Detergent-resistant microdomains (lipid rafts) in endomembranes of the wild halophytes
Olga Rozentsvet A , Irina Nesterkina B , Natalia Ozolina B and Viktor Nesterov
A C
+ Author Affiliations
- Author Affiliations
A Institute of Ecology of the Volga Basin Russian Academy of Science, 10, Komzin Str, Togliatti 445003, Russia.
B Siberian Institute of Plant Physiology and Biochemistry, Siberian Branch, Russian Academy of Sciences, 132, Lermontov Str, Irkutsk 664033, Russia.
C Corresponding author. Email: nesvik1@mail.ru
Functional Plant Biology 46(9) 869-876 https://doi.org/10.1071/FP18263
Submitted: 16 October 2018 Accepted: 14 May 2019 Published: 14 June 2019
Abstract
In the present work, we studied detergent-resistant membrane microdomains (DRM) of chloroplasts and mitochondria – organelles that provide photosynthesis and respiration in a plant cell. The objects of the study were euhalophyte Salicorniaperennans Willd., which relates to salt-accumulating plants and glycohalophyte Artemisia santonica L., which relates to salt-excluder plants. To get DRM, the chloroplast and mitochondria fractions were solubilised with a solution containing Triton X-100. The resulting material was introduced in sucrose gradient of 35–25–15–5% and centrifuged at 200 000 g, 2 h. The presence of an opalescent detergent-resistant zone of membranes in 15% sucrose layer and a specific lipid composition of this zone were the signs of successful rafts obtaining of. The isolated DRM are sterol- and cerebroside-enriched (27–89% of the sum of membrane lipids) domains with a high degree of saturation of fatty acids composition (more than 50% of the sum). The main DRM-specific lipids of chloroplast of A. santonica glycohalophyte are cerebrosides, whereas those of S. perennans euhalophyte are sterols. The revealed differences in the composition of raft-forming lipids in chloroplast and mitochondria halophyte membranes, differing in the salt-resistance strategy, suggest the participation of rafts in salt-resistance mechanisms.
Additional keywords: chloroplast and mitochondria, detergent-resistant microdomains, lipid rafts, lipids, euhalophyte, glycohalophyte, salt-resistance strategies.
References
Allakhverdiev SI, Sakamoto A, Nishiyama Y, Inaba N, Murata N (2000) Ionic and osmotic effects of NaCl-induced inactivation of photosystems I and II in Synechococcus sp. Plant Physiology 123, 1047–1056.| Ionic and osmotic effects of NaCl-induced inactivation of photosystems I and II in Synechococcus sp.Crossref | GoogleScholarGoogle Scholar | 10889254PubMed |
Allakhverdiev SI, Nishiyama Y, Miyairi S, Yamamoto H, Inagaki N, Kanesaki Y, Murata N (2002) Salt stress inhibits the repair of photodamaged photosystem II by suppressing the transcription and translation of psbA genes in Synechocystis. Plant Physiology 130, 1443–1453.
| Salt stress inhibits the repair of photodamaged photosystem II by suppressing the transcription and translation of psbA genes in Synechocystis.Crossref | GoogleScholarGoogle Scholar | 12428009PubMed |
Alscher RG, Erturk N, Heath LS (2002) Role of superoxide dismutases (SODs) in controlling oxidative stress in plants. Journal of Experimental Botany 53, 1331–1341.
| Role of superoxide dismutases (SODs) in controlling oxidative stress in plants.Crossref | GoogleScholarGoogle Scholar | 11997379PubMed |
Bargmann BO, Laxalt A, Riet B, Schooten B, Merquiol E, Testerink C, Haring M, Bartels D, Munnik T (2009) Multiple PLDs required for high salinity tolerance and water deficit tolerance in plants. Plant & Cell Physiology 50, 78–89.
| Multiple PLDs required for high salinity tolerance and water deficit tolerance in plants.Crossref | GoogleScholarGoogle Scholar |
Bligh EG, Dyer WJ (1959) A rapid method of total lipid extraction and purification. Canadian Journal of Biochemistry and Physiology 37, 911–917.
| A rapid method of total lipid extraction and purification.Crossref | GoogleScholarGoogle Scholar | 13671378PubMed |
Bouvier-Navé P, Benveniste P (1995) Sterol acyl transferase and steryl ester hydrolase activities in a tobacco mutant which overproduces sterols. Plant Science 110, 11–19.
