Vitrification Solutions for Plant Cryopreservation: Modification and Properties
Status PubMed-not-MEDLINE Jazyk angličtina Země Švýcarsko Médium electronic
Typ dokumentu časopisecké články, přehledy
PubMed
34961099
PubMed Central
PMC8707230
DOI
10.3390/plants10122623
PII: plants10122623
Knihovny.cz E-zdroje
- Klíčová slova
- cryoprotectant, glassy state, toxicity, ultra-low temperature,
- Publikační typ
- časopisecké články MeSH
- přehledy MeSH
Many plants cannot vitrify themselves because they lack glassy state-inducing substances and/or have high water content. Therefore, cryoprotectants are used to induce vitrification. A cryoprotectant must have at least the following primary abilities: high glass-forming property, dehydration strength on a colligative basis to dehydrate plant cells to induce the vitrification state, and must not be toxic for plants. This review introduces the compounds used for vitrification solutions (VSs), their properties indicating a modification of different plant vitrification solutions, their modifications in the compounds, and/or their concentration. An experimental comparison is listed based on the survival or regeneration rate of one particular species after using more than three different VSs or their modifications. A brief overview of various cryopreservation methods using the Plant Vitrification Solution (PVS) is also included. This review can help in alert researchers to newly introduced PVSs for plant vitrification cryoprotocols, their properties, and the choice of their modifications in the compounds and/or their concentration.
Zobrazit více v PubMed
Engelmann F. Use of biotechnologies for the conservation of plant biodiversity. Vitr. Cell. Dev. Biol. Anim. 2011;47:5–16. doi: 10.1007/s11627-010-9327-2. DOI
Wang M.-R., Bi W., Shukla M.R., Ren L., Hamborg Z., Blystad D.-R., Saxena P.K., Wang Q.-C. Epigenetic and Genetic Integrity, Metabolic Stability, and Field Performance of Cryopreserved Plants. Plants. 2021;10:1889. doi: 10.3390/plants10091889. PubMed DOI PMC
Engelmann F. In vitro conservation methods. In: Callow J.A., Ford Lloyd B.V., Newbury H.J., editors. Biotechnology and Plant Genetic Resources. CAB International; Oxford, UK: 1997. pp. 119–162.
Wang M.-R., Chen L., Da Silva J.A.T., Volk G.M., Wang Q.-C. Cryobiotechnology of apple (Malus spp.): Development, progress and future prospects. Plant Cell Rep. 2018;37:689–709. doi: 10.1007/s00299-018-2249-x. PubMed DOI
Panis B. Sixty years of plant cryopreservation: From freezing hardy mulberry twigs to establishing reference crop collections for future generations. Acta Hortic. 2019:1–8. doi: 10.17660/ActaHortic.2019.1234.1. DOI
Zámečník J., Šesták J. Hot Topics in Thermal Analysis and Calorimetry. Volume 8. Springer; Singapore: 2010. Constrained States Occurring in Plants Cryo-Processing and the Role of Biological Glasses; pp. 291–310.
Benson E.E. Cryopreservation of Phytodiversity: A Critical Appraisal of Theory & Practice. Crit. Rev. Plant Sci. 2008;27:141–219. doi: 10.1080/07352680802202034. DOI
Hirsh A.G. Vitrification in plants as a natural form of cryoprotection. Cryobiology. 1987;24:214–228. doi: 10.1016/0011-2240(87)90024-1. PubMed DOI
Volk G.M., Walters C. Plant vitrification solution 2 lowers water content and alters freezing behavior in shoot tips during cryoprotection. Cryobiology. 2006;52:48–61. doi: 10.1016/j.cryobiol.2005.09.004. PubMed DOI
Grout B.W.W. Genetic Preservation of Plant Cells in Vitro. Springer; Singapore: 1995. Introduction to the in Vitro Preservation of Plant Cells, Tissues and Organs; pp. 1–20.
Benson E.E. Plant Cryopreservation: A Practical Guide. Springer; New York, NY, USA: 2008. Cryopreservation theory; pp. 15–32.
Benson E.E. Plant Conservation Biotechnology. CRC Press; Boca Raton, FL, USA: 1999. Cryopreservation; pp. 109–122.
Sakai A., Kobayashi S., Oiyama I. Cryopreservation of nucellar cells of navel orange (Citrus sinensis Osb. var. brasiliensis Tanaka) by vitrification. Plant Cell Rep. 1990;9:30–33. doi: 10.1007/BF00232130. PubMed DOI
Uragami A., Sakai A., Nagai M., Takahashi T. Survival of cultured cells and somatic embryos of Asparagus officinalis cryopreserved by vitrification. Plant Cell Rep. 1989;8:418–421. doi: 10.1007/BF00270083. PubMed DOI
Leunufna S., Keller E.R.J. Investigating a new cryopreservation protocol for yams (Dioscorea spp.) Plant Cell Rep. 2003;21:1159–1166. doi: 10.1007/s00299-003-0652-3. PubMed DOI
Jiroutová P., Sedlák J. Cryobiotechnology of Plants: A Hot Topic not Only for Gene Banks. Appl. Sci. 2020;10:4677. doi: 10.3390/app10134677. DOI
Roque-Borda C., Kulus D., de Souza A.V., Kaviani B., Vicente E. Cryopreservation of Agronomic Plant Germplasm Using Vitrification-Based Methods: An Overview of Selected Case Studies. Int. J. Mol. Sci. 2021;22:6157. doi: 10.3390/ijms22116157. PubMed DOI PMC
Agrawal A., Singh S., Malhotra E.V., Meena D.P.S., Tyagi R.K. In Vitro Conservation and Cryopreservation of Clonally Propagated Horticultural Species. In: Rajasekharan P., Rao V., editors. Conservation and Utilization of Horticultural Genetic Resources. Springer; New York, NY, USA: 2019. pp. 529–578.
