Effects of ROS-induced oxidative stress and programmed cell death on pollen viability after cryopreservation

Ren Ruifen; Li Zedi; Zhu Mengting; Liu Yan; Zhang Kongying

doi:10.12171/j.1000-1522.20210027

Journal of Beijing Forestry University > 2022 > 44(2): 82-90. > DOI: 10.12171/j.1000-1522.20210027

Ren Ruifen, Li Zedi, Zhu Mengting, Liu Yan, Zhang Kongying. Effects of ROS-induced oxidative stress and programmed cell death on pollen viability after cryopreservation[J]. Journal of Beijing Forestry University, 2022, 44(2): 82-90. DOI: 10.12171/j.1000-1522.20210027

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Effects of ROS-induced oxidative stress and programmed cell death on pollen viability after cryopreservation

1.
Beijing Key Laboratory of Ornamental Plants Germplasm Innovation & Molecular Breeding, National Engineering Research Center for Floriculture, Beijing Laboratory of Urban and Rural Ecological Environment, School of Landscape Architecture, Beijing Forestry University, Beijing 100083, China
2.
Luoyang Aerospace Peony Garden Co. Ltd, Luoyang 471000, Henan, China

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Received Date: January 26, 2021
Revised Date: May 07, 2021
Accepted Date: November 24, 2021
Available Online: January 27, 2022
Published Date: February 24, 2022

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Abstract

Abstract

Objective After cryopreservation, pollen viability shows various changes, studies show that ROS is one of the main reasons for the changes of pollen viability after cryopreservation. Therefore, this study investigated the relationship between pollen viability and ROS induced oxidative stress and programmed cell death after cryopreservation, to further reveal the role of ROS in pollen viability changes after cryopreservation.
Method The pollen of P. lactiflora ‘Fen Yu Nu’ was used as material, the changes of pollen viability, ROS production, oxidative stress and programmed cell death after cryopreservation for different lengths of time were compared and analyzed.
Result During the cryopreservation of pollen, the O₂•− content of ROS components was relatively high after 1 and 3 months of cryopreservation, and the H₂O₂ content significantly increased with the extension of storage time, while •OH content began to decrease after 3 months, both H₂O₂ and •OH contents were significantly correlated with pollen viability. Secondly, the content of malondialdehyde (MDA), an index of oxidative damage, was significantly increased after 3 months of liquid nitrogen (LN) storage, which was significantly correlated with pollen viability, H₂O₂ and •OH contents. The activity of caspase-3-like protease, an indicator of programmed cell death (PCD), was higher than that of the fresh pollen after 1 and 3 months of liquid nitrogen freezing, and the apoptosis rate was significantly increased after 5 and 8 months of LN stored, and the apoptosis rate was significantly correlated with pollen viability, H₂O₂ and •OH contents. In addition, appropriate concentration of exogenous oxidative damage inhibitors (AsA, GSH) and apoptosis-like inhibitors (caspase-3 inhibitors) significantly improved pollen viability after 8 months of cryopreservation.
Conclusion During the cryopreservation of P. lactiflora ‘Fen Yu Nu’ pollen, ROS components have an important effect on pollen viability after cryopreservation, the effects of H₂O₂ and •OH are particularly prominent. The oxidative stress response and programmed cell death induced by H₂O₂and •OH are important reasons for the changes of pollen viability after liquid nitrogen cryopreservation.
- germplasm conservation,
- cryopreservation,
- pollen,
- active oxygen,
- oxidative stress,
- programmed cell death

