Freezing Tolerance of Plant Cells: From the Aspect of Plasma Membrane and Microdomain

  • Daisuke Takahashi
  • Matsuo Uemura
  • Yukio KawamuraEmail author
Part of the Advances in Experimental Medicine and Biology book series (AEMB, volume 1081)


Freezing stress is accompanied by a state change from water to ice and has multiple facets causing dehydration; consequently, hyperosmotic and mechanical stresses coupled with unfavorable chilling stress act in a parallel way. Freezing tolerance varies widely among plant species, and, for example, most temperate plants can overcome deleterious effects caused by freezing temperatures in winter. Destabilization and dysfunction of the plasma membrane are tightly linked to freezing injury of plant cells. Plant freezing tolerance increases upon exposure to nonfreezing low temperatures (cold acclimation). Recent studies have unveiled pleiotropic responses of plasma membrane lipids and proteins to cold acclimation. In addition, advanced techniques have given new insights into plasma membrane structural non-homogeneity, namely, microdomains. This chapter describes physiological implications of plasma membrane responses enhancing freezing tolerance during cold acclimation, with a focus on microdomains.


Plant Cold acclimation Plasma membrane Microdomain Freezing tolerance Proteome 



Acyl-coenzyme A-binding protein


Acylated sterylglycoside


Blue-copper-binding protein


Bax inhibitor


Brassinosteroid insensitive


C-repeat-binding factor


Calcium-dependent protein kinase


Cryo-scanning electron microscopy


Detergent-resistant membrane


Dynamin-related protein


Fasciclin-like arabinogalactan protein




Free sterol


O-glycosyl hydrolase family 17


Glycosyl inositol phosphoryl ceramide


Glycerophosphoryl diester phosphodiesterase-like protein




Hexagonal II


Hypersensitive-induced reaction


Long-chain base


LCB kinase


Lipid transfer protein


Plasmodesmata callose-binding protein




Phospholipase D


Posttranslational modification




Sterol glycosyltransferase


Slow anion channel 1 homolog


Sphingolipid Δ8 LCB desaturase


Syntaxin of plants





This study was, in part, supported by JSPS KAKENHI Grant numbers JP27328 (to D.T.), JP25292205 (to Y.K.), and JP22120003 and JP24370018 (to M.U.) and Humboldt Research Fellowship from the Alexander von Humboldt Foundation to D.T.