Bettoni J.C., Bonnart R., Volk G.M. Challenges in implementing plant shoot tip cryopreservation technologies. Plant Cell Tissue Organ Cult. (PCTOC) 2021;144:21–34. doi: 10.1007/s11240-020-01846-x. DOI
Malik S.K., Chaudhury R. Conservation and Utilization of Horticultural Genetic Resources. Springer; Singapore: 2019. Cryopreservation Techniques for Conservation of Tropical Horticultural Species Using Various Explants; pp. 579–594.
Panis B., Lambardi M. Status of cryopreservation technologies in plants (crops and forest trees) Role Biotechnol. 2005;5:43–54.
Sakai P.A., Hirai D., Niino T. Plant Cryopreservation: A Practical Guide. Springer; Singapore: 2008. Development of PVS-Based Vitrification and Encapsulation–Vitrification Protocols; pp. 33–57.
Höfer M., Hanke M.-V. Cryopreservation of fruit germplasm. Vitr. Cell. Dev. Biol. Anim. 2017;53:372–381. doi: 10.1007/s11627-017-9841-6. DOI
Kulus D., Zalewska M. Cryopreservation as a tool used in long-term storage of ornamental species—A review. Sci. Hortic. 2014;168:88–107. doi: 10.1016/j.scienta.2014.01.014. DOI
Bi W.-L., Pan C., Hao X.-Y., Cui Z.-H., Kher M.M., Marković Z., Wang Q.-C., da Silva J.A.T. Cryopreservation of grapevine (Vitis spp.)—A review. In Vitro Cell. Dev. Biol. Plant. 2017;53:449–460. doi: 10.1007/s11627-017-9822-9. DOI
Yamamoto S., Rafique T., Fukui K., Sekizawa K., Niino T. V-cryo-plate procedure as an effective protocol for cryobanks: Case study of mint cryopreservation. Cryo Lett. 2012;33:12–23. PubMed
Yamamoto S.-I., Rafique T., Priyantha W.S., Fukui K., Matsumoto T., Niino T. Development of a cryopreservation procedure using aluminium cryo-plates. Cryo Lett. 2011;32:256–265. PubMed
Kim H.H., Yoon J.W., Park Y.E., Cho E.G., Sohn J.K., Kim T.K., Engelmann F. Cryopreservation of potato cultivated varieties and wild species: Critical factors in droplet vitrification. Cryo Lett. 2006;27:223–234. PubMed
Panis B., Nguyẽn T.n.T. Cryopreservation of Musa Germplasm. Volume 5 Bioversity International; Rome, Italy: 2001.
Carra A., Carimi F., Bettoni J.C., Pathirana R. Synthetic Seeds. Springer; Singapore: 2019. Progress and Challenges in the Application of Synthetic Seed Technology for Ex Situ Germplasm Conservation in Grapevine (Vitis spp.) pp. 439–467.
Fahy G.M., Wowk B., Wu J., Paynter S. Improved vitrification solutions based on the predictability of vitrification solution toxicity. Cryobiology. 2004;48:22–35. doi: 10.1016/j.cryobiol.2003.11.004. PubMed DOI
Teixeira A.S., González-Benito M.E., Molina-García A.D. Glassy State and Cryopreservation of Mint Shoot Tips. Biotechnol. Prog. 2013;29:707–717. doi: 10.1002/btpr.1711. PubMed DOI
Zámečník J., Faltus M., Bilavčík A., Kotková R. Current Frontiers Cryopreservation. IntechOpen; London, UK: 2012. Comparison of cryopreservation methods of vegetatively propagated crops based on thermal analysis; pp. 333–358.
Murashige T., Skoog F. A Revised Medium for Rapid Growth and Bio Assays with Tobacco Tissue Cultures. Physiol. Plant. 1962;15:473–497. doi: 10.1111/j.1399-3054.1962.tb08052.x. DOI
Santarius K.A. Freezing of Isolated Thylakoid Membranes in Complex Media. VII. The Effect of Bovine Serum Albumin. Biochem. Physiol. Pflanz. 1991;187:149–162. doi: 10.1016/S0015-3796(11)80119-8. DOI
Elmoazzen H., Elliott J., McGann L. Cryoprotectant equilibration in tissues. Cryobiology. 2005;51:85–91. doi: 10.1016/j.cryobiol.2005.05.003. PubMed DOI
Kanaze F.I., Kokkalou E., Niopas I., Georgarakis M., Stergiou A., Bikiaris D. Thermal analysis study of flavonoid solid dispersions having enhanced solubility. J. Therm. Anal. Calorim. 2006;83:283–290. doi: 10.1007/s10973-005-6989-9. DOI
Tao D., Li P.H. Classification of plant cell cryoprotectants. J. Theor. Biol. 1986;123:305–310. doi: 10.1016/S0022-5193(86)80245-4. DOI
Rall W.F., Fahy G.M. Ice-free cryopreservation of mouse embryos at −196 °C by vitrification. Nat. Cell Biol. 1985;313:573–575. doi: 10.1038/313573a0. PubMed DOI
Gao D., Liu J., Liu C., McGann L., Watson P., Kleinhans F., Mazur P., Critser E., Critser J. Andrology: Prevention of osmotic injury to human spermatozoa during addition and removal of glycerol. Hum. Reprod. 1995;10:1109–1122. doi: 10.1093/oxfordjournals.humrep.a136103. PubMed DOI
Hubálek Z. Protectants used in the cryopreservation of microorganisms. Cryobiology. 2003;46:205–229. doi: 10.1016/S0011-2240(03)00046-4. PubMed DOI
Golan M., Jelinkova S., Kratochvilova I., Skládal P., Pešl M., Rotrekl V., Pribyl J. AFM Monitoring the Influence of Selected Cryoprotectants on Regeneration of Cryopreserved Cells Mechanical Properties. Front. Physiol. 2018;9:804. doi: 10.3389/fphys.2018.00804. PubMed DOI PMC
Gerber D.W., Byerrum R.U., Gee R.W., Tolbert N. Glycerol concentrations in crop plants. Plant Sci. 1988;56:31–38. doi: 10.1016/0168-9452(88)90182-3. DOI
Sillanpää M., Ncibi C. A Sustainable Bioeconomy. Springer; Berlin/Heidelberg, Germany: 2017. Biochemicals; pp. 141–183.