| Sterol acyl transferase and steryl ester hydrolase activities in a tobacco mutant which overproduces sterols.Crossref | GoogleScholarGoogle Scholar |
Carraretto L, Teardo E, Checchetto V, Finazzi G, Uozumi N, Szabo I (2016) Ion channels in plant bioenergetic organelles chloroplast and mitochondria: from molecular identification to function. Molecular Plant 9, 371–395.
| Ion channels in plant bioenergetic organelles chloroplast and mitochondria: from molecular identification to function.Crossref | GoogleScholarGoogle Scholar | 26751960PubMed |
Cosentino C (2008) Na+/H+ transporters of the halophyte Mesembryanthemum crystallinum L. PhD thesis. Vom Fachbereich Biologie der Technischen Universitat Darmstadt, Darmstadt, Germany.
Flowers TJ, Colmer TD (2008) Salinity tolerance in halophytes. New Phytologist 179, 945–963.
| Salinity tolerance in halophytes.Crossref | GoogleScholarGoogle Scholar | 18565144PubMed |
Gennis RB (1989) ‘Biomembranes. Molecular structure and function.’ (Springer-Verlag: New York)
Harder T, Scheiffele P, Verkade P, Simons K (1998) Lipid-domain structure of the plasma membrane revealed by patching of membrane components. Journal of Cell Biology 141, 929–942.
| Lipid-domain structure of the plasma membrane revealed by patching of membrane components.Crossref | GoogleScholarGoogle Scholar | 9585412PubMed |
Hartmann MA (1998) Plant sterols and the membrane environment. Trends in Plant Science 3, 170–175.
| Plant sterols and the membrane environment.Crossref | GoogleScholarGoogle Scholar |
Hernández-Pinzón I, Ross JH, Barnes KA, Damant AP, Murphy DJ (1999) Composition and role of tapetal lipid bodies in the biogenesis of the pollen coat of Brassica napus. Planta 208, 588–598.
| Composition and role of tapetal lipid bodies in the biogenesis of the pollen coat of Brassica napus.Crossref | GoogleScholarGoogle Scholar | 10420651PubMed |
Horvath SE, Daum G (2013) Lipids of mitochondria. Progress in Lipid Research 52, 590–614.
| Lipids of mitochondria.Crossref | GoogleScholarGoogle Scholar | 24007978PubMed |
Jha D, Shirley N, Tester M, Roy SJ (2010) Variation in salinity tolerance and shoot sodium accumulation in Arabidopsis ecotypes linked to differences in the natural expression levels of transporters involved in sodium transport. Plant, Cell & Environment 33, 793–804.
Jouhet J, Marechal E, Baldan B, Bligny R, Joyard J, Block M (2004) Phosphate deprivation induces transfer of DGDG galactolipid from chloroplast to mitochondria. Journal of Cell Biology 167, 863–874.
| Phosphate deprivation induces transfer of DGDG galactolipid from chloroplast to mitochondria.Crossref | GoogleScholarGoogle Scholar | 15569715PubMed |
Kobayashi IK, Endo K, Wada H (2016) Roles of lipids in photosynthesis. In ‘Lipids in plant and algae development’. (Eds Y Nakamura, Y Li-Beisson) pp. 21–49. (Springer International Publishing: Cham, Switzerland)
Laloi M, Perret A-N, Chatre L, Melser S, Cantrel C, Vaultier M-N, Zachowski A, Bathany K, Schmitter J-M, Vallet M, Lessire R, Hartmann M-A, 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 Physiology 143, 461–472.
| Insights into the role of specific lipids in the formation and delivery of lipid microdomains to the plasma membrane of plant cells.Crossref | GoogleScholarGoogle Scholar | 17114270PubMed |
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 Physiology 144, 402–418.
| Characterization of lipid rafts from Medicago truncatula root plasma membranes: a proteomic study reveals the presence of a raft-associated redox system.Crossref | GoogleScholarGoogle Scholar | 17337521PubMed |
Lokhande VH, Suprasanna P (2012) Prospects of halophytes in understanding and managing abiotic stress tolerance. In ‘Environmental adaptations and stress tolerance of plants in the era of climate change’. (Eds P Ahmad, MNV Prasad) pp. 29–56. (Springer Science + Business Media: Berlin)
López-Pérez L, Martínez-Ballesta MC, Maurel C, Carvajal M (2009) Changes in plasma membrane lipids, aquaporins, and proton pumps of broccoli roots as an adaptation mechanism to salinity. Phytochemistry 70, 492–500.