  1. Amid A, Lytovchenko A, Fernie AR, Warren G, Thorlby GJ (2012) The sensitive to freezing3 mutation of Arabidopsis thaliana is a cold-sensitive allele of homomeric acetyl-CoA carboxylase that results in cold-induced cuticle deficiencies. J Exp Bot 63:5289–5299PubMedPubMedCentralCrossRefGoogle Scholar
  2. Ashraf M, Foolad MR (2007) Roles of glycine betaine and proline in improving plant abiotic stress resistance. Environ Exp Bot 59:206–216CrossRefGoogle Scholar
  3. Baldwin L, Domon J-M, Klimek JF, Fournet F, Sellier H, Gillet F, Pelloux J, Lejeune-Hénaut I, Carpita NC, Rayon C (2014) Structural alteration of cell wall pectins accompanies pea development in response to cold. Phytochemistry 104:37–47PubMedCrossRefGoogle Scholar
  4. Bhat RA, Miklis M, Schmelzer E, Schulze-Lefert P, Panstruga R (2005) Recruitment and interaction dynamics of plant penetration resistance components in a plasma membrane microdomain. Proc Natl Acad Sci U S A 102:3135–3140PubMedPubMedCentralCrossRefGoogle Scholar
  5. Borner GHH, Sherrier DJ, Weimar T, Mchaelson LV, Hawkins ND, MacAskill A, Napier JA, Beale MH, Lilley KS, Dupree P (2005) Analysis of detergent-resistant membranes in Arabidopsis: evidence for plasma membrane lipid rafts. Plant Physiol 137:104–116PubMedPubMedCentralCrossRefGoogle Scholar
  6. Bozkurt TO, Richardson A, Dagdas YF, Mongrand S, Kamoun S, Raffaele S (2014) The plant membrane-associated REMORIN1.3 accumulates in discrete perihaustorial domains and enhances susceptibility to Phytophthora infestans. Plant Physiol 165:1005–1018PubMedPubMedCentralCrossRefGoogle Scholar
  7. Buré C, Cacas J-L, Mongrand S, Schmitter J-M (2014) Characterization of glycosyl inositol phosphoryl ceramides from plants and fungi by mass spectrometry. Anal Bioanal Chem 406:995–1010PubMedCrossRefGoogle Scholar
  8. Charron J-BF, Breton G, Badawi M, Sarhan F (2002) Molecular and structural analyses of a novel temperature stress-induced lipocalin from wheat and Arabidopsis. FEBS Lett 517:129–132CrossRefGoogle Scholar
  9. Chen Q-F, Xiao S, Chye M-L (2008) Overexpression of the Arabidopsis 10-kilodalton acyl-coenzyme A-binding protein ACBP6 enhances freezing tolerance. Plant Physiol 148:304–315PubMedPubMedCentralCrossRefGoogle Scholar
  10. Chen M, Markham JE, Cahoon EB (2012) Sphingolipid Δ8 unsaturation is important for glucosylceramide biosynthesis and low-temperature performance in Arabidopsis. Plant J 69:769–781PubMedCrossRefGoogle Scholar
  11. Danyluk J, Perron A, Houde M, Limin A, Fowler B, Benhamou N, Sarhan F (1998) Accumulation of an acidic dehydrin in the vicinity of the plasma membrane during cold acclimation of wheat. Plant Cell 10:623–638PubMedPubMedCentralCrossRefGoogle Scholar
  12. DeBono A, Yeats TH, Rose JKC, Bird D, Jetter R, Kunst L, Samuels L (2009) Arabidopsis LTPG is a glycosylphosphatidylinositol-anchored lipid transfer protein required for export of lipids to the plant surface. Plant Cell 21:1230–1238PubMedPubMedCentralCrossRefGoogle Scholar
  13. Degenkolbe T, Giavalisco P, Zuther E, Seiwert B, Hincha DK, Willmitzer L (2012) Differential remodeling of the lipidome during cold acclimation in natural accessions of Arabidopsis thaliana. Plant J 72:972–982PubMedCrossRefGoogle Scholar
  14. Demir F, Horntrich C, Blachutzik JO, Scherzer S, Reinders Y, Kierszniowska S, Schulze WX, Harms GS, Hedrich R, Geiger D, Kreuzer I (2013) Arabidopsis nanodomain-delimited ABA signaling pathway regulates the anion channel SLAH3. Proc Natl Acad Sci U S A 110:8296–8301PubMedPubMedCentralCrossRefGoogle Scholar
  15. Domon J-M, Baldwin L, Acket S, Caudeville E, Arnoult S, Zub H, Gillet F, Lejeune-Hénaut I, Brancourt-Hulmel M, Pelloux J, Rayon C (2013) Cell wall compositional modifications of Miscanthus ecotypes in response to cold acclimation. Phytochemistry 85:51–61PubMedCrossRefGoogle Scholar
  16. Dutilleul C, Benhassaine-Kesri G, Demandre C, Rézé N, Launay A, Pelletier S, Renou J-P, Zachowski A, Baudouin E, Guillas I (2012) Phytosphingosine-phosphate is a signal for AtMPK6 activation and Arabidopsis response to chilling. New Phytol 194:181–191PubMedCrossRefGoogle Scholar
  17. Eisenhaber B, Bork P, Eisenhaber F (1999) Prediction of potential GPI-modification sites in proprotein sequences. J Mol Biol 292:741–758PubMedCrossRefGoogle Scholar
  18. Endler A, Persson S (2011) Cellulose synthases and synthesis in Arabidopsis. Mol Plant 4:199–211PubMedCrossRefGoogle Scholar
