Research Progress in Plant Antifreeze Protein

doi:10.11983/CBB22248

Abstract

Abstract: Temperature is one of the major environmental determinants of plant geographical distribution. Plants distri- buted at high latitudes or altitudes usually suffer a period of sub-zero temperature during their life cycle. When the ambient temperature drops to the freezing point, the water molecules in plants form ice crystals, causing fatal damage to plant tissue structure. In order to adapt to the freezing environment, the pathogenesis-related protein PR (PR) and its related WRKY transcription factors in cold climate plants have evolved into antifreeze proteins (AFPs) that can bind specifically to the ice surface and effectively inhibit the formation and growth of ice crystals. Currently, AFPs have been identified in nearly 100 plant species, such as winter rye (Secale cereale). Compared with insect AFPs, plant AFPs have extremely high recrystallization inhibition activity, which can effectively prevent the formation of large ice crystals in vivo. Both low temperature and pathogens can induce AFP synthesis in cold climate plants. Interestingly, only the cold-induced AFPs have dual molecular functions as hydrolase/antifreeze activity. The PR-AFPs, however, possess only one of hydrolase/antifreeze activites, whose conversion is controlled/regulated by post-translational peptide differential folding, as suggested with growing evidence. AFP has gradually become one of the hot targets in botanical research due to its unique molecular function and its promising applications. This paper will provide a systematic review of recent progress in this area.

Key words: plant antifreeze protein, antifreeze activity, molecular evolution, expression regulation

Xiaoyun Dong, Jiaping Wei, Junmei Cui, Zefeng Wu, Guoqiang Zheng, Hui Li, Ying Wang, Haiyan Tian, Zigang Liu. Research Progress in Plant Antifreeze Protein[J]. Chinese Bulletin of Botany, 2023, 58(6): 966-981.

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URL: https://www.chinbullbotany.com/EN/10.11983/CBB22248

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Figures/Tables 5

References 107

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物种名称	材料	AFPs的亚细胞定位	分子量 (kDa)	属性	同源蛋白	参考文献
欧白英 (Solanum dulcamara)	茎	细胞膜和细胞质	67	富含甘氨酸(23.7%), TH=-0.3°C, >30 mg?mL^-1, 高RI活性	WRKY转录因子	Duman, 1994
冬黑麦 (Secale cereale)	叶	质外体	15-38	0.1 mg?mL^-1, TH=0.03°C	几丁质酶、葡聚糖酶和类甜蛋白	Hon et al., 1994, 1995
南极发草 (Deschampsia antarctica)	叶	质外体	29	富含亮氨酸	磺肽素受体激酶	John et al., 2009
白菜型冬油菜 (Brassica rapa)	叶	细胞质和细胞核	38	-	β-1,3-葡聚糖酶	Liu et al., 2019
胡萝卜 (Daucus carota)	根	质外体	36	1 mg?mL^-1时, TH=-0.35°C, 高RI活性	多聚半乳糖醛酸酶抑制剂蛋白	Worrall et al., 1998; Meyer et al., 1999
沙冬青 (Ammopiptanthus mongolicus)	叶	细胞质	40	热稳定蛋白, 糖基化, 20 mg?mL^-1时, TH=0.9°C	凝集素	费云标等, 1994; Yong et al., 2000
冬小麦 (Triticum aestivum)	叶	质外体	21.3	热稳定蛋白, 富含β-折叠和无规则卷曲	类甜蛋白	Chun et al., 1998; Kontogiorgo, 2007
黑麦草 (Lolium perenne)	叶	质外体	29	有RI活性	-	Sidebottom et al., 2000; Pudney et al., 2003
蓝叶云杉 (Picea pungens)	叶	质外体	27	0.4 mg?mL^-1时, TH=(2.02± 0.40)°C	几丁质酶	Jarzabek et al., 2009
无芒雀麦 (Bromus inermis)	细胞培养	分泌物和质外体	33	钙离子非依赖抗冻活性, 六角双锥体冰晶形态	I型几丁质酶	Nakamura et al., 2008
连翘 (Forsythia suspensa)	树皮和叶	细胞质	20	热稳定蛋白, 高RI活性 (6 μg?mL^-1)	与脱水蛋白同源	Simpson et al., 2005
蜡梅 (Chimonanthus praecox)	花冠	质外体	33	1.5 mg?mL^-1时, TH=0.52°C	I型几丁质酶	Zhang et al., 2011
沙棘 (Hippophae rhamnoides)	枝条	质外体	41	糖基化, 热不稳定蛋白, TH=0.19°C, 9倍RI	多聚半乳糖醛酸酶抑制剂蛋白	Gupta et al., 2012
萝卜 (Raphanus sativus)	块茎和叶	质外体	1.32	块茎: TH=(0.2±0.03)°C; 叶: TH=(0.18±0.02)°C	-	Kawahara et al., 2009
欧洲云杉 (Picea abies)	叶	质外体	27和70	0.4 mg?mL^-1时,TH=(2.19± 0.83)°C	几丁质酶	Sabala et al., 1996; Jarzabek et al., 2009
桃 (Prunus persica)	树皮	细胞质、细胞核和木质部薄壁细胞	60	热稳定蛋白, 28.3 μg?mL^-1时, TH=0.06°C	脱水蛋白	Wisniewski et al., 1999

