Abstract
Several lipid classes constitute the universal matrix of the biological membranes. With their amphipathic nature, lipids not only build the continuous barrier that confers identity to every cell and organelle, but they are also active actors that modulate the activity of the proteins immersed in the lipid bilayer. The plasma membrane H+-ATPase, an enzyme from plant cells, is an excellent example of a transmembrane protein whose activity is influenced by the hydrophilic compartments at both sides of the membrane and by the hydrophobic domains of the lipid bilayer. As a result, an extensive documentation of the effect of numerous amphiphiles in the enzyme activity can be found. Detergents, membrane glycerolipids, and sterols can produce activation or inhibition of the enzyme activity. In some cases, these effects are associated with the lipids of the membrane bulk, but in others, a direct interaction of the lipid with the protein is involved. This review gives an account of reports related to the action of the membrane lipids on the H+-ATPase activity.
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Abbreviations
- ABA:
-
Abscisic acid
- A. thaliana :
-
Arabidopsis thaliana
- ATP:
-
Adenosine triphosphate
- A. sativa :
-
Avena sativa
- CMC:
-
Critical micelle concentration
- FA:
-
Fatty acid
- FB1 :
-
Fumonisin B1
- GA3:
-
Gibberellic acid 3
- LCB:
-
Long-chain base
- LPC:
-
Lysophosphatidylcholine
- N. tabacum :
-
Nicotiana tabacum
- PA:
-
Phosphatidic acid
- PC:
-
Phosphatidylcholine
- PE:
-
Phosphatidylethanolamine
- PG:
-
Phosphatidylglycerol
- PI:
-
Phosphatidylinositol
- PM H+-ATPase:
-
Plasma membrane H+-ATPase
- Pma1:
-
Yeast plasma membrane H+-ATPase, isoform 1
- PS:
-
Phosphatidylserine
- V. radiata :
-
Vigna radiata
References
Andersson MX, Larsson KE, Tjellström H, Liljenberg C, Sandelius AS (2005) Phosphate-limited oat: the plasma membrane and the tonoplast as major targets for phospholipid-to-glycolipid replacement and stimulation of phospholipases in the plasma membrane. J Biol Chem 280:27578–27586
Arnqvist L, Persson M, Jonsson L, Dutta PC, Sitbon F (2008) Overexpression of CYP710A1 and CYP710A4 in transgenic Arabidopsis plants increases the level of stigmasterol at the expense of sitosterol. Planta 227:309–317
Arora R, Palta JP (1991) A loss in the plasma membrane ATPase activity and its recovery coincides with incipient freeze–thaw injury and post thaw recovery in onion bulb scale tissue. Plant Physiol 95:846–852
Bohn M, Heinz E, Lüthje S (2001) Lipid composition and fluidity of plasma membranes isolated from corn (Zea mays L.) roots. Arch Biochem Biophys 387:35–40
Brauer D, Tu SI (1989) Phospholipid requirement of the vanadate-sensitive ATPase from maize roots evaluated by two methods. Plant Physiol 89:867–874
Briskin DP, Reynolds-Niesman I (1989) Change in target molecular size of the red beet plasma membrane ATPase during solubilization and reconstitution. Plant Physiol 90:394–397
Bultynck L, Geuns J, Van Ginkel G, Caubergs RJ (1997) Properties of plasma membranes of Phsp 70-ipt transformed tobacco (Nicotiana tabacum). Phytochemistry 45:1337–1341
Cacas JL, Furt F, Le Guédard M, Schmitter JM, Buré C, Gerbeau-Pissot P, Moreau P, Bessoule JJ, Simon-Plas F, Mongrand S (2012) Lipids of plant membrane rafts. Prog Lipid Res 51:272–299
Carmona-Salazar L, El Hafidi M, Enríquez-Arredondo C, Vázquez-Vázquez C, González de la Vara LE, Gavilanes-Ruíz M (2011) Isolation of detergent-resistant membranes from plant photosynthetic and non-photosynthetic tissues. Anal Biochem 417:220–227
Carmona-Salazar L, El Hafidi M, Gutiérrez-Nájera N, Noyola-Martínez L, González-Solís A, Gavilanes-Ruíz M (2015) Fatty acid profiles from the plasma membrane and detergent resistant membranes of two plant species. Phytochemistry 109:25–35