Warner R.M., Ampo E., Nelson D., Benson J.D., Eroglu A., Higgins A.Z. Rapid quantification of multi-cryoprotectant toxicity using an automated liquid handling method. Cryobiology. 2021;98:219–232. doi: 10.1016/j.cryobiol.2020.10.017. PubMed DOI PMC
Suzuki M., Tandon P., Ishikawa M., Toyomasu T. Development of a new vitrification solution, VSL, and its application to the cryopreservation of gentian axillary buds. Plant Biotechnol. Rep. 2008;2:123–131. doi: 10.1007/s11816-008-0056-5. DOI
Nishizawa S., Sakai A., Amano Y., Matsuzawa T. Cryopreservation of asparagus (Asparagus officinalis L.) embryogenic suspension cells and subsequent plant regeneration by vitrification. Plant Sci. 1993;91:67–73. doi: 10.1016/0168-9452(93)90189-7. DOI
Lu Z., Liu C.T. A new approach to understanding and measuring glass formation in bulk amorphous materials. Intermetallics. 2004;12:1035–1043. doi: 10.1016/j.intermet.2004.04.032. DOI
Kuleshova L., Mac Farlaneb D.R., Trounson A., Shaw J. Sugars Exert a Major Influence on the Vitrification Properties of Ethylene Glycol-Based Solutions and Have Low Toxicity to Embryos and Oocytes. Cryobiology. 1999;38:119–130. doi: 10.1006/cryo.1999.2153. PubMed DOI
Murthy S., Singh G. Examination of the concentration dependence of Tg of binary aqueous solutions. Thermochim. Acta. 2008;469:116–119. doi: 10.1016/j.tca.2008.01.007. DOI
Jonnalagadda S., Robinson D.H. Effect of the inclusion of PEG on the solid-state properties and drug release from polylactic acid films and microcapsules. J. Appl. Polym. Sci. 2004;93:2025–2030. doi: 10.1002/app.20667. DOI
Zondervan R., Kulzer F., Berkhout G.C.G., Orrit M. Local viscosity of supercooled glycerol near Tg probed by rotational diffusion of ensembles and single dye molecules. Proc. Natl. Acad. Sci. USA. 2007;104:12628–12633. doi: 10.1073/pnas.0610521104. PubMed DOI PMC
Talja R.A., Roos Y.H. Phase and state transition effects on dielectric, mechanical, and thermal properties of polyols. Thermochim. Acta. 2001;380:109–121. doi: 10.1016/S0040-6031(01)00664-5. DOI
Simperler A., Kornherr A., Chopra R., Bonnet P.A., Jones W., Motherwell A.W.D.S., Zifferer G. Glass Transition Temperature of Glucose, Sucrose, and Trehalose: An Experimental and in Silico Study. J. Phys. Chem. B. 2006;110:19678–19684. doi: 10.1021/jp063134t. PubMed DOI
Roberts A., Finnigan W., Kelly P., Faulkner M., Breitling R., Takano E., Scrutton N., Blaker J., Hay S. Non-covalent protein-based adhesives for transparent substrates—Bovine serum albumin vs. recombinant spider silk. Mater. Today Bio. 2020;7:100068. doi: 10.1016/j.mtbio.2020.100068. PubMed DOI PMC
Anonym Data Safety Sheet—Formamide. 2015. [(accessed on 27 November 2021)]. Available online: https://www.carlroth.com/medias/SDB-4095-IE-EN.pdf?context=bWFzdGVyfHNlY3VyaXR5RGF0YXNoZWV0c3wyNjc1NzV8YXBwbGljYXRpb24vcGRmfHNlY3VyaXR5RGF0YXNoZWV0cy9oNzIvaDc2LzkwNDYwODU3MzAzMzQucGRmfDUyOGVmNzI4NzM3MmU1NDQwYmIzZDYwODI5OTYxNDU2NmZhOWJlNTVkMzVlOWRlZTk2NjQyNjNkYzliMzI0OTk.