物种名称	材料	AFPs的亚细胞定位	分子量 (kDa)	属性	同源蛋白	参考文献
欧白英 (Solanum dulcamara)	茎	细胞膜和细胞质	67	富含甘氨酸(23.7%), TH=-0.3°C, >30 mg?mL^-1, 高RI活性	WRKY转录因子	Duman, 1994
冬黑麦 (Secale cereale)	叶	质外体	15-38	0.1 mg?mL^-1, TH=0.03°C	几丁质酶、葡聚糖酶和类甜蛋白	Hon et al., 1994, 1995
南极发草 (Deschampsia antarctica)	叶	质外体	29	富含亮氨酸	磺肽素受体激酶	John et al., 2009
白菜型冬油菜 (Brassica rapa)	叶	细胞质和细胞核	38	-	β-1,3-葡聚糖酶	Liu et al., 2019
胡萝卜 (Daucus carota)	根	质外体	36	1 mg?mL^-1时, TH=-0.35°C, 高RI活性	多聚半乳糖醛酸酶抑制剂蛋白	Worrall et al., 1998; Meyer et al., 1999
沙冬青 (Ammopiptanthus mongolicus)	叶	细胞质	40	热稳定蛋白, 糖基化, 20 mg?mL^-1时, TH=0.9°C	凝集素	费云标等, 1994; Yong et al., 2000
冬小麦 (Triticum aestivum)	叶	质外体	21.3	热稳定蛋白, 富含β-折叠和无规则卷曲	类甜蛋白	Chun et al., 1998; Kontogiorgo, 2007
黑麦草 (Lolium perenne)	叶	质外体	29	有RI活性	-	Sidebottom et al., 2000; Pudney et al., 2003
蓝叶云杉 (Picea pungens)	叶	质外体	27	0.4 mg?mL^-1时, TH=(2.02± 0.40)°C	几丁质酶	Jarzabek et al., 2009
无芒雀麦 (Bromus inermis)	细胞培养	分泌物和质外体	33	钙离子非依赖抗冻活性, 六角双锥体冰晶形态	I型几丁质酶	Nakamura et al., 2008
连翘 (Forsythia suspensa)	树皮和叶	细胞质	20	热稳定蛋白, 高RI活性 (6 μg?mL^-1)	与脱水蛋白同源	Simpson et al., 2005
蜡梅 (Chimonanthus praecox)	花冠	质外体	33	1.5 mg?mL^-1时, TH=0.52°C	I型几丁质酶	Zhang et al., 2011
沙棘 (Hippophae rhamnoides)	枝条	质外体	41	糖基化, 热不稳定蛋白, TH=0.19°C, 9倍RI	多聚半乳糖醛酸酶抑制剂蛋白	Gupta et al., 2012
萝卜 (Raphanus sativus)	块茎和叶	质外体	1.32	块茎: TH=(0.2±0.03)°C; 叶: TH=(0.18±0.02)°C	-	Kawahara et al., 2009
欧洲云杉 (Picea abies)	叶	质外体	27和70	0.4 mg?mL^-1时,TH=(2.19± 0.83)°C	几丁质酶	Sabala et al., 1996; Jarzabek et al., 2009
桃 (Prunus persica)	树皮	细胞质、细胞核和木质部薄壁细胞	60	热稳定蛋白, 28.3 μg?mL^-1时, TH=0.06°C	脱水蛋白	Wisniewski et al., 1999

