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Advances in cryopreservation of in vitro-derived propagules: technologies and explant sources

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Abstract

Genetic improvements in plant breeding are dependent upon having access to novel plant genetic resources that are available in plant genebanks. Many crops that are vegetatively-propagated are maintained as plants in the field or greenhouse, making them vulnerable to biotic and abiotic threats. Increasingly, plant genebanks are using cryopreservation technologies to secure vegetatively propagated collections at secondary locations. Droplet vitrification and cryo-plate cryopreservation methods have been used to successfully cryopreserve the shoot tips of many plant species. New propagule types, including small leaf square-bearing adventitious buds, stem disc-bearing adventitious buds, microtubers and rhizome buds are alternative explants for use in cryopreservation. This review describes new technologies for in-vitro based cryopreservation systems that have advanced the field of plant cryopreservation. Future advances will allow even more diverse germplasm to be successfully preserved in cryobanks.

Key message

New technologies for in-vitro based cryopreservation systems have advanced the field of plant cryopreservation since the twenty first century. Further advances will certainly facilitate even more diverse germplasm to be successfully preserved in cryobanks.

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Abbreviations

ABIM:

Adventitious bud induction medium

AFLP:

Amplified fragment length polymorphism

AD:

Apical dome

D Cryo-plate:

Dehydration cryo-plate

DMSO:

Dimethyl sulfoxide

ISSR:

Inter simple sequence repeat

LN:

Liquid nitrogen

LNV:

Liquid nitrogen vapor

LP:

Leaf primordium

LS:

Loading solution

MSAP:

Methylation-sensitive amplified polymorphism

MS:

Murashige and Skoog (1962) medium

PGR:

Plant growth regulator

PVS:

Plant vitrification solution

PVS2:

Plant vitrification solution 2

PVS3:

Plant vitrification solution 3

RAPD:

Random amplified polymorphic DNA

SD-BABs:

Stem disc-bearing adventitious buds

SSR:

Simple sequence repeat

SLS-BABs:

Small leaf square-bearing adventitious buds

V Cryo-plate:

Vitrification cryo-plate

References

  • Arizaga MV, Villalobos Navarro OF, Castillo Martinez CR, Cruz Gutiérrez EJ, López Delgado HA, Watanabe K, Yamamoto SI, Niino T (2017a) Improvement to the D cryo-plate protocol applied to practical cryopreservation of in vitro grown potato shoot tips. Hortic J. https://doi.org/10.2503/hortj.OKD-2002

    Article  Google Scholar 

  • Arizaga MV, Yamamoto SI, Tanaka D, Fukui K, Nohara N, Nishikawa T, Watanabe KN (2017b) Cryopreservation of in vitro shoot tips of ulluco (Ullucus tuberosus Cal.) using D cryo-plate method. CryoLetters 38:419–427

    PubMed  Google Scholar 

  • Arizaga MV, Cancino GS, Iñiguez JC, Gutiérrez EJC, Reyes LAG, Yamamoto S, Tanaka D, Vazquez SGO, Watanabe K, Niino T (2019) Cryopreservation of in vitro shoot tips of chayote (Sechium spp.) by D cryo-plate method. Acta Hortic 1234:293–299

    Google Scholar 

  • Banasiak M, Snyman SJ (2017) Exploring in vitro germplasm conservation options for sugarcane (Saccharum spp. hybrids) in South Africa. In Vitro Cell Dev Biol-Plant 53:402–409

    Google Scholar 

  • Bednarek PT, Orłowska R (2019) Plant tissue culture environment as a switch-key of (epi)genetic changes. Plant Cell Tissue Org Cult. https://doi.org/10.1007/s11240-019-01724-1

    Article  Google Scholar 

  • Benelli C, De Carlo A, Engelmann F (2013) Recent advances in the cryopreservation of shoot-derived germplasm of economically important fruit trees of Actinidia, Diospyros, Malus, Olea, Prunus. Biotechnol Adv 31:175–185

    CAS  PubMed  Google Scholar 

  • Benson EE (2008) Cryopreservation of phytodiversity: a critical appraisal of theory & practice. Crit Rev Plant Sci 27:141–219

    CAS  Google Scholar 

  • Bettoni JC, Bonnart R, Shepherd AN, Kretzschmar AA, Volk GM (2019a) Cryopreservation of grapevine (Vitis spp.) shoot tips from growth chamber-sourced plants and histological observations. Vitis 58:71–78

    CAS  Google Scholar 

  • Bettoni JC, Bonnart R, Shepherd AN, Kretzschmar AA, Volk GM (2019b) Modifications to a Vitis shoot tip cryopreservation procedure: effect of shoot tip size and use of cryoplates. CryoLetters 40:103–112