Chapman KD, Ohlrogge JB (2012) Compartmentation of triacylglycerol accumulation in plants. J Biol Chem 287:2288–2294
Chen M, Saucedo-García M, Plasencia J, Gavilanes-Ruíz M, Cahoon EB (2009) Plant sphingolipids: structure, synthesis, and function. In: Wada H, Murata N (eds) Lipids in photosynthesis: essential and regulatory functions. Advances in photosynthesis and respiration. Springer, New York, pp 77–116
Coccuci MC, Marré E (1984) Lysophosphatidylcholine-activate, vanadate-inihibited Mg2+-ATPase from radish microsomes. Biochim Biophys Acta 771:42–52
Cooke DT, Munkonge FM, Burden RS, James CS (1991) Fluidity and lipid composition of oat and rye shoot plasma membrane: effect of sterol perturbation by xenobiotics. Biochim Biophys Acta 1061:156–162
Cooke DT, Ros R, Burden RS, James CS (1993) A comparison of the influence of sterols on the specific activity of the H+-ATPases in isolated plasma membrane vesicles from oat, rye and rice shoots. Physiol Plant 88:397–402
Cooke DT, Burden RS, James CS, Seco T, Sierra B (1994) Influence of sterols on plasma membrane proton-pumping ATPase activity and membrane fluidity in oat shoots. Plant Physiol 32:769–773
Cornelius F (1995) Cholesterol modulation of molecular activity of reconstituted shark Na+, K+-ATPase. Biochim Biophys Acta 1235:205–212
De Michelis MI, Papini R, Pugliarello MC (1997) Multiple effects of lysophosphatidylcholine on the activity of the plasma membrane H+-ATPase of radish seedlings. Bot Acta 110:43–48
Douglas TJ (1985) NaCl effects on 4-desmethylsterol composition of plasma-membrane-enriched preparations from citrus roots. Plant Cell Environ 8:687–692
Duby G, Boutry M (2009) The plant plasma membrane proton pump ATPase: a highly regulated P-type ATPase with multiple physiological roles. Eur J Physiol 457:645–655
Fuglsang AT, Borch J, Bych K, Jahn TP, Roepstorff P, Palmgren MG (2003) The binding site for regulatory 14-3-3 protein in plant plasma membrane H+-ATPase. J Biol Chem 278:42266–42272
Furt F, Konig S, Bessoule JJ, Sargueil F, Zallot R, Stanislas T, Noirot E, Lherminier J, Simon-Plas F, Heilmann I, Mongrand S (2010) Polyphosphoinositides are enriched in plant membrane rafts and form microdomains in the plasma membrane. Plant Physiol 152:2173–2187
Gomès E, Venema K, Simon-Plas F, Milat ML, Palmgren MG, Blein JP (1996) Activation of the plant plasma membrane H+-ATPase. Is there a direct interaction between lysophosphatidylcholine and the C-terminal part of the enzyme? FEBS Lett 398:48–52
Grandmougin-Ferjani A, Schuller-Muller I, Hartmann MA (1997) Sterol modulation of the plasma membrane H+-ATPase activity from corn roots reconstituted into soybean lipids. Plant Physiol 113:163–174
Gutiérrez-Nájera N, Muñoz-Clares RA, Palacios-Bahena S, Ramírez J, Sánchez-Nieto S, Plasencia J, Gavilanes-Ruíz M (2005) Fumonisin B1, a sphingoid toxin, is a potent inhibitor of the plasma membrane H+-ATPase. Planta 221:589–596
Harper JF, Surwow PK, Sussman MR (1989) Molecular cloning and sequence of cDNA encoding the plasma membrane proton pump (H+-ATPase) of Arabidopsis thaliana. Proc Natl Acad Sci USA 86:1234–1238
Hartmann MA (2004) Sterol metabolism and functions in higher plants. In: Daum G (ed) Lipid metabolism and membrane biogenesis. Topics in current genetics. Springer, Berlin, pp 183–211
Hartmann MA, Benveniste P (1987) Plant membrane sterols: isolation, identification and biosynthesis. Methods Enzymol 148:632–650
Haruta M, Burch HL, Nelson RB, Barrett-Wilt G, Kline KG, Mohsin SB, Young JC, Otegui MS, Sussman MR (2010) Molecular characterization of mutant Arabidopsis plants with reduced plasma membrane proton pump activity. J Biol Chem 285:17918–17929
Hong H, Tamm LK (2004) Elastic coupling of integral membrane protein stability to lipid bilayer forces. Proc Natl Acad Sci USA 101:4065–4070
