Advertisement

Plant Cell, Tissue and Organ Culture (PCTOC)

, Volume 138, Issue 1, pp 193–205 | Cite as

Combined pre-treatments enhance antioxidant metabolism and improve survival of cryopreserved kiwifruit shoot tips

  • Liya Mathew
  • David J. Burritt
  • Andrew McLachlan
  • Ranjith PathiranaEmail author
Original Article
  • 79 Downloads

Abstract

The number of species conserved by cryopreservation is increasing thanks to the development of robust vitrification-based protocols. Managing oxidative stress is critical for the successful application of cryopreservation to plant tissues. This research was aimed at understanding the protective effect of pre-treatment of stock plantlets with cold, and their shoot tips with sucrose and an antioxidant (ascorbate) during cryopreservation by droplet vitrification (DV). The levels of enzymatic and non-enzymatic oxidative markers as well as oxidative damage in pre-treated and untreated shoot tips of Actinidia chinensis var. chinensis ‘Hort16A’ at different stages of DV and recovery were studied. All the antioxidant markers showed a significant increase in shoot tips from cold-acclimated plantlets pre-treated with a combination of sucrose and ascorbate compared with untreated shoot tips throughout the steps, especially 24 h after recovery from cryopreservation. Oxidative damage markers; lipid peroxides and protein carbonyls were significantly lower in pre-treated shoot tips than in untreated shoot tips after cryopreservation, suggesting better protection as a result of the pre-treatments used. These observations were confirmed in recovery studies where shoot tips that were harvested from cold-hardened plantlets, and pre-treated with sucrose and ascorbate, showed 40% regeneration against 0% in cryopreserved shoot tips that were not pre-treated.

Key message

Combined pre-treatments with cold, sucrose and ascorbate enhance antioxidant metabolism and improve survival of cryopreserved kiwifruit shoot tips.

Keywords

Actinidia spp. Ascorbate Oxidative stress Oxidative damage Tissue culture Vitrification Conservation 

Notes

Acknowledgements

Authors thank Andrew Mullan and Belinda Diepenheim for technical assistance and Tony Corbett for preparing the figures. The research was funded by Kiwifruit Royalty Investment Programme of The New Zealand Institute for Plant and Food Research Limited.

Author contributions

RP and DJB conceptualised the research, and designed the experiments, LM, DJB and RP –conducted the research. RP wrote the manuscript with DJB and LM, AM—conducted the statistical analysis, interpreted results and wrote sections of the manuscript.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflicts of interest with the contents of this article.

Supplementary material

11240_2019_1617_MOESM1_ESM.pdf (114 kb)
Supplementary material 1 (PDF 113 kb)