    PubMed  Google Scholar 

  • Bi W-L, Pan C, Liu J, Wang Q-C (2016) Greenhouse performance, genetic stability and biochemical compounds in Chrysanthemum morifolium ‘Hangju’ plants regenerated from cryopreserved shoot tips. Acta Physiol Plant 38:268. https://doi.org/10.1007/s11738-016-2288-2

    Article  CAS  Google Scholar 

  • Bi W-L, Pan C, Hao X-Y, Cui Z-H, Kher MM, Marković Z, Wang Q-C, da TeixeiraSilva JA (2017) Cryopreservation of grapevine (Vitis spp.)—a review. Vitro Cell Dev Biol-Plant 53:449–460

    CAS  Google Scholar 

  • Bi W-L, Hao X-Y, Cui Z-H, Volk GM, Wang Q-C (2018) Droplet-vitrification cryopreservation of in vitro-grown shoot tips of grapevine (Vitis spp.). In Vitro Cell Dev Biol-Plant 54:590–599

    Google Scholar 

  • Carmona-Martín E, Regalado JJ, Padilla IMG, Westendorp N, Encina CL (2014) A new and efficient micropropagation method and its breeding applications in Asparagusgenera. Plant Cell Tissue Org Cult 119:479–488

    Google Scholar 

  • Carmona-Martín E, Regalado JJ, Perán-Quesada R, Encina CL (2018) Cryopreservation of rhizome buds of Asparagus officinalis L. (cv. Morado de Huétor) and evaluation of their genetic stability. Plant Cell Tissue Org Cult 133:395–403

    Google Scholar 

  • Cervera M, Navarro A, Navarro L, Peña L (2008) Production of transgenic adult plants from clementine mandarin by enhancing cell competence for transformation and regeneration. Tree Physiol 28:55–66

    CAS  PubMed  Google Scholar 

  • Chen T-Y, Chen J-T, Chang W-C (2002) Multiple shoot formation and plant regeneration from stem nodal explants of Paphiopedilum orchids. In Vitro Cell Dev Biol-Plant 38:595–597

    CAS  Google Scholar 

  • Chen H-Y, Liu J, Pan C, Yu J-W, Wang Q-C (2018) In vitro regeneration of adventitious buds from leaf explants and their subsequent cryopreservation in highbush blueberry. Plant Cell Tissue Org Cult 134:193–204

    CAS  Google Scholar 

  • Chua SP, Normah MN (2011) Effect of preculture, PVS2 and vitamin C on survival of recalcitrant Nephelium ramboutan-ake shoot tips after cryopreservation by vitrification. CryoLetters 32:506–515

    CAS  PubMed  Google Scholar 

  • Condello E, Caboni E, Andrè E, Piette B, Druart P, Swennen R, Panis B (2011) Cryopreservation of apple in vitro axillary buds using droplet-vitrification. CryoLetters 32:175–185

    CAS  PubMed  Google Scholar 

  • Cordeiro LS, Simões-Gurgel C, Albarello N, Engelmann F (2015) Cryopreservation of in vitro-grown shoot tips of Cleome rosea Vahl (Cleomaceae) using the V cryo-plate technique. In Vitro Cell Dev Biol-Plant 51:688–695

    CAS  Google Scholar 

  • Curtis IS, Mirkov TE (2012) Influence of surfactants on growth and regeneration from mature internodal stem segments of sweet orange (Citrus sinensis) cv. Hamlin. Plant Cell Tissue Org Cult 108:345–352

    CAS  Google Scholar 

  • De Carlo A, Benelli C, Lambardi M (2000) Development of a shoot-tip vitrification protocol and comparison with encapsulation-based procedures for plum (Prunus domestica L.) cryopreservation. CryoLetters 21:215–222

    PubMed  Google Scholar 

  • Dhungana SA, Kunitake H, Niino T, Yamamoto SI, Fukui K, Tanaka D, Maki S, Matsumoto T (2017) Cryopreservation of blueberry shoot tips derived from in vitro and current shoots using D cryo-plate technique. Plant Biotechnol. https://doi.org/10.5511/plantbiotechnology.16.1231b

  • Dumet D, Diebiru E, Adeyemi A, Akinyemi O, Gueye B, Franco J (2013) Cryopreservation for the 'in perpetuity' conservation of yam and cassava genetic resources. CryoLetters 34:107–118

    CAS  PubMed  Google Scholar 

  • Engelmann F (1997) In vitro conservation methods. In: Callow JA, Ford-Lloyd BV, Newbury HJ (eds) Biotechnology and plant genetic resources. CAB International, Oxford, pp 119–161

    Google Scholar 

  • Engelmann F (2000) Importance of cryopreservation for the conservation of plant genetic resources. In: Engelmann F and Takagi H (eds) Cryopreservation of tropical plant germplasm: current research progress and application. IPGRI, Tsukuba, pp 8–20

    Google Scholar 

  • Engelmann F (2011) Use of biotechnologies for the conservation of plant biodiversity. In Vitro Cell Dev Biol-Plant 47:5–16