蛋白名称	蛋白来源	受体植物	转基因表型	参考文献
afa3	冬季比目鱼 (Pseudopleuronectes americanus)	烟草	重组蛋白在细胞内积累, 抑制冰晶重结晶	Hightower et al., 1991
Type I afp	冬季比目鱼 (P. americanus)	烟草和马铃薯	重组proAFP蛋白在4°C积累, 但在25°C无积累; LT50降低1°C	Wallis et al., 1997; Kenward et al., 1999
TaAFPI	冬季比目鱼(P. americanus)	冬小麦	蛋白质在质外体中积累; 表现出很强的抗冻活性, 即使在-7°C也表现出很强的耐冷性	Khanna and Daggard, 2006
DcAFP	胡萝卜(Daucus carota)	烟草和拟南芥	在-2°C表现出耐冷性, 在质外体积累	Worrall et al., 1998; Meyer et al., 1999
Type II afp	美绒杜父鱼 (Hemitripterus americanus)	烟草	积累的蛋白质无抗冻活性	Kenward et al., 1999
sbwAFP	云杉蚜虫 (Choristoneura fumiferana)	烟草	冰核蛋白在质外体中积累; 提取物显示TH/RI活性	Holmberg et al., 2001
THPI	云杉蚜虫(C. fumiferana)	拟南芥	转基因植株的耐寒性增强	Zhu et al., 2010
dAFP-1	火色甲虫 (Dendroides canadensis)	拟南芥	在质外体中积累, TH=0.42°C	Huang et al., 2002
MpAFP149	沙漠甲虫 (Microdera punctipennis)	烟草	在质外体中积累; 在-1°C时, 耐冷性增强	Wang et al., 2008
LpIRIa和LpIRIb	黑麦草(Lolium perenne)	拟南芥	在-8-4°C范围内提高存活率	Zhang et al., 2010
LpAFP、LpIRI2和LpIRI3	多年生黑麦草(L. perenne)	拟南芥	在-6°C时, 离子渗漏降低12%-39%; 在-8- -5°C范围内提高存活率	Bredow et al., 2017
BrAFP1	白菜型冬油菜(Brassica rapa)	拟南芥	在-4°C提高存活率	Dong et al., 2020
IRIPs	南极发草 (Deschampsia antarctica)	拟南芥	过表达植株抗冻活性增强, 提取液中有RI活性	John et al., 2009

蛋白名称	蛋白来源	受体植物	转基因表型	参考文献
afa3	冬季比目鱼 (Pseudopleuronectes americanus)	烟草	重组蛋白在细胞内积累, 抑制冰晶重结晶	Hightower et al., 1991
Type I afp	冬季比目鱼 (P. americanus)	烟草和马铃薯	重组proAFP蛋白在4°C积累, 但在25°C无积累; LT50降低1°C	Wallis et al., 1997; Kenward et al., 1999
TaAFPI	冬季比目鱼(P. americanus)	冬小麦	蛋白质在质外体中积累; 表现出很强的抗冻活性, 即使在-7°C也表现出很强的耐冷性	Khanna and Daggard, 2006
DcAFP	胡萝卜(Daucus carota)	烟草和拟南芥	在-2°C表现出耐冷性, 在质外体积累	Worrall et al., 1998; Meyer et al., 1999
Type II afp	美绒杜父鱼 (Hemitripterus americanus)	烟草	积累的蛋白质无抗冻活性	Kenward et al., 1999
sbwAFP	云杉蚜虫 (Choristoneura fumiferana)	烟草	冰核蛋白在质外体中积累; 提取物显示TH/RI活性	Holmberg et al., 2001
THPI	云杉蚜虫(C. fumiferana)	拟南芥	转基因植株的耐寒性增强	Zhu et al., 2010
dAFP-1	火色甲虫 (Dendroides canadensis)	拟南芥	在质外体中积累, TH=0.42°C	Huang et al., 2002
MpAFP149	沙漠甲虫 (Microdera punctipennis)	烟草	在质外体中积累; 在-1°C时, 耐冷性增强	Wang et al., 2008
LpIRIa和LpIRIb	黑麦草(Lolium perenne)	拟南芥	在-8-4°C范围内提高存活率	Zhang et al., 2010
LpAFP、LpIRI2和LpIRI3	多年生黑麦草(L. perenne)	拟南芥	在-6°C时, 离子渗漏降低12%-39%; 在-8- -5°C范围内提高存活率	Bredow et al., 2017
BrAFP1	白菜型冬油菜(Brassica rapa)	拟南芥	在-4°C提高存活率	Dong et al., 2020
IRIPs	南极发草 (Deschampsia antarctica)	拟南芥	过表达植株抗冻活性增强, 提取液中有RI活性	John et al., 2009