SpringerLink
Log in

Low temperature alters plasma membrane lipid composition and ATPase activity of pineapple fruit during blackheart development

  • Published:
Journal of Bioenergetics and Biomembranes Aims and scope Submit manuscript

Abstract

Plasma membrane (PM) plays central role in triggering primary responses to chilling injury and sustaining cellular homeostasis. Characterising response of membrane lipids to low temperature can provide important information for identifying early causal factors contributing to chilling injury. To this end, PM lipid composition and ATPase activity were assessed in pineapple fruit (Ananas comosus) in relation to the effect of low temperature on the development of blackheart, a form of chilling injury. Chilling temperature at 10 °C induced blackheart development in concurrence with increase in electrolyte leakage. PM ATPase activity was decreased after 1 week at low temperature, followed by a further decrease after 2 weeks. The enzyme activity was not changed during 25 °C storage. Loss of total PM phospholipids was found during postharvest senescence, but more reduction was shown from storage at 10 °C. Phosphatidylcholine and phosphatidylethanolamine were the predominant PM phospholipid species. Low temperature increased the level of phosphatidic acid but decreased the level of phosphatidylinositol. Both phospholipid species were not changed during storage at 25 °C. Postharvest storage at both temperatures decreased the levels of C18:3 and C16:1, and increased level of C18:1. Low temperature decreased the level of C18:2 and increased the level of C14:0. Exogenous application of phosphatidic acid was found to inhibit the PM ATPase activity of pineapple fruit in vitro. Modification of membrane lipid composition and its effect on the functional property of plasma membrane at low temperature were discussed in correlation with their roles in blackheart development of pineapple fruit.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Subscribe and save

Springer+ Basic
EUR 32.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or Ebook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • Ahn S, Im Y, Chung G, Seong K, Cho B (2000) Sensitivity of plasma membrane H+ -ATPase of cucumber root system in response to low root temperature. Plant Cell Rep 19:831–835

    Article  CAS  Google Scholar 

  • Anderson RA, Boronenkov IV, Doughman SD, Kunz J, Loijens JC (1999) Phosphatidylinositol phosphate kinases, a multifaceted family of signaling enzymes. J Biol Chem 274:9907–9910

    Article  CAS  Google Scholar 

  • Badea C, Basu SK (2009) The effect of low temperature on metabolism of membrane lipids in plants and associated gene expression. Plant Omics J 2:78–84

    CAS  Google Scholar 

  • Beja-Tal S, Borochov A (1994) Age-related changes in biochemical and physical properties of carnation petal plasma membranes. J Plant Physiol 143:195–199

    Article  CAS  Google Scholar 

  • Benabdellah K, Azcón-Aguilar C, Ferrol N (2000) Alterations in the plasma membrane polypeptide pattern of tomato roots (Lycopersicon esculentum) during the development of arbuscular mycorrhiza. J Exp Bot 51:747–754

    Article  CAS  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. Physiol Plant 109:117–122

    Article  Google Scholar 

  • Berglund AH, Calucci MFQL, Navari-Izzo F, Pinzino C, Liljenberg C (2002) Alterations of wheat root plasma membrane lipid composition induced by copper stress result in changed physicochemical properties of plasma membrane lipid vesicles. Biochim Biophys Acta - Biomembranes 1564:466–472

    Article  CAS  Google Scholar 

  • Borochov A, Halevy AH, Shinitzky M (1982) Senescence and the fluidity of rose retal membranes : relationship to phospholipid metabolism. Plant Physiol 69:296–299

    Article  CAS  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

    Article  CAS  Google Scholar 

  • Brown DJ, DuPont FM (1989) Lipid composition of plasma membranes and endomembranes prepared from roots of barley (Hordeum vulgare L.). Plant Physiol 90:955–961

    Article  CAS  Google Scholar 

  • Camoni L, Lucente CD, Pallucca R, Visconti S, Aducci P (2012) Binding of phosphatidic acid to 14-3-3 proteins hampers their ability to activate the plant plasma membrane H+ -ATPase. IUBMB Life 64:710–716

    Article  CAS  Google Scholar 

  • Catucci L, Leo VD, Milano F, Giotta L, Vitale R, Agostiano A et al (2012) Oxidoreductase activity of chromatophores and purified cytochrome bc1 complex from Rhodobacter sphaeroides: a possible role of cardiolipin. J Bioenerg Biomembr 44:487–493

    Article  CAS  Google Scholar 

  • Choi Y-J, Tomás-Barberán AF, Saltveit ME (2005) Wound-induced phenolic accumulation and browning in lettuce (Lactuca sativa L.) leaf tissue is reduced by exposure to n-alcohols. Postharvest Biol Technol 37:47–55