    Google Scholar 

  • Engelmann F, Arnao MT, Wu Y, Escobar R (2008) Development of encapsulation dehydration. In: Reed BM (ed) Plant cryopreservation: a practical guide. Springer, New York, pp 59–75

    Google Scholar 

  • Engelmann-Sylvestre I, Engelmann F (2015) Cryopreservation of in vitro-grown shoot tips of Clinopodium odorum using aluminum cryo-plates. In Vitro Cell Dev Biol-Plant 51:185–191

    CAS  Google Scholar 

  • Espasandin FD, Brugnoli EA, Ayala PG, Ayala LP, Ruiz OA, Sansberro PA (2019) Long-term preservation of Lotus tenuis adventitious buds. Plant Cell Tissue Org Cult 136:373–382

    CAS  Google Scholar 

  • Fahy GM, MacFarlande DR, Angell CA, Meryman HT (1984) Vitrification as an approach to cryopreservation. Cryobiology 21:413–426

    Google Scholar 

  • Feng C-H, Yin Z-F, Ma Y-L, Chen L, Zhang Z-B, Wang B, Li B-Q, Huang Y-S, Wang Q-C (2011) Cryopreservation of sweetpotato (Ipomoea batatas) and its pathogen eradication by cryotherapy. Biotechnol Adv 29:84–93

    CAS  PubMed  Google Scholar 

  • Funnekotter B, Bunn E, Mancera RL (2017) Cryo-mesh: a simple alternative cryopreservation protocol. CryoLetters 38:155–159

    CAS  PubMed  Google Scholar 

  • Gallard A, Panis B, Dorion N, Swennen R, Grapin A (2008) Cryopreservation of Pelargonium apices by droplet-vitrification. CryoLetters 29:243–251

    PubMed  Google Scholar 

  • Gentile A, Monticelli S, Damiano C (2002) Adventitious shoot regeneration in peach [Prunus persica (L.) Batsch]. Plant Cell Rep 20:1011–1016

    CAS  Google Scholar 

  • Gisbert C, Dabauza M, Correal E, Swennen R, Panis B (2015) Cryopreservation of Bituminaria bituminosa varieties and hybrids. Cryobiology 71:279–285

    CAS  PubMed  Google Scholar 

  • Harding K (2004) Genetic integrity of cryopreserved plant cells: a review. CryoLetters 25:3–22

    PubMed  Google Scholar 

  • Harvengt L, Meier-Dinkel A, Dumas E, Collin E (2004) Establishment of a cryopreserved gene bank of European elms. Can J For Res 34:43–55

    Google Scholar 

  • Höfer M, Hanke M-V (2017) Cryopreservation of fruit germplasm. In Vitro Cell Dev Biol-Plant 53:372–381

    Google Scholar 

  • Ibrahim S, Normah MN (2013) The survival of in vitro shoot tips of Garcinia mangostana L. after cryopreservation by vitrification. Plant Growth Regul 70:237–246

    CAS  Google Scholar 

  • Imsomboon T, Thammasiri K, Kosiyajinda P, Chuenboonngarm N, Panvisavas N (2019) Cryopreservation of non-precultured protocorms of Acampe rigida (Buch.-Ham. ex Sm.) using V cryo-plate and D cryo-plate methods. Acta Hortic 1234:269–278

    Google Scholar 

  • Jenderek MM, Reed BM (2017) Cryopreserved storage of clonal germplasm in the USDA National Plant Germplasm System. In Vitro Cell Dev Biol-Plant 53:299–308

    CAS  Google Scholar 

  • Kaczmarczyk A, Rokka V-M, Keller ERJ (2011) Potato shoot tip cryopreservation—a review. Potato Res 54:45–79

    Google Scholar 

  • Kartha KK (1985) Cryopreservation of plant cell and organs. CRC Press, Boca Raton

    Google Scholar 

  • Kartha KK, Leung NL, Mroginski LA (1982) In vitro growth responses and plant regeneration from cryopreserved meristems of cassava (Manihot esculenta Crantz). Z Pflanzenphysiol 107:133–140

    Google Scholar 

  • Keller ERJ, Dreiling M (2003) Potato cryopreservation in Germany-using the droplet method for the establishment of a new large collection. Acta Hortic 623:193–200

    Google Scholar 

  • Keller ERJ, Senula A, Grübe M, Diekmann K, Dehmer HJ (2014) Fifteen years of cryopreservation in the IPK Genebank—experience, conclusions and outlook. Acta Hortic 1039:249–264

    Google Scholar 

  • Kim H-H, Lee J-K, Yoon J-W, Ji J-J, Nam S-S, Hwang H-S, Cho E-G, Engelmann F (2006) Cryopreservation of garlic bulbil primordia by the droplet-vitrification procedure. CryoLetters 27:143–153