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References

[1]	Rowe A W. Cryopreservation of red cells and platets[M]. Baltimore: University Park Press, 1980.
[2]	张亚利, 尚晓倩, 刘燕. 花粉超低温保存研究进展[J]. 北京林业大学学报, 2006, 28(4): 139−147. doi: 10.3321/j.issn:1000-1522.2006.04.026 Zhang Y L, Shang X Q, Liu Y. Advances in research of pollen cryopreservation[J]. Journal of Beijing Forestry University, 2006, 28(4): 139−147. doi: 10.3321/j.issn:1000-1522.2006.04.026
[3]	Ren R F, Li Z D, Li B L, et al. Changes of pollen viability of ornamental plants after long-term preservation in a cryopreservation pollen bank[J]. Cryobiology, 2019, 89: 14−20.
[4]	Len J S, Koh W S, Tan S X. The roles of reactive oxygen species and antioxidants in cryopreservation [J/OL]. Bioscience Reports, 2019, 39(8): BSR20191601[2021−01−01] https://doi.org/10.1042/BSR20191601.
[5]	Jia M X, Shi Y, Di W, et al. ROS-induced oxidative stress is closely related to pollen deterioration following cryopreservation[J]. In Vitro Cellular & Developmental Biology-Plant, 2017, 53(4): 433−439.
[6]	Mittler R. Oxidative stress, antioxidatnts and stress tolerance[J]. Trends in Plant Science, 2002, 7(9): 405−410. doi: 10.1016/S1360-1385(02)02312-9
[7]	Jia M X, Jiang X R, Xu J, et al. CAT and MDH improve the germination and alleviate the oxidative stress of cryopreserved Paeonia and Magnolia pollen[J]. Acta Physiologiae Plantarum, 2018, 40(2): 37−47. doi: 10.1007/s11738-018-2612-0
[8]	Ren R F, Jiang X R, Di W, et al. HSP70 improves the viability of cryopreserved Paeonia lactiflora pollen by regulating oxidative stress and apoptosis-like programmed cell death events[J]. Plant Cell, Tissue and Organ Culture, 2019, 139(2): 53−64.
[9]	Ren R F, Li Z D, Zhang L L, et al. Enzymatic and nonenzymatic antioxidant systems impact the viability of cryopreserved Paeonia suffruticosa pollen[J]. Plant Cell, Tissue and Organ Culture, 2021, 144(1): 233−246. doi: 10.1007/s11240-020-01794-6
[10]	Ren R F, Li Z D, Zhou H, et al. Changes in apoptosis-like programmed cell death and viability during the cryopreservation of pollen from Paeonia suffruticosa[J]. Plant Cell, Tissue and Organ Culture, 2020, 140(1): 357−368.
[11]	Jiang X R, Di W, Jia M X, et al. MDH and CAT increase the germination of cryopreserved Paeonia pollen by regulating the ROS and apoptosis-like events[J]. Acta Horticulturae, 2019, 1234: 105−112.
[12]	Mittler R, Vanderauwera S, Gollery M, et al. Reactive oxygen gene network of plants[J]. Trends in Plant Science, 2004, 9(10): 490−498. doi: 10.1016/j.tplants.2004.08.009
[13]	Chen G Q, Ren L, Zhang J, et al. Cryopreservation affects ROS-induced oxidative stress and antioxidant response in Arabidopsis seedlings[J]. Cryobiology, 2015, 70(1): 38−47. doi: 10.1016/j.cryobiol.2014.11.004
[14]	王爱国, 罗广华. 植物的超氧物自由基与羟胺反应的定量关系[J]. 植物生理学通讯, 1990(6): 55−57. Wang A G, Luo G M. Quantitative relation between the reaction of hydroxylamine and superoxide anion radicals in plants[J]. Plant Physiology Communications, 1990(6): 55−57.
[15]	李合生. 植物生理生化实验原理和技术[M]. 北京: 高等教育出版社, 2000: 260−261. Li H S. Assay of malondialdehyde in plants: experiment principle and technology of plant physiology and biochemistry [M]. Beijing: Higher Education Press, 2000: 260−261.
[16]	Gogorcena Y, Iturbe-Omaetxe I, Escuredo P, et al. Antioxidant defenses against activated oxygen in pea nodules subjected to water stress[J]. Plant Physiology, 1995, 108(2): 753−759. doi: 10.1104/pp.108.2.753