  19. Eriksson SK, Kutzer M, Procek J, Gröbner G, Harryson P (2011) Tunable membrane binding of the intrinsically disordered dehydrin Lti30, a cold-induced plant stress protein. Plant Cell 23:2391–2404PubMedPubMedCentralCrossRefGoogle Scholar
  20. Ferguson MA (1999) The structure, biosynthesis and functions of glycosylphosphatidylinositol anchors, and the contributions of trypanosome research. J Cell Sci 112:2799–2809PubMedGoogle Scholar
  21. Frescatada-Rosa M, Stanislas T, Backues SK, Reichardt I, Men S, Boutté Y, Jürgens G, Moritz T, Bednarek SY, Grebe M (2014) High lipid order of Arabidopsis cell-plate membranes mediated by sterol and DYNAMIN-RELATED PROTEIN1A function. Plant J 80:745–757PubMedPubMedCentralCrossRefGoogle Scholar
  22. Fujita M, Umemura M, Yoko-o T, Jigami Y (2006) PER1 is required for GPI-phospholipase A2 activity and involved in lipid remodeling of GPI-anchored proteins. Mol Biol Cell 17:5253–5264PubMedPubMedCentralCrossRefGoogle Scholar
  23. Fujiwara M, Hamada S, Hiratsuka M, Fukao Y, Kawasaki T, Shimamoto K (2009) Proteome analysis of detergent-resistant membranes (DRMs) associated with OsRac1-mediated innate immunity in rice. Plant Cell Physiol 50:1191–1200PubMedPubMedCentralCrossRefGoogle Scholar
  24. 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 152:2173–2187PubMedPubMedCentralCrossRefGoogle Scholar
  25. Gordon-Kamm WJ, Steponkus PL (1984a) Lamellar-to-hexagonalII phase transitions in the plasma membrane of isolated protoplasts after freeze-induced dehydration. Proc Natl Acad Sci U S A 81:6373–6377PubMedPubMedCentralCrossRefGoogle Scholar
  26. Gordon-Kamm WJ, Steponkus PL (1984b) The behavior of the plasma membrane following osmotic contraction of isolated protoplasts: implications in freezing injury. Protoplasma 123:83–94CrossRefGoogle Scholar
  27. Grison MS, Brocard L, Fouillen L, Nicolas W, Wewer V, Dörmann P, Nacir H, Benitez-Alfonso Y, Claverol S, Germain V, Boutté Y, Mongrand S, Bayer EM (2015) Specific membrane lipid composition is important for plasmodesmata function in Arabidopsis. Plant Cell 27:1228–1250PubMedPubMedCentralCrossRefGoogle Scholar
  28. Guo L, Yang H, Zhang X, Yang S (2013) Lipid transfer protein 3 as a target of MYB96 mediates freezing and drought stress in Arabidopsis. J Exp Bot 64:1755–1767PubMedPubMedCentralCrossRefGoogle Scholar
  29. Gutierrez-Carbonell E, Takahashi D, Lüthje S, González-Reyes JA, Mongrand S, Contreras-Moreira B, Abadía A, Uemura M, Abadía J, López-Millán AF (2016) A shotgun proteomic approach reveals that Fe deficiency causes marked changes in the protein profiles of plasma membrane and detergent-resistant microdomain preparations from Beta vulgaris roots. J Proteome Res 15:2510–2524PubMedCrossRefGoogle Scholar
  30. Hannah MA, Wiese D, Freund S, Fiehn O, Heyer AG, Hincha DK (2006) Natural genetic variation of freezing tolerance in Arabidopsis. Plant Physiol 142:98–112PubMedPubMedCentralCrossRefGoogle Scholar
  31. Hannun YA, Luberto C (2000) Ceramide in the eukaryotic stress response. Trends Cell Biol 10:73–80PubMedCrossRefPubMedCentralGoogle Scholar
  32. Hao H, Fan L, Chen T, Li R, Li X, He Q, Botella MA, Lin J (2014) Clathrin and membrane microdomains cooperatively regulate RbohD dynamics and activity in Arabidopsis. Plant Cell 26:1729–1745PubMedPubMedCentralCrossRefGoogle Scholar
  33. Hayashi S, Ishii T, Matsunaga T, Tominaga R, Kuromori T, Wada T, Shinozaki K, Hirayama T (2008) The glycerophosphoryl diester phosphodiesterase-like proteins SHV3 and its homologs play important roles in cell wall organization. Plant Cell Physiol 49:1522–1535PubMedCrossRefGoogle Scholar
  34. Huang X, Zhang Y, Zhang X, Shi Y (2017) Long-chain base kinase1 affects freezing tolerance in Arabidopsis thaliana. Plant Sci 259:94–103PubMedCrossRefGoogle Scholar
  35. 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 26:1331–1344Google Scholar
  36. Ishikawa T, Aki T, Yanagisawa S, Uchimiya H, Kawai-Yamada M (2015) Overexpression of BAX INHIBITOR-1 links plasma membrane microdomain proteins to stress. Plant Physiol 169:1333–1343PubMedPubMedCentralCrossRefGoogle Scholar
  37. Jarsch IK, Konrad SSA, Stratil TF, Urbanus SL, Szymanski W, Braun P, Braun K-H, Ott T (2014) Plasma membranes are subcompartmentalized into a plethora of coexisting and diverse microdomains in Arabidopsis and Nicotiana benthamiana. Plant Cell 26:1698–1711PubMedPubMedCentralCrossRefGoogle Scholar
  38. Ji H, Wang Y, Cloix C, Li K, Jenkins GI, Wang S, Shang Z, Shi Y, Yang S, Li X (2015) The Arabidopsis RCC1 family protein TCF1 regulates freezing tolerance and cold acclimation through modulating lignin biosynthesis. PLoS Genet 11:e1005471PubMedPubMedCentralCrossRefGoogle Scholar
