sp. palisade cells induced by a rapid temperature decrease. PLoS One 8:e57259

    PubMed Central  CAS  Article  PubMed  Google Scholar 

  • Kasamo K (1988a) Inhibition of tonoplast and plasma membrane H+ -ATPase activity in rice (Oryza sativa L.) culture cells by local anesthetics. Plant Cell Physiol 29:215–221

    CAS  Google Scholar 

  • Kasamo K (1988b) Response of tonoplast and plasma membrane ATPase in chilling sensitive and insensitive rice (Oryza sativa L.) culture cells to low temperature. Plant Cell Physiol 29:1085–1094

    CAS  Google Scholar 

  • Kasamo K (1990) Mechanism for the activation of plasma membrane H+ -ATPase from rice (Oryza sativa L.) culture cells by molecular species of a phospholipid. Plant Physiol 93:1049–1052

    PubMed Central  CAS  Article  PubMed  Google Scholar 

  • Kasamo K, Kagita F, Yamanishi H, Sakaki T (1992) Low temperature-induced changes in the thermotropic properties and fatty acid composition of the plasma membrane and tonoplast of cultured rice (Oryza sativa L.) cells. Plant Cell Physiol 33(4):609–616

    CAS  Google Scholar 

  • Kasamo K, Yamaguchi M, Nakamura Y (2000) Mechanism of the chilling-induced decrease in proton pumping across the tonoplast of rice cells. Plant Cell Physiol 41:840–849

    CAS  Article  PubMed  Google Scholar 

  • Kawamura Y (2007) Chilling induces a decrease in pyrophosphate-dependent H+ -accumulation associated with a DpHvacpHvac-stat in mung bean, a chill-sensitive plant. Plant Cell Environ 31:288–300

    Article  PubMed  Google Scholar 

  • Kooijman EE, Chupin V, deKruijff B, Burger K (2003) Modulation of membrane curvature by phosphatidic acid and lysophosphatidic acid. Traffic 4:162–174

    CAS  Article  PubMed  Google Scholar 

  • Leach RP, Wheeler KP, Flowers TJ, Yeo AR (1990) Molecular markers for ion compartmentation in cells of higher plants, II. Lipid composition of the tonoplast of the halophyte Suaeda maritima (l.) DUM. J Exp Bot 41:1089–1994

    CAS  Article  Google Scholar 

  • Liu XY, Teng YB, Li B, Meng QW (2013) Enhancement of low-temperature tolerance in transgenic tomato plants overexpressing Lefad7 through regulation of trienoic fatty acids. Photosynthetica 51:238–244

    CAS  Article  Google Scholar 

  • Lurie S, Ronen R, Lipsker Z, Aloni B (1994) Effects of paclobutrazol and chilling temperatures on lipids, antioxidants and ATPase activity of plasma membrane isolated from green bell pepper fruits. Physiol Plant 91:593–598

    CAS  Article  Google Scholar 

  • Lyons JM (1973) Chilling injury in plants. Annu Rev Plant Biol 24:445–466

    CAS  Article  Google Scholar 

  • Maeshima M (2000) Review: Vacuolar H+-pyrophosphatase. Biochimica et Biophysica Acta 1465:37–51

    CAS  Article  PubMed  Google Scholar 

  • Matsuura-Endo C, Maeshima M, Yoshida S (1990) Subunit composition of vacuolar membrane H(+)-ATPase from mung bean. Eur J Biochem 187:745–751

    CAS  Article  PubMed  Google Scholar 

  • Mayer AM (1987) Polyphenol oxidase and peroxidase in plants–Recent progress. Phytochemistry 26:11–20

    Article  Google Scholar 

  • Moing A, Renaud C, Gaudillere M, Raymond P, Roudeillac P, Denoyes-Rothan B (2001) Biochemical changes during fruit development of four strawberry cultivars. J Am Soc Hort Sci 126:394–403

    CAS  Google Scholar 

  • Müller ML, Jensen M, Taiz L (1999) The vacuolar H+ -ATPase of lemon fruits is regulated by variable H+/ATP coupling and slip. J Biol Chem 274:10706–10716

    Article  PubMed  Google Scholar 

  • Nakamura Y, Sakakibara Y, Kobayashi H, Kasamo K (1997) Rapid reconstitution of tonoplast H+ -translocating pyrophosphatase from cultured rice cells into liposomes. Plant Cell Physiol 38:371–374

    CAS  Article  PubMed  Google Scholar 

  • Nilprapruck P, Pradisthakarn N, Authanithee F, Keebjan P (2008) Effect of exogenous methyl jasmonate on chilling injury and quality of pineapple (Ananas comosus L.) cv. Pattavia. Pattavia. Silpakorn U Sci Tech J 2:33–42