| Changes in plasma membrane lipids, aquaporins, and proton pumps of broccoli roots as an adaptation mechanism to salinity.Crossref | GoogleScholarGoogle Scholar | 19264331PubMed |
Los DA (2014) ‘Fatty acid desaturases.’ (Scientific World: Moscow) [In Russian]
Martin SW, Konopka JB (2004) Lipid raft polarization contributes to hyphal growth in Candida albicans. Eukaryotic Cell 3, 675–684.
| Lipid raft polarization contributes to hyphal growth in Candida albicans.Crossref | GoogleScholarGoogle Scholar | 15189988PubMed |
Mellgren RL (2008) Detergent-resistant membrane subfractions containing proteins of plasma membrane, mitochondrial, and internal membrane origins. Journal of Biochemical and Biophysical Methods 70, 1029–1036.
| Detergent-resistant membrane subfractions containing proteins of plasma membrane, mitochondrial, and internal membrane origins.Crossref | GoogleScholarGoogle Scholar | 17870178PubMed |
Mongrand S, Morel J, Laroche J, Claverol S, Carde J, Hartmann M, Bonneu M, Simon-Plas F, Lessire R, Bessoule J (2004) Lipid rafts in higher plant cells: purification and characterization of Triton X-100-insoluble microdomains from tobacco plasma membrane. Journal of Biological Chemistry 279, 36277–36286.
| Lipid rafts in higher plant cells: purification and characterization of Triton X-100-insoluble microdomains from tobacco plasma membrane.Crossref | GoogleScholarGoogle Scholar | 15190066PubMed |
Mongrand S, Stanislas T, Bayer EM, Lherminier J, Simon-Plas F (2010) Membrane rafts in plant cells. Trends in Plant Science 15, 656–663.
| Membrane rafts in plant cells.Crossref | GoogleScholarGoogle Scholar | 20934367PubMed |
Moreau P, Bessoule JJ, Mongrand S, Testet E, Vincent P, Cassagne C (1998) Lipid trafficking in plant cells. Progress in Lipid Research 37, 371–391.
| Lipid trafficking in plant cells.Crossref | GoogleScholarGoogle Scholar | 10209654PubMed |
Nakamura Y, Li-Beisson Y (2016) ‘Lipids in plant and algae development.’ (Springer Science+Business Media: Berlin)
Nesterov VN, Nesterkina IS, Rozentsvet OA, Ozolina NV, Salyaev RK (2017) Detection of lipid–protein microdomains (rafts) and investigation of their functional role in the chloroplast membranes of halophytes. Doklady. Biochemistry and Biophysics 476, 303–305.
| Detection of lipid–protein microdomains (rafts) and investigation of their functional role in the chloroplast membranes of halophytes.Crossref | GoogleScholarGoogle Scholar | 29101751PubMed |
Noctor G, de Paepe R, Foyer CH (2007) Mitochondrial redox biology and homeostasis in plants. Trends in Plant Science 12, 125–134.
| Mitochondrial redox biology and homeostasis in plants.Crossref | GoogleScholarGoogle Scholar | 17293156PubMed |
Ozolina NV, Nesterkina IS, Kolesnikova EV, Salyaev RK, Nurminsky VN, Rakevich AL, Martynovich EF, Chernyshov MY (2013) Tonoplast of Beta vulgaris L. contains detergent-resistant membrane microdomains. Planta 237, 859–871.
| Tonoplast of Beta vulgaris L. contains detergent-resistant membrane microdomains.Crossref | GoogleScholarGoogle Scholar | 23143221PubMed |
Pike LJ (2006) Rafts defined: a report on the keystone symposium on lipid rafts and cell function. Journal of Lipid Research 47, 1597–1598.
| Rafts defined: a report on the keystone symposium on lipid rafts and cell function.Crossref | GoogleScholarGoogle Scholar | 16645198PubMed |
Rengasamy P (2006) World salinization with emphasis on Australia. Journal of Experimental Botany 57, 1017–1023.
| World salinization with emphasis on Australia.Crossref | GoogleScholarGoogle Scholar | 16510516PubMed |
Rozentsvet OA, Nesterov VN, Sinyutina NF (2012) The effect of copper ions on the lipid composition of subcellular membranes in Hydrilla verticillata. Chemosphere 89, 108–113.