  39. Johnson KL, Jones BJ, Bacic A, Schultz CJ (2003) The fasciclin-like arabinogalactan proteins of Arabidopsis: a multigene family of putative cell adhesion molecules. Plant Physiol 133:1911–1925PubMedPubMedCentralCrossRefGoogle Scholar
  40. Kawamura Y, Uemura M (2003) Mass spectrometric approach for identifying putative plasma membrane proteins of Arabidopsis leaves associated with cold acclimation. Plant J 36:141–154PubMedCrossRefGoogle Scholar
  41. Kierszniowska S, Seiwert B, Schulze WX (2009) Definition of Arabidopsis sterol-rich membrane microdomains by differential treatment with methyl-β-cyclodextrin and quantitative proteomics. Mol Cell Proteomics 8:612–623PubMedPubMedCentralCrossRefGoogle Scholar
  42. Kim H, Lee SB, Kim HJ, Min MK, Hwang I, Suh MC (2012) Characterization of glycosylphosphatidylinositol-anchored lipid transfer protein 2 (LTPG2) and overlapping function between LTPG/LTPG1 and LTPG2 in cuticular wax export or accumulation in Arabidopsis thaliana. Plant Cell Physiol 53:1391–1403PubMedCrossRefGoogle Scholar
  43. Kline-Jonakin KG, Barrett-Wilt GA, Sussman MR (2011) Quantitative plant phosphoproteomics. Curr Opin Plant Biol 14:507–511PubMedCrossRefPubMedCentralGoogle Scholar
  44. Konrad SSA, Popp C, Stratil TF, Jarsch IK, Thallmair V, Folgmann J, Marín M, Ott T (2014) S-acylation anchors remorin proteins to the plasma membrane but does not primarily determine their localization in membrane microdomains. New Phytol 203:758–769PubMedCrossRefPubMedCentralGoogle Scholar
  45. Kosová K, Holková L, Prášil IT, Prášilová P, Bradáčová M, Vítámvás P, Čapková V (2008) Expression of dehydrin 5 during the development of frost tolerance in barley (Hordeum vulgare). J Plant Physiol 165:1142–1151PubMedCrossRefGoogle Scholar
  46. Koster KL, Lynch DV (1992) Solute accumulation and compartmentation during the cold acclimation of Puma rye. Plant Physiol 98:108–113PubMedPubMedCentralCrossRefGoogle Scholar
  47. Krügel U, Veenhoff LM, Langbein J, Wiederhold E, Liesche J, Friedrich T, Grimm B, Martinoia E, Poolman B, Kühn C (2008) Transport and sorting of the Solanum tuberosum sucrose transporter SUT1 is affected by posttranslational modification. Plant Cell 20:2497–2513PubMedPubMedCentralCrossRefGoogle Scholar
  48. Kubacka-Zębalska M, Kacperska A (1999) Low temperature-induced modifications of cell wall content and polysaccharide composition in leaves of winter oilseed rape (Brassica napus L. var. oleifera L.). Plant Sci 148:59–67CrossRefGoogle Scholar
  49. Kusumi A, Nakada C, Ritchie K, Murase K, Suzuki K, Murakoshi H, Kasai RS, Kondo J, Fujiwara T (2005) Paradigm shift of the plasma membrane concept from the two-dimensional continuum fluid to the partitioned fluid: high-speed single-molecule tracking of membrane molecules. Annu Rev Biophys Biomol Struct 34:351–378PubMedCrossRefGoogle Scholar
  50. Laloi M, Perret A-M, 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 (2006) Insights into the role of specific lipids in the formation and delivery of lipid microdomains to the plasma membrane of plant cells. Plant Physiol 143:461–472PubMedCrossRefGoogle Scholar
  51. Lefebvre B, Furt F, Hartmann M-A, Michaelson LV, Carde J-P, Sargueil-Boiron F, Rossignol M, Napier JA, Cullimore J, Bessoule J-J, 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 144:402–418PubMedPubMedCentralCrossRefGoogle Scholar
  52. Levitt J (1980) Responses of plants to environmental stresses, 2nd edn. Academic, New YorkGoogle Scholar
  53. Levy A, Erlanger M, Rosenthal M, Epel BL (2007) A plasmodesmata-associated β-1,3-glucanase in Arabidopsis: a plasmodesmal β-1,3-glucanase. Plant J 49:669–682PubMedCrossRefGoogle Scholar
  54. Li W, Li M, Zhang W, Welti R, Wang X (2004) The plasma membrane–bound phospholipase Dδ enhances freezing tolerance in Arabidopsis thaliana. Nat Biotechnol 22:427–433PubMedCrossRefGoogle Scholar
  55. Li X, Wang X, Yang Y, Li R, He Q, Fang X, Luu D-T, Maurel C, Lin J (2011) Single-molecule analysis of PIP2;1 dynamics and partitioning reveals multiple modes of Arabidopsis plasma membrane aquaporin regulation. Plant Cell 23:3780–3797PubMedPubMedCentralCrossRefGoogle Scholar
  56. Li B, Takahashi D, Kawamura Y, Uemura M (2012a) Comparison of plasma membrane proteomic changes of Arabidopsis suspension-cultured cells (T87 line) after cold and ABA treatment in association with freezing tolerance development. Plant Cell Physiol 53:543–554PubMedCrossRefPubMedCentralGoogle Scholar