Hunter GW, Negash S, Squier TC (1999) Phosphatidylethanolamine modulates Ca-ATPase function and dynamics. Biochemistry 38:1356–1364
Ibarz E, Palmgren MG, Palazón J, Piñol MT, Serrano R (1994) Activation of plant plasma membrane H+-ATPase by the non-ionic detergent Brij 58. Biochim Biophys Acta 1196:93–96
Imai Y, Liu X, Yamagishi J, Mori K, Neya S, Hoshino T (2010) Computational analysis of water residence on ceramide and sphingomyelin bilayer membranes. J Mol Graph Model 29:461–469
Ishikawa M, Yoshida S (1985) Seasonal changes in plasma membranes and mitochondria isolated from Jerusalem artichoke tubers. Possible relationship to cold hardiness. Plant Cell Physiol 26:1331–1344
Janicka-Russak M, Kabała K, Wdowikowska A, Kłobus G (2012) Response of plasma membrane H+-ATPase to low temperature in cucumber roots. J Plant Res 125:291–300
Jelich-Ottmann C, Weiler EW, Oecking C (2001) Binding of regulatory 14-3-3 proteins to the C terminus of the plant plasma membrane H+-ATPase involves part of its autoinhibitory region. J Biol Chem 276:39852–39857
Jian LC, Sun LH, Dong HZ (1982) Adaptive changes in ATPase activity in the cells of winter wheat seedlings during cold hardening. Plant Physiol 70:127–131
Johansson F, Sommarin M, Larsson C (1994) Rapid purification of the plasma membrane H+-ATPase in its non-activated form using FPLC. Physiol Plant 92:389–396
Johansson F, Olbe M, Sommarin M, Larsson C (1995) Brij58, a polyoxyethylene acyl ether, creates membrane vesicles of uniform sideness. A new tool to obtain inside-out (cytoplasmic side-out) plasma membrane vesicles. Plant J 7:165–173
Justesen BH, Hansen RW, Martens HJ, Theorin L, Palmgren MG, Martinez KL, Pomorski TH, Fulgsang AT (2013) Active plasma membrane P-type H+-ATPase reconstituted into nanodiscs is a monomer. J Biol Chem 288:26419–26429
Kanczewska J, Marco S, Vandermeeren C, Maudoux O, Rigaud JL, Boutry M (2005) Activation of the plant plasma membrane H+-ATPase by phosphorylation and binding of 14-3-3 proteins converts a dimer into a hexamer. Proc Natl Acad Sci USA 102:11675–11680
Kasamo K (1990) Mechanism for activation of plasma membrane H+-ATPase from rice (Oryza sativa L.) culture cells by molecular species of a phospholipid. Plant Physiol 93:1049–1052
Kasamo K (2003) Regulation of plasma membrane H+-ATPase activity by the membrane environment. J Plant Res 116:517–523
Kasamo K, Nouchi I (1987) The role of phospholipids in plasma membrane ATPase activity in Vigna radiate L. (Mung bean) roots and hypocotyls. Plant Physiol 83:323–328
Kasamo K, Yamanishi H (1991) Functional reconstitution of plasma membrane H+-ATPase from mung bean (Vigna radiate L.) hypocotyls in liposomes prepared with various molecular species of phospholipids. Plant Cell Physiol 32:1219–1225
Kerkeb L, Donaire JP, Venema K, Rodríguez-Rosales MP (2001) Tolerance to NaCl induces changes in plasma membrane lipid composition, fluidity and H+-ATPase activity of tomato calli. Physiol Plant 113:217–224
Kim HS, Oh JM, Luan S, Carlson JE, Ahn SJ (2013) Cold stress causes rapid but differential changes in properties of plasma membrane H+-ATPase of camelina and rapeseed. J Plant Physiol 170:828–837
Laganowsky A, Reading E, Allison TM, Ulmschneider MB, Degiacomi MT, Baldwin AJ, Robinson CV (2014) Membrane proteins bind lipids selectively to modulate their structure and function. Nature 510:172–175
Lee AG (2003) Lipid–protein interactions in biological membranes: a structural perspective. Biomembranes 1612:1–40
Lee AG (2011) Biological membranes: the importance of molecular detail. Trends Biochem Sci 36:493–500
Lee MC, Hamamoto S, Schekman R (2002) Ceramide biosynthesis is required for the formation of the oligomeric H+-ATPase Pma1p in the yeast endoplasmic reticulum. J Biol Chem 277:22395–22401