    CAS  Google Scholar 

  • Nishida I, Murata N (1996) Chilling sensitivity in plants and cyanobacteria. The crucial contribution of membrane lipids. Annu Rev Plant Physiol Plant Mol Biol 47:541–568

    CAS  Article  PubMed  Google Scholar 

  • Nukulthornprakit O, Siriphanich J (2005) Hydrogen peroxide and ascorbic acid contents, superoxide dismutase and catalase activities in Smooth Cayenne and Queen pineapples during cold storage. Acta Hortic 682:611–615

    Google Scholar 

  • Orr W, White TC, Iu B, Robert L, Singh J (1995) Characterization of a low-temperature-induced cDNA from winter Brassica napus encoding the 70 kDa subunit of tonoplast ATPase. Plant Mol Biol 28:943–948

    CAS  Article  PubMed  Google Scholar 

  • Parkin Kl, Kuo S-J (1989) Chilling-induced lipid degradation in cucumber (Cucumis sativa L cv hybrid C) fruit. Plant Physiol 90:1049–1056

    PubMed Central  CAS  Article  PubMed  Google Scholar 

  • Paull RE, Chen C (2003) Postharvest physiology, handling and storage of pineapple, the pineapple: botany, production and uses. CABI Publishing, New York

    Book  Google Scholar 

  • Paull RE, Rohrbach KG (1985) Symptom development of chilling injury in pineapple fruit (Ananas comosus). J Am Soc Hort Sci 110:100–105

    Google Scholar 

  • Pinton R, Cakmak I, Marschner H (1994) Zinc deficiency enhanced NAD(P)H-dependent superoxide radical production in plasma membrane vesicles isolated from roots of bean plants. J Exp Bot. 45:45–50

    CAS  Article  Google Scholar 

  • Porta H, Rocha-Sosa M (2002) Plant lipoxygenases, physiological and molecular features. Plant Physiol 130:15–21

    PubMed Central  CAS  Article  PubMed  Google Scholar 

  • Pusittigul I, Kondo S, Siriphanich J (2012) Internal browning of pineapple (Ananas comosus L.) fruit and endogenous concentrations of abscisic acid and gibberellins during low temperature storage. Sci Hortic 146:45–51

    CAS  Article  Google Scholar 

  • Roth MG (2008) Molecular mechanisms of PLD function in membrane. Traffic 9:1233–1239

    CAS  Article  PubMed  Google Scholar 

  • Roughan PG, Batta RD (1968) Quantitative analysis of sulfolipid (sulfoquinovosyl diglyceride) and galactolipids (monogalactosyl and digalactosyl diglycerides) in plant tissues. Anal Biochem 22:74–88

    CAS  Article  PubMed  Google Scholar 

  • Rouser G, Fleischer S, Yamamoto A (1970) Two dimensional thin layer chromatographic separation of polar lipids and determination of phospholipids by phosphorus analysis of spots. Lipids 4:494–496

    Article  Google Scholar 

  • Saradhuldhat P, Paull RE (2007) Pineapple organic acid metabolism and accumulation during fruit development. Sci Hortic 112:297–303

    CAS  Article  Google Scholar 

  • Schulze WX, Schneider T, Starck S, Martinoia E, Trentmann O (2012) Cold acclimation induces changes in Arabidopsis tonoplast protein abundance and activity and alters phosphorylation of tonoplast monosaccharide transporters. Plant J 69:529–542

    CAS  Article  PubMed  Google Scholar 

  • Shiratake K, Kanayama Y, Maeshima M, Yamaki S (1997) Changes in H+ -pumps and a tonoplast intrinsic protein of vacuolar membranes during the development of pear fruit. Plant Cell Physiol 38:1039–1045

    CAS  Article  PubMed  Google Scholar 

  • Smith LG (1983) Cause and development of blackheart in pineapples chilling. Trop Agric 60(1):31–35

    Google Scholar 

  • Steponkus PL, Lynch DV (1989) Freeze/thaw-induced destabilization of the plasma membrane and the effects of cold acclimation. J Bioenerg Biomembr 21:21–41

    CAS  Article  PubMed  Google Scholar 

  • Stewart RJ, Sawyer BJB, Bucheli CS, Robinson SP (2001) Polyphenol oxidase is induced by chilling and wounding in pineapple. Aust J Plant Physiol 28(3):181–191

    CAS  Google Scholar 

  • Stewart RJ, Sawyer BJB, Robinson SP (2002) Blackheart development following chilling in fruit of susceptible and resistant pineapple cultivars. Aust J of Exp Agric 42(2):195–199

