Enhancement in androgenesis efficiency in barley (Hordeum vulgare L.) and bread wheat (Triticum aestivum L.) by the addition of dimethyl sulfoxide to the mannitol pretreatment medium

Plant Cell, Tissue and Organ Culture

Volumn 125, Issue 1, 2016, Pages 11-22

  Echávarri, Begoña ^a   Cistué, Luis ^a  

^a CSIC   (Spain)

Author keywords

Androgenesis; Barley; Bread wheat; Dimethyl sulfoxide; Doubled haploids; Pretreatment

Indexed keywords

CYTOLOGY; DIMETHYL SULFOXIDE; FOOD PRODUCTS; INFORMATION DISSEMINATION; LIPID BILAYERS; ORGANIC SOLVENTS;

ANDROGENESIS; BARLEY; BREAD WHEAT; DOUBLED HAPLOID; PRE-TREATMENT;

PLANTS (BOTANY);

EID: 84960402658     PISSN: 01676857     EISSN: 15735044     Source Type: Journal    
DOI: 10.1007/s11240-015-0923-z     Document Type: Article

References (85)

1. Ahkong Q, Fisher D, Tampion W, Lucy JA (1975) Mechanism of cell fusion. Nature 253:194–195
2. Ashwood-Smith MJ (1967) Radioprotective and cryoprotective properties of dimethyl sulfoxide in cellular systems. Ann NY Acad Sci 141:45–62
3. Bektasoglu B, Celik SE, Ozyürek M, Güçlü K, Apak R (2006) Novel hydroxyl radical scavenging antioxidant activity assay for water-soluble antioxidants using a modified CUPRAC method. Biochem Bioph Res Co 345:1194–1200
4. Brodelius P, Nilsson K (1983) Permeabilization of immobilized plant cells, resulting in release of intracellularly stored products with preserved cell viability. Eur J Appl Microbiol Biot 17:275–280
5. Caredda S, Clément C (1999) Androgenesis and albinism in Poaceae: influence of genotype and carbohydrates. In: Clément C, Pacini E, Audran JC (eds) Anther and pollen: from biology to biotechnology, 3rd edn. Springer, Berlin, pp 211–226
6. Cistué L, Ramos A, Castillo AM, Romagosa I (1994) Production of large number of doubled haploid plants from barley anthers pretreated with high concentrations of mannitol. Plant Cell Rep 13:709–712
7. Cistué L, Ziauddin A, Simion E, Kasha KJ (1995) Effects of culture conditions on isolated microspore response of barley cultivar Igri. Plant Cell Tiss Org Cult 42:163–169
8. Cistué L, Ramos A, Castillo AM (1999) Influence of anther pretreatment and culture medium composition on the production of barley doubled haploids from model and low responding cultivars. Plant Cell Tiss Org Cult 55:159–166
9. Cistué L, Vallés MP, Echávarri B, Sanz JM, Castillo A (2003) Barley anther culture. In: Maluszynski M, Kasha KJ, Forster BP, Szarejko I (eds) Doubled haploid production in crop plants: a manual, 1st edn. Kluwer, Dordrecht, pp 29–34
10. Cistué L, Soriano M, Castillo AM, Valles MP, Sanz JM, Echávarri B (2006) Production of doubled haploids in durum wheat (Triticum turgidum L.) through isolated microspore culture. Plant Cell Rep 25:257–264
11. Cistué L, Romagosa I, Batlle F, Echávarri B (2009) Improvements in the production of doubled haploids in durum wheat (Triticum turgidum L.) through isolated microspore culture. Plant Cell Rep 28:727–735
12. Clapham D (1973) Haploid Hordeum plants from anthers in vitro. Z Pflanzenzucht 69:142–155
13. Datta SK (2005) Androgenic haploids: factors controlling development and its application in crop improvement. Curr Sci 89:1870–1878
14. Datta SK, Wenzel G (1987) Isolated microspore derived plant formation via embryogenesis in Triticum aestivum L. Plant Sci 48:49–54
15. David NA (1972) The pharmacology of dimethylsulfoxide 6544. Annu Rev Pharmacolog 12:353–374
16. Davis DG, Wergin WP, Dusbabek KE (1978) Effects of organic solvents on growth and ultrastructure of plant cell suspensions. Pestic Biochem Phys 8:84–97
17. de Ménorval MA, Mir LM, Fernández ML, Reigada R (2012) Effects of dimethyl sulfoxide in cholesterol-containing lipid membranes: a comparative study of experiments in Silico and with cells. PLoS ONE 7:e41733
