造礁珊瑚热适应相关功能基因的研究进展

马玉玲; 俞小鹏; 余克服; 陈俊伶; 郑月; 陈健

造礁珊瑚热适应相关功能基因的研究进展

马玉玲^1,,
俞小鹏^1, ,,
余克服^{1, 2,},
陈俊伶¹,
郑月¹,
陈健¹

1.
广西大学广西南海珊瑚礁研究重点实验室/珊瑚礁研究中心/海洋学院，广西南宁 530004
2.
南方海洋科学与工程广东省实验室（广州），广东广州 511458

基金项目: 国家自然科学基金重大项目（42030502 ）、广西科技基地与人才专项（桂科 AD25069075）、国家自然科学基金重点项目(42090041)、国家自然科学基金（ 42406143）；广西研究生教育创新计划资助项目（YCBZ2024045）。

详细信息

作者简介:
马玉玲（2001—），女，广西崇左人，硕士，主要研究生物与生态方向。E-mail：2327301017@st.gxu.edu.cn

通讯作者:
余克服，教授，主要从事南海珊瑚礁地质和生态环境方面的研究工作。E-mail：kefuyu@scsio.ac.cn；俞小鹏，助理教授，主要从事南海珊瑚生态与环境适应机制研究工作。E-mail：yuxiaopeng100@foxmail.com

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出版历程
- 收稿日期: 2025-01-12
- 修回日期: 2025-05-07
- 网络出版日期: 2025-05-30

摘要

摘要: 全球变暖和极端高温事件导致了珊瑚大规模白化，引起全球珊瑚礁生态系统的快速退化。识别热适应相关的功能基因有助于进一步揭示珊瑚对全球变暖的响应及适应策略，科学预测珊瑚礁生态系统的发育趋势。但目前对珊瑚共生功能体热适应分子机制的认识非常不足。因此，本文综述了珊瑚热适应相关功能基因的研究进展。热适应相关基因在珊瑚受到热胁迫后会产生一系列的连锁反应。首先，Toll受体等识别受体识别到热胁迫后参与信号通路激活进而启动免疫响应过程，主要包括：热休克蛋白基因上调使变性多肽重新折叠；抗氧化蛋白基因上调避免活性氧损伤；细胞凋亡与细胞焦亡基因清除“有害”细胞。随着热胁迫加剧，珊瑚会启动一系列复杂过程共同维持细胞稳态，包括：光保护蛋白基因快速修复虫黄藻光系统、宿主荧光蛋白基因维持氧化平衡；钙离子通道蛋白基因维持细胞内Ca²⁺水平稳定；代谢基因保持代谢平衡以确保营养供给；细胞周期调控基因抑制细胞复制以保存能量；细胞骨架基因维持珊瑚骨架的完整性；泛素相关基因调节蛋白质的去泛素化等。此外，反复出现的热胁迫对珊瑚具有驯化作用，可能通过减缓珊瑚宿主代谢、减少热胁迫相关蛋白质的损伤、提高抗氧化物和铵同化酶等活性等提高珊瑚耐热性。
- 全球变暖 /
- 造礁珊瑚 /
- 热适应 /
- 功能基因 /
- 热驯化
Abstract: Global warming and extreme thermal events have induced widespread coral bleaching, leading to the rapid degradation of coral reef ecosystems across the globe. Identifying functional genes associated with thermotolerance is crucial for elucidating coral adaptation mechanisms to climate warming and enabling scientific predictions regarding coral reef ecosystem trajectories. However, the current understanding of the molecular mechanism of coral holobiont in response to heat stress is very insufficient. Therefore, this paper reviews the research progress of functional genes related to coral thermal adaptation. Initially, pattern recognition receptors (PRRs), including Toll-like receptors (TLRs), play a crucial role in detecting heat stress and activating downstream signaling cascades, thereby initiating the immune response process. These responses primarily involve: upregulation of heat shock proteins (HSPs) to facilitate the refolding of denatured polypeptides; induction of antioxidant protein genes to mitigate oxidative damage caused by reactive oxygen species (ROS); genes associated with apoptosis and pyroptosis play a crucial role in eliminating "harmful" cells. As thermal stress intensifies, corals initiate a sophisticated network of cellular processes to maintain. As heat stress intensifies, corals initiate a series of complex processes to jointly maintain cellular homeostasis. This includes: rapid activation of photoprotective protein genes to repair the photosynthetic apparatus of Symbiodiniaceae; expression of host fluorescent proteins to maintain redox balance; calcium channel proteins maintain the stability of intracellular Ca²⁺ levels; modulation of metabolic pathways to ensure adequate nutrient supply; inhibition of cell cycle progression to conserve energy; maintenance of cytoskeletal integrity to preserve structural stability; and regulation of ubiquitin-proteasome system for protein quality control. Furthermore, recurrent thermal stress events can induce acclimatization in corals, potentially enhancing their thermal tolerance through multiple mechanisms: downregulation of host metabolic rate, protection of heat-sensitive proteins, and upregulation of antioxidant enzymes and ammonium assimilation pathways.
- global warming /
- coral reef /
- thermal adaptation /
- functional genes /
- thermal acclimation