    Article  Google Scholar 

  • Teisson C, Combres JC, Prevel PM, Marchal J (1979) Internal browning of pineapples. Fruits 34(4):245–261

    CAS  Google Scholar 

  • Testerink C, Munnik T (2011) Molecular, cellular, and physiological responses to phosphatidic acid formation in plants. J Exp Bot 62(7):2349–2361

    CAS  Article  PubMed  Google Scholar 

  • Theocharis A, Cle′ment C, Barka EdA (2012) Physiological and molecular changes in plants grown at low temperatures. Planta 235:1091–1105

    CAS  Article  PubMed  Google Scholar 

  • Thompson J, Froese C, Madey E, Smith M, Hong Y (1998) Lipid metabolism during plant senescence. Prog Lipid Res 37:119–141

    CAS  Article  PubMed  Google Scholar 

  • Uemura M, Steponkus PL (1994) A contrast of the plasma membrane lipid composition of oat and rye leaves in relation to freezing toIerance. Plant Physiol 104:479–496

    PubMed Central  CAS  PubMed  Google Scholar 

  • Weerahewa D, Adikaram NKB (2005) Some biochemical factors underlying the differential susceptibility of two pineapple cultivars to internal browning disorder. Cey J Sci (Bio Sci) 34:7–20

    Google Scholar 

  • Welti R, Li W, Li M, Sang Y, Biesiada H, Zhou H, Rajashekar C, Williams T, Wang X (2002) Profiling membrane lipids in plant stress responses. Role of phospholipase Dα in freezing induced lipid changes in Arabidopsis J Biol Chem 277:31994–32002

    CAS  Google Scholar 

  • Wismer WV, Worthing WM, Yada RY, Marangoni AG (1998) Membrane lipid dynamics and lipid peroxidation in the early stages of low-temperature sweetening in tubers of Solanum tuberosum. Physiol Plant 102:396–410

    CAS  Article  Google Scholar 

  • Wormit A, Trentmann O, Feifer I, Lohr C, Tjaden J, Meyer S, Schmidt U, Martinoia E, Neuhaus HE (2006) Molecular identification and physiological characterization of a novel monosaccharide transporter from Arabidopsis involved in vacuolar sugar transport. Plant Cell 18:3476–3490

    PubMed Central  CAS  Article  PubMed  Google Scholar 

  • Yamaguchi M, Kasamo K (1993) Modulation of the activity of purified tonoplast H+ -ATPase from mung bean (Vigna radiata L.) hypocotyls by various lipids. Plant Cell Physiol 34:411–419

    Google Scholar 

  • Yamaguchi M, Kasamo K (2001) Modulation in the activity of purified tonoplast H+ -ATPase by tonoplast glycolipids prepared from cultured rice (Oryza sativa L. var. Boro) cells. Plant Cell Physiol. 42:516–523

    CAS  Article  PubMed  Google Scholar 

  • Yin Y-G, Tominaga T, Iijima Y, Aoki K, Shibata D, Ashihara H, Nishimura S, Ezura H, Matsukura C (2010) Metabolic alterations in organic acids and γ-aminobutyric acid in developing tomato (Solanum lycopersicum L.) ruits. Plant Cell Physiol 51:1300–1314

    CAS  Article  PubMed  Google Scholar 

  • Yoshida S (1994) Low temperature-induced cytoplasmic acidosis in cultured mung bean (Vigna radiata [L.] Wilczek) cells. Plant Physiol 104:1131–1138

    PubMed Central  CAS  PubMed  Google Scholar 

  • Yoshida S, Matsuura-Endo C (1991) Comparison of temperature dependency of tonoplast proton translocation between plants sensitive and insensitive to chilling. Plant Physiol 95:504–508

    PubMed Central  CAS  Article  PubMed  Google Scholar 

  • Yoshida S, Matsuura C, Etani S (1989) Impairment of tonoplast H+ -ATPase as an initial physiological response of cells to chilling in mung bean (Vigna radiata [L.] Wilczek). Plant Physiol 89(2):634–642

    PubMed Central  CAS  Article  PubMed  Google Scholar 

  • Yoshida S, Hotsubo K, Kawamura Y, Murai M, Arakawa K, Takezawa D (1999) Alterations of intracellular pH in response to low temperature stresses. J Plant Res 112:225–236

    CAS  Article  Google Scholar 

  • Youryon P, Wongs-Aree C, McGlasson WB, Glahan S, Kanlayanarat S (2007) Internal browning occurrences of ‘queen’ pineapple under various low temperatures. Acta Hortic 804:555–560