    Article  CAS  Google Scholar 

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

    CAS  Google Scholar 

  • Franck C, Lammertyn J, Ho Q, Verboven P, Verlinden B, Nicola B (2007) Browning disorders in pear fruit. Postharvest Biol Technol 43:1–13

    Article  CAS  Google Scholar 

  • Hernandez A, Cooke D, Clarkson D (2002) In vivo activation of plasma membrane H+ -ATPase hydrolytic activity by complex lipid-bound unsaturated fatty acids in Ustilago maydis. Eur J Biochem 269:1006–1011

    Article  CAS  Google Scholar 

  • Hewajulige I, Wijeratnam RW, Wijesundera RMA (2003) Fruit calcium concentration and chilling injury during low temperature storage of pineapple. J Sci Food Agric 83:1451–1454

    Article  CAS  Google Scholar 

  • Hewajulige IG, Wijeratnam SW, Wijesundera RL (2006) Pre-harvest application of calcium to control black heart disorder in Mauritius pineapples during low-temperature storage. J Sci Food Agric 86:420–424

    Article  CAS  Google Scholar 

  • Hinz G, Hillmer S, Bäumer M, Hohl I (1999) Vacuolar storage proteins and the putative vacuolar sorting receptor BP-80 exit the golgi apparatus of develo** pea cotyledons in different transport vesicles. The Plant Cell 11:1509–1524

    CAS  Google Scholar 

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

    Article  CAS  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 

  • Kaniuga Z, Saczynska V, Miskiewicz E, Garstka M (1999) The fatty acid composition of phosphatidylglycerol and sulfoquinovosyldiacylglycerol of Zea mays genotypes differing in chilling susceptibility. J Plant Physiol 154(2):256–263

    Article  CAS  Google Scholar 

  • Kasamo K (1988) 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

    Article  CAS  Google Scholar 

  • Kasamo K, Sakakibara Y (1995) The plasma membrane H+ -ATPase from higher plants : functional reconstitution into liposomes and its regulation by phospholipids. Plant Sci 111:117–131

    Article  CAS  Google Scholar 

  • Kasamo K, Yamanishi H (1991) Functional reconstitution of plasma membrane H+ -ATPase from mung bean (Vigna radiata L.) hypocotyls in liposomes prepared with various molecular species of phospholipids. Plant Cell Physiol 32(8):1219–1225

    CAS  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 

  • Knowles NR, Knowles LO (1989) Correlations between electrolyte leakage and degree of saturation of polar lipids from aged potato (Solanum tuberosum L) tuber tissue. Ann Bot 63:331–338

    Google Scholar 

  • Kodama H, Hamada Т, Horiguchi G, Nishimura M, Iba K (1994) Genetic enhancement of cold tolerance by expression of a gene for chloroplast ω-3-fatty-acid desaturase in transgenic tobacco. Plant Physiol 105:601–605

    CAS  Google Scholar 

  • Kojima M, Suzuki H, Ohnishi M, Ito S (1998) Effects of growth temperature on lipids of adzuki bean cells. Phytochemistry 47(8):1483–1487

    Article  CAS  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

    Article  CAS  Google Scholar 

  • Kukavica B, Quartacci MF, Veljović-Jovanović S, Navari-Izzo F (2007) Lipid composition of pea (Pisum sativum l.) and maize (Zea mays l.) root plasma membrane and membrane–bound peroxidase and superoxide dismutase. Arch Biol Sci 59(4):295–302

    Article  Google Scholar 

  • Lee S, Singh A, Chung G, Ahn S, Noh E, Steudle E (2004) Exposure of roots of cucumber (Cucumis sativus) to low temperature severely reduces root pressure, hydraulic conductivity and active transport nutrients. Physiol Plant 120:413–420

    Article  CAS  Google Scholar 

  • Lindberg S, Banaś A, Stymne S (2005) Effects of different cultivation temperatures on plasma membrane ATPase activity and lipid composition of sugar beet roots. Plant Physiol Biochem 43:261–268

    Article  CAS  Google Scholar 

  • Lukatkin AS (2002) Contribution of oxidative stress to the development of cold-induced damage to leaves of chilling-sensitive plants: Reactive oxygen species formation during plant chilling. Russ J Plant Physiol 49(5):622–627

    Article  CAS  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

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • M’Voula-Tsieri M, Hartmann-Bouillon MA, Benveniste P (1981) Properties of nucleoside diphosphatases in purified membrane fractions from maize coleoptiles. I. Study of latency. Plant Sci Lett 20:379–386