| The effect of copper ions on the lipid composition of subcellular membranes in Hydrilla verticillata.Crossref | GoogleScholarGoogle Scholar | 22608709PubMed |
Rozentsvet OA, Nesterov VN, Bogdanova ES (2017) Structural, physiological, and biochemical aspects of salinity tolerance of halophytes. Russian Journal of Plant Physiology: a Comprehensive Russian Journal on Modern Phytophysiology 64, 464–477.
| Structural, physiological, and biochemical aspects of salinity tolerance of halophytes.Crossref | GoogleScholarGoogle Scholar |
Rozentsvet O, Nesterov V, Bogdanova E, Kosobryukhov A, Subova S, Semenova G (2018) Structural and molecular strategy of photosynthetic apparatus organization of wild flora halophytes. Plant Physiology and Biochemistry 129, 213–220.
| Structural and molecular strategy of photosynthetic apparatus organization of wild flora halophytes.Crossref | GoogleScholarGoogle Scholar | 29894861PubMed |
Sakurai I, Shen J-R, Leng J, Ohashi S, Kobayashi M, Wada H (2006) Lipids in oxygen-evolving photosystem II complexes of cyanobacteria and higher plants. Journal of Biochemistry 140, 201–209.
| Lipids in oxygen-evolving photosystem II complexes of cyanobacteria and higher plants.Crossref | GoogleScholarGoogle Scholar | 16822813PubMed |
Shabala S, Mackay A (2011) Ion transport in halophytes. Advances in Botanical Research 57, 151–199.
| Ion transport in halophytes.Crossref | GoogleScholarGoogle Scholar |
Shabala S, Jayakumar B, Hedric R (2014) Salt bladders: do they matter? Trends in Plant Science 19, 687–691.
| Salt bladders: do they matter?Crossref | GoogleScholarGoogle Scholar | 25361704PubMed |
Simons K, Ikonen E (1997) Functional rafts in cell membranes. Nature 387, 569–572.
| Functional rafts in cell membranes.Crossref | GoogleScholarGoogle Scholar | 9177342PubMed |
Simons K, Sampaio JL (2011) Membrane organization and lipid rafts. Cold Spring Harbor Perspectives in Biology 3, a004697
| Membrane organization and lipid rafts.Crossref | GoogleScholarGoogle Scholar | 21628426PubMed |
Tapken W, Murphy AS (2015) Membrane nanodomains in plants: capturing form, function, and movement. Journal of Experimental Botany 66, 1573–1586.
| Membrane nanodomains in plants: capturing form, function, and movement.Crossref | GoogleScholarGoogle Scholar | 25725094PubMed |
Valitova JN, Sulkarnayeva AG, Minibayeva FV (2016) Plant sterols: diversity, biosynthesis, and physiological function. Biochemistry 81, 819–834.
| Plant sterols: diversity, biosynthesis, and physiological function.Crossref | GoogleScholarGoogle Scholar | 27677551PubMed |
Wang Z, Benning C (2012) Chloroplast lipid synthesis and lipid trafficking through ER-plastid membrane contact sites. Biochemical Society Transactions 40, 457–463.
| Chloroplast lipid synthesis and lipid trafficking through ER-plastid membrane contact sites.Crossref | GoogleScholarGoogle Scholar | 22435830PubMed |
Wang B, Luttge U, Ratajczak R (2004) Specific regulation of SOD isoforms by NaCl and osmotic stress in leaves of the C3 halophyte Suaeda salsa L. Journal of Plant Physiology 161, 285–293.
| Specific regulation of SOD isoforms by NaCl and osmotic stress in leaves of the C3 halophyte Suaeda salsa L.Crossref | GoogleScholarGoogle Scholar | 15077627PubMed |
Wang X, Shen Z, Miao X (2016) Nitrogen and hydrophosphate affects glycolipids composition in microalgae. Scientific Reports 6, 30145
| Nitrogen and hydrophosphate affects glycolipids composition in microalgae.Crossref | GoogleScholarGoogle Scholar | 27440670PubMed |
Zamani S, Bybordi A, Khorshidi S, Nezami T (2010) Effects of NaCl salinity levels on lipids and proteins of canola (Brassica napus L.) cultivars. Advances in Environmental Biology 4, 397–403.
