Research Progress of Hyperhydricity Mechanism in Plant Seedling Growth

doi:10.11983/CBB21126

Abstract

Abstract: Hyperhydricity (HH) or vitrification is a physiological disorder during plant growth, which shows a typical translucent phenotype like water-soaked that often occurs in the plant tissue culture. Vitrification is one of the three main influencing factors that limit the tissue culture technology and the commercialized production of seedlings during the plant tissue culture, but its molecular mechanism is still unclear by far. Using plantlets from the tissue culture as a research object often lead to an interference of man-made factors, which can be avoided by non-tissue culture material to reveal the molecular mechanism of vitrification in nature. This review summarized the recent progress of mechanism for inducing HH in non-tissue culture plants, including the abnormal deposit of suberin, the reduction of cuticular wax, the lipid peroxidation in cellular membranes and the disrupted transmembrane transport of ion or water, to provide new clues and thinking for hyperhydricity in plant seedling growth.

Key words: aquaporins, cell membrane, cuticular wax, hyperhydricity, suberin

Qingping Zhao, Yuping liang, Fangyuan Zhou, Xiang Zhao. Research Progress of Hyperhydricity Mechanism in Plant Seedling Growth[J]. Chinese Bulletin of Botany, 2022, 57(1): 90-97.

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URL: https://www.chinbullbotany.com/EN/10.11983/CBB21126