Matsumoto T. Cryopreservation of Plant Genetic Resources: Conventional and New Methods. Rev. Agric. Sci. 2017;5:13–20. doi: 10.7831/ras.5.13. DOI
Vozovyk K., Bobrova O., Prystalov A., Shevchenko N., Kuleshova L. Amorphous state stability of plant vitrification solutions. Biologija. 2020;66:66. doi: 10.6001/biologija.v66i1.4190. DOI
Matsumoto T., Sakai A., Yamada K. Cryopreservation of in vitro-grown apical meristems of wasabi (Wasabia japonica) by vitrification and subsequent high plant regeneration. Plant Cell Rep. 1994;13:442–446. doi: 10.1007/BF00231963. PubMed DOI
Kawai K., Suzuki T., Oguni M. Low-Temperature Glass Transitions of Quenched and Annealed Bovine Serum Albumin Aqueous Solutions. Biophys. J. 2006;90:3732–3738. doi: 10.1529/biophysj.105.075986. PubMed DOI PMC
Kim H.-H., Lee Y.-G., Shin D.-J., Ko H.-C., Gwag J.-G., Cho E.-G., Engelmann F. Development of alternative plant vitrification solutions in droplet-vitrification procedures. Cryo Lett. 2009;30:320–334. doi: 10.17660/ActaHortic.2011.908.20. PubMed DOI
Notman R., Noro M., O’Malley B., Anwar J. Molecular Basis for Dimethylsulfoxide (DMSO) Action on Lipid Membranes. J. Am. Chem. Soc. 2006;128:13982–13983. doi: 10.1021/ja063363t. PubMed DOI
Kim H.-H., Kim J.-B., Baek H.-J., Cho E.-G., Chae Y.-A., Engelmann F. Evolution of DMSO concentration in garlic shoot tips during a vitrification procedure. Cryo Lett. 2004;25:91–100. PubMed
Kim J.-B., Kim H.-H., Baek H.-J., Cho E.-G., Kim Y.-H., Engelmann F. Changes in sucrose and glycerol content in garlic shoot tips during freezing using PVS3 solution. Cryo Lett. 2005;26:103–112. PubMed
Volk G.M., Harris J.L., Rotindo K.E. Survival of mint shoot tips after exposure to cryoprotectant solution components. Cryobiology. 2006;52:305–308. doi: 10.1016/j.cryobiol.2005.11.003. PubMed DOI
Hakura A., Mochida H., Yamatsu K. Dimethyl sulfoxide (DMSO) is mutagenic for bacterial mutagenicity tester strains. Mutat. Res. Lett. 1993;303:127–133. doi: 10.1016/0165-7992(93)90025-Q. PubMed DOI
Kapp R., Jr., Eventoff B. Mutagenicity of dimethylsulfoxide (DMSO): In vivo cytogenetics study in the rat. Teratog. Carcinog. Mutagenesis. 1981;1:141–145. doi: 10.1002/tcm.1770010203. PubMed DOI
Vogin E.E., Carson S., Cannon G., Linegar C.R., Rubin L.F. Chronic toxicity of DMSO in primates. Toxicol. Appl. Pharmacol. 1970;16:606–612. doi: 10.1016/0041-008X(70)90065-7. PubMed DOI
Halmagyi A., Valimareanu S., Coste A., Deliu C., Isac V. Cryopreservation of Malus shoot tips and subsequent plant regeneration. Rom. Biotechnol. Lett. 2010;15:80.
Volk G. Application of Functional Genomics and Proteomics to Plant Cryopreservation. Curr. Genom. 2010;11:24–29. doi: 10.2174/138920210790217945. PubMed DOI PMC
Franceschi V.R., Horner H.T. Calcium oxalate crystals in plants. Bot. Rev. 1980;46:361–427. doi: 10.1007/BF02860532. DOI
Prychid C.J., Jabaily R.S., Rudall P. Cellular Ultrastructure and Crystal Development in Amorphophallus (Araceae) Ann. Bot. 2008;101:983–995. doi: 10.1093/aob/mcn022. PubMed DOI PMC
Ranjbar H., Ahmadi H., Sheshdeh R.K., Ranjbar H. Application of relative sensitivity function in parametric optimization of a tri-ethylene glycol dehydration plant. J. Nat. Gas Sci. Eng. 2015;25:39–45. doi: 10.1016/j.jngse.2015.04.028. DOI
Bhattacharya S. Cryopreservation Biotechnology in Biomedical and Biological Sciences. IntechOpen; London, UK: 2018. Cryoprotectants and their usage in cryopreservation process; p. 7.
Steuter A.A., Mozafar A., Goodin J.R. Water Potential of Aqueous Polyethylene Glycol. Plant Physiol. 1981;67:64–67. doi: 10.1104/pp.67.1.64. PubMed DOI PMC
Popova E., Bukhov N., Popov A., Kim H.-H. Cryopreservation of protocorm-like bodies of the hybrid orchid Bratonia (Miltonia flavescens × Brassia longissima) Cryo Lett. 2010;31:426–437. PubMed
Fuller B.J. Cryoprotectants: The essential antifreezes to protect life in the frozen state. Cryo Lett. 2004;25:375–388. PubMed
Sipen P., Anthony P., Davey M.R. Cryopreservation of scalps of Malaysian bananas using a pre-growth method. Cryo Lett. 2011;32:197–205. PubMed
Acker J.P., McGann L.E. Protective effect of intracellular ice during freezing? Cryobiology. 2003;46:197–202. doi: 10.1016/S0011-2240(03)00025-7. PubMed DOI
Bryant G., Koster K.L., Wolfe J. Membrane behaviour in seeds and other systems at low water content: The various effects of solutes. Seed Sci. Res. 2001;11:17–25. doi: 10.1079/SSR200056. DOI
Shendurse A., Khedkar C. Glucose: Properties and analysis. Encycl. Food Health. 2016;3:239–247.
