Abstract
Key message
After cryopreservation, the NO content in pollen increased, inducing programmed cell death as a key reason for reduced viability.
Abstract
Low recovery of biomaterials after cryopreservation is a bottleneck that limits the application of this technology. At present, the mechanism of viability decline after cryopreservation is not fully understood. In this study, the effects of nitric oxide (NO) on programmed cell death (PCD) and its relationship with viability were investigated, using Paeonia lactiflora 'Fen Yu Nu' pollen with significantly decreased viability after cryopreservation. The results showed that: the activity of caspase-3-like and caspase-9-like protease and the apoptosis rate of pollen cells were significantly increased, the expression level of the promoting PCD (pro-PCD) genes was up-regulated, while the expression level of the inhibiting PCD (anti-PCD) genes was down-regulated after preservation in liquid nitrogen (LN); the NO content in pollen cells increased significantly after LN exposure. The correlation analysis showed that NO was significantly correlated with pollen viability and all indicators of PCD. The addition of a NO carrier SNP after LN storage reduced pollen viability, increased endogenous NO content, decreased mitochondrial membrane potential level, activated caspase-3-like and caspase-9-like protease in pollen cells, and increased cell apoptosis rate. The expression levels of pro-PCD genes PDCD2 and ATG8CL were significantly up-regulated, while the expression levels of anti-PCD genes DAD1, BI-1 and LSD1 were significantly down-regulated. The addition of NO scavenger c-PTIO improved pollen viability, and produced the opposite effect of sodium nitroferricyanide (III) dihydrate (SNP), but did not change the mitochondrial membrane potential. These results suggest that NO induced PCD during the cryopreservation of pollen, which was one of the reasons for the significant decrease of pollen viability after cryopreservation.
Similar content being viewed by others
References
Baust JM, Buskirk RV, Baust JG (2002) Gene activation of the apoptotic caspase cascade following cryogenic storage. Cell Preserv Technol 1:63–80
Beligni MV, Fath A, Bethke PC, Lamattina L, Jones RL (2002) Nitric oxide acts as an antioxidant and delays programmed cell death in barley aleurone layers. Plant Physiol 129(4):1642–1650
Broda M, Millar AH, Van Aken O (2018) Mitophagy: a mechanism for plant growth and survival. Trends Plant Sci 23(5):434–450
Carimi F, Zottini M, Costa A, Cattelan I, De Michele R, Terzi M, Lo Schiavo F (2005) NO signalling in cytokinin-induced programmed cell death. Plant, Cell Environ 28(9):1171–1178
Chen YY, Sun RH, Han WL (2001) Nuclear translocation of PDCD5 (TFAR19): an early signal for apoptosis. FEBS Lett 509:191–196
Chen LN, Wang Y, Chen YY (2006) Short interfering RNA against the PDCD5 attenuates cell apoptosis and caspase-3 activity induced by Bax overexpression. Apoptosis 11:101–111
Da Silva D, Lachaud C, Cotelle V, Brière C, Grat S, Mazars C, Thuleau P (2011) Nitric oxide production is not required for dihydrosphingosine-induced cell death in tobacco BY-2 cells. Plant Signal Behav 6(5):736–739
Delledonne M (2005) NO news is good news for plants. Curr Opin Plant Biol 8:390–396
De Michele R, Vurro E, Rigo C, Costa A, Elviri L, Di Valentin M, Careri M, Zottini M, di Toppi LS, Lo Schiavo F (2009) Nitric oxide is involved in cadmium-induced programmed cell death in Arabidopsis suspension cultures. Plant Physiol 150:217–228
del Rio LA, Sandalio LM, Corpas FJ, Palma JM, Barroso JB (2006) Reactive oxygen species and reactive nitrogen species in peroxisomes. Production, scavenging, and role in cell signaling. Plant Physiol 141:330–335
Dietrich RA, Richberg MH, Schmidt R, Dean C, Dangl JL (1997) A novel zinc finger protein is encoded by style of debase the Arabidopsis LSD1 gene and functions as a negative regulator of plant cell death. Cell 88:685–694
Engelmann F (2004) Plant cryopreservation: progress and prospects. In vitro cellular & developmental biology. Plant 40(5):427–433
Epple P, Mack AA, Morris VR, Dan JL (2003) Antagonistic control of oxidative stress-induced cell death in Arabidopsis by two related, plant-specific zinc finger proteins. Proc Natl Acad Sci 100(11):6831–6836
He HY, Huang WJ, Oo TL, Gu MH, He LF (2017) Nitric oxide inhibits aluminum induced programmed cell death in peanut (Arachis hypoganea L.) root tips. J Hazard Mater 333:285–292
He HY, Oo TL, Huang WJ, He LF, Gu MH (2019) Nitric oxide acts as an antioxidant and inhibits programmed cell death induced by aluminum in the root tips of peanut (Arachis hypogaea L.). Sci Rep 9:9516
Huang DJ, Huo JQ, Zhang J, Wang CL, Wang B, Fang H, Liao WB (2019) Protein S-nitrosylation in programmed cell death in plants. Cell Mol Life Sci 76:1877–1887
Jiang XR, Ren RF, Di W, Jia MX, Li ZD, Liu Y, Gao RF (2019a) Hydrogen peroxide and nitric oxide are involved in programmed cell death induced by cryopreservation in Dendrobium protocorm-like bodies. Plant Cell Tiss Organ Cult (PCTOC) 137:553–563
Jiang XR, Di W, Jia MX, Li ZD, Ren RF, Xu J, Li BL, Liu Y (2019b) MDH and CAT increase the germination of cryopreserved Paeonia pollen by regulating the ROS and apoptosis-like events. Acta Hort 1234:105–112