https://www.chinbullbotany.com/EN/Y2022/V57/I1/90

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References 49

[1]	高弘扬, 许丹芸, 周良云, 罗碧, 杨全 (2019). 试管苗玻璃化现象的研究进展. 现代农业科技 (20), 52-56, 59.
[2]	黄世安, 董晓庆, 朱守亮 (2021). 园艺植物表皮蜡质研究进展. 安徽农业科学 49, 6-10.
[3]	李海兵, 周娜, 赵姣, 李翔, 冯秋妍, 赵喜亭, 李明军 (2010). 怀山药种质资源的包埋玻璃化超低温保存与植株再生. 植物学报 45, 379-383. DOI
[4]	吕敏, 夏秀英, 徐品三, 李波, 郭照东 (2014). 蓝莓玻璃化试管苗的显微结构及生理生化特性变化. 植物生理学报 50, 453-460.
[5]	牟香丽, 王超, 王帅 (2013). 甘蓝无蜡粉突变体叶表皮蜡质超微结构观察. 中国蔬菜 (4), 32-37.
[6]	田田, 刘鹏飞, 乔光, 文晓鹏 (2015). 玛瑙红樱桃离体快繁及组培苗的变异检测. 西南大学学报(自然科学版) 37, 30-37.
[7]	王玉英, 王琴, 李枝林, 魏全涛, 商正蕊, 凌青 (2020). 虎雪兰玻璃化超低温法脱毒技术的研究. 北方园艺 (5), 61-66.
[8]	徐铭, 赵子健, 夏秀英 (2020). 植物水孔蛋白PIP2表达量快速无标记检测. 大连理工大学学报 60, 15-21.
[9]	赵一鸣, 隋宝凤, 张欣燕, 侯凯琳, 刘柏玲 (2019). 组织培养中玻璃化现象的研究进展. 国土与自然资源研究 (6), 68-74.
[10]	Adlassnig W, Peroutka M, Lendl T (2011). Traps of carnivorous pitcher plants as a habitat: composition of the fluid, biodiversity and mutualistic activities. Ann Bot 107, 181-194. DOI URL
[11]	Alonso-Serra J, Safronov O, Lim KJ, Fraser-Miller SJ, Blokhina OB, Campilho A, Chong SL, Fagerstedt K, Haavikko R, Helariutta Y, Immanen J, Kangasjärvi J, Kauppila TJ, Lehtonen M, Ragni L, Rajaraman S, Räsänen RM, Safdari P, Tenkanen M, Yli-Kauhaluoma JT, Teeri TH, Strachan CJ, Nieminen K, Salojärvi J (2019). Tissue-specific study across the stem reveals the chemistry and transcriptome dynamics of birch bark. New Phytol 222, 1816-1831. DOI PMID
[12]	Andersen TG, Barberon M, Geldner N (2015). Suberization-the second life of an endodermal cell. Curr Opin Plant Biol 28, 9-15. DOI PMID
[13]	Bakir Y, Eldem V, Zararsiz G, Unver T (2016). Global transcriptome analysis reveals differences in gene expression patterns between nonhyperhydric and hyperhydric peach leaves. Plant Genome 9, 2.
[14]	Barták M, Pláteníková E, Carreras H, Hájek J, Morkusová J, Mateos AC, Marečková M (2018). Effect of UV-B radiation on the content of UV-B absorbing compounds and photosynthetic parameters in Parmotrema austrosinense from two contrasting habitats. Plant Biol 20, 808-816. DOI URL
[15]	Beisson F, Li Y, Bonaventure G, Pollard M, Ohlrogge JB (2007). The acyltransferase GPAT5 is required for the synthesis of suberin in seed coat and root of Arabidopsis. Plant Cell 19, 351-368. PMID
[16]	Bose J, Pottosin II, Shabala SS, Palmgren MG, Shabala S (2011). Calcium efflux systems in stress signaling and adaptation in plants. Front Plant Sci 2, 85.
[17]	Costa A, Luoni L, Marrano CA, Hashimoto K, Köster P, Giacometti S, De Michelis MI, Kudla J, Bonza MC (2017). Ca²⁺-dependent phosphoregulation of the plasma membrane Ca²⁺-ATPase ACA8 modulates stimulus-induced calcium signatures. J Exp Bot 68, 3215-3230. DOI PMID
[18]	Debergh P, Harbaoui Y, Lemeur R (1981). Mass propagation of globe artichoke (Cynara scolymus): evaluation of different hypotheses to overcome vitrification with special reference to water potential. Physiol Plant 53, 181-187. DOI URL
[19]	Delarue M, Santoni V, Caboche M, Bellini C (1997). cristal mutations in Arabidopsis confer a genetically heritable, recessive, hyperhydric phenotype. Planta 202, 51-61. PMID
[20]	Ellison AM, Gotelli NJ (2002). Nitrogen availability alters the expression of carnivory in the northern pitcher plant, Sarracenia purpurea. Proc Natl Acad Sci USA 99, 4409-4412. DOI URL
[21]	Fedi F, O'Neill CM, Menard G, Trick M, Dechirico S, Corbineau F, Bailly C, Eastmond PJ, Penfield S (2017). Awake1, an ABC-type transporter, reveals an essential role for suberin in the control of seed dormancy. Plant Physiol 174, 276-283. DOI URL
[22]	Fontes MA, Otoni WC, Carolino SMB, Brommonschenkel SH, Fontes EPB, Fári M, Louro RP (1999). Hyperhydricity in pepper plants regenerated in vitro: involvement of BiP (Binding Protein) and ultrastructural aspects. Plant Cell Rep 19, 81-87. DOI PMID
[23]	Gribble KD, Sarafis V, Conroy J (2003). Vitrified plants: towards an understanding of their nature. Phytomorphology 53, 1-10.
[24]	Hassannejad S, Bernard F, Mirzajani F, Gholami M (2012). SA improvement of hyperhydricity reversion in thymus daenensis shoots culture may be associated with polyamines changes. Plant Physiol Biochem 51, 40-46. DOI URL
[25]	Hsu YF, Yan JW, Song Y, Zheng M (2021). Sarracenia purpurea glycerol-3-phosphate acyltransferase 5 confers plant tolerance to high humidity in Arabidopsis thaliana. Physiol Plant 173, 1221-1229. DOI URL
[26]	Jackson MB (1985). Ethylene and responses of plants to soil waterlogging and submergence. Annu Rev Plant Physiol 36, 145-174. DOI URL
[27]	Ladaniya MS (2011). Physico-chemical, respiratory and fungicide residue changes in wax coated mandarin fruit stored at chilling temperature with intermittent warming. J Food Sci Technol 48, 150-158.
[28]	Lee BH, Lee H, Xiong LM, Zhu JK (2002). A mitochondrial complex I defect impairs cold-regulated nuclear gene expression. Plant Cell 14, 1235-1251. DOI URL
[29]	Lee EJ, Kim KY, Zhang J, Yamaoka Y, Gao P, Kim H, Hwang JU, Suh MC, Kang B, Lee Y (2021). Arabidopsis seedling establishment under waterlogging requires ABCG5- mediated formation of a dense cuticle layer. New Phytol 229, 156-172. DOI URL
[30]	Li Y, Hou XY, Li XT, Zhao X, Wu ZN, Xiao Y, Guo YJ (2020). Will the climate of plant origins influence the chemical profiles of cuticular waxes on leaves of Leymus chinensis in a common garden experiment? Ecol Evol 10, 543-556. DOI URL
[31]	Muneer S, Soundararajan P, Jeong BR (2016). Proteomic and antioxidant analysis elucidates the underlying mechanism of tolerance to hyperhydricity stress in in vitro shoot cultures of Dianthus caryophyllus. J Plant Growth Regul 35, 667-679. DOI URL
[32]	Panda D, Sarkar RK (2014). Mechanism associated with nonstructural carbohydrate accumulation in submergence tolerant rice (Oryza sativa L.) cultivars. J Plant Interact 9, 62-68. DOI URL
[33]	Phan CT, Hegedus P (1986). Possible metabolic basis for the developmental anomaly observed in in vitro culture, called ‘vitreous plants'. Plant Cell Tiss Org 6, 83-94. DOI URL
[34]	Philippe G, Sørensen I, Jiao C, Sun XP, Fei ZJ, Domozych DS, Rose JK (2020). Cutin and suberin: assembly and origins of specialized lipidic cell wall scaffolds. Curr Opin Plant Biol 55, 11-20. DOI PMID
[35]	Phillips DJ, Matthews GJ (1964). Growth and development of carnation shoot tips in vitro. Bot Gaz 125, 7-12. DOI URL
[36]	Phukan UJ, Jeena GS, Tripathi V, Shukla RK (2018). MaRAP2-4, a waterlogging-responsive ERF from Mentha, regulates bidirectional sugar transporter AtSWEET10 to modulate stress response in Arabidopsis. Plant Biotechnol J 16, 221-233. DOI PMID
[37]	Rae L, Lao NT, Kavanagh TA (2011). Regulation of multiple aquaporin genes in Arabidopsis by a pair of recently duplicated DREB transcription factors. Planta 234, 429-444. DOI URL
[38]	Rosa M, Prado C, Podazza G, Interdonato R, González JA, Hilal M, Prado FE (2009). Soluble sugars-metabolism, sensing and abiotic stress: a complex network in the life of plants. Plant Signal Behav 4, 388-393. DOI URL
[39]	Sade N, Vinocur BJ, Diber A, Shatil A, Ronen G, Nissan H, Wallach R, Karchi H, Moshelion M (2009). Improving plant stress tolerance and yield production: is the tonoplast aquaporin SlTIP2;2 a key to isohydric to anisohydric conversion? New Phytol 181, 651-661. DOI PMID
[40]	Serra O, Hohn C, Franke R, Prat S, Molinas M, Figueras M (2010). A feruloyl transferase involved in the biosynthesis of suberin and suberin-associated wax is required for maturation and sealing properties of potato periderm. Plant J 62, 277-290. DOI URL
[41]	Soundararajan P, Manivannan A, Cho YS, Jeong BR (2017). Exogenous supplementation of silicon improved the recovery of hyperhydric shoots in Dianthus caryophyllus L. by stabilizing the physiology and protein expression. Front Plant Sci 8, 738. DOI PMID
[42]	Sreelekshmi R, Siril EA (2020). Influence of polyamines on hyperhydricity reversion and its associated mechanism during micropropagation of China pink (Dianthus chinensis L.). Physiol Mol Biol Plants 26, 2035-2045. DOI URL
[43]	Tian J, Cheng YQ, Kong XY, Liu M, Jiang FL, Wu Z (2017). Induction of reactive oxygen species and the potential role of NADPH oxidase in hyperhydricity of garlic plantlets in vitro. Protoplasma 254, 379-388. DOI PMID
[44]	Tylová E, Pecková E, Blascheová Z, Soukup A (2017). Casparian bands and suberin lamellae in exodermis of lateral roots: an important trait of roots system response to abiotic stress factors. Ann Bot 120, 71-85. DOI URL
[45]	van den Dries N, Giannì S, Czerednik A, Krens FA, de Klerk GJM (2013). Flooding of the apoplast is a key factor in the development of hyperhydricity. J Exp Bot 64, 5221-5230. DOI URL
[46]	Yang O, Popova OV, Süthoff U, Lüking I, Dietz KJ, Golldack D (2009). The Arabidopsis basic leucine zipper transcription factor AtbZIP24 regulates complex transcriptional networks involved in abiotic stress resistance. Gene 436, 45-55. DOI URL
[47]	Zhang J, Zhang XD, Wang RP, Li WQ (2014). The plasma membrane-localised Ca²⁺-ATPase ACA8 plays a role in sucrose signaling involved in early seedling development in Arabidopsis. Plant Cell Rep 33, 755-766. DOI PMID
[48]	Zhu DL, Wu Z, Cao GY, Li JG, Wei J, Tsuge T, Gu HY, Aoyama T, Qu LJ (2014). TRANSLUCENT GREEN, an ERF family transcription factor, controls water balance in Arabidopsis by activating the expression of aquaporin genes. Mol Plant 7, 601-615. DOI URL
[49]	Zilberman D, Gehring M, Tran RK, Ballinger T, Henikoff S (2007). Genome-wide analysis of Arabidopsis thaliana DNA methylation uncovers an interdependence between methylation and transcription. Nat Genet 39, 61-69. PMID