[17]	Ma W W, Xu W A, Xu H, et al. Nitric oxide modulates cadmium influx during cadmium-induced programmed cell death in tobacco BY-2 cells[J]. Planta, 2010, 232(2): 325−335. doi: 10.1007/s00425-010-1177-y
[18]	Prochazkova D, Sairam R K, Srivastava G C, et al. Oxidative stress and antioxidant activity as the basis of senescence in maize leaves[J]. Plant Science, 2001, 161(4): 765−771. doi: 10.1016/S0168-9452(01)00462-9
[19]	Nakano Y, Asada K. Hydrogen peroxide is scavenged by ascorbate-specific peroxidase in spinach chloroplasts[J]. Plant and Cell Physiology, 1981, 22(5): 867−880.
[20]	Kampfenkel K, Montagu M V, Inzé D. Extraction and determination of ascorbate and dehydroascorbate from plant tissue[J]. Analytical Biochemistry, 1995, 225: 165−167. doi: 10.1006/abio.1995.1127
[21]	Fang J Y, Wetten A, Johnston J. Headspace volatile markers for sensitivity of cocoa (Theobroma cacao L.) somatic embryos to cryopreservation[J]. Plant Cell Reports, 2008, 27(3): 453−461. doi: 10.1007/s00299-007-0487-4
[22]	Zhang D, Ren L, Chen G Q, et al. ROS-induced oxidative stress and apoptosis-like event directly affect the cell viability of cryopreserved embryogenic callus in Agapanthus praecox[J]. Plant Cell Reports, 2015, 34(9): 1499−1513. doi: 10.1007/s00299-015-1802-0
[23]	Fleck R A, Benson E E, Bremner D H, et al. A comparative study of antioxidant protection in cryopreserved unicellular algae Euglena gracilis and Haematococcus pluvialis[J]. Cryoletters, 2003, 24(4): 213−228.
[24]	Dröge W. Free radicals in the physiological control of cell function[J]. Physiology Review, 2002, 82(1): 47−95.
[25]	Asada K. The water-water cycle in chloroplasts: Scavenging of active oxygens and dissipation of excess photons[J]. Annual Review of Plant Physiology and Plant Molecular Biology, 1990, 50: 601−639.
[26]	Agarwal S. Increased antioxidant activity in Cassia seedlings under UV-B radiation[J]. Biologia Plantarum, 2007, 51(1): 157−160. doi: 10.1007/s10535-007-0030-z
[27]	Benson E E. Free radical damage in stored plant germplasm [M]. Rome: International Board for Plant Genetic Resources, 1990.
[28]	Benson E E, Bremner D. Oxidative stress in the frozen plant: a free radical point of view [M]//Fuller B J, Lane N, Benson E E. Life in the frozen state. Boca Raton: CRC Press, 2004: 205−241.
[29]	Uchendu E E, Leonard S W, Traber M G, et al. Vitamins C and E improve regrowth and reduce lipid peroxidation of blackberry shoot tips following cryopreservation[J]. Plant Cell Reports, 2010, 29: 25−35.
[30]	Uchendu E E, Muminova M, Gupta S, et al. Antioxidant and anti-stress compounds improve regrowth of cryopreserved Rubus shoot tips[J]. In Vitro Cellular & Developmental Biology-Plant, 2010, 46(4): 386−393.
[31]	Reape T J, McCabe P F. Apoptotic-like regulation of programmed cell death in plants[J]. Apoptosis, 2010, 15: 249−256. doi: 10.1007/s10495-009-0447-2
[32]	Baust J M, Buskirk R V, Baust J G. Gene activation of the apoptotic caspase cascade following cryogenic storage[J]. Cell Preservation Technology, 2002, 1(1): 63−80. doi: 10.1089/15383440260073301
[33]	Bissoyi A, Pramanik K. Role of the apoptosis pathway in cryopreservation-induced cell death in mesenchymal stem cells derived from umbilical cord blood[J]. Biopreservation and Biobanking, 2014, 12(4): 246−254. doi: 10.1089/bio.2014.0005

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Effects of ROS-induced oxidative stress and programmed cell death on pollen viability after cryopreservation