    CAS  PubMed  Google Scholar 

  • Kim H-H, Lee J-K, Hwang H-S, Engelmann F (2007) Cryopreservation of garlic germplasm collections using droplet-vitrification technique. CryoLetters 28:471–482

    CAS  PubMed  Google Scholar 

  • Kim H-H, Popova E, Shin D-J, Yi J-Y, Kim CH, Lee J-S, Yoon M-K, Engelmann F (2012) Cryobanking of Korean Allium germplasm collections: results from a 10 year experience. CryoLetters 33:45–57

    CAS  PubMed  Google Scholar 

  • Kohmura H, Sakai A, Chokyu S, Yakuwa T (1992) Cryopreservation of in vitro-cultured multiple bud clusters of asparagus (Asparagus officinalis L. cv. Hiroshimagreen (2n = 30) by the techniques of vitrification. Plant Cell Rep 11:433–437

    CAS  PubMed  Google Scholar 

  • Köpnick C, Grübe M, Stock J, Senula A, Mock HP, Nagel M (2018) Changes of soluble sugars and ATP content during DMSO droplet freezing and PVS3 droplet vitrification of potato shoot tips. Cryobiology 85:79–86

    PubMed  Google Scholar 

  • Kulus D, Zalewska M (2014) Cryopreservation as a tool used in long-term storage of ornamental species—a review. Sci Hortic 168:88–107

    Google Scholar 

  • Kumu Y, Harada T, Yakuwa T (1983) Development of a whole plant from a shoot tip of Asparagus officinalis L. frozen down to – 196 °C. J Fac Agric Hokkaido Univ 61:285–294

    Google Scholar 

  • Lambardi M, Shaarawi S (2017) Importance of in vitro culture for developing cryopreservation strategies of woody plants. Acta Hortic 1187:177–188

    Google Scholar 

  • Laojunta T, Tamiya K, Narumi-Kawasaki T, Fukai S (2018) Cryopreservation of in vitro grown Torenia using the cryo-plate vitrification method. Acta Hortic 1208:125–130

    Google Scholar 

  • Latta R (1971) Preservation of suspensions cultures of plant cells by freezing. Can J Bot 49:1253–1254

    Google Scholar 

  • Li B-Q, Feng C-H, Wang M-R, Hu L-Y, Volk GM, Wang Q-C (2015) Recovery patterns, histological observations and genetic integrity in Malus shoot tips cryopreserved using droplet-vitrification and encapsulation-dehydration procedures. J Biotechnol 214:182–191

    CAS  PubMed  Google Scholar 

  • Li J-W, Ozudogru EA, Li J, Wang M-R, Bi W-L, Lambardi M, Wang Q-C (2017) Cryobiotechnology of forest trees: recent advances and future prospects. Biodivers Conserv 27:795–814

    Google Scholar 

  • Li J-W, Zhang X-C, Wang M-R, Bi W-L, Faisal M, Teixeira da Silva JA, Volk JM, Wang Q-C (2019) Development, progress and future prospects in cryobiotechnology of Lilium spp. Plant Methods 15:125. https://doi.org/10.1186/s13007-019-0506-9

    Article  PubMed  PubMed Central  Google Scholar 

  • Luis B, Cordova II, Thammasiri K (2016) Cryopreservation on a cryo-plate of Arundina graminifolia protocorms, dehydrated with silica gel and drying beads. CryoLetters 37:68–76

    Google Scholar 

  • Magyar-Tábori K, Dobránszki J, Teixeira da Silva JA, Bulley SM, Hudák I (2010) The role of cytokinins in shoot organogenesis in apple. Plant Cell Tissue Org Cult 101:251–267

    Google Scholar 

  • Matsumoto T (2017) Cryopreservation of plant genetic resources: conventional and new methods. Rev Agric Sci 5:13–20

    Google Scholar 

  • Matsumoto T, Yoshimatsu K, Kawahara N, Yamamoto SI, Niino T (2014) Development of in vitro propagation by node culture and cryopreservation by v-cryo-plate method for Perilla frutescens Adv Hortic Sci 28:79–83

    Google Scholar 

  • Matsumoto T, Yamamoto SI, Fukui K, Rafique T, Engelmann F, Niino T (2015) Cryopreservation of persimmon shoot tips from dormant buds using the D cryo-plate technique. Hortic J 84:106–110

    CAS  Google Scholar 

  • Murashige T, Skoog F (1962) A revised medium for rapid growth and bioassays with tobacco tissue cultures. Physiol Plant 15:473–497

    CAS  Google Scholar 

  • Niina R, Castillo F, Bassil NV, Wada S, Reed BM (2010) Genetic stability of cryopreserved shoot tips of Rubus germplasm. In Vitro Cell Dev Biol-Plant 46:246–256

