Acclimation-induced changes in cell membrane composition and influence on cryotolerance of in vitro shoots of native plant species

Plant Cell, Tissue and Organ Culture

Volumn 114, Issue 1, 2013, Pages 83-96

  Funnekotter, Bryn ^a,b   Kaczmarczyk, Anja ^a,b   Turner, Shane R ^b,c   Bunn, Eric ^b,c   Zhou, Wenxu ^c   Smith, Steven ^c   Flematti, Gavin ^c   Mancera, Ricardo L ^a,d  

^a CURTIN UNIVERSITY   (Australia)

^b BOTANIC GARDENS AND PARKS AUTHORITY   (Australia)

^c UNIVERSITY OF WESTERN AUSTRALIA   (Australia)

^d CURTIN UNIVERSITY   (Australia)

Author keywords

Arabidopsis thaliana; Cryopreservation; Grevillea scapigera; Loxocarya cinerea; Phospholipids; Sterols; Vitrification

Indexed keywords

ARABIDOPSIS THALIANA; CRYO-PRESERVATION; GREVILLEA SCAPIGERA; LOXOCARYA CINEREA; STEROLS;

ALCOHOLS; BIOLOGICAL MATERIALS PRESERVATION; CELL MEMBRANES; CYTOLOGY; VITRIFICATION;

PHOSPHOLIPIDS;

ARABIDOPSIS THALIANA; GREVILLEA SCAPIGERA; LOXOCARYA;

EID: 84879206845     PISSN: 01676857     EISSN: None     Source Type: Journal    
DOI: 10.1007/s11240-013-0308-0     Document Type: Article

References (76)