References

  1. Bachiri Y, Song GQ, Plessis P, Shoar-Ghaffari A, Rekab T, Morisset C (2001) Routine cryopreservation of kiwifruit (Actinidia spp) germplasm by encapsulation-dehydration: importance of plant growth regulators. Cryoletters 22(1):61–74Google Scholar
  2. Banowetz GM, Dierksen KP, Azevedo MD, Stout R (2004) Microplate quantification of plant leaf superoxide dismutases. Anal Biochem 332(2):314–320Google Scholar
  3. Beatson R, Datson P, Ferguson A, Montefiori M (2014) Use of kiwifruit germplasm resources for genetic improvement. Acta Hortic 1048:25–34Google Scholar
  4. Becana M, Moran JF, Iturbe-Ormaetxe I (1998) Iron-dependent oxygen free radical generation in plants subjected to environmental stress: toxicity and antioxidant protection. Plant Soil 201(1):137–147.  https://doi.org/10.1023/a:1004375732137 Google Scholar
  5. Bela K, Horváth E, Gallé Á, Szabados L, Tari I, Csiszár J (2015) Plant glutathione peroxidases: emerging role of the antioxidant enzymes in plant development and stress responses. J Plant Physiol 176:192–201Google Scholar
  6. Benson EE (2008) Cryopreservation of phytodiversity: a critical appraisal of theory & practice. Crit Rev Plant Sci 27:141–219Google Scholar
  7. Bettoni JC, Dalla Costa M, Gardin JPP, Kretzschmar AA, Pathirana R (2016) Cryotherapy: a new technique to obtain grapevine plants free of viruses. Rev Bras Frutic.  https://doi.org/10.1590/0100-29452016833 Google Scholar
  8. Campos PS, Quartin V, Ramalho JC, Nunes MA (2003) Electrolyte leakage and lipid degradation account for cold sensitivity in leaves of Coffea sp. plants. J Plant Physiol 160(3):283–292.  https://doi.org/10.1078/0176-1617-00833 Google Scholar
  9. Carimi F, Carra A, Panis B, Pathirana R (2016) Strategies for conservation of endangered wild grapevine (Vitis vinifera L. subsp. sylvestris (C.C. Gmel.) Hegi). Acta Hortic 1115:81–86.  https://doi.org/10.17660/ActaHortic.2016.1115.13 Google Scholar
  10. Chang YJ, Reed BM (1999) Extended cold acclimation and recovery medium alteration improve regrowth of Rubus shoot tips following cryopreservation. Cryoletters 20(6):371–376Google Scholar
  11. Chen G-Q, Ren L, Zhang J, Reed BM, Zhang D, Shen X-H (2015) Cryopreservation affects ROS-induced oxidative stress and antioxidant response in Arabidopsis seedlings. Cryobiology 70(1):38–47.  https://doi.org/10.1016/j.cryobiol.2014.11.004 Google Scholar
  12. Cribb AE, Leeder JS, Spielberg SP (1989) Use of a microplate reader in an assay of glutathione reductase using 5, 5′-dithiobis (2-nitrobenzoic acid). Anal Biochem 183(1):195–196Google Scholar
  13. Ferguson A, Seal A (2008) Kiwifruit. In: Hancock JF (ed) Temperate fruit crop breeding. Springer, Dordrecht, pp 235–264Google Scholar
  14. Fki L, Bouaziz N, Chkir O, Benjemaa-Masmoudi R, Rival A, Swennen R, Drira N, Panis B (2013) Cold hardening and sucrose treatment improve cryopreservation of date palm meristems. Biol Plant 57(2):375–379.  https://doi.org/10.1007/s10535-012-0284-y Google Scholar
  15. Fretz A, Lorz H (1995) Cryopreservation of in vitro cultures of barley (Hordeum vulgare L. and H. murinum L.) and transgenic cells of wheat (Triticum aestivum L.). J Plant Physiol 146(4):489–496.  https://doi.org/10.1016/s0176-1617(11)82013-4 Google Scholar
  16. Fryer HJ, Davis GE, Manthorpe M, Varon S (1986) Lowry protein assay using an automatic microtiter plate spectrophotometer. Anal Biochem 153(2):262–266Google Scholar
  17. Funnekotter B, Sortey A, Bunn E, Turner SR, Mancera RL (2016) Influence of abiotic stress preconditioning on antioxidant enzymes in shoot tips of Lomandra sonderi (Asparagaceae) prior to cryostorage. Aust J Bot 64(3):260–268.  https://doi.org/10.1071/bt16006 Google Scholar