    Google Scholar 

  • Niino T, Yamamoto S, Fukui K, Martínez CRC, Arizaga MV, Matsumoto T, Engelmann F (2013) Dehydration improves cryopreservation of mat rush (Juncus decipiens Nakai) basal stem buds on cryo-plates. CryoLetters 34:549–560

    CAS  PubMed  Google Scholar 

  • Niino T, Watanabe K, Nohara N, Rafique T, Yamamoto S-i, Fukui K, Arizaga MV, Martinez CRC, Matsumoto T, Engelmann F (2014) Cryopreservation of mat rush lateral buds by air dehydration using aluminum cryo-plate. Plant Biotechnol 31:281–287

    CAS  Google Scholar 

  • Niino T, Arizaga MV (2015) Cryopreservation for preservation of potato genetic resources. Breed Sci 65:41–52

    CAS  PubMed  PubMed Central  Google Scholar 

  • Niino T, Yamamoto S, Matsumoto T, Engelmann F, Arizaga MV, Tanaka D (2019) Development of V and D cryo-plate methods as effective protocols for cryobanking. Acta Hortic 1234:249–262

    Google Scholar 

  • Nishizawa S, Sakai A, Amano Y, Matsuzawa T (1993) Cryopreservation of asparagus (Asparagus officinalis) embryogenic suspension cells and subsequent plant regeneration by vitrification. Plant Sci 91:67–73

    CAS  Google Scholar 

  • Normah MN, Sulong N, Reed BM (2019) Cryopreservation of shoot tips of recalcitrant and tropical species: advances and strategies. Cryobiology 87:1–14

    CAS  PubMed  Google Scholar 

  • Nukari A, Uosukainen M, Laamanen J, Rantala S (2011) Cryopreservation of horticultural plants at MTT. In: Grapin A, Keller ERJ, Lynch PT, Panis B, Revilla Bahillo A, Engelmann F (eds) Proceeding of the final meeting COST Action 871 Cryo-Planet ‘Cryopreservation of crop species in Europe’. pp 93–97

  • Ozudogru EA, Lambardi M (2016) Cryotechniques for the long-term conservation of embryogenic cultures from woody plants. In: Germanà MA, Lambardi M (eds) Vitro embryogenesis in higher plants, methods in molecular biology. Springer, New York, pp 537–550

    Google Scholar 

  • Pan C, Liu J, Bi W-L, Chen H-Y, Engelmann F, Wang Q-C (2018) Cryopreservation of small leaf squares-bearing adventitious buds of Lilium Oriental hybrid ‘Siberia’ by vitrification. Plant Cell Tissue Org Cult 133:159–164

    CAS  Google Scholar 

  • Panis B (2019) Sixty years of plant cryopreservation: from freezing hardy mulberry twigs to establishing reference crop collections for future generations. Acta Hortic 1234:1–7

    Google Scholar 

  • Panis B, Lambardi M (2006) Status of cryopreservation technologies in plants (crops and forest trees). In: Ruane J, Sonnino A (eds) The role of biotechnology in exploring and protecting agricultural genetic resources. FAO, Rome, pp 61–78

    Google Scholar 

  • Panis B, Piette B, Swennen R (2005) Droplet vitrification of apical meristems: a cryopreservation protocol applicable to all Musaceae. Plant Sci 168:45–55

    CAS  Google Scholar 

  • Panta A, Panis B, Ynouye C, Swennen R, Roca W (2014) Development of a PVS2 droplet vitrification method for potato cryopreservation. CryoLetters 35:255–266

    CAS  PubMed  Google Scholar 

  • Pathirana R, McLachlan A, Hedderley D, Panis B, Carimi F (2016) Pre-treatment with salicylic acid improves plant regeneration after cryopreservation of grapevine (Vitis spp.) by droplet vitrification. Acta Physiol Plant 38:12. https://doi.org/10.1007/s11738-015-2026-1

    Article  CAS  Google Scholar 

  • Pennycooke JC, Towill LE (2000) Cryopreservation of shoot tips from in vitro plants of sweet potato [Ipomoea batatas (L.) Lam.] by vitrification. Plant Cell Rep 19:733–737

    CAS  PubMed  Google Scholar 

  • Peredo EL, Arroyo-Garcia R, Reed BM, Revilla MA (2008) Genetic and epigenetic stability of cryopreserved and coldstored hops (Humulus lupulus L. Cryobiology 57:234–241

    CAS  PubMed  Google Scholar 

  • Polzin F, Sylvestre I, Déchamp E, Ilbert P, Etienne H, Engelmann F (2014) Effect of activated charcoal on multiplication of African yam (Dioscorea cayenensis-rotundata) nodal segments using a temporary immersion bioreactor (RITA®). In Vitro Cell Dev Biol-Plant 50:210–216

    CAS  Google Scholar 

  • Rafique T, Yamamoto S-i, Fukui K, Mahmood Z, Niino T (2015) Cryopreservation of sugarcane using the V cryo-plate technique. CryoLetters 36:51–59