Bhandari B.R., Roos Y.H. Dissolution of sucrose crystals in the anhydrous sorbitol melt. Carbohydr. Res. 2003;338:361–367. doi: 10.1016/S0008-6215(02)00466-4. PubMed DOI
Göldner E.M., Seitz U., Reinhard E. Cryopreservation of Digitalis lanata Ehrh. cell cultures: Preculture and freeze tolerance. Plant Cell Tissue Organ Cult. 1991;24:19–24. doi: 10.1007/BF00044260. DOI
Salaj T., Matusikova I., Panis B., Swennen R., Salaj J. Recovery and characterisation of hybrid firs (Abies alba × A. cephalonica, Abies alba × A. numidica) embryogenic tissues after cryopreservation. Cryo Lett. 2010;31:206–217. PubMed
Subramanian S., Raj A., Kumar R., Rana S.K., Jha A.K., Gautam S. Isolation, Culturing and cryopreservation of putative granulosa stem cells from buffalo ovaries. Int. J. Cell Sci. Biotechnol. 2014;4:20–25.
Carpenter J.F., Crowe J.H. The mechanism of cryoprotection of proteins by solutes. Cryobiology. 1988;25:244–255. doi: 10.1016/0011-2240(88)90032-6. PubMed DOI
Santarius K.A., Giersch C. Cryopreservation of spinach chloroplast membranes by low-molecular-weight carbohydrates: II. Discrimination between colligative and noncolligative protection. Cryobiology. 1983;20:90–99. doi: 10.1016/0011-2240(83)90063-9. PubMed DOI
Sikora A., Dupanov V.O., Kratochvíl J., Zamecnik J. Transitions in Aqueous Solutions of Sucrose at Subzero Temperatures. J. Macromol. Sci. Part B. 2007;46:71–85. doi: 10.1080/00222340601036819. DOI
Sakai A., Kobayashi S., Oiyama I. Survival by Vitrification of Nucellar Cells of Navel Orange (Citrus sinensis var. brasiliensis Tanaka) Cooled to −196 °C. J. Plant Physiol. 1991;137:465–470. doi: 10.1016/S0176-1617(11)80318-4. PubMed DOI
Sopalun K., Kanchit K., Ishikawa K. Vitrification-based cryopreservation of Grammatophyllum speciosum protocorm. Cryo Lett. 2010;31:347–357. PubMed
Horvath A., Wayman W.R., Urbányi B., Ware K.M., Dean J.C., Tiersch T.R. The relationship of the cryoprotectants methanol and dimethyl sulfoxide and hyperosmotic extenders on sperm cryopreservation of two North-American sturgeon species. Aquaculture. 2005;247:243–251. doi: 10.1016/j.aquaculture.2005.02.007. DOI
Bronshteyn V.L., Steponkus P.L. Nucleation and Growth of Ice Crystals in Concentrated Solutions of Ethylene Glycol. Cryobiology. 1995;32:1–22. doi: 10.1006/cryo.1995.1001. DOI
Rall W. Factors affecting the survival of mouse embryos cryopreserved by vitrification. Cryobiology. 1987;24:387–402. doi: 10.1016/0011-2240(87)90042-3. PubMed DOI
Turner S., Senaratna T., Touchell D., Bunn E., Dixon K., Tan B. Stereochemical arrangement of hydroxyl groups in sugar and polyalcohol molecules as an important factor in effective cryopreservation. Plant Sci. 2001;160:489–497. doi: 10.1016/S0168-9452(00)00420-9. PubMed DOI
Kim H.-H., Yoon J.-W., Kim J.-B., Engelmann F., Cho E.-G. Thermal analysis of garlic shoot tips during a vitrification procedure. Cryo Lett. 2005;26:33–44. PubMed
Wu Y., Zhao Y., Zhou M., Engelmann F. Plant Genetic Resources Network in East Asia. Proceedings of the Meeting for the Regional Network for Conservation and Use of Plant Genetic Resources in East Asia, Ulaanbaatar, Mongolia, 13–16 August 2001. International Plant Genetic Resources Institute (IPGRI); Rome, Italy: 2002. Cryopreservation of temperate fruit tree germplasm; pp. 77–88.