    Google Scholar 

  • Yu C, Wang H-S, Yang S, Tang X-F, Duan M, Meng Q-W (2009) Overexpression of endoplasmic reticulum omega-3 fatty acid desaturase gene improves chilling tolerance in tomato. Plant Physiol Biochem 47:1102–1112

    CAS  Article  PubMed  Google Scholar 

  • Zhang C, Tian S (2009) Crucial contribution of membrane lipids’unsaturation to acquisition of chilling-tolerance in peach fruit stored at 0 & #xB0;C. Food Chem 115:405–411

    CAS  Article  Google Scholar 

  • Zhang C, Tian S (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

    CAS  Article  Google Scholar 

  • Zhang W, Wang C, Qin C, Wood T, Olafsdottir G, Welti R, Wang X (2003) The Oleate-stimulated phospholipase D, PLD and phosphatidic acid decrease H2O2-induced cell death in Arabidopsis. Plant Cell 15:2285–2295

    PubMed Central  CAS  Article  PubMed  Google Scholar 

  • Zhang Y, Zhu H, Zhang Q, Li M, Yan M, Wang R, Wang L, Welti R, Zhang W, Wang X (2009) Phospholipase Dα1 and phosphatidic acid Regulate NADPH oxidase activity and production of reactive oxygen species in ABA-mediated stomatal closure in Arabidopsis. Plant Cell 21:2357–2377

    PubMed Central  CAS  Article  PubMed  Google Scholar 

  • Zhang J, Liu H, Sun J, Li B, Zhu Q, Chen S, Zhang H (2012) Arabidopsis fatty Acid desaturase FAD2 is required for salt tolerance during seed germination and early seedling growth. PLoS one 7:e30355

    PubMed Central  CAS  Article  PubMed  Google Scholar 

  • Zhang XD, Wang RP, Zhang FJ, Tao FQ, Li WQ (2013) Lipid profiling and tolerance to low-temperature stress in Thellungiella salsuginea in comparison with Arabidopsis thaliana. Biologia Pantarum 57:149–153

    CAS  Article  Google Scholar 

  • Zhou Y, Tan X (1992) Mechanism of pineapple blackheart after low temperature treatment and gibberellin treatment. Acta Phytophysiologica Sinica 18:341–347

    CAS  Google Scholar 

  • Zhou Y, Tan X (1997) Mechanism of blackheart development induced by low temperature and gibberellic acid in pineapple fruit. Acta Hortic 425:587–593

    Google Scholar 

  • Zhou Y, Dahler JM, Underhill SJR, Wills RBH (2003a) Enzymes associated with blackheart development in pineapple fruit. Food Chem 80(4):565–572

    CAS  Article  Google Scholar 

  • Zhou Y, O’Hare TJ, Jobin-Decor M, Underhill SJR, Wills RB, Graham MW (2003b) Transcriptional regulation of a pineapple polyphenol oxidase gene and its relationship to blackheart. Plant Biotechnol Journal 1:463–478

    CAS  Article  Google Scholar 

  • Zhou Y, Pan X, Qu H, Underhill SJR (2014) Low temperature alters plasma membrane lipid composition and ATPase activity of pineapple fruit during blackheart development. J Bioenerg Biomembr 46:59–69

    CAS  Article  PubMed  Google Scholar 

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Acknowledgments

This work was funded by the National Natural Science Foundation of China and the Australia Centre for International Agriculture Research (ACIAR).

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  1. Queensland Alliance for Agriculture and Food Innovation, University of Queensland, St Lucia, QLD, 4072, Australia

    Yuchan Zhou & Steven J. R. Underhill

  2. Faculty of Science, Education and Engineering, University of the Sunshine Coast, Sippy Downs, QLD, 4556, Australia

    Yuchan Zhou & Steven J. R. Underhill

  3. Key Laboratory of Plant Resources Conservation and Sustainable Utilization, South China Botanical Garden, Chinese Academy of Sciences, Guangzhou, 510650, China

    Xiaoping Pan & Hongxia Qu

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  1. Yuchan Zhou
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  2. Xiaoping Pan
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  3. Hongxia Qu
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Correspondence to Yuchan Zhou.

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Zhou, Y., Pan, X., Qu, H. et al. Tonoplast Lipid Composition and Proton Pump of Pineapple Fruit During Low-Temperature Storage and Blackheart Development. J Membrane Biol 247, 429–439 (2014). https://doi.org/10.1007/s00232-014-9650-3

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  • DOI: https://doi.org/10.1007/s00232-014-9650-3

Keywords

  • Tonoplast
  • Vacuolar H+-ATPase
  • Vacuolar H+-pyrophosphatase
  • Lipid composition
  • Chilling injury
  • Pineapple fruit