1. Anchordoguy TJ, Rudolph AS, Carpenter JF, Crowe JH (1987) Modes of interaction of cryoprotectants with membrane phospholipids during freezing. Cryobiology 24(4): 324-331.
2. Bajaj Y (1995) Cryopreservation of plant cell, tissue and organ culture for the conservation of germplasm and biodiversity. In: Bajaj Y (ed) Biotechnology in agriculture and forestry. Cryopreservation of plant germplasm I, vol 32. pp 3-28.
3. Beck JG, Mathieu D, Loudet C, Buchoux S, Dufourc EJ (2007) Plant sterols in "rafts": a better way to regulate membrane thermal shocks. FASEB J 21(8): 1714-1723.
4. Benson EE (1990) Free radical damage in stored plant germplasm. International Board for Plant Genetic Resources, Rome.
5. Benson EE (2008) Cryopreservation theory. In: Reed BM (ed) Plant cryopreservation: a practical guide. Springer, New York, pp 15-32.
6. Briggs BG, Johnson LAS (2001) New species of Harperia, Loxocarya, Onychosepalum, Platychorda and Tremulina (Restionaceae) in Western Australia. Telopea 9(2): 247-257.
7. Catala R, Salinas J (2008) Review. Regulatory mechanisms involved in cold acclimation response. Span J Agric Res 6: 211-220.
8. Chang Y, Barker RE, Reed BM (2000) Cold acclimation improves recovery of cryopreserved grass (Zoysia and Lolium sp.). CryoLetters 21(2): 107-116.
9. Clouse SD (2002) Arabidopsis mutants reveal multiple roles for sterols in plant development. Plant Cell 14(9): 1995-2000.
10. Crowe JH, Crowe LM, Carpenter JF, Aurell Westrom C (1987) Stabilization of dry phospholipid bilayers and proteins by sugars. Biochem J 242(1): 1-10.
11. Crowe JH, Crowe LM, Carpenter JF, Rudolph AS, Wistrom CA, Spargo BJ, Anchordoguy TJ (1988) Interactions of sugars with membranes. Biochim Biophys Acta 947(2): 367-384.
12. Day JG, Harding KC, Nadarajan J, Benson EE (2008) Cryopreservation: conservation of bioresources at ultra low temperatures. In: Walker J, Rapley R (eds) Molecular biomethods handbook. Humana Press, Hertfordshire UK, pp 917-947.
13. Demel RA, De Kruyff B (1976) The function of sterols in membranes. Biochim Biophys Acta 457(2): 109-132.
14. Dereuddre J, Hassen N, Blandin S, Kaminski M (1991) Resistance of alginate-coated somatic embryos of carrot (Daucus carota L.) to desiccation and freezing in liquid nitrogen: 2. Thermal analysis. Cryoletters 12: 135-148.
15. Geuns J, van Loenhout HEM, Valcke RLM, Loven KV, Redig P, Veselov SY, Kudoyarova GR, van Onckelen HA, Vendrig JC (1997) Sterols and polyamines in IPT-transformed tobacco plants. Phytochemistry 44(5): 797-804.
16. Grunwald C (1971) Effects of free sterols, steryl ester, and steryl glycoside on membrane permeability. Plant Physiol 48(5): 653-655.
17. Grunwald C (1978) Function of sterols. Philos Trans R Soc Lond B Biol Sci 284(10002): 541-558.
18. Gunstone FD, Harwood JL (2007) Occurrence and characterization of oils and fats. In: Gunstone FD, Harwood JL, Dijkstra AJ (eds) The lipid handbook. CRC Press, Boca Raton, pp 37-141.
19. Guye MG (1989) Phospholipid, sterol composition and ethylene production in relation to choline-induced chill-tolerance in mung bean (Vigna radiata L. Wilcz.) during a chill-warm cycle. J Exp Bot 40(3): 369-374.
20. Hammerstedt RH, Graham JK, Nolan JP (1990) Cryopreservation of mammalian sperm: what we ask them to survive. J Androl 11(1): 73-88.
21. Hartmann MA (1998) Plant sterols and the membrane environment. Trends Plant Sci 3(5): 170-175.
22. Hartmann M-A (2004) Sterol metabolism and functions in higher plants. In: Daum G (ed) Lipid metabolism and membrane biogenesis, vol 6., Topics in current geneticsSpringer, Berlin, pp 183-211.
23. Hughes ZE, Mancera RL (2013) Molecular dynamics simulations of mixed DOPC-β-sitosterol bilayers and their interactions with DMSO. Soft Matter 9: 2920-2935.
24. Hughes ZE, Mark AE, Mancera RL (2012) Molecular dynamics simulations of the interactions of DMSO with DPPC and DOPC phospholipid membranes. J Phys Chem B 116(39): 11911-11923.
25. Kaczmarczyk A, Shvachko N, Lupysheva Y, Hajirezaei MR, Keller ER (2008) Influence of alternating temperature preculture on cryopreservation results for potato shoot tips. Plant Cell Rep 27(9): 1551-1558.
26. Kaczmarczyk A, Turner SR, Bunn E, Mancera RL, Dixon KW (2011) Cryopreservation of threatened native Australian species-what have we learned and where to from here? In Vitro Cell Dev Biol Plant 47(1): 17-25.