HTML全文

图 1 热适应相关功能基因变化示意图

Fig. 1 Schematic diagram of changes in functional genes related to thermal adaptation

下载: 全尺寸图片幻灯片

图 2 热胁迫后造礁珊瑚关键热适应基因变化。（蓝色为下调，红色为上调）

Fig. 2 Key heat adaptation gene changes in corals after heat stress.(Blue is downregulated and upregulated in red)

下载: 全尺寸图片幻灯片

表 1 珊瑚热适应相关功能基因列表

Tab. 1 List of functional genes related to coral's thermal adaptation

	研究对象	采用技术	GenBank Acc.	基因（蛋白）	已开展研究珊瑚物种	研究区域	潜在功能	热胁迫响应过程	参考文献
免疫相关基因	珊瑚宿主	RNA-Seq ；cDNA 微阵列分析	NW018149896	Nf-kβ1	Acropora millepora、 Acropora aspera	大堡礁	DNA修复，染色质稳定相关	温度升高表达量降低	van de Water et al ^[45] van de Water et al ^[46]
			NW018149776	Nf-kβ2	Acropora millepora、 Acropora aspera	大堡礁	DNA修复，染色质稳定相关	温度升高表达量降低	van de Water et al ^[45] van de Water et al ^[46]
			NW018148758	补体因子c3样蛋白（C3-Am）	Montastraea faveolata； Acropora millepora、 Acropora aspera	加勒比海；大堡礁	免疫相关；病原体的直接杀伤	温度升高表达量升高	Desalvo et al^[47] van de Water et al ^[45] van de Water et al ^[46]
	珊瑚宿主；虫黄藻	RNA-Seq ；cDNA 微阵列分析	XM020776963	C型凝集素	Montastraea faveolata； Acropora millepora、 Pocillopora damicornis	加勒比海；南海	识别病原菌达到免疫作用	温度升高表达量降低	吴逸波^[48] Wu et al ^[49] Desalvo et al ^[39]
	珊瑚宿主；虫黄藻	RNA-Seq ；cDNA 微阵列分析	NW018150402	半乳糖凝集素（galectin）		加勒比海；南海	识别病原菌达到免疫作用	温度升高表达量降低	吴逸波^[48] Wu et al ^[49] Desalvo et al ^[39]
	珊瑚宿主	RNA-Seq ；cDNA 微阵列分析	—	HSP16	Porites astreoides	墨西哥湾	抗氧化作用；抗凋亡	温度升高表达量升高	Kenkel et al ^[50]
			—	HSP32	Pocillopora damicornis	琉球群岛	抗氧化作用；抗凋亡		Thummasan et al ^[51]
			GAL06223	HSP60	Pocillopora damicornis； Seriatopora caliendrum； Montastraea faveolata	琉球群岛；地中海；加勒比海	促进新合成蛋白的折叠阻止细胞凋亡		Thummasan et al ^[51] Seveso et al ^[52] Desalvo et al ^[39]
			DR987088	TCP-1		琉球群岛；地中海；加勒比海	促进新合成蛋白的折叠阻止细胞凋亡
	珊瑚宿主；虫黄藻		NW018148923	HSP70	Acropora tenuis、 Acropora muricata ； Goniopora djiboutiensis ；Porites lutea	印度洋；缅甸海；南海	抑制细胞凋亡；变性蛋白重折叠		Louis et al ^[53] Li et al ^[54] Xiao et al ^[55] Sharp et al ^[56]
	珊瑚宿主；虫黄藻		DR988373	HSP90	Montastraea faveolata； Acropora tenuis	加勒比海；琉球群岛	负责新合成多肽的构象成熟和变性蛋白的再成熟		Desalvo et al ^[39] 张懿丹^[57] Yuyama et al ^[27]
	珊瑚宿主		—	HSP100	Pocillopora damicornis	南海	水解酶活性；降解变性多肽聚合体		张懿丹^[57]
	珊瑚宿主；虫黄藻	RNA-Seq；cDNA 微阵列分析	DR987062	Glutathione S-transferasesigma（GST-S）	Montastraea faveolata； Favia favus； Mussismilia sp. Siderastrea sp.； Porites sp.、 Acropora sp. ； Porites lutea Acropora pruinosa	加勒比海；红海；南大西洋；大加纳利岛；南海	免疫作用	温度升高表达量升高	黄晖等^[14] Desalvo et al ^[39] Levy et al ^[58] Martignago et al ^[59] Camilo et al ^[60] Vilas et al ^[61] 蒙林庆等 ^[62] Yu et al ^[8]
			DR988371	Glutathione S-tranferaseMu（GST-M）			细胞防御相关	温度升高表达量降低