Liang Y, Zhang W, Chen Q, Liu Y, Ding R (2006) Effect of exogenous silicon (Si) on H+ ATPase activity, phospholipids and fluidity of plasma membrane in leaves of salt-stressed barley (Hordeum vulgare L.). Environ Exp Bot 57:212–219
López-Pérez L, Martínez-Ballesta MC, Maurel C, Carvajal M (2009) Changes in plasma membrane lipids, aquaporins and proton pump of broccoli roots, as an adaptation mechanism to salinity. Phytochemistry 70:492–500
Lynch DV, Steponkus PL (1987) Plasma membrane lipid alterations associated with cold acclimation of winter rye seedlings (Secale cereale L. cv Puma). Plant Physiol 83:761–767
MacCallum JL, Tieleman DP (2011) Hydrophobicity scales: a thermodynamic looking glass into lipid–protein interactions. Trends Biochem Sci 36:653–662
Mansour MMF, van Hasselt PR, Kuiper PJC (1994) Plasma membrane lipid alterations induced by NaCl in winter wheat roots. Physiol Plant 92:473–478
Markham JE, Jaworski JG (2007) Rapid measurement of sphingolipids from Arabidopsis thaliana by reversed-phase high-performance liquid chromatography coupled to electrospray ionization tandem mass spectrometry. Rapid Commun Mass Spectrom 21:1304–1314
Martínez-Cortina C, Ros R, Cooke DT, James CS, Sanz A (1992) The lipid composition, fluidity, and Mg2+-ATPase activity of rice (Oryza sativa L. cv. Bahia) shoot plasma membranes: effects of ABA and GA3. J Plant Growth Regul 11:195–201
Martinière A, Shvedunova M, Thomson AJW, Evans NH, Penfield S, Runions J, McWatters HG (2011) Homeostasis of plasma membrane viscosity in fluctuating temperatures. New Phytol 192:328–337
Martz F, Sutinen ML, Kiviniemi S, Palta JP (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
Memon AR, Chen Q, Boss WF (1989) Inositol phospholipids activate plasma membrane ATPase in plants. Biochem Biophys Res Commun 162:1295–1301
Minami A, Fujiwara M, Furuto A, Fukao Y, Yamashita T, Kamo M, Kawamura Y, Uemura M (2009) Alterations in detergent-resistant plasma membrane microdomains in Arabidopsis thaliana during cold acclimation. Plant Cell Physiol 50:341–359
Mongrand S, Morel J, Laroche J, Claverol S, Carde JP, Hartmann MA, Bonneu M, Simon-Plas F, Lessire R, Bessoule JJ (2004) Lipid rafts in higher plant cells purification and characterization of triton X-100-insoluble microdomains from tobacco plasma membrane. J Biol Chem 279:36277–36286
Mongrand S, Stanislas T, Bayer EM, Lherminier J, Simon-Plas F (2010) Membrane rafts in plant cells. Trends Plant Sci 15:656–663
Monk BC, Montesinos C, Leonard K, Serrano R (1989) Sidedness of yeast plasma membrane vesicles and mechanisms of activation of the ATPase by detergents. Biochim Biophys Acta 981:226–234
Mouritsen OG (2005) Life as a matter of fat the emerging science of lipidomics. Springer, Berlin
Norberg P, Liljenberg C (1991) Lipids of plasma membranes prepared from oat root cells: effects of induced water-deficit tolerance. Plant Physiol 96:1136–1141
Oh JM, Kim HS, Bae HJ, Ahn SJ (2014) Jatropha is vulnerable to cold injury due to impaired activity and expression of plasma membrane H+-ATPase. Acta Physiol Plant 36:231–241
Okazaki Y, Saito K (2014) Roles of lipids as signaling molecules and mitigators during stress response in plants. Plant J 79:584–596
Olsson A, Johansson F, Sommarin M, Larsson C (1995) Multiple regulatory sites in the C-terminal autoinhibitory domain of the plasma membrane H+-ATPase. Plant J 8:959–962
Örvar BL, Sangwan V, Omann F, Dhindsa RS (2000) Early steps in cold sensing by plant cells: the role of actin cytoskeleton and membrane fluidity. Plant J 23:785–794
Ottmann C, Marco S, Jaspert N, Marcon C, Schauer N, Weyand M, Vandermeeren C, Duby G, Boutry M, Wittinghofer A, Rigaud JL, Oecking C (2007) Structure of a 14-3-3 coordinated hexamer of the plant plasma membrane H+-ATPase by combining X-ray crystallography and electron cryomicroscopy. Mol Cell 25:427–440