18. Delmer DP (1979) Dimethylsulfoxide as a potential tool for analysis of compartmentation in living plant cells. Plant Physiol 64:623–629
19. Devaux P, Kasha KJ (2009) Overview of barley doubled haploid production. In: Touraev A, Forster BP, Jain SM (eds) Advances in haploid production in higher plants. Springer, Berlin, pp 47–63
20. Dwivedi SL, Britt AB, Tripathi L, Sharma S, Upadhyaya HD, Ortiz R (2015) Haploids: constraints and opportunities in plant breeding. Biotechnol Adv 33:812–829
21. Echávarri B, Soriano M, Cistué L, Vallés MP, Castillo AM (2008) Zinc sulphate improved microspore embryogenesis in barley. Plant Cell Tiss Org 93:295–301
22. Esteves P, Belzile F (2014) Improving the efficiency of isolated microspore culture in six-row spring barley: optimization of key physical factors. Plant Cell Rep 33:993–1001
23. Esteves P, Clermont I, Marchand S, Belzile F (2014) Improving the efficiency of isolated microspore culture in six-row spring barley: exploring novel growth regulators to maximize embryogenesis and reduce albinism. Plant Cell Rep 33:871–879
24. Ferrie AM, Caswell KL (2011) Isolated microspore culture techniques and recent progress for haploid and doubled haploid plant production. Plant Cell Tiss Org 104:301–309
25. Forster BP, Heberle-Bors E, Kasha KJ, Touraev A (2007) The resurgence of haploids in higher plants. Trends Plant Sci 12:368–375
26. Galvao J, Davis B, Tilley M, Normando E, Duchen MR, Cordeiro MF (2014) Unexpected low-dose toxicity of the universal solvent DMSO. FASEB J 28:1317–1330
27. Germanà MA (2011) Anther culture for haploid and doubled haploid production. Plant Cell Tiss Org 104:283–300
28. Gurtovenko AA, Anwar J (2007) Modulating the structure and properties of cell membranes: the molecular mechanism of action of dimethyl sulfoxide. J Phys Chem B 111:10453–10460
29. Haydu Z, Lázár G, Dudits D (1977) Increased frequency of polyethylene glycol induced protoplast fusion by dimethylsulfoxide. Plant Sci Lett 10:357–360
30. He F, Liu W, Zheng S, Zhou L, Ye B, Qi Z (2012) Ion transport through dimethyl sulfoxide (DMSO) induced transient water pores in cell membranes. Mol Membr Biol 29:107–113
31. Hu T, Kasha KJ (1997) Improvement of isolated microspore culture in wheat (Triticum aestivum L.) through ovary co-culture. Plant Cell Rep 16:520–525
32. Huang B (2006) Cellular membranes in stress sensing and regulation of plant adaptation to abiotic stresses. In: Bingru Huang (ed) Plant-environment interactions, 3rd edn. Taylor and Francis group, pp 1–26
33. Hunter CP (1988) Plant regeneration from microspores of barley, Hordeum vulgare L. Ph.D. thesis. Wye College, Univ London, London
34. Islam S, Tuteja N (2012) Enhancement of androgenesis by abiotic stress and other pretreatments in major crop species. Plant Sci 182:134–144
35. Jacob SW, Herschler R (1986) Pharmacology of DMSO. Cryobiology 23:14–27
36. Jacquard C, Asakaviciute R, Hamalian AM, Sangwan RS, Devaux P, Clément C (2006) Barley anther culture: effects of annual cycle and spike position on microspore embryogenesis and albinism. Plant Cell Rep 25:375–381
37. Jacquard C, Nolin F, Hécart C, Grauda D, Rashal I, Dhondt-Cordelier S, Sangwan R, Devaux P, Mazeyrat-Gourbeyre F, Clément C (2009) Microspore embryogenesis and programmed cell death in barley: effects of copper on albinism in recalcitrant cultivars. Plant Cell Rep 28:1329–1339
38. Jensen CJ (1983) Producing haploid plants by chromosome elimination. In: Han H (ed) Cell and tissue culture techniques for cereal crop improvement. Science Press, Beijing, pp 55–80
39. Kao KN, Saleem S, Abrams M, Pedras M, Horn D, Mallard C (1991) Culture conditions for induction of green plants from barley microspores by anther culture methods. Plant Cell Rep 9:595–601