Kim H.-H., Popova E.V., Yi J.-Y., Cho G.-T., Park S.-U., Lee S.-C., Engelmann F. Cryopreservation of hairy roots of Rubia akane (Nakai) using a droplet-vitrification procedure. Cryo Lett. 2011;31:473–484. PubMed
Hong S., Yin M., Shao X., Wang A., Xu W. Cryopreservation of embryogenic callus of Dioscorea bulbifera by vitrification. Cryo Lett. 2009;30:64–75. PubMed
Cho E.G., Hor Y.L., Kim H.H., Rao V.R., Engelmann F. Cryopreservation of Citrus madurensis zygotic embryonic axes by vitrification: Importance of pregrowth and preculture conditions. Cryo Lett. 2002;22:391–396. PubMed
Ivchenko T.V., Vitsenya T.I., Shevchenko N.A., Bashtan N.O., Kornienko S.I. Hypothermic and Low-Temperature Storage of Garlic (Allium sativum L.) for in Vitro Collections. Probl. Cryobiol. Cryomedicine. 2017;27:110–120. doi: 10.15407/cryo27.02.110. DOI
Ishikawa K., Harata K., Mii M., Sakai A., Yoshimatsu K., Shimomura K. Cryopreservation of zygotic embryos of a Japanese terrestrial orchid (Bletilla striata) by vitrification. Plant Cell Rep. 1997;16:754–757. doi: 10.1007/s002990050314. PubMed DOI
Ray A., Bhattacharya S. Cryopreservation of in vitro grown nodal segments of Rauvolfia serpentina by PVS2 vitrification. Cryo Lett. 2009;29:321–328. PubMed
Sajini K.K., Karun A., Amamath C.H., Engelmann F. Cryopreservation of coconut (Cocos nucifera L.) zygotic embryos by vitrification. Cryo Lett. 2011;32:317–328. PubMed
Panis B., Swennen R. Society for Low Temperature Biology. Annual Scientific Meeting, AGM and Symposium. Validation, Safety and Ethical Issues Impacting the Low Temperature Storage of Biological Resources. Cryo Letters; Lewes, UK: 2007. Plant cryopreservation: Applications, constraints and prospects; pp. 1–29.
Tokatli Y.O., Akdemir H. Cryopreservation of Fraser photinia (Photinia × fraseri Dress.) via vitrification-based one-step freezing techniques. Cryo Lett. 2010;31:40–49. PubMed
Volk G.M., Maness N., Rotindo K. Cryopreservation of garlic (Allium sativum L.) using plant vitrification solution 2. Cryo Lett. 2004;25:219–226. PubMed
March G.G.-D., De Boucaud M.-T., Chmielarz P. Cryopreservation of Prunus avium L. embryogenic tissues. Cryo Lett. 2006;26:341–348. PubMed
Engelmann-Sylvestre I., Engelmann F. Cryopreservation of in vitro-grown shoot tips of Clinopodium odorum using aluminium cryo-plates. Vitr. Cell. Dev. Biol. Anim. 2015;51:185–191. doi: 10.1007/s11627-015-9668-y. DOI
Li B.-Q., Feng C.-H., Wang M.-R., Hu L.-Y., Volk G., Wang Q.-C. Recovery patterns, histological observations and genetic integrity in Malus shoot tips cryopreserved using droplet-vitrification and encapsulation-dehydration procedures. J. Biotechnol. 2015;214:182–191. doi: 10.1016/j.jbiotec.2015.09.030. PubMed DOI
Vollmer R., Villagaray R., Castro M., Anglin N., Ellis D. Cryopreserved potato shoot tips showed genotype-specific response to sucrose concentration in rewarming solution (RS) Plant Cell Tissue Organ Cult. (PCTOC) 2018;136:353–363. doi: 10.1007/s11240-018-1520-8. DOI
Wang M.-R., Zhang Z., Zámečník J., Bilavčík A., Blystad D.-R., Haugslien S., Wang Q.-C. Droplet-vitrification for shoot tip cryopreservation of shallot (Allium cepa var. aggregatum): Effects of PVS3 and PVS2 on shoot regrowth. Plant Cell Tissue Organ Cult. 2020;140:185–195. doi: 10.1007/s11240-019-01721-4. DOI
Bettoni J.C., Kretzschmar A.A., Bonnart R., Shepherd A., Volk G.M. Cryopreservation of 12 Vitis Species Using Apical Shoot Tips Derived from Plants Grown In Vitro. HortScience. 2019;54:976–981. doi: 10.21273/HORTSCI13958-19. DOI
Hammond S.D.H., Viehmannova I., Zamecnik J., Panis B., Faltus M. Droplet-vitrification methods for apical bud cryopreservation of yacon [Smallanthus sonchifolius (Poepp. and Endl.) H. Rob.] Plant Cell Tissue Organ Cult. (PCTOC) 2021;147:197–208. doi: 10.1007/s11240-021-02116-0. DOI
Niedermeyer W., Parish G.R., Moor H. Reactions of yeast cells to glycerol treatment alterations to membrane structure and glycerol uptake. Protoplasma. 1977;92:177–193. doi: 10.1007/BF01279457. PubMed DOI
Brison M., de Boucaud M.-T., Dosba F. Cryopreservation of in vitro grown shoot tips of two interspecific Prunus rootstocks. Plant Sci. 1995;105:235–242. doi: 10.1016/0168-9452(94)04045-1. DOI
Serrano-Martinez F., Casas J.L. Cryopreservation of Tetraclinis articulata (vahl.) Masters. Cryo Lett. 2011;32:248–255. PubMed
Maruyama E., Kinoshita I., Ishii K., Ohba K., Sakai A. Germplasm conservation of Guazuma crinita, a useful tree in the Peru-Amazon, by the cryopreservation of in vitro-cultured multiple bud clusters. Plant Cell Tissue Organ Cult. (PCTOC) 1997;48:161–165. doi: 10.1023/A:1005858324187. DOI
Wang Q., Batuman Ö., Li P., Bar-Joseph M., Gafny R. A simple and efficient cryopreservation of in vitro-grown shoot tips of Troyer’citrange [Poncirus trifoliata (L.) Raf. × Citrus sinensis (L.) Osbeck.] by encapsulation-vitrification. Euphytica. 2002;128:135–142. doi: 10.1023/A:1020683305690. DOI
Vujović T., Jevremović D., Marjanović T., Ružić Đ. Cryopreservation of Serbian autochthonous plum ‘Crvena Ranka’ using aluminium cryo-plates. Genetika. 2021;53:283–294. doi: 10.2298/GENSR2101283V. DOI
Lambardi M., Fabbri A., Caccavale A. Cryopreservation of white poplar (Populus alba L.) by vitrification of in vitro-grown shoot tips. Plant Cell Rep. 2000;19:213–218. doi: 10.1007/s002990050001. PubMed DOI
Shin D.J., Kong H., Popova E.V., Moon H.K., Park S.Y., Park S.-U., Lee S.C., Kim H.H. Cryopreservation of Kalopanax septemlobus embryogenic callus using vitrification and droplet-vitrification. Cryo Lett. 2012;33:402–410. PubMed
Barraco G., Sylvestre I., Iapichino G., Engelmann F. Investigating the cryopreservation of nodal explants of Lithodora rosmarinifolia (Ten.) Johnst., a rare, endemic Mediterranean species. Plant Biotechnol. Rep. 2012;7:141–146. doi: 10.1007/s11816-012-0241-4. DOI
Lee Y.-Y., Balaraju K., Song J.-Y., Yi J.-Y., Lee S.-Y., Lee J.-R., Yoon M., Kim H.-H. Cryopreservation of in vitro grown shoot tips of strawberry (Fragaria × ananassa Duch.) genetic resources by droplet-vitrification. Korean J. Plant Resour. 2019;32:689–697.