  57. Li R, Liu P, Wan Y, Chen T, Wang Q, Mettbach U, Baluska F, Samaj J, Fang X, Lucas WJ, Lin J (2012b) A membrane microdomain-associated protein, Arabidopsis Flot1, is involved in a Clathrin-independent endocytic pathway and is required for seedling development. Plant Cell 24:2105–2122PubMedPubMedCentralCrossRefGoogle Scholar
  58. Liu P, Li R-L, Zhang L, Wang Q-L, Niehaus K, Baluška F, Šamaj J, Lin J-X (2009) Lipid microdomain polarization is required for NADPH oxidase-dependent ROS signaling in Picea meyeri pollen tube tip growth. Plant J 60:303–313PubMedCrossRefGoogle Scholar
  59. Liu Z, Jia Y, Ding Y, Shi Y, Li Z, Guo Y, Gong Z, Yang S (2017) Plasma membrane CRPK1-mediated phosphorylation of 14-3-3 proteins induces their nuclear import to fine-tune CBF signaling during cold response. Mol Cell 66:117–128PubMedCrossRefPubMedCentralGoogle Scholar
  60. Livingston DP, Henson CA (1998) Apoplastic sugars, fructans, fructan exohydrolase, and invertase in winter oat: responses to second-phase cold hardening. Plant Physiol 116:403–408PubMedCentralCrossRefPubMedGoogle Scholar
  61. Livingston DP, Premakumar R, Tallury SP (2006) Carbohydrate partitioning between upper and lower regions of the crown in oat and rye during cold acclimation and freezing. Cryobiology 52:200–208PubMedCrossRefGoogle Scholar
  62. Livingston DP, Henson CA, Tuong TD, Wise ML, Tallury SP, Duke SH (2013) Histological analysis and 3D reconstruction of winter cereal crowns recovering from freezing: a unique response in oat (Avena sativa L.). PLoS One 8:e53468PubMedPubMedCentralCrossRefGoogle Scholar
  63. Lv X, Jing Y, Xiao J, Zhang Y, Zhu Y, Julian R, Lin J (2017) Membrane microdomains and the cytoskeleton constrain AtHIR1 dynamics and facilitate the formation of an AtHIR1-associated immune complex. Plant J 90:3–16PubMedCrossRefGoogle Scholar
  64. Lynch DV, Steponkus PL (1987) Plasma membrane lipid alterations associated with cold acclimation of winter rye seedlings (Secale cereale L. cv Puma). Plant Physiol 83:761–767PubMedPubMedCentralCrossRefGoogle Scholar
  65. MacMillan CP, Mansfield SD, Stachurski ZH, Evans R, Southerton SG (2010) Fasciclin-like arabinogalactan proteins: specialization for stem biomechanics and cell wall architecture in Arabidopsis and Eucalyptus: FLAs specialized for stem biomechanics and cell walls. Plant J 62:689–703PubMedCrossRefGoogle Scholar
  66. Malinsky J, Opekarová M, Grossmann G, Tanner W (2013) Membrane microdomains, rafts, and detergent-resistant membranes in plants and fungi. Annu Rev Plant Biol 64:501–529PubMedCrossRefGoogle Scholar
  67. Markham JE, Li J, Cahoon EB, Jaworski JG (2006) Separation and identification of major plant sphingolipid classes from leaves. J Biol Chem 281:22684–22694PubMedCrossRefGoogle Scholar
  68. McNeil PL, Kirchhausen T (2005) An emergency response team for membrane repair. Nat Rev Mol Cell Biol 6:499–505PubMedCrossRefGoogle Scholar
  69. 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 50:341–359PubMedCrossRefGoogle Scholar
  70. Minami A, Furuto A, Uemura M (2010) Dynamic compositional changes of detergent-resistant plasma membrane microdomains during plant cold acclimation. Plant Signal Behav 5:1115–1118PubMedPubMedCentralCrossRefGoogle Scholar
  71. Minami A, Tominaga Y, Furuto A, Kondo M, Kawamura Y, Uemura M (2015) Arabidopsis dynamin-related protein 1E in sphingolipid-enriched plasma membrane domains is associated with the development of freezing tolerance. Plant J 83:501–514PubMedCrossRefGoogle Scholar
  72. Mishra MK, Chaturvedi P, Singh R, Singh G, Sharma LK, Pandey V, Kumari N, Misra P (2013) Overexpression of WsSGTL1 gene of Withania somnifera enhances salt tolerance, heat tolerance and cold acclimation ability in transgenic Arabidopsis plants. PLoS One 8:e63064PubMedPubMedCentralCrossRefGoogle Scholar
  73. Mishra MK, Singh G, Tiwari S, Singh R, Kumari N, Misra P (2015) Characterization of Arabidopsis sterol glycosyltransferase TTG15/UGT80B1 role during freeze and heat stress. Plant Signal Behav 10:e1075682PubMedPubMedCentralCrossRefGoogle Scholar
  74. Mongrand S, Morel J, Laroche J, Claverol S, Carde J-P, Hartmann M-A, Bonneu M, Simon-Plas F, Lessire R, Bessoule J-J (2004) Lipid rafts in higher plant cells: purification and characterization of Triton X-100-insoluble microdomains from tobacco plasma membrane. J Biol Chem 279:36277–36286PubMedCrossRefGoogle Scholar
  75. Morel J, Claverol S, Mongrand S, Furt F, Fromentin J, Bessoule J-J, Blein J-P, Simon-Plas F (2006) Proteomics of plant detergent-resistant membranes. Mol Cell Proteomics 5:1396–1411PubMedCrossRefGoogle Scholar