    PubMed  Google Scholar 

  • Rafique T, Yamamoto S-i, Fukui K, Tanaka D, Arizaga MV, Abbas M, Matsumoto T, Niino T (2016) Cryopreservation of shoot-tips from different sugarcane varieties using cryo-plate techniques. Pak J Agric Sci 53:151–158

    Google Scholar 

  • Ranalli P (2007) The canon of potato science: microtubers. Potato Res 50:301–304

    Google Scholar 

  • Sakai A (1956) Survival of plant tissue of super-low temperature. Contrib Inst Temp Sci Haikkaido Univ Ser B 14:17

    Google Scholar 

  • Sakai A (1960) Survival of the twigs of woody plants at -196 °C. Nature 185:392–394

    Google Scholar 

  • Sakai A, Engelmann F (2007) Vitrification, encapsulation-vitrification and droplet-vitrification: a review. CryoLetters 28:151–172

    CAS  PubMed  Google Scholar 

  • 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 9:30–33

    CAS  PubMed  Google Scholar 

  • Sakai A, Hirai D, Niino T (2008) Development of PVS-based vitrification and encapsulation-vitrification protocols. In: Reed BM (ed) Plant cryopreservation: a practical guide. Springer, New York, pp 33–58

    Google Scholar 

  • Salama A, Popova E, Jones MP, Shukla MR, Fisk NS, Saxena PK (2018) Cryopreservation of the critically endangered golden paintbrush (Castilleja levisecta Greenm.): from nature to cryobank to nature. In Vitro Cell Dev Biol-Plant 54:69–78

    CAS  Google Scholar 

  • Sant R, Panis B, Taylor M, Tyagi A (2008) Cryopreservation of shoot-tips by droplet vitrification applicable to all taro (Colocasia esculenta var. esculenta) accessions. Plant Cell Tissue Org Cult 92:107–111

    Google Scholar 

  • Sekizawa K, Yamamoto S-i, Rafique T, Fukui K, Niino T (2011) Cryopreservation of in vitro-grown shoot tips of carnation (Dianthus caryophyllus L.) by vitrification method using aluminium cryoplates. Plant Biotechnol 28:401–405

    Google Scholar 

  • Souza FVD, Kaya E, Vieira LJ, Souza EH, Amorim VBO, Skogerboe D, Matsumoto T, Alves AAC, da Silva Ledo CA, Jenderek MM (2016) Droplet-vitrification and morphohistological studies of cryopreserved shoot tips of cultivated and wild pineapple genotypes. Plant Cell Tissue Org Cult 126:351–360

    Google Scholar 

  • Stevens ME, Pijut PM (2018) Rapid in vitro shoot multiplication of the recalcitrant species Juglans nigra L. Vitro Cell Dev Biol-Plant 54:309–317

    CAS  Google Scholar 

  • Tanaka D, Akimoto-Kato A, NiinoT. Matsumoto T (2014) Cryopreservation of chrysanthemum using aluminium Cryo-plate protocol. Cryobiology 69:520–521

    Google Scholar 

  • Tanaka D, Akimoto-Kato A, Kusaba M, Taniguchi K, Niino T, Maki S, Matsumoto T (2016) cryopreservation of chrysanthemum shoot tips by D cryo-plate method. Cryobiology 23:1–7

    Google Scholar 

  • Tanaka D, Sakuma Y, Yamamoto S, Matsumoto T, Niino T (2019a) Development of the V cryo-plate method for cryopreservation of in vitro rakkyo (Allium chinense G. Don). Acta Hortic 1234:287–292

    Google Scholar 

  • Tanaka D, Yamamoto S, Matsumoto T, Arizaga MV, Niino T (2019b) Development of effective cryopreservation protocols using aluminium cryo-plates for mulberry. Acta Hortic 1234:263–268

    Google Scholar 

  • Teixeira da Silva JA (2003) Chrysanthemum: advances in tissue culture, cryopreservation, postharvest technology, genetics and transgenic biotechnology. Biotechnol Adv 21:715–766

    CAS  PubMed  Google Scholar 

  • Teixeira da Silva JA, Gulyás A, Magyar-Tábori K, Wang M-R, Wang Q-C, Dobránszki J (2019) In vitro tissue culture of apple and other Malus species: recent advances and applications. Planta 249:975–1006

    CAS  PubMed  Google Scholar 

  • Uchendu EE, Shukl M, Saxena PK, Keller JER (2016) Cryopreservation of potato microtubers: the critical roles of sucrose and desiccation. Plant Cell Tissue Organ Cult 124:649–656

    CAS  Google Scholar 

  • Ukhatova YV, Dunaeva SE, Antonova OY, Apalikova OV, Pozdniakova KS, Novikova LY, Shuvalova LE, Gavrilenko TA (2017) Cryopreservation of red raspberry cultivars from the VIR in vitro collection using a modified droplet vitrification method. In Vitro Cell Dev Biol-Plant 53:394–401