  18. Gamborg OL, Miller RA, Ojima K (1968) Nutrient requirements of suspension cultures of soybean root cells. Exp Cell Res 50(1):151–158.  https://doi.org/10.1016/0014-4827(68)90403-5 Google Scholar
  19. Gillespie KM, Ainsworth EA (2007) Measurement of reduced, oxidized and total ascorbate content in plants. Nat Protoc 2(4):871–874Google Scholar
  20. Gillespie KM, Rogers A, Ainsworth EA (2011) Growth at elevated ozone or elevated carbon dioxide concentration alters antioxidant capacity and response to acute oxidative stress in soybean (Glycine max). J Exp Bot 62(8):2667–2678.  https://doi.org/10.1093/jxb/erq435 Google Scholar
  21. Gupta S, Reed BM (2006) Cryopreservation of shoot tips of blackberry and raspberry by encapsulation-dehydration and vitrification. Cryoletters 27(1):29–42Google Scholar
  22. Hakozaki M, Yoshida Y, Suzuki M (1996) Viability of calli from hypocotyl of kiwifruit seedlings exposed to liquid nitrogen. Environ Control Biol 34(2):147–151Google Scholar
  23. Johnston JW, Harding K, Benson EE (2007) Antioxidant status and genotypic tolerance of Ribes in vitro cultures to cryopreservation. Plant Sci 172(3):524–534Google Scholar
  24. Lee DH, Lee CB (2000) Chilling stress-induced changes of antioxidant enzymes in the leaves of cucumber: in gel enzyme activity assays. Plant Sci 159(1):75–85Google Scholar
  25. Li J, Guo Y (1996) Cryopreservation of cultured Actinidia deliciosa calli. J Fruit Sci 13(2):88–91Google Scholar
  26. Liu YL, Suzuki T, Kasai N, Harada T (1998) Effects of cold acclimation and freezing solution treatment on the survival of frozen lateral buds excised from in vitro-cultured shoots of tara vine (Actinidia arguta). J Jpn Soc Hortic Sci 67(4):562–566Google Scholar
  27. Lynch PT, Siddika A, Johnston JW, Trigwell SM, Mehra A, Benelli C, Lambardi M, Benson EE (2011) Effects of osmotic pretreatments on oxidative stress, antioxidant profiles and cryopreservation of olive somatic embryos. Plant Sci 181(1):47–56.  https://doi.org/10.1016/j.plantsci.2011.03.009 Google Scholar
  28. Marković Z, Chatelet P, Preiner D, Sylvestre I, Kontić JK, Engelmann F (2014) Effect of shooting medium and source of material on grapevine (Vitis Vinifera L.) shoot tip recovery after cryopreservation. Cryoletters 35(1):40–47Google Scholar
  29. Mathew L, McLachlan A, Jibran R, Burritt DJ, Pathirana R (2018) Cold, antioxidant and osmotic pre-treatments maintain the structural integrity of meristematic cells and improve plant regeneration in cryopreserved kiwifruit shoot tips. Protoplasma 255(4):1065–1077.  https://doi.org/10.1007/s00709-018-1215-3 Google Scholar
  30. Mehlhorn H, Lelandais M, Korth H, Foyer C (1996) Ascorbate is the natural substrate for plant peroxidases. FEBS Lett 378(3):203–206.  https://doi.org/10.1016/0014-5793(95)01448-9 Google Scholar
  31. Mihaljević B, Katušin-Ražem B, Ražem D (1996) The reevaluation of the ferric thiocyanate assay for lipid hydroperoxides with special considerations of the mechanistic aspects of the response. Free Radical Biol Med 21(1):53–63Google Scholar
  32. Miller G, Shulaev V, Mittler R (2008) Reactive oxygen signaling and abiotic stress. Physiol Plant 133(3):481–489.  https://doi.org/10.1111/j.1399-3054.2008.01090.x Google Scholar
  33. Murashige T, Skoog F (1962) A revised medium for rapid growth and bioassays with tobacco tissue cultures. Physiol Plant 15:473–497Google Scholar
  34. Nakano Y, Asada K (1981) Hydrogen peroxide is scavenged by ascorbate-specific peroxidase in spinach chloroplasts. Plant Cell Physiol 22(5):867–880Google Scholar