Sakai A. Cryopreservation of Tropical Plant Germplasm: Current Research Progress and Application. CGIAR; Montpellier, France: 2000. Development of cryopreservation techniques; pp. 1–7.
Langis R., Schnabel B., Earle E., Steponkus P. Cryopreservation of Brassica campestris L. cell suspensions by vitrification. Cryo Lett. 1989;10:421–428.
Kim H.-H., Cho E.-G., Baek H.-J., Kim C.-Y., Keller E.R.J., Engelmann F. Cryopreservation of garlic shoot tips by vitrification: Effects of dehydration, rewarming, unloading and regrowth conditions. Cryo Lett. 2004;25:59–70. PubMed
Towill L. Cryopreservation of isolated mint shoot tips by vitrification. Plant Cell Rep. 1990;9:178–180. doi: 10.1007/BF00232174. PubMed DOI
Grospietsch M., Stodulkova E., Zamecnik J. Effect of osmotic stress on the dehydration tolerance and cryopreservation of Solanum tuberosum shoot tips. Cryo Lett. 1999;20:339–346.
Suranthran P., Gantait S., Sinniah U.R., Subramaniam S., Alwee S.S.R.S., Roowi S.H. Effect of loading and vitrification solutions on survival of cryopreserved oil palm polyembryoids. Plant Growth Regul. 2012;66:101–109. doi: 10.1007/s10725-011-9633-7. DOI
Mallon R., Bunn E., Turner S.R., Gonzalez M.L. Cryopreservation of Centaurea ultreiae (Compositae) a critically endangered species from Galicia (Spain) Cryo Lett. 2008;29:363–370. PubMed
Turner S.R., Senaratna T., Bunn E., Tan B., Dixon K., Touchell D.H. Cryopreservation of Shoot Tips from Six Endangered Australian Species using a Modified Vitrification Protocol. Ann. Bot. 2001;87:371–378. doi: 10.1006/anbo.2000.1346. DOI
Halmagyi A., Deliu C., Coste A., Keul M., Cheregi O., Cristea V. Vitrification of potato shoot tips for germplasm cryopreservation. Contrib. Bot. 2004;39:187–193.
Shevchenko N., Mozgovska A., Bobrova O., Bashtan N., Kovalenko G., Ivchenko T. Post-Thaw Survival of Meristems from In Vitro Sweet Potato (Ipomoea batatas (L.) Lam.) Plants. Biol. Life Sci. Forum. 2020;4:43. doi: 10.3390/IECPS2020-08769. DOI
Watanabe K., Steponkus P.L. Vitrification of Oryza sativa L. cell suspensions. Cryo Lett. 1995;16:255–262.
Folgado R., Panis B., Sergeant K., Renaut J., Swennen R., Hausman J.-F. Unravelling the effect of sucrose and cold pretreatment on cryopreservation of potato through sugar analysis and proteomics. Cryobiology. 2015;71:432–441. doi: 10.1016/j.cryobiol.2015.09.006. PubMed DOI
Dumet D., Grapin A., Bailly C., Dorion N. Revisiting crucial steps of an encapsulation/desiccation based cryopreservation process: Importance of thawing method in the case of Pelargonium meristems. Plant Sci. 2002;163:1121–1127. doi: 10.1016/S0168-9452(02)00323-0. DOI
Matsumoto T. An approach to enhance dehydration tolerance of alginate-coated dried meristems cooled to −196 °C. Cryo Lett. 1995;16:299–306.
Reed B.M. Plant Cryopreservation: A Practical Guide. Springer; Berlin/Heidelberg, Germany: 2008. Cryopreservation—Practical considerations; pp. 3–13.