材料类型	基因或蛋白名称	作用	调节玻璃化机制	参考文献
非组培材料	ABCG5	ABC转运蛋白G亚家族成员	通过调节表皮蜡质形成, 使表皮角质层的厚度降低, 渗透率明显增加, 外界水分大量渗入引发玻璃化	Lee et al., 2021
	ACA8	IIB亚家族中的P型自抑制Ca²⁺-ATP酶	主要参与调节胞内Ca²⁺的输出, 维持细胞内的低Ca²⁺水平, 突变后细胞膜完整性受损, 细胞内离子大量泄漏引发玻璃化	Zhang et al., 2014
	CRI1	拟南芥cristal突变体, 功能未知	突变后可能通过促进细胞渗透压升高、细胞分裂素水平增高以及表面的角质层改变导致植物玻璃化	Delarue et al., 1997
	FRO1	编码NADH脱氢酶	编码的NADH脱氢酶是线粒体电子传递链的一个亚基, 突变后导致线粒体内电子传递异常, 活性氧大量积累, 细胞膜的完整性受损, 细胞内离子大量泄漏引发玻璃化	Lee et al., 2002
	GPAT5	甘油-3-磷酸酰基转移酶5	通过影响软木脂及其相关蜡质的合成使植物的渗透率增加, 导致高湿环境中水分大量渗入引发玻璃化	Hsu et al., 2021
	TIP1;1	编码水孔蛋白	超表达后导致叶肉细胞间水分过度积累引发玻璃化	Zhu et al., 2014
	TG	拟南芥ERF家族转录因子	超表达后通过影响水孔蛋白基因TIP1;1功能导致叶肉细胞间水分过度积累引发玻璃化	Zhu et al., 2014
组培材料	ACS1和ACOI	乙烯合成相关基因	基因表达被抑制后通过降低内源乙烯含量间接促进H₂O₂含量降低和气孔开度增加, 促进玻璃化植物的失水和复壮	Sreelekshmi and Siril, 2020
	BiP蛋白同源蛋白	受生理胁迫表达	在植物玻璃化中的作用机制目前还不清楚	Fontes et al., 1999
	PAL	苯丙氨酸解氨酶	突变后降低木质素的合成引发玻璃化	Phan and Hegedus, 1986
	NADPH氧化酶	烟酰胺腺嘌呤二核苷酸磷酸氧化酶	通过诱导活性氧的产生引发玻璃化	Tian et al., 2017