Palmgren MG, Sommarin M (1989) Lysophosphatidylcholine stimulates ATP-dependent proton accumulation in isolated oat root plasma membrane vesicles. Plant Physiol 90:1009–1014
Palmgren MG, Sommarin M, Ulvskov P, Jørgensen PL (1988) Modulation of plasma membrane H+-ATPase from oat roots by lysophosphatidylcholine, free acids and phospholipase A2. Physiol Plant 74:11–19
Palmgren MG, Askerlund P, Fredrikson K, Widell S, Sommarin M, Larsson C (1990a) Sealed inside-out and right-side-out plasma membrane vesicles. Optimal conditions for formation and separation. Plant Physiol 92:871–880
Palmgren MG, Larsson C, Sommarin M (1990b) Proteolytic activation of the plant plasma membrane H+-ATPase by removal of a terminal segment. J Biol Chem 265:13423–13426
Palmgren MG, Sommarin M, Ulvskov P, Larsson C (1990c) Effect of detergents on the H+-ATPase activity of inside-out and right-side-out plant plasma membrane vesicles. Biochim Biophys Acta 1021:133–140
Palmgren MG, Sommarin M, Serrano R, Larsson C (1991) Identification of an autoinhibitory domain in the C-terminal region of the plant plasma membrane H+-ATPase. J Biol Chem 266:20470–20475
Palta JP, Li PH (1980) Alterations in membrane transport properties by freezing injury in herbaceous plants. Evidence against rupture theory. Physiol Plant 50:169–175
Palta JP, Whitaker BD, Weiss LS (1993) Plasma membrane lipids associated with genetic variability in freezing tolerance and cold acclimation of Solanum species. Plant Physiol 103:793–803
Pedchenko VK, Nasirova GF, Palladina TA (1990) Lysophosphatidylcholine specifically stimulates plasma membrane H+-ATPase from corn roots. FEBS Lett 275:205–208
Pedersen BP, Buch-Pedersen MJ, Morth JP, Palmgren MG, Nissen P (2007) Crystal structure of the plasma membrane proton pump. Nature 450:1111–1114
Phillips R, Ursell T, Wiggins P, Sens P (2009) Emerging roles for lipids in shaping membrane–protein function. Nature 459:379–385
Quartacci MF, Glisic O, Stevanovic B, Navari-Izzo F (2002) Plasma membrane lipids in the resurrection plant Ramonda serbica following dehydration and rehydration. J Exp Bot 53:2159–2166
Rodríguez-Rosales MP, Kerkeb L, Bueno P, Donaire JP (1999) Changes induced by NaCl in lipid content and composition, lipoxygenase, plasma membrane H+-ATPase and antioxidant enzyme activities of tomato (Lycopersicon esculentum Mill) calli. Plant Sci 143:143–150
Ros R, Cooke DT, Burden RS, James CS (1990) Effects of the herbicide MCPA, and the heavy metals, cadmium and nickel on the lipid composition, Mg2+-ATPase activity and fluidity of plasma membranes from rice, Oryza sativa (cv. Bahia) shoots. J Exp Bot 41:457–462
Ros R, Cooke DT, Martinez-Cortina C, Picazo I (1992) Nickel and Cadmium-related changes in growth, plasma membrane lipid composition, ATPase hydrolytic activity and proton-pumping of rice (Oryza sativa L. cv Bahía) shoots. J Exp Bot 256:1475–1481
Rossard S, Roblin G, Atanassova R (2010) Ergosterol triggers characteristic elicitation steps in Beta vulgaris leaf tissues. J Exp Bot 61:1807–1816
Sandermann H (1978) Regulation of membrane enzymes by lipids. Biochim Biophys Acta 515:209–237
Sandstrom RP, Cleland RE (1989) Selective delipidation of the plasma membrane by surfactants. Enrichment of sterols and activation of ATPase. Plant Physiol 90:1524–1531
Sandstrom RP, Deboer AH, Lomax TL, Cleland RE (1987) Latency of plasma membrane H+-ATPase in vesicles isolated by aqueous phase partitioning. Plant Physiol 85:693–698
Saucedo-García M, Guevara-García A, González-Solís A, Cruz-García F, Vázquez-Santana S, Markham JE, Lozano-Rosas G, Dietrich CR, Ramos-Vega M, Cahoon EB, Gavilanes-Ruíz M (2011) MPK6, sphinganine and the LCB2a gene from serine palmitoyltransferase are required in the signaling pathway that mediates cell death induced by long chain bases in Arabidopsis. New Phytol 191:943–957