  35. Ozudogru EA, Kaya E (2012) Cryopreservation of Thymus cariensis and T. vulgaris shoot tips: comparison of three vitrification-based methods. Cryoletters 33(5):363–375Google Scholar
  36. Paglia DE, Valentine WN (1967) Studies on the quantitative and qualitative characterization of erythrocyte glutathione peroxidase. J Lab Clin Med 70(1):158–169Google Scholar
  37. Panta A, Panis B, Ynouye C, Swennen R, Roca W, Tay D, Ellis D (2015) Improved cryopreservation method for the long-term conservation of the world potato germplasm collection. Plant Cell Tissue Organ Cult 120(1):117–125.  https://doi.org/10.1007/s11240-014-0585-2 Google Scholar
  38. Pathirana R, McLachlan A, Hedderley D, Carra A, Carimi F, Panis B (2015) Removal of leafroll viruses from infected grapevine plants by droplet vitrification. Acta Hortic 1083:491–498Google Scholar
  39. Pathirana R, Deroles S, Hoeata K, Montefiori M, Tyson J, Wang T, Datson PM, Hellens RP (2016a) Fast-tracking kiwifruit breeding through mutagenesis. Acta Hortic 1127:217–222.  https://doi.org/10.17660/ActaHortic.2016.1127.34 Google Scholar
  40. Pathirana R, McLachlan A, Hedderley D, Panis B, Carimi F (2016b) Pre-treatment with salicylic acid improves plant regeneration after cryopreservation of grapevine (Vitis spp.) by droplet vitrification. Acta Physiol Plant 38:1–11Google Scholar
  41. Phang IC, Leung DWM, Taylor HH, Burritt DJ (2011) Correlation of growth inhibition with accumulation of Pb in cell wall and changes in response to oxidative stress in Arabidopsis thaliana seedlings. Plant Growth Regul 64(1):17–25.  https://doi.org/10.1007/s10725-010-9527-0 Google Scholar
  42. Prasad TK (1996) Mechanisms of chilling-induced oxidative stress injury and tolerance in developing maize seedlings: changes in antioxidant system, oxidation of proteins and lipids, and protease activities. Plant J 10(6):1017–1026Google Scholar
  43. Rahman I, Kode A, Biswas SK (2006) Assay for quantitative determination of glutathione and glutathione disulfide levels using enzymatic recycling method. Nat Protoc 1(6):3159–3165Google Scholar
  44. Reed BM (1993) Responses to ABA and cold acclimation are genotype dependent for cryopreserved blackberry and raspberry meristems. Cryobiology 30(2):179–184.  https://doi.org/10.1006/cryo.1993.1017 Google Scholar
  45. Reznick AZ, Packer L (1994) Oxidative damage to proteins: spectrophotometric method for carbonyl assay. Method Enzymol 233:357–363Google Scholar
  46. Roach T, Ivanova M, Beckett RP, Minibayeva FV, Green I, Pritchard HW, Kranner I (2008) An oxidative burst of superoxide in embryonic axes of recalcitrant sweet chestnut seeds as induced by excision and desiccation. Physiol Plant 133(2):131–139Google Scholar
  47. 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.  https://doi.org/10.1007/bf00232130 Google Scholar
  48. Sala JM (1998) Involvement of oxidative stress in chilling injury in cold-stored mandarin fruits. Postharvest Biol Technol 13(3):255–261Google Scholar
  49. Schweikert K, Burritt DJ (2012) The organophosphate insecticide Coumaphos induces oxidative stress and increases antioxidant and detoxification defences in the green macroalgae Ulva pertusa. Aquat Toxicol 122:86–92Google Scholar
  50. Song G, Hou W, Wang Q, Wang J, Jin X (2006) Effect of low temperature on eutrophicated waterbody restoration by Spirodela polyrhiza. Bioresour Technol 97(15):1865–1869Google Scholar
  51. Summermatter K, Sticher L, Métraux J-P (1995) Systemic responses in Arabidopsis thaliana infected and challenged with Pseudomonas syringae pv syringae. Plant Physiol 108(4):1379–1385Google Scholar