    Article  Google Scholar 

  • Martz F, Sutinen M, Kiviniemi S, Palta J (2006) Changes in freezing tolerance, plasma membrane H+ -ATPase activity and fatty acid composition in Pinus resinosa needles during cold acclimation and de-acclimation. Tree Physiol 26:783–790

    Article  CAS  Google Scholar 

  • Meijer HJ, Munnik T (2003) Phospholipid-based signaling in plants. Annu Rev Plant Biol 54:265–306

    Article  CAS  Google Scholar 

  • Mikami K, Murata N (2003) Membrane fluidity and the perception of environmental signals in cyanobacteria and plants. Prog Lipid Res 42:527–543

    Article  CAS  Google Scholar 

  • Munnik T, Vermeer JE (2010) Osmotic stress-induced phosphoinositide and inositol phosphate signalling in plants. Plant Cell Environ 33:655–669

    Article  CAS  Google Scholar 

  • Navari-Izzo F, Quartacci MF, Melfi D, Izzo R (1993) Lipid composition of plasma membranes isolated from sunflower seedlings grown under water-stress. Physiol Plant 87:508–514

    Article  CAS  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. Silpakorn Univ Sci Technol 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

    Article  CAS  Google Scholar 

  • Norberg P, Liljenberg C (1991) Lipids of plasma membranes prepared from oat root cells : effects of induced water-deficit tolerance. Plant Physiol 96(4):1136–1141

    Article  CAS  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 Horticult 682:611–615

    Google Scholar 

  • Palta JP, Meade LS (1989) During cold acclimation of potato species, an increase in 18:2 and a decrease in 16:0 in plasma membrane phospholipids coincide with an increase in freezing stress resistance. Plant Physiol 89:S–89

    Google Scholar 

  • Pan Y-Y, Wang X, Ma L-G, Sun D-Y (2005) Characterization of phosphatidylinositol-specific phospholipase C (PI-PLC) from Lilium daviddi pollen. Plant Cell Physiol 46(10):1657–1665

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

  • Paull RE, Rohrbach KG (1985) Symptom development of chilling injury in pineapple fruit (Ananas comosus). J Am Soc Horticultral 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

    Article  CAS  Google Scholar 

  • Portillo F (2000) Regulation of plasma membrane H+-ATPase in fungi and plants. Biochim Biophys Acta 1469:31–42

    Article  CAS  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 Horticult 146:45–51

    Article  CAS  Google Scholar 

  • Quartacci M, 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

    Article  CAS  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 

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

    Google Scholar 

  • SmoleńAska-Sym G, Kacperska A (1994) Phosphatidylinositol metabolism in low temperature-affected winter oilseed rape leaves. Physiol Plant 91:1–8

    Google Scholar 

  • Stalleart VM, Geuns JMC (1994) Phospholipid and free sterol composition of hypocotyl plasma membranes of ageing mung bean seedlings. Phytochemistry 36:1177–1180

    Article  CAS  Google Scholar 

  • Stevenson JM, Perera IY, Heilmann I, Persson S, Boss WF (2000) Inositol signaling and plant growth. Trends Plant Sci 5(6):252–258

    Article  CAS  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 

  • Surjus A, Durand M (1996) Lipid changes in soybean root membranes in response to salt treatment. J Exp Bot 47:17–23

    Article  CAS  Google Scholar 

  • Takemiya A, Shimazaki K (2010) Phosphatidic acid inhibits blue light-induced stomatal opening via inhibition of protein phosphatase 1. Plant Physiol 153:1555–1562

    Article  CAS  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

    Article  CAS  Google Scholar 

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

    Article  CAS  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

    CAS  Google Scholar 

  • Vega S, Rio A d, Bamberg J, Palta J (2004) Evidence for the up-regulation of stearoyl-ACP (D9) desaturase gene rxpression during cold acclimation. Am J Potato Res 81:125–135

    Article  CAS  Google Scholar 

  • Vossen JH, Abd-El-Haliem A, Fradin EF, Berg GCMvd, Ekengren SK, Meijer HJ et al (2010) Identification of tomato phosphatidylinositol-specific phospholipase-C (PI-PLC) family members and the role of PLC4 and PLC6 in HR and disease resistance. Plant J 62:224–239

    Article  CAS  Google Scholar 

  • Wang X (2001) Plant phospholipases. Annu Rev Plant Physiol Plant Mol Biol 52:211–231