    CAS  Google Scholar 

  • Volk GM, Bonnart R, Shepherd A, Yin ZF, Lee L, Polek M, Krueger R (2017) Citrus cryopreservation: viability of diverse taxa and histological observations. Plant Cell Tissue Org Cult 128:327–334

    CAS  Google Scholar 

  • Volk GM, Jenderek MM, Staats E, Shepherd A, Bonnart R, Ledo A, Ayala-Silva T (2019a) Challenges in the development of a widely applicable method for sugarcane (Saccharum spp.) shoot tip cryopreservation. Acta Hortic 1234:335–342

    Google Scholar 

  • Volk GM, Jenderek MM, Walters C, Bonnart R, Shepherd A, Skogerboe D, Hall BD, Moreland B, Krueger R, Polek M (2019b) Implementation of Citrus shoot tip cryopreservation in the USDA-ARS National Plant Germplasm System. Acta Hortic 1234:329–334

    Google Scholar 

  • Vujović T, Chatelet P, Ružića D, Engelmann F (2015) Cryopreservation of Prunus spp. using aluminum cryo-plates. Sci Hortic 195:173–182

    Google Scholar 

  • Wang QC, Batuman Ö, Li P, Bar-Joseph M, Gafny R (2002a) 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 128:135–142

    CAS  Google Scholar 

  • Wang QC, Batuman Ö, Li P, Bar-Joseph M, Gafny R (2002b) Cryopreservation of in vitro-grown shoot tips of ‘Troyer’ citrange [Poncirus trifoliata (L.) Raf. × Citrus sinensis (L.) Osbeck.] by encapsulation-dehydration. Plant Cell Rep 20:901–906

    CAS  Google Scholar 

  • Wang QC, Perl A (2006) Cryopreservation in floricultural crops. In: Teixeira da Silva JA (ed) Floricultural, ornamental and plant biotechnology: advances and topics. Global Science Books, London, pp 523–539

    Google Scholar 

  • Wang B, Yin Z-F, Feng C-H, Shi X, Li Y-P, Wang Q-C (2008) Cryopreservation of potato shoot tips. In: Benkeblia N, Tennant P (eds) Potato I fruit, vegetable and cereal science and biotechnology, 2 (Special Issue 1). Global Science Book, London, pp 46–53

    Google Scholar 

  • Wang B, Wang R-R, Cui Z-H, Bi WL, Li J-W, Li B-Q, Ozudogru AE, Volk GM, Wang Q-C (2014) Potential applications of cryogenic technologies to plant genetic improvement and pathogen eradication. Biotechnol Adv 32:583–395

    CAS  PubMed  Google Scholar 

  • Wang L-Y, Li Y-D, Sun H-Y, Liu H-G, Tang X-D, Wang Q-C, Zhang Z-D (2017) An efficient droplet-vitrification cryopreservation for valuable blueberry germplasm. Sci Hortic 219:60–69

    CAS  Google Scholar 

  • Wang MR, Chen L, Teixeira da Silva JA, Volk GM, Wang Q-C (2018) Cryobiotechnology of apple (Malus spp.): development, progress and future prospects. Plant Cell Rep 37:689–709

    CAS  PubMed  Google Scholar 

  • Wang M-R, Zhang Z, Zámečník J, Bilavčík A, Blystad D-R, Haugslien S, Wang Q-C (2020) Droplet-vitrification for shoot tip cryopreservation of shallot (Allium cepa var. aggregatum): effects of PVS3 and PVS2 on shoot regrowth. Plant Cell Tissue Org Cult 140:185–195

    CAS  Google Scholar 

  • Wilms H, Rhee JH, Rivera RL, Longin K, Panis B (2019) Developing coconut cryopreservation protocols and establishing cryo-genebank at RDA; a collaborative project between RDA and Bioversity International. Acta Hortic 1234:343–348

    Google Scholar 

  • Withers LA (1985) Cryopreservation of cultured plant cells and protoplasts. In: Kartha KK (ed) Cryopreservation of plant cells and organs. CRC Press, Boca Raton, pp 243–267

    Google Scholar 

  • Yamamoto S-i, Rafique T, Priyantha WS, Fukui K, Matsumoto T, Niino T (2011) Development of a cryopreservation procedure using aluminum cryo-plates. CryoLetters 32:256–265

    CAS  PubMed  Google Scholar 

  • Yamamoto S-i, Fukui K, Rafique T, Khan NI, Castillo Martinez CR, Sekizawa K, Matsumoto T, Niino T (2012a) Cryopreservation of in vitro-grown shoot tips of strawberry by the vitrification method using aluminium cryo-plates. Plant Gen Res 10:14–19