材料类型	基因或蛋白名称	作用	调节玻璃化机制	参考文献
非组培材料	ABCG5	ABC转运蛋白G亚家族成员	通过调节表皮蜡质形成, 使表皮角质层的厚度降低, 渗透率明显增加, 外界水分大量渗入引发玻璃化	Lee et al., 2021
	ACA8	IIB亚家族中的P型自抑制Ca²⁺-ATP酶	主要参与调节胞内Ca²⁺的输出, 维持细胞内的低Ca²⁺水平, 突变后细胞膜完整性受损, 细胞内离子大量泄漏引发玻璃化	Zhang et al., 2014
	CRI1	拟南芥cristal突变体, 功能未知	突变后可能通过促进细胞渗透压升高、细胞分裂素水平增高以及表面的角质层改变导致植物玻璃化	Delarue et al., 1997
	FRO1	编码NADH脱氢酶	编码的NADH脱氢酶是线粒体电子传递链的一个亚基, 突变后导致线粒体内电子传递异常, 活性氧大量积累, 细胞膜的完整性受损, 细胞内离子大量泄漏引发玻璃化	Lee et al., 2002
	GPAT5	甘油-3-磷酸酰基转移酶5	通过影响软木脂及其相关蜡质的合成使植物的渗透率增加, 导致高湿环境中水分大量渗入引发玻璃化	Hsu et al., 2021
	TIP1;1	编码水孔蛋白	超表达后导致叶肉细胞间水分过度积累引发玻璃化	Zhu et al., 2014
	TG	拟南芥ERF家族转录因子	超表达后通过影响水孔蛋白基因TIP1;1功能导致叶肉细胞间水分过度积累引发玻璃化	Zhu et al., 2014
组培材料	ACS1和ACOI	乙烯合成相关基因	基因表达被抑制后通过降低内源乙烯含量间接促进H₂O₂含量降低和气孔开度增加, 促进玻璃化植物的失水和复壮	Sreelekshmi and Siril, 2020
	BiP蛋白同源蛋白	受生理胁迫表达	在植物玻璃化中的作用机制目前还不清楚	Fontes et al., 1999
	PAL	苯丙氨酸解氨酶	突变后降低木质素的合成引发玻璃化	Phan and Hegedus, 1986
	NADPH氧化酶	烟酰胺腺嘌呤二核苷酸磷酸氧化酶	通过诱导活性氧的产生引发玻璃化	Tian et al., 2017