40. Kasha KJ, Simion E, Oro R, Yao QA, Hu TC, Carlson AR (2001) An improved in vitro technique for isolated microspore culture of barley. Euphytica 120:379–385
41. Kasha KJ, Simion E, Oro R, Shim YS (2003) Barley isolated microspore culture protocol. In: Maluszynski M, Kasha KJ, Forster BP, Szarejko I (eds) Doubled haploid production in crop plants: a manual, 1st edn. Kluwer, Dordrecht, pp 43–48
42. Kim H, Ralph J (2010) Solution-state 2D NMR of ball-milled plant cell wall gels in DMSO-d6/pyridine-d5. Org Biomol Chem 8:576–591
43. Konzac C, Polle EA, Liu W, Zheng Y (2002) Methods for generating doubled haploid plants. United States Patent US 6362393 B1
44. Lantos C, Weyen J, Orsini JM, Gnad H, Schlieter B, Lein V, Kontowski S, Jacobi A, Mihály R, Broughton S, Pauk J (2013) Efficient application of in vitro anther culture for different European winter wheat (Triticum aestivum L.) breeding programmes. Plant Breed 132:149–154
45. Li H, Devaux P (2003) High frequency regeneration of barley doubled haploid plants from isolated microspore culture. Plant Sci 164:379–386
46. Liu W, Zheng MY, Konzak CF (2002) Improving green plant production via isolated microspore culture in bread wheat (Triticum aestivum L.). Plant Cell Rep 20:821–824
47. Los DA, Murata N (2004) Membrane fluidity and its roles in the perception of environmental signals. Biochem Bioph Acta 1666:144–157
48. Los DA, Mironov KS, Allakhverdiev SI (2013) Regulatory role of membrane fluidity in gene expression and physiological functions. Photosynth Res 116:489–509
49. Lyman GH, Preisler HD, Papahadjopoulos D (1976) Membrane action of DMSO and other chemical inducers of Friend Leukaemic cell differentiation. Nature 262:361–363
50. Malik B, Pirzadah TB, Tahir I, Rehman RU, Hakeem KR, Abdin MZ (2014) Plant signaling: response to reactive oxygen species. In: Hakeem KR et al (eds) Plant signaling: understanding the molecular crosstalk. Springer, Heidelberg, pp 1–38
51. Maluszynski M, Kasha KJ, Forster BP, Szarejko I (2003) Doubled haploid production in crop plants: a manual, 1st edn. Kluwer, Dordrecht
52. Maraschin SF, de Priester W, Spaink HP, Wang M (2005) Androgenic switch: an example of plant embryogenesis from the male gametophyte perspective. J Exp Bot 56:1711–1726
53. Mittler R (2002) Oxidative stress, antioxidants and stress tolerance. Trends Plant Sci 7:405–410
54. Munnik T, Meijer HJ (2001) Osmotic stress activates distinct lipid and MAPK signaling pathways in plants. FEBS Lett 498:172–178
55. Muñoz-Amatriaín M, Svensson JT, Castillo AM, Cistué L, Close TJ, Vallés MP (2006) Transcriptome analysis of barley anthers: effect of mannitol treatment on microspore embryogenesis. Physiol Plant 127:551–560
56. Murashige T, Skoog F (1962) A revised medium for rapid growth and bioassays with tobacco tissue cultures. Physiol Plant 15:473–497
57. Norwood TH, Zeigler CJ (1982) The use of dimethyl sulfoxide in mammalian cell fusion. In: Shay JW (ed) Techniques in somatic cell genetics. Plenum Press, New York, pp 33–45
58. Norwood TH, Zeigler CJ, Martin GM (1976) Dimethyl sulfoxide enhances polyethylene glycol-mediated somatic cell fusion. Somat Cell Genet 2:263–270
59. Olmedilla A (2010) Microspore embryogenesis. In: Pua EC, Davey MR (eds) Plant developmental biology—biotechnological perspectives, vol 2. Springer, Berlin, pp 27–43
60. 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
61. Ouyang TW, Hu H, Chuang CC, Tseng CC (1973) Induction of pollen plants from anthers of Triticum aestivum L. cultured in vitro. Sci Sin 16:79–95
62. Phillis JW, Estevez AY, O’Regan MH (1998) Protective effects of the free radical scavengers, dimethyl sulfoxide and ethanol, in cerebral ischemia in gerbils. Neuroscience L 244:109–111