  76. Nagano M, Ishikawa T, Ogawa Y, Iwabuchi M, Nakasone A, Shimamoto K, Uchimiya H, Kawai-Yamada M (2014) Arabidopsis Bax inhibitor-1 promotes sphingolipid synthesis during cold stress by interacting with ceramide-modifying enzymes. Planta 240:77–89PubMedCrossRefGoogle Scholar
  77. Nagano M, Ishikawa T, Fujiwara M, Fukao Y, Kawano Y, Kawai-Yamada M, Shimamoto K (2016) Plasma membrane microdomains are essential for Rac1-RbohB/H-mediated immunity in rice. Plant Cell 28:1966–1983PubMedPubMedCentralCrossRefGoogle Scholar
  78. 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 23:785–794PubMedCrossRefGoogle Scholar
  79. 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 103:793–803PubMedPubMedCentralCrossRefGoogle Scholar
  80. Pearce RS (1988) Extracellular ice and cell shape in frost-stressed cereal leaves: a low-temperature scanning-electron-microscopy study. Planta 175:313–324PubMedCrossRefGoogle Scholar
  81. Pearce RS, Fuller MP (2001) Freezing of barley studied by infrared video thermography. Plant Physiol 125:227–240PubMedPubMedCentralCrossRefGoogle Scholar
  82. Peng L (2002) Sitosterol-β-glucoside as primer for cellulose synthesis in plants. Science 295:147–150PubMedCrossRefGoogle Scholar
  83. Raffaele S, Bayer E, Lafarge D, Cluzet S, German Retana S, Boubekeur T, Leborgne-Castel N, Carde J-P, Lherminier J, Noirot E, Satiat-Jeunemaitre B, Laroche-Traineau J, Moreau P, Ott T, Maule AJ, Reymond P, Simon-Plas F, Farmer EE, Bessoule J-J, Mongrand S (2009) Remorin, a Solanaceae protein resident in membrane rafts and plasmodesmata, impairs potato virus X movement. Plant Cell 21:1541–1555PubMedPubMedCentralCrossRefGoogle Scholar
  84. Rahman LN, McKay F, Giuliani M, Quirk A, Moffatt BA, Harauz G, Dutcher JR (2013) Interactions of Thellungiella salsuginea dehydrins TsDHN-1 and TsDHN-2 with membranes at cold and ambient temperatures—surface morphology and single-molecule force measurements show phase separation, and reveal tertiary and quaternary associations. Biochim Biophys Acta 1828:967–980PubMedCrossRefGoogle Scholar
  85. Rajashekar CB, Zhou H-E, Zhang Y, Li W, Wang X (2006) Suppression of phospholipase Dα1 induces freezing tolerance in Arabidopsis: response of cold-responsive genes and osmolyte accumulation. J Plant Physiol 163:916–926PubMedCrossRefGoogle Scholar
  86. Reddy A, Caler EV, Andrews NW (2001) Plasma membrane repair is mediated by Ca2+-regulated exocytosis of lysosomes. Cell 106:157–169PubMedCrossRefGoogle Scholar
  87. Rinne PLH, Kaikuranta PM, Van Der Schoot C (2001) The shoot apical meristem restores its symplasmic organization during chilling-induced release from dormancy: chilled AM restores its symplasmic network. Plant J 26:249–264PubMedCrossRefGoogle Scholar
  88. Rinne PLH, Welling A, Vahala J, Ripel L, Ruonala R, Kangasjärvi J, van der Schoot C (2011) Chilling of dormant buds hyperinduces FLOWERING LOCUS T and recruits GA-inducible 1,3-β-glucanases to reopen signal conduits and release dormancy in Populus. Plant Cell 23:130–146PubMedPubMedCentralCrossRefGoogle Scholar
  89. Schrick K, Fujioka S, Takatsuto S, Stierhof Y-D, Stransky H, Yoshida S, Jürgens G (2004) A link between sterol biosynthesis, the cell wall, and cellulose in Arabidopsis. Plant J 38:227–243PubMedCrossRefGoogle Scholar
  90. Simons K, Ikonen E (1997) Functional rafts in cell membranes. Nature 387:569–572PubMedCrossRefGoogle Scholar
  91. Singer SJ, Nicolson GL (1972) The fluid mosaic model of the structure of cell membranes. Science 175:720–731PubMedCrossRefGoogle Scholar
  92. Solecka D, Zebrowski J, Kacperska A (2008) Are pectins involved in cold acclimation and de-acclimation of winter oil-seed rape plants? Ann Bot 101:521–530PubMedPubMedCentralCrossRefGoogle Scholar
  93. Steponkus PL (1984) Role of the plasma membrane in freezing injury and cold acclimation. Annu Rev Plant Physiol 35:543–584CrossRefGoogle Scholar
  94. 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 U S A 85:9026–9030PubMedPubMedCentralCrossRefGoogle Scholar
  95. Südhof TC (2002) Synaptotagmins: why so many? J Biol Chem 277:7629–7632PubMedCrossRefPubMedCentralGoogle Scholar
  96. Tähtiharju S, Palva T (2001) Antisense inhibition of protein phosphatase 2C accelerates cold acclimation in Arabidopsis thaliana. Plant J 26:461–470PubMedCrossRefPubMedCentralGoogle Scholar