27. Kent B, Garvey CJ, Lenné T, Porcar L, Garamus VM, Bryant G (2010) Measurement of glucose exclusion from the fully hydrated DOPE inverse hexagonal phase. Soft Matter 6(6): 1197-1202.
28. Kim H, Min HK, Kong G (2009) Quantitative analysis of phosphatidylcholines and phosphatidylethanolamines in urine of patients with breast cancer by nanoflow liquid chromatography/tandem mass spectrometry. Anal Bioanal Chem 393(6-7): 1649-1656.
29. Klotke J, Kopka J, Gatzke N, Heyer AG (2004) Impact of soluble sugar concentrations on the acquisition of freezing tolerance in accessions of Arabidopsis thaliana with contrasting cold adaptation-evidence for a role of raffinose in cold acclimation. Plant Cell Environ 27(11): 1395-1404.
30. Kong L, von Aderkas P (2011) A novel method of cryopreservation without a cryoprotectant for immature somatic embryos of conifer. Plant Cell Tissue Organ Cult 106(1): 115-125.
31. Kreck CA, Mandumpal JB, Mancera RL (2011) Prediction of the glass transition in aqueous solutions of simple amides by molecular dynamics simulations. Chem Phys Lett 501(4-6): 273-277.
32. Kushnarenko SV, Romadanova NV, Reed BM (2009) Cold acclimation improves regrowth of cryopreserved apple shoot tips. CryoLetters 30(1): 47-54.
33. Lenné T, Bryant G, Garvey CJ, Keiderling U, Koster KL (2006) Location of sugars in multilamellar membranes at low hydration. Phys B 385: 862-864.
34. Lenné T, Bryant G, Holcomb R, Koster KL (2007) How much solute is needed to inhibit the fluid to gel membrane phase transition at low hydration? Biochim Biophys Acta Biomembr 1768(5): 1019-1022.
35. Lenné T, Garvey CJ, Koster KL, Bryant G (2009) Effects of sugars on lipid bilayers during dehydration-SAXS/WAXS measurements and quantitative model. J Phys Chem B 113(8): 2486-2491.
36. Leshem YY (1992) Sterols. In: Leshem YY, Shewfel RL, Willmer CM (eds) Plant membranes: a biophysical approach to structure, development and senescence. Kluwer, Dordrecht, pp 57-64.
37. Leunufna S, Keller ER (2005) Cryopreservation of yams using vitrification modified by including droplet method: effects of cold acclimation and sucrose. CryoLetters 26(2): 93-102.
38. 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(4): 761-767.
39. Mandumpal JB, Kreck CA, Mancera RL (2011) A molecular mechanism of solvent cryoprotection in aqueous DMSO solutions. Phys Chem Chem Phys 13(9): 3839-3842.
40. McKersie BD, Thompson JE (1979) Influence of plant sterols on the phase properties of phospholipid bilayers. Plant Physiol 63(5): 802-805.
41. Min HK, Kong G, Moon MH (2010) Quantitative analysis of urinary phospholipids found in patients with breast cancer by nanoflow liquid chromatography-tandem mass spectrometry: II. Negative ion mode analysis of four phospholipid classes. Anal Bioanal Chem 396(3): 1273-1280.
42. Mollo L, Martins MCM, Oliveira VF, Nievola CC, Figueiredo-Ribeiro RdCL (2011) Effects of low temperature on growth and non-structural carbohydrates of the imperial bromeliad Alcantarea imperialis cultured in vitro. Plant Cell Tiss Organ Cult 107(1): 141-149.
43. Mouritsen OG, Zuckermann MJ (2004) What's so special about cholesterol? Lipids 39(11): 1101-1113.
44. Murashige T (1962) A revised medium for rapid growth and bio assays with tobacco tissue cultures. Physiol Plant 15(3): 473.
45. 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(3): 793.
46. Quartacci MF, 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(354): 77-84.
47. Reed BM (1996) Pretreatment strategies for cryopreservation of plant tissues. In vitro conservation of plant genetic resources. Universiti Kebangsaan, Malaysia.
48. Reed BM (2008) Cryopreservation-practical considerations. In: Reed BM (ed) Plant cryopreservation. A practical guide. Springer, New York, pp 3-13.
49. Reed BM, Uchendu E (2008) Controlled rate cooling. In: Reed BM (ed) Plant cryopreservation: a practical guide. Springer, New York, pp 77-92.
50. Sakai A (2004) Plant cryopreservation. In: Fuller BJ, Lane N, Benson EE (eds) Life in the frozen state. CRC Press, Boca Raton, pp 329-345.
51. Sakai A, Kobayashi S, Oiyama I (1990) Cryopreservation of nucellar cells of navel orange (Citrus sinensis Osb. var. brasiliensis Tanaka) by vitrification. Plant Cell Rep 9(1): 30-33.
52. Sasaki H, Ichimura K, Oda M (1996) Changes in sugar content during cold acclimation and deacclimation of cabbage seedlings. Ann Bot 78(3): 365-369.