Jiang XR (2019) Study on the mechanism of programmed cell death during vitrification-cryopreservation in Dendrobium protocorm-like bodies. Beijing Forestry University (in Chinese)
Kawei-Yamada M, Jin L, Yoshinaga K, Hirata A, Uchimiya H (2001) Mammalian Bax-induced plant cell death can be down-regulated by overexpression ofArabidopsis Bax inhibitor-l (AtBI-1). Proc Natl Acad Sci USA 98:12295–12300
Kasprowicz A, Szuba A, Volkmann D, Baluska F, Wojtaszek P (2009) Nitric oxide modulates dynamic actin cytoskeleton and vesicle trafficking in a cell type-specific manner in root apices. J Exp Bot 60:1605–1617
Kerr JF, Wyllie AH, Currie AR (1972) Apoptosis: a basic biological phenomenon with wide-ranging implications in tissue kinetics. Br J Cancer 26(4):239–257
Makishima T, Yoshimi M, Komiyama S, Hara N, Nishimoto T (2000) A subunit of the mammalian oligosaccharyltransferase, DAD1, interacts with Mcl-1, one of the bcl-2 protein family. J Biochem 128(3):399–405
Ma W, Xu W, Xu H, Chen Y, He Z, Ma M (2010) Nitric oxide modulates cadmium influx during cadmium-induced programmed cell death in tobacco BY-2 cells. Planta 232(2):325–335
Mira M, Hill RD, Stasolla C (2016) Regulation of programmed cell death by phytoglobins. J Exp Bot 67(20):5901–5908
Mortazavi SMH, Arzani K, Moieni A (2010) Optimizing storage and in vitro germination of date palm (Phoenix dactylifera) pollen. J Agric Sci Technol 12(2):181–189
Ren RF, Li ZD, Li BL, Xu J, Jiang XR, Liu Y, Zhang KY (2019a) Changes of pollen viability of ornamental plants after long-term preservation in a cryopreservation pollen bank. Cryobiology 89:14–20
Ren RF, Jiang XR, Di W, Li ZD, Li BL, Xu J, Liu Y (2019b) HSP70 improves the viability of cryopreserved Paeonia lactiflora pollen by regulating oxidative stress and apoptosis-like programmed cell death events. Plant Cell Tiss Organ Cult (PCTOC) 139:53–64
Ren RF, Li ZD, Zhou H, Zhang LL, Jiang XR, Liu Y (2020a) Changes in apoptosis-like programmed cell death and viability during the cryopreservation of pollen from Paeonia suffruticosa. Plant Cell Tiss Organ Cult (PCTOC) 140:357–368
Ren RF, Li ZD, Jiang XR, Liu Y (2020b) The ROS-associated programmed cell death causes the decline of pollen viability recovered from cryopreservation in Paeonia lactiflora. Plant Cell Rep 39:941–952
Shibuya K, Shimizu K, Yamada T, Ichimura K (2011) Expression of autophagy-associated ATG8 genes during petal senescence in Japanese morning glory. J Japan Soc Hort Sci 80(1):89–95
Wang YQ, Chen C, Loake GJ, Chu CC (2010) Nitric oxide: promoter or suppressor of programmed cell death? Protein Cell 1(2):133–142
Wan YL, Hong AY, Zhang YX, Liu Y (2019) Selection and validation of reference genes of Paeonia lactiflora in growth development and light stress. Physiol Mol Biol Plants 25(4):1097–1105
Xu J, Li BL, Liu Q, Shi Y, Peng JG, Jia MX, Liu Y (2014) Wide-scale pollen banking of ornamental plants through cryopreservation. CryoLetters 35:312–319
Ye Y, Li Z, Xing D (2013) Nitric oxide promotes MPK6-mediated caspase-3-like activation in cadmium-induced Arabidopsis thaliana programmed cell death. Plant Cell Environ 36:1–15
Zaninotto F, La Camera S, Polverari A, Delledonne M (2006) Cross talk between reactive nitrogen and oxygen species during the hypersensitive disease resistance response. Plant Physiol 141(2):379–383
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 inAgapanthus praecox. Plant Cell Rep 34(9):1499–1513
Zhang HY, Wang WX, Yin H, Zhao XM, Du YG (2012) Oligochitosan induces programmed cell death in tobacco suspension cells. Carbohyd Polym 87:2270–2278
Zhao YY, Chen JX, Tao XY, Zheng XJ, Mao LC (2014) The possible role of BAX and BI-1 genes in chilling-induced cell death in cucumber fruit. Acta Physiol Plant 36:1345–1351
Acknowledgements
This research was supported by the National Natural Science Foundation of China (No. 31370693 and No. 31770741). And we thank Jiao Pengcheng and Ji Jiaojiao (Core Facility, Center of Biomedical Analysis, Tsinghua University) for technical support with flow cytometry analysis. We particularly thank Prof. Barbara M. Reed for editing the manuscript.
Author information
Authors and Affiliations
Contributions
Ruifen Ren designed the research, completed the experiments, analyzed the data and drafted the manuscript. Hao Zhou offered some help on the material collection. Lingling Zhang offered some help on the technical aspects of the experiment. Xueru Jiang offered some help on the research design. Yan Liu conceived the project, supervised the analysis and critically revised the manuscript. All authors read and approved the manuscript.
Corresponding author
Ethics declarations
Conflict of interest
The authors declare that they have no conflict of interest.
Additional information
Communicated by Qiaochun Wang.
Publisher's Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Supplementary Information
Below is the link to the electronic supplementary material.
Rights and permissions
About this article
Cite this article
Ren, R., Zhou, H., Zhang, L. et al. Cryopreserved-pollen viability is regulated by NO-induced programmed cell death. Plant Cell Rep 40, 2383–2395 (2021). https://doi.org/10.1007/s00299-021-02779-1
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00299-021-02779-1