  97. Takahashi D, Kawamura Y, Yamashita T, Uemura M (2012) Detergent-resistant plasma membrane proteome in oat and rye: similarities and dissimilarities between two monocotyledonous plants. J Proteome Res 11:1654–1665PubMedCrossRefPubMedCentralGoogle Scholar
  98. Takahashi D, Kawamura Y, Uemura M (2013a) Changes of detergent-resistant plasma membrane proteins in oat and rye during cold acclimation: association with differential freezing tolerance. J Proteome Res 12:4998–5011PubMedCrossRefGoogle Scholar
  99. Takahashi D, Kawamura Y, Uemura M (2013b) Detergent-resistant plasma membrane proteome to elucidate microdomain functions in plant cells. Front Plant Sci 4:27PubMedPubMedCentralGoogle Scholar
  100. Takahashi D, Li B, Nakayama T, Kawamura Y, Uemura M (2013c) Plant plasma membrane proteomics for improving cold tolerance. Front Plant Sci 4:90PubMedPubMedCentralGoogle Scholar
  101. Takahashi D, Imai H, Kawamura Y, Uemura M (2016a) Lipid profiles of detergent resistant fractions of the plasma membrane in oat and rye in association with cold acclimation and freezing tolerance. Cryobiology 72:123–134PubMedPubMedCentralCrossRefGoogle Scholar
  102. Takahashi D, Kawamura Y, Uemura M (2016b) Cold acclimation is accompanied by complex responses of glycosylphosphatidylinositol (GPI)-anchored proteins in Arabidopsis. J Exp Bot 67:5203–5215PubMedPubMedCentralCrossRefGoogle Scholar
  103. Tanner W, Malinsky J, Opekarová M (2011) In plant and animal cells, detergent-resistant membranes do not define functional membrane rafts. Plant Cell 23:1191–1193PubMedPubMedCentralCrossRefGoogle Scholar
  104. Tanz SK, Castleden I, Hooper CM, Vacher M, Small I, Millar HA (2013) SUBA3: a database for integrating experimentation and prediction to define the SUBcellular location of proteins in Arabidopsis. Nucleic Acids Res 41:1185–1191CrossRefGoogle Scholar
  105. Tapken W, Murphy AS (2015) Membrane nanodomains in plants: capturing form, function, and movement. J Exp Bot 66:1573–1586PubMedCrossRefGoogle Scholar
  106. Tarazona P, Feussner K, Feussner I (2015) An enhanced plant lipidomics method based on multiplexed liquid chromatography-mass spectrometry reveals additional insights into cold- and drought-induced membrane remodeling. Plant J 84:621–633PubMedCrossRefPubMedCentralGoogle Scholar
  107. Thalhammer A, Bryant G, Sulpice R, Hincha DK (2014) Disordered Cold Regulated15 proteins protect chloroplast membranes during freezing through binding and folding, but do not stabilize chloroplast enzymes in vivo. Plant Physiol 166:190–201PubMedPubMedCentralCrossRefGoogle Scholar
  108. Thomashow MF (1998) Role of cold-responsive genes in plant freezing tolerance. Plant Physiol 118:1–8PubMedPubMedCentralCrossRefGoogle Scholar
  109. Thomashow MF (1999) Plant cold acclimation: freezing tolerance genes and regulatory mechanisms. Annu Rev Plant Biol 50:571–599CrossRefGoogle Scholar
  110. Titapiwatanakun B, Blakeslee JJ, Bandyopadhyay A, Yang H, Mravec J, Sauer M, Cheng Y, Adamec J, Nagashima A, Geisler M, Sakai T, Friml J, Peer WA, Murphy AS (2009) ABCB19/PGP19 stabilises PIN1 in membrane microdomains in Arabidopsis. Plant J 57:27–44PubMedCrossRefGoogle Scholar
  111. Udenfriend S, Kodukula K (1995) How glycosylphosphatidylinositol-anchored membrane proteins are made. Annu Rev Biochem 64:563–591PubMedCrossRefPubMedCentralGoogle Scholar
  112. Uemura M, Steponkus PL (1989) Effect of cold acclimation on the incidence of two forms of freezing injury in protoplasts isolated from rye leaves. Plant Physiol 91:1131–1137PubMedPubMedCentralCrossRefGoogle Scholar
  113. Uemura M, Steponkus PL (1994) A contrast of the plasma membrane lipid composition of oat and rye leaves in relation to freezing tolerance. Plant Physiol 104:479–496PubMedPubMedCentralCrossRefGoogle Scholar
  114. Uemura M, Yoshida S (1984) Involvement of plasma membrane alterations in cold acclimation of winter rye seedlings (Secale cereale L. cv Puma). Plant Physiol 75:818–826PubMedPubMedCentralCrossRefGoogle Scholar
  115. Uemura M, Joseph RA, Steponkus PL (1995) Cold acclimation of Arabidopsis thaliana (effect on plasma membrane lipid composition and freeze-induced lesions). Plant Physiol 109:15–30PubMedPubMedCentralCrossRefGoogle Scholar
  116. Uemura M, Tominaga Y, Nakagawara C, Shigematsu S, Minami A, Kawamura Y (2006) Responses of the plasma membrane to low temperatures. Physiol Plant 126:81–89CrossRefGoogle Scholar
  117. Vu HS, Shiva S, Roth MR, Tamura P, Zheng L, Li M, Sarowar S, Honey S, McEllhiney D, Hinkes P, Seib L, Williams TD, Gadbury G, Wang X, Shah J, Welti R (2014) Lipid changes after leaf wounding in Arabidopsis thaliana: expanded lipidomic data form the basis for lipid co-occurrence analysis. Plant J 80:728–743PubMedCrossRefGoogle Scholar