63. Qi W, Ding D, Salvi RJ (2008) Cytotoxic effects of dimethyl sulphoxide (DMSO) on cochlear organotypic cultures. Hear Res 236:52–60
64. Rall WF, Fahy GM (1985) Ice-free cryopreservation of mouse embryos at −196°C by vitrification. Nature 313:573–575
65. 2+ influx. Plant J 27:1–12
66. Sanmartín-Suárez C, Soto-Otero R, Sánchez-Sellero I, Méndez-Álvarez E (2011) Antioxidant properties of dimethyl sulfoxide and its viability as a solvent in the evaluation of neuroprotective antioxidants. J Pharmacol Toxicol Method 63:209–215
67. Santos NC, Figueira-Coelho J, Martins-Silva J, Saldanha C (2003) Multidisciplinary utilization of dimethyl sulfoxide: pharmacolical, cellular and molecular aspects. Biochem Pharmacol 65:1035–1041
68. Santra M, Ankrah N, Santra DK, Kidwell KK (2012) An improved wheat microspore culture technique for the production of doubled haploid plants. Crop Sci 52:2314–2320
69. Sawai M, Takase K, Teraoka H, Tsukada K (1990) Reversible G1 arrest in the cell cycle of human lymphoid cell lines by dimethyl sulfoxide. Exp Cell Res 187:4–10
70. Shariatpanahi ME, Bal U, Heberle-Bors E, Touraev A (2006) Stresses applied for the re-programming of plant microspores towards in vitro embryogenesis. Physiol Plant 127:519–534
71. Simic MG (1988) Mechanisms of inhibition of free-radical processes in mutagenesis and carcinogenesis. Mutat Res 202:377–386
72. Snedeker WH, Gaunya WS (1970) Dimethyl sulfoxide as a cryoprotective agent for freezing bovine semen. J Anim Sci 30:953–956
73. Srinivas S, Sironmani TA, Shanmugam G (1991) Dimethyl sulfoxide inhibits the expression of early growth response genes and arrests fibroblasts at quiescence. Exp Cell Res 196:279–286
74. Sumida K, Igarashi Y, Toritsuka N, Matsushita T, Abe-Tomizawa K, Aoki M, Urushidani T, Yamada H, Ohno Y (2011) Effects of DMSO on gene expression in human and rat hepatocytes. Hum Exp Toxicol 30:1701–1709
75. Tarrand JJ, LaSala PR, Han XY, Rolston KV, Kontoyiannis DP (2012) Dimethyl Sulfoxide enhances effectiveness of skin antiseptics and reduces contamination rates of blood cultures. J Clin Microbiol 50:1552–1557
76. Touraev A, Vicente O, Heberle-Bors E (1997) Initiation of microspore embryogenesis by stress. Trends Plant Sci 2:297–302
77. Touraev A, Pfosser M, Heberle-Boss E (2001) The microspore: a haploid multipurpose cell. Adv Bot Res 35:53–109
78. Wang M, van Bergen S, Van Duijn B (2000) Insights into a key developmental switch and its importance for efficient plant breeding. Plant Physiol 124:523–530
79. Wędzony M, Forster BP, Zur I, Golemiec E, Szechyńska-Hebda M, Dubas E, Gotębiowska G (2009) Progress in doubled haploid technology in higher plants. In: Touraev A, Forster BP, Jain SM (eds) Advances in haploid production in higher plants. Springer, Dordrecht, pp 1–33
80. Xiong L, Schumaker KS, Zhu JK (2002) Cell signaling during cold, drought and salt stress. Plant Cell 14:S165–S183
81. Yu ZW, Quinn PJ (1994) Dimethyl sulphoxide: a review of its applications in cell biology. Bioscience Rep 14:259–281
82. Yu ZW, Quinn PJ (1998) The modulation of membrane structure and stability by dimethyl sulphoxide (Review). Mol Membr Biol 15:59–68
83. Zheng MY (2003) Microspore culture in wheat (Triticum aestivum)- doubled haploid production via induced embryogenesis. Plant Cell Tiss Organ Cult 73:213–230
84. Zheng MY, Weng Y, Liu W, Konzak CF (2002) The effect of ovary-conditioned medium on microspore embryogenesis in common wheat (Triticum aestivum L.). Plant Cell Rep 20:802–807
85. Zoriniants S, Tashpulatov AS, Heberle-Bors E, Touraev A (2005) The role of stress in the induction of haploid microspore embryogenesis. In: Palmer CE, Keller WA, Kasha KJ (eds) Biotechnology in agriculture and forestry, vol 56., Haploids in crop improvement IISpringer, Berlin, pp 35–52