    CAS  Google Scholar 

  • Yamamoto S-i, Rafique T, Fukui K, Sekizawa K, Koyama A, Ichihashi T, Niino T (2012b) Development of an effective cryopreservation protocol using aluminum cryo-plates for in vitro-grown shoot tips of mulberries (Morus spp.) originated from the tropics and subtropics. Sanshi-Konchu Biotechnol 81:57–62

    Google Scholar 

  • Yamamoto S-i, Rafique T, Fukui K, Sekizawa K, Niino T (2012c) V cryo-plate procedure as an effective protocol for cryobanks—case study of mint cryopreservation. CryoLetters 33:12–23

    CAS  PubMed  Google Scholar 

  • Yamamoto S-i, Rafique W, Arizaga W, Fukui MV, Gutierrez MV, Castillo K, Martinez EJC, Watanabe CR, Niino CRC (2015) The aluminum cryo-plate increases efficiency of cryopreservation protocols for potato shoot tips. Am J Potato Res 92:250–257

    Google Scholar 

  • Yap LV, Normah MN, Clyde MM, Chin HF (2011) Cryopreservation of Garcinia cowa shoot tips by vitrification: the effects of sucrose preculture and loading treatment on ultrastructural changes in meristematic cells. CryoLetters 32:188–196

    CAS  PubMed  Google Scholar 

  • Yin Z-F, Zhao B, Bi W-L, Chen L, Wang Q-C (2013) Direct shoot regeneration from basal leaf segments of Lilium and assessment of genetic stability in regenerants by ISSR and AFLP markers. In Vitro Cell Dev Biol-Plant 49:333–342

    CAS  Google Scholar 

  • Yin Z-F, Bi W-L, Chen L, Zhao B, Wang Q-C (2014) An efficient, widely applicable cryopreservation of Lilium shoot tips by droplet-vitrification. Acta Physiol Plant 36:1683–1692

    CAS  Google Scholar 

  • Zhang J-M, Xin X, Yin G-K, Lu X-X, Chen X-L (2014) In vitro conservation and cryopreservation in national genebank of China. Acta Hortic 1039:309–317

    Google Scholar 

  • Zhang J-M, Han L, Lu X-X, Volk GM, Xin X, Yin G-K, He J-J, Wang L, Chen X-L (2017) Cryopreservation of Jerusalem artichoke cultivars using an improved droplet-vitrification method. Plant Cell Tissue Org Cult 128:577–587

    CAS  Google Scholar 

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Acknowledgements

Q-C W thanks a project supported by the National Key R&D Program of China (project number 2019YFD1001800). M L thanks the Italian RGV-FAO project (2017–2019) for the financial support. BP gratefully acknowledges the Genebank CGIAR Research Program and the CGIAR Research Program on Roots, Tubers and Bananas (RTB) and the Directorate-General for Development, Belgium (DGD) for the financial support to the project 'Safeguarding vegetatively-propagated crop diversity to nourish people now and in the future'. Kathryn Chen from National Laboratory for Genetic Resources Preservation, Fort Collins of USA, provided the artwork shown in Fig. 2. USDA is an equal opportunity employer.

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Authors and Affiliations

  1. State Key Laboratory of Crop Stress Biology in Arid Region, College of Horticulture, Northwest A&F University, Yangling, 712100, Shaanxi, People’s Republic of China

    Min-Rui Wang & Qiao-Chun Wang

  2. CNR-IBE, Institute of Bio-Economy, National Research Council (CNR), Via Madonna de Piano 10, 50019, Sesto Fiorentino, Florence, Italy

    Maurizio Lambardi

  3. IRD Representation in Benin, Résidence Les Cocotiers, 08 BP 841, Cotonou, Benin

    Florent Engelmann

  4. New Zealand Institute for Plant & Food Research Ltd, Palmerston North, New Zealand

    Ranjith Pathirana

  5. Biotechnics, K.U. Leuven, Willem de Croylaan 42, 3001, Leuven, Belgium

    Bart Panis

  6. Bioversity International, Willem de Croylaan 42, 3001, Leuven, Belgium

    Bart Panis

  7. National Laboratory for Genetic Resources Preservation, 1111 S. Mason St, Fort Collins, CO, 80521, USA

    Gayle M. Volk

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  1. Min-Rui Wang
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  2. Maurizio Lambardi
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  3. Florent Engelmann
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  4. Ranjith Pathirana
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  5. Bart Panis
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  6. Gayle M. Volk
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  7. Qiao-Chun Wang
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Correspondence to Bart Panis, Gayle M. Volk or Qiao-Chun Wang.

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Wang, MR., Lambardi, M., Engelmann, F. et al. Advances in cryopreservation of in vitro-derived propagules: technologies and explant sources. Plant Cell Tiss Organ Cult 144, 7–20 (2021). https://doi.org/10.1007/s11240-020-01770-0

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