  118. Wang L, Li H, Lv X, Chen T, Li R, Xue Y, Jiang J, Jin B, Baluška F, Šamaj J, Wang X, Lin J (2015) Spatiotemporal dynamics of the BRI1 receptor and its regulation by membrane microdomains in living Arabidopsis cells. Mol Plant 8:1334–1349PubMedCrossRefGoogle Scholar
  119. Wanner LA, Junttila O (1999) Cold-induced freezing tolerance in Arabidopsis. Plant Physiol 120:391–400PubMedPubMedCentralCrossRefGoogle Scholar
  120. Webb MS, Steponkus PL (1993) Freeze-induced membrane ultrastructural alterations in rye (Secale cereale) leaves. Plant Physiol 101:955–963PubMedPubMedCentralCrossRefGoogle Scholar
  121. Webb MS, Hui SW, Steponkus PL (1993) Dehydration-induced lamellar-to-hexagonal-II phase transitions in DOPE/DOPC mixtures. Biochim Biophys Acta 1145:93–104PubMedCrossRefGoogle Scholar
  122. Webb MS, Uemura M, Steponkus PL (1994) A comparison of freezing injury in oat and rye: two cereals at the extremes of freezing tolerance. Plant Physiol 104:467–478PubMedPubMedCentralCrossRefGoogle Scholar
  123. Webb MS, Irving TC, Steponkus PL (1995) Effects of plant sterols on the hydration and phase behavior of DOPE/DOPC mixtures. Biochim Biophys Acta 1239:226–238PubMedCrossRefGoogle Scholar
  124. Welin BV, Olson A, Nylander M, Palva ET (1994) Characterization and differential expression of dhn/lea/rab-like genes during cold acclimation and drought stress in Arabidopsis thaliana. Plant Mol Biol 26:131–144PubMedCrossRefGoogle Scholar
  125. Welti R, Li W, Li M, Sang Y, Biesiada H, Zhou H-E, 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 277:31994–32002PubMedCrossRefPubMedCentralGoogle Scholar
  126. Yadeta KA, Elmore JM, Coaker G (2013) Advancements in the analysis of the Arabidopsis plasma membrane proteome. Front Plant Sci 4:97PubMedPubMedCentralGoogle Scholar
  127. Yamada T, Kuroda K, Jitsuyama Y, Takezawa D, Arakawa K, Fujikawa S (2002) Roles of the plasma membrane and the cell wall in the responses of plant cells to freezing. Planta 215:770–778PubMedCrossRefGoogle Scholar
  128. Yamazaki T, Kawamura Y, Minami A, Uemura M (2008) Calcium-dependent freezing tolerance in Arabidopsis involves membrane resealing via Synaptotagmin SYT1. Plant Cell 20:3389–3404PubMedPubMedCentralCrossRefGoogle Scholar
  129. Yang H, Richter GL, Wang X, Młodzińska E, Carraro N, Ma G, Jenness M, Chao D, Peer WA, Murphy AS (2013) Sterols and sphingolipids differentially function in trafficking of the Arabidopsis ABCB19 auxin transporter. Plant J 74:37–47PubMedCrossRefGoogle Scholar
  130. Yoshida S, Uemura M (1984) Protein and lipid compositions of isolated plasma membranes from orchard grass (Dactylis glomerata L.) and changes during cold acclimation. Plant Physiol 75:31–37PubMedPubMedCentralCrossRefGoogle Scholar
  131. Zabotin AI, Barisheva TS, Zabotina OA, Larskaya IA, Lozovaya VV, Beldman G, Voragen AGJ (1998) Alterations in cell walls of winter wheat roots during low temperature acclimation. J Plant Physiol 152:473–479CrossRefGoogle Scholar
  132. Zhao Y, Jensen ON (2009) Modification-specific proteomics: strategies for characterization of post-translational modifications using enrichment techniques. Proteomics 9:4632–4641PubMedPubMedCentralCrossRefGoogle Scholar
  133. Zhou Y, Zeng L, Fu X, Mei X, Cheng S, Liao Y, Deng R, Xu X, Jiang Y, Duan X, Baldermann S, Yang Z (2016) The sphingolipid biosynthetic enzyme Sphingolipid delta8 desaturase is important for chilling resistance of tomato. Sci Rep 6:38742PubMedPubMedCentralCrossRefGoogle Scholar
  134. Zuther E, Juszczak I, Ping Lee Y, Baier M, Hincha DK (2015) Time-dependent deacclimation after cold acclimation in Arabidopsis thaliana accessions. Sci Rep 5:12199PubMedPubMedCentralCrossRefGoogle Scholar

Copyright information

© Springer Nature Singapore Pte Ltd. 2018

Authors and Affiliations

  • Daisuke Takahashi
    • 1
  • Matsuo Uemura
    • 2
  • Yukio Kawamura
    • 3
    Email author
  1. 1.Central Infrastructure Group Genomics and Transcript ProfilingMax-Planck-Institute of Molecular Plant PhysiologyPotsdamGermany
  2. 2.United Graduate School of Agricultural Sciences and Department of Plant-biosciences, Faculty of AgricultureIwate UniversityMoriokaJapan
  3. 3.Cryobiofrontier Research Center and Department of Plant-biosciences, and United Graduate School of Agricultural SciencesIwate UniversityMoriokaJapan

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