    Article  CAS  Google Scholar 

  • Wang CY, Kramer GF, Whitaker BD, Lusby WR (1992) Temperature preconditioning increases tolerance to chilling injury and alters lipid composition in zucchini squash. J Plant Physiol 140:229–235

    Article  CAS  Google Scholar 

  • Wang YS, Tian SP, Xu Y (2005) Effects of high oxygen concentration on pro and anti-oxidant enzymes in peach fruits during postharvest periods. Food Chem 91(1):99–104

    Article  CAS  Google Scholar 

  • Wang H, Qian Z, Ma S, Zhou Y, Patrick JW, Duan X et al (2013) Energy status of ripening and postharvest senescent fruit of litchi (Litchi chinensis Sonn). BMC Plant Biol 13:55

    Article  CAS  Google Scholar 

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

    Google Scholar 

  • Whitaker BD (1993) Lipid changes in microsomes and crude plastid fractions during storage of tomato fruits at chilling and nonchilling temperatures. Phytochemistry 32:265–271

    Article  CAS  Google Scholar 

  • White F, Cooke D, Earnshaw M, Clarkson D, Burden R (1990) Does plant growth temperature modulate the membrane composition and ATPase activities of tonoplast and plasma membranes fractions from rye roots? Phytochemistry 29:3385–3393

    Article  CAS  Google Scholar 

  • Widell S, Larsson C (1990) A critical evaluation of markers used in plasma membrane purification. In: Larsson C, Mole IM (eds) The plant plasma membrane. Springer-Verlag, Berlin, pp 16–44

    Chapter  Google Scholar 

  • Wijeratnam RSW, Hewajulige IGN, Wijesundera RLC, Abeysekere M (2006) Fruit calcium concentration and chilling injury during low temperature storage of pineapple. Acta Horticult 702:203–208

    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

    Article  CAS  Google Scholar 

  • Wu J, Seliskar DM, Gallagher JL (2005) The response of plasma membrane lipid composition in callus of the halophyte spartina patens (poaceae) to salinity stress. Am J Bot 92(5):852–858

    Article  CAS  Google Scholar 

  • Xue H, Chen X, Li G (2007) Involvement of phospholipid signaling in plant growth and hormone effects. Curr Opin Plant Biol 10:483–489

    Article  CAS  Google Scholar 

  • Yang Y-q, Wang X-f (2005) Changes of plasma membrane H+ -ATPase activities of glycine max seeds by PEG treatment. Fores Stud China 7:7–11

    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 Horticult 804:555–560

    Google Scholar 

  • Youryon P, Wongs-Aree C, McGlasson WB, Glahan S, Kanlayanarat S (2013) Alleviation of internal browning in pineapple fruit by peduncle infiltration with solutions of calcium chloride or strontium chloride under mild chilling storage. Int Food Res J 20:239–246

    CAS  Google Scholar 

  • Zamani S, Bybordi A, Khorshidi MB, Nezami T (2010) Effects of NaCl salinity levels on lipids and proteins of canola (Brassica Napus L.) cultivars. Adv Environ Biol 4:397–403

    CAS  Google Scholar 

  • Zhai S-M, Gao Q, Xue H-W, Sui Z-H, Yue G-D, Yang A-F et al (2012) Overexpression of the phosphatidylinositol synthase gene from Zea mays in tobacco plants alters the membrane lipids composition and improves drought stress tolerance. Planta 235:69–84

    Article  CAS  Google Scholar 

  • Zhang C, Tian S (2009) Crucial contribution of membrane lipid sunsaturation to acquisition of chilling-tolerance in peach fruit stored at 0 °C. Food Chem 115:405–411

    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

    Article  CAS  Google Scholar 

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

    Article  CAS  Google Scholar 

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

    Article  CAS  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. Biol Pantarum 57:149–153

    Article  CAS  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

    Article  CAS  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 J 1:463–478

    Article  CAS  Google Scholar 

  • Zhou Y, Setz N, Niemietz C, Qu H, Offler C, Tyerman S et al (2007) Aquaporins and unloading of phloem-imported water in coats of develo** bean seeds. Plant Cell Environ 30(12):1566–1577

    Article  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

  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

    ** Pan & Hongxia Qu

Authors
  1. Yuchan Zhou
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. ** Pan
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Hongxia Qu
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Steven J. R. Underhill
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Yuchan Zhou.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Zhou, Y., Pan, X., Qu, H. et al. Low temperature alters plasma membrane lipid composition and ATPase activity of pineapple fruit during blackheart development. J Bioenerg Biomembr 46, 59–69 (2014). https://doi.org/10.1007/s10863-013-9538-4

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s10863-013-9538-4

Keywords

Search

Navigation