53. Schiller J, Süß R, Fuchs B, Müller M, Zschörnig O, Arnold K (2003) Combined application of TLC and matrix-assisted laser desorption and lonisation time-of-flight mass spectrometry (MALDI-TOF MS) to phospholipid analysis of brain. Chromatographia 57: 297-302.
54. Schuler I, Milon A, Nakatani Y, Ourisson G, Albrecht AM, Benveniste P, Hartman MA (1991) Differential effects of plant sterols on water permeability and on acyl chain ordering of soybean phosphatidylcholine bilayers. Proc Natl Acad Sci USA 88(16): 6926-6930.
55. Sen A, Hui SW (1988) Direct measurement of headgroup hydration of polar lipids in inverted micelles. Chem Phys Lipids 49(3): 179-184.
56. Steponkus PL (1984) Role of the plasma membrane in freezing injury and cold acclimation. Ann Rev Plant Physiol 35(1): 543-584.
57. Suzuki M, Ishikawa M, Okuda H, Noda K, Kishimoto T, Nakamura T, Ogiwara I, Shimura I, Akihma T (2006) Physiological changes in gentian axillary buds during two-step preculturing with sucrose that conferred high levels of tolerance to desiccation and cryopreservation. Ann Bot 97(6): 1073-1081.
58. Taji T, Ohsumi C, Iuchi S, Seki M, Kasuga M, Kobayashi M, Yamaguchi-Shinozaki K, Shinozaki K (2002) Important roles of drought-and cold-inducible genes for galactinol synthase in stress tolerance in Arabidopsis thaliana. Plant J 29(4): 417-426.
59. Thomashow MF (1998) Role of cold-responsive genes in plant freezing tolerance. Plant Physiol 118(1): 1-7.
60. Touchell DH, Dixon KW, Tan B (1992) Cryopreservation of shoot-tips of Grevillea scapigera (Proteaceae): a rare and endangered plant from Western Australia. Aust J Bot 40(3): 305-310.
61. Touchell DH, Turner SR, Bunn E, Dixon KW (2002) Cryostorage of somatic tissue of endangered Australian species. In: Bajaj YPS (ed) Cryopreservation of plant germplasm II, vol 50. Springer, Berlin, pp 357-371.
62. Towill LE, Bonnart R, Volk GM (2006) Cryopreservation of Arabidopsis thaliana shoot tips. CryoLetters 27(6): 353-360.
63. Turner SR, Senaratna T, Touchell DH, Bunn E, Dixon KW, Tan B (2001) Stereochemical arrangement of hydroxyl groups in sugar and polyalcohol molecules as an important factor in effective cryopreservation. Plant Sci 160(3): 489-497.
64. 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(2): 479-496.
65. 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(1): 15-30.
66. Uemura M, Tominaga Y, Nakagawara C, Shigematsu S, Minami A, Kawamura Y (2005) Responses of the plasma membrane to low temperatures. Physiol Plant 126(1): 81-89.
67. Valluru R, van den Ende W (2011) Myo-inositol and beyond-emerging networks under stress. Plant Sci 181(4): 387-400.
68. Vandenbussche B, Leuridan S, Verdoodt V, Gysemberg M, de Proft M (1999) Changes in sugar content and fatty acid composition of in vitro sugar beet shoots after cold acclimation: influence on survival after cryopreservation. Plant Growth Regul 28(3): 157-163.
69. Wanner LA, Junttila O (1999) Cold-induced freezing tolerance in Arabidopsis. Plant Physiol 120(2): 391-400.
70. Waterhouse KE, Hofmo PO, Tverdal A, Miller RR (2006) Within and between breed differences in freezing tolerance and plasma membrane fatty acid composition of boar sperm. Reproduction 131(5): 887-894.
71. 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 Dα in freezing-induced lipid changes in Arabidopsis. J Biol Chem 277(35): 31994-32002.
72. Western Australian Herbarium (1998) FloraBase-the Western Australian flora. Department of Environment and Conservation. http://florabase. dec. wa. gov. au/.
73. White T, Bursten S, Federighi D, Lewis RA, Nudelman E (1998) High-resolution separation and quantification of neutral lipid and phospholipid species in mammalian cells and sera by multi-one-dimensional thin-layer chromatography. Anal Biochem 258(1): 109-117.
74. Wolfe J, Bryant G (1999) Freezing, drying, and/or vitrification of membrane-solute-water systems. Cryobiology 39(2): 103-129.
75. Yuanyuan M, Yali Z, Jiang L, Hongbo S (2010) Roles of plant soluble sugars and their responses to plant cold stress. Afr J Biotechnol 8(10): 2004-2010.
76. Zhu GY, Geuns J, Dussert S, Swennen R, Panis B (2006) Change in sugar, sterol and fatty acid composition in banana meristems caused by sucrose-induced acclimation and its effects on cryopreservation. Physiol Plant 128(1): 80-94.