  52. Suzuki M, Niino T, Akihama T (1994) Cryopreservation of shoot tips of kiwifruit seedlings by the alginate encapsulation-dehydration technique. Plant Tissue Cult Lett 11:122–128Google Scholar
  53. Tunc-Ozdemir M, Miller G, Song L, Kim J, Sodek A, Koussevitzky S, Misra AN, Mittler R, Shintani D (2009) Thiamin confers enhanced tolerance to oxidative stress in Arabidopsis. Plant Physiol 151(1):421–432.  https://doi.org/10.1104/pp.109.140046 Google Scholar
  54. Uchendu EE, Reed BM (2009) Desiccation tolerance and cryopreservation of in vitro grown blueberry and cranberry shoot tips. Acta Hortic 810(2):567–574Google Scholar
  55. Uchendu EE, Leonard SW, Traber MG, Reed BM (2010a) Vitamins C and E improve regrowth and reduce lipid peroxidation of blackberry shoot tips following cryopreservation. Plant Cell Rep 29(1):25–35Google Scholar
  56. Uchendu EE, Muminova M, Gupta S, Reed BM (2010b) Antioxidant and anti-stress compounds improve regrowth of cryopreserved Rubus shoot tips. In Vitro Cell Dev Biol Plant 46(4):386–393.  https://doi.org/10.1007/s11627-010-9292-9 Google Scholar
  57. Uchendu EE, Shukla M, Saxena PK, Keller JER (2016) Cryopreservation of potato microtubers: the critical roles of sucrose and desiccation. Plant Cell Tissue Organ Cult 124(3):649–656.  https://doi.org/10.1007/s11240-015-0916-y Google Scholar
  58. Volk GM, Walters C (2006) Plant vitrification solution 2 lowers water content and alters freezing behavior in shoot tips during cryoprotection. Cryobiology 52(1):48–61.  https://doi.org/10.1016/j.cryobiol.2005.09.004 Google Scholar
  59. Volk GM, Bonnart R, Krueger R, Lee R (2012) Cryopreservation of Citrus shoot tips using micrografting for recovery. Cryoletters 33(6):418–426Google Scholar
  60. Walker MA, Mckersie BD (1993) Role of the ascorbate-glutathione antioxidant system in chilling resistance of tomato. J Plant Physiol 141(2):234–239Google Scholar
  61. Wang QC, Mawassi M, Sahar N, Li P, Violeta CT, Gafny R, Sela I, Tanne E, Perl A (2004) Cryopreservation of grapevine (Vitis spp.) embryogenic cell suspensions by encapsulation-vitrification. Plant Cell Tissue Organ Cult 77(3):267–275.  https://doi.org/10.1023/b:ticu.0000018393.58928.b1 Google Scholar
  62. 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.  https://doi.org/10.1016/j.scienta.2017.03.007 Google Scholar
  63. Wen B, Cai CT, Wang RL, Song SQ, Song JL (2012) Cytological and physiological changes in recalcitrant Chinese fan palm (Livistona chinensis) embryos during cryopreservation. Protoplasma 249(2):323–335Google Scholar
  64. Wu Y, Zhao Y, Engelmann F, Zhou M (2000) Cryopreservation of kiwi shoot tips. Cryo letters 22(5):277–284Google Scholar
  65. Xu X, Gu Q, Cai Z, Deng X, Zhang Q (2006) Cryopreservation of in vitro cultured kiwifruit shoot-tips by vitrification and their regeneration. Acta Hortic Sin 33(4):842–844Google Scholar
  66. Zhang D, Ren L, Chen GQ, Zhang J, Reed BM, Shen XH (2015) ROS-induced oxidative stress and apoptosis-like event directly affect the cell viability of cryopreserved embryogenic callus in Agapanthus praecox. Plant Cell Rep 34(9):1499–1513.  https://doi.org/10.1007/s00299-015-1802-0 Google Scholar
  67. Zhu GY, Geuns JMC, 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.  https://doi.org/10.1111/j.1399-3054.2006.00713.x Google Scholar

Copyright information

© Springer Nature B.V. 2019

Authors and Affiliations

  1. 1.The New Zealand Institute for Plant & Food Research LimitedPalmerston NorthNew Zealand
  2. 2.Department of BotanyUniversity of OtagoDunedinNew Zealand

Personalised recommendations