Sakai A., Engelmann F. Vitrification, encapsulation-vitrification and droplet-vitrification: A review. Cryo Lett. 2007;28:151–172. PubMed
Volk G.M., Shepherd A.N., Bonnart R. Successful Cryopreservation of Vitis Shoot Tips: Novel Pre-treatment Combinations Applied to Nine Species. Cryo Lett. 2019;39:322–330. PubMed
Benelli C., Carvalho L., EL Merzougui S., Petruccelli R. Two Advanced Cryogenic Procedures for Improving Stevia rebaudiana (Bertoni) Cryopreservation. Plants. 2021;10:277. doi: 10.3390/plants10020277. PubMed DOI PMC
O’Brien C., Hiti-Bandaralage J.C.A., Folgado R., Lahmeyer S., Hayward A., Folsom J., Mitter N. First report on cryopreservation of mature shoot tips of two avocado (Persea americana Mill.) rootstocks. Plant Cell Tissue Organ Cult. (PCTOC) 2021;144:103–113. doi: 10.1007/s11240-020-01861-y. DOI
Sharma S., Parasher K., Mukherjee P., Sharma Y.P. Cryopreservation of a Threatened Medicinal Plant, Valeriana Jatamansi Jones, Using Vitrification and Assessment of Biosynthetic Stability of Regenerants. Cryo Lett. 2021;42:300–308. PubMed
Fahy G.M., Macfarlane D.R., Angell C.A., Meryman H.T. Vitrification as an approach to cryopreservation. Cryobiology. 1984;21:407–426. doi: 10.1016/0011-2240(84)90079-8. PubMed DOI
Kim H.-H., Lee J.-K., Yoon J.-W., Ji J.-J., Nam S.-S., Hwang H.-S., Cho E.-G., Engelmann F. Cryopreservation of garlic bulbil primordia by the droplet-vitrification procedure. Cryo Lett. 2006;27:143–153. PubMed
Kartha K., Leung N., Mroginski L. In vitro Growth Responses and Plant Regeneration from Cryopreserved Meristems of Cassava (Manihot esculenta Crantz) Zeitschrift für Pflanzenphysiologie. 1982;107:133–140. doi: 10.1016/S0044-328X(82)80099-8. DOI
Ellis D., Skogerboe D., Andre C., Hellier B., Volk G. Implementation of garlic cryopreservation techniques in the national plant germplasm system. Cryo Lett. 2006;27:99–106. PubMed
Tanaka D., Niino T., Isuzugawa K., Hikage T., Uemura M. Cryopreservation of shoot apices of in-vitro grown gentian plants: Comparison of vitrification and encapsulation-vitrification protocols. Cryo Lett. 2004;25:167–176. PubMed
Kaczmarczyk A., Shvachko N., Lupysheva Y., Hajirezaei M.-R., Keller E.R.J. Influence of alternating temperature preculture on cryopreservation results for potato shoot tips. Plant Cell Rep. 2008;27:1551–1558. doi: 10.1007/s00299-008-0574-1. PubMed DOI PMC
Schaefer-Menuhr A., Schumacher H.-M., Mix-Wagner G. Long-term storage of old potato varieties by cryopreservation of meristems in liquid nitrogen. Landbauforsch. Voelkenrode. 1994;44:301–313.
Martinez-Montero M.E., Martinez J., Engelmann F. Cryopreservation of sugarcane somatic embryos. Cryo Lett. 2008;29:229–242. PubMed
Senula A.D., Keller E.R.J., Sanduijav T., Yohannes T. Cryopreservation of cold-acclimated mint (Mentha spp.) shoot tips using a simple vitrification protocol. Cryo Lett. 2007;28:1–12. PubMed
Bettoni J.C., Marković Z., Bi W., Volk G.M., Matsumoto T., Wang Q.-C. Grapevine Shoot Tip Cryopreservation and Cryotherapy: Secure Storage of Disease-Free Plants. Plants. 2021;10:2190. doi: 10.3390/plants10102190. PubMed DOI PMC
Panis B., Nagel M., Houwe I.V.D. Challenges and Prospects for the Conservation of Crop Genetic Resources in Field Genebanks, in In Vitro Collections and/or in Liquid Nitrogen. Plants. 2020;9:1634. doi: 10.3390/plants9121634. PubMed DOI PMC
Gámez-Pastrana R., González-Arnao M.T., Martínez-Ocampo Y., Engelmann F. Thermal events in calcium alginate beads during encapsulation dehydration and encapsulation-vitrification protocols. Acta Hortic. 2011;908:47–54. doi: 10.17660/ActaHortic.2011.908.3. DOI
Funnekotter B., Mancera R.L., Bunn E. Advances in understanding the fundamental aspects required for successful cryopreservation of Australian flora. Vitr. Cell. Dev. Biol. Anim. 2017;53:289–298. doi: 10.1007/s11627-017-9850-5. DOI
Funnekotter B., Bunn E., Mancera R.L. Cryo-mesh: A simple alternative cryopreservation protocol. Cryo Lett. 2017;38:155–159. PubMed
Nadarajan J., Pritchard H.W. Biophysical Characteristics of Successful Oilseed Embryo Cryoprotection and Cryopreservation Using Vacuum Infiltration Vitrification: An Innovation in Plant Cell Preservation. PLoS ONE. 2014;9:e96169. doi: 10.1371/journal.pone.0096169. PubMed DOI PMC
Bruňáková K., Zámečník J., Urbanová M., Čellárová E. Dehydration status of ABA-treated and cold-acclimated Hypericum perforatum L. shoot tips subjected to cryopreservation. Thermochim. Acta. 2011;525:62–70. doi: 10.1016/j.tca.2011.07.022. DOI
Šesták J., Zamecnik J. Can clustering of liquid water and thermal analysis be of assistance for better understanding of biological germplasm exposed to ultra-low temperatures. J. Therm. Anal. Calorim. 2007;88:411–416. doi: 10.1007/s10973-006-8232-8. DOI