Serrano R, Montesinos C, Sánchez J (1988) Lipid requirements of the plasma membrane ATPase from oat roots and yeast. Plant Sci 56:117–122
Shi Y, An L, Zhang M, Huang C, Zhang H, Xu S (2008) Regulation of the plasma membrane during exposure to low temperatures in suspension-cultured cells from a cryophyte (Chorispora bungeana). Protoplasma 232:173–181
Shinitzky M (1984) Membrane fluidity and cellular functions. In: Shinitzy M (ed) Physiology of membrane fluidity. CRC Press, Boca Raton, pp 1–51
Smith AW (2012) Lipid–protein interactions in biological membranes: a dynamic perspective. Biomembranes 1818:172–177
Sondergaard TE, Schulz A, Palmgren MG (2004) Energization of transport processes in plants. Roles of the plasma membrane H+-ATPase. Plant Physiol 136:2475–2482
Starling AP, East JM, Lee AG (1995) Effects of phospholipid fatty acyl chain length on phosphorylation and dephosphorylation of the Ca2+-ATPase. Biochem J 310:875–879
Uemura M, Steponkus PL (1994) A comparison of freezing injury in oat and rye: two cereals at the extremes of freezing tolerance. Plant Physiol 104:479–496
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
Van Meer G, Voelker DR, Feigenson GW (2008) Membrane lipids: where they are and how they behave. Nat Rev Mol Cell Biol 9:112–124
Vara F, Serrano R (1982) Partial purification and properties of the proton-translocating ATPase of plant plasma membranes. J Biol Chem 257:12826–12830
Von Heijne G (2006) Membrane-protein topology. Nat Rev Mol Cell Biol 7:909–918
Wang Q, Chang A (2002) Sphingoid base synthesis is required for oligomerization and cell surface stability of the yeast plasma membrane ATPase, Pma1. Proc Natl Acad Sci 99:12853–12858
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
White PJ, Earnshaw MJ, Cooke DT, Clarkson DT, Burden RS (1990) Does plant growth temperature modulate the membrane composition and ATPase activities of tonoplast and plasma-membrane fractions from rye roots? Phytochemistry 29:3385–3393
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 92:852–858
Yamamoto E, Akimoto T, Yasui M, Yasuoka K (2014) Origin of subdiffusion of water molecules on cell membrane surfaces. Sci Rep 4:1–7
Yoshida S, Uemura M (1986) Lipid composition of plasma membrane and tonoplasts isolated from etiolated seedlings of mung bean. Plant Physiol 82:807–812
Zhang JH, Liu YP, Pan QH, Zhan JC, Wang XQ, Huang WD (2006) Changes in membrane-associated H+-ATPase activities and amounts in young grape plants during the cross adaptation to temperature stresses. Plant Sci 70:768–777
Zhou Q, Zhang C, Cheng S, Wei B, Liu X, Ji S (2014) Changes in energy metabolism accompanying pitting in blueberries stored at low temperature. Food Chem 164:493–501
Acknowledgments
The authors are indebted to Ana Sofía Flores-Sierra for assistance in proofreading the manuscript and Diego González-Halphen for its critical reviewing. Experimental work from author´s articles was conducted with the technical help of Consuelo Enríquez-Arredondo and Laurel Fabila-Ibarra. This work was supported by Dirección General del Personal Académico, Universidad Nacional Autónoma de México (PAPIIT IN210812), from Consejo Nacional de Ciencia y Tecnología (101521) and Facultad de Química, UNAM (PAIP 50009115).
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Morales-Cedillo, F., González-Solís, A., Gutiérrez-Angoa, L. et al. Plant lipid environment and membrane enzymes: the case of the plasma membrane H+-ATPase. Plant Cell Rep 34, 617–629 (2015). https://doi.org/10.1007/s00299-014-1735-z
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DOI: https://doi.org/10.1007/s00299-014-1735-z