			NW018149119	谷胱甘肽过氧化物酶（GSH-Px）			ECM固结，过氧化物酶活性；增强细胞抗氧化能力；增强免疫力	温度升高表达量升高
			NW018150375	超氧化物歧化酶（SOD）
			DR987689	过氧化氢酶（CAT）
			DR988170	锌指蛋白基因（Zn²⁺-metalloprotease）	Montastraea faveolata； Acropora millepora； Porites lutea	加勒比海；大堡礁；南海	锌离子结合转录因子	温度升高表达量升高	Desalvo et al ^[39] Császár et al ^[63] 许昌有等^[64]
			FE039547	Ferritin		加勒比海；大堡礁；南海	铁离子结合；平衡铁浓度	温度升高表达量升高	Desalvo et al ^[39] Császár et al ^[63] 许昌有等^[64]
			CAON1879	细胞色素（p450）	Montastraea faveolata； Pocillopora damicornis； Acropora aspera	加勒比海；南海；大堡礁	参与细胞解毒；抗氧化	温度升高表达量升高	Louis et al ^[11] Liu et al ^[65] Rosic et al ^[66]
		免疫相关基因	珊瑚宿主；虫黄藻	RNA-Seq；RNAi；cDNA 微阵列分析	—	TRX	Acropora tenuis； Diploria strigosa； Acropora cervicornis、 Montastraea faveolata	琉球群岛；百慕大群岛；佛罗里达群岛	螯合活性氧	温度升高表达量升高	Morgan et al ^[67] Yuyama et al ^[37] Edge et al ^[68]
			珊瑚宿主；虫黄藻	RNA-Seq；RNAi；cDNA 微阵列分析	FE040110	NADH-ubiquinone	Montastraea faveolata； Galaxea facicularis； Acropora sp.	琉球群岛	线粒体电子传递；建立合成ATP所需的跨膜质子梯度	温度升高表达量降低	Voolstra et al ^[69]
	珊瑚宿主；虫黄藻		RNA-Seq	NW018150375	Bcl-2	Acropora aspera、 Acropora millepora	大堡礁	调控凋亡	温度升高表达量升高	T.D.A et al ^[70] Pernice et al ^[71]
				NW018150269	caspase 3	Acropora millepora； Pocillopora damicornis； Orbicella faveolata 、 Porites Astreoides；	大堡礁；琉球群岛、南海；加勒比海	细胞凋亡指示剂		Pernice et al ^[71] Thummasan et al ^[51] Yu et al ^[72] Shrestha et al ^[73]
				—	Gasdermins	Pocillopora damicornis	南海	引发细胞焦亡		Jiang et al ^[74]
	珊瑚宿主		RNA-Seq ；cDNA 微阵列分析	NW018148758	补体因子c3样蛋白（C3-Am）	Montastraea faveolata； Acropora millepora、 Acropora aspera	加勒比海；大堡礁	免疫相关；病原体的直接杀伤	温度升高表达量升高	Desalvo et al ^[39] van de Water et al ^[45] van de Water et al ^[46]
				DR988012	组蛋白（H3）	Montastraea faveolata； Acropora formosa	加勒比海、墨西哥湾；大堡礁	核小体组装	温度升高表达量降低	Desalvo et al ^[39] Miller et al ^[75] Voolstra et al ^[76]
				DR988033	组蛋白（H2A）
				DR987246	H2A 家族
代谢相关基因	珊瑚宿主	RNA-Seq；cDNA 微阵列分析	FE040151	MAT 1α	Montastraea faveolata； Galaxea facicularis； Acropora sp.	加勒比海、西大西洋	S-腺苷甲硫氨酸生物合成	温度升高表达量升高	Desalvo et al ^{[39, 47]} Watanabe et al ^[77] Voolstra et al ^[69]
		RNA-Seq	—	异柠檬酸裂解酶（IL）	Acropora millepora； Pocillopora astreoides； Pocillopora woodjonesi、 Pocillopora kelleheri、 Pocillopora verrucose	大堡礁	从脂质β-氧化产物中合成碳水化合物	温度升高表达量升高	Rocker et al ^[78] Kenkel et al ^[79] Sun et al ^[7]
			—	苹果酸合酶（MS）		墨西哥湾	从脂质β-氧化产物中合成碳水化合物	温度升高表达量升高
			—	丙酮酸羧激酶（PEPCK）		南海	促进糖异生增强	温度升高表达量升高
			—	丙酮酸羧化酶（PC）		南海	促进糖异生增强	温度升高表达量升高
			—	甘油醛-3-磷酸脱氢酶（GAPDHs）	Pavona decussata	南海；	参与糖降解，维持珊瑚能量代谢平衡	温度升高表达量升高	Zhang et al ^[80]
			—	丙酮酸脱氢酶复合物（DLATs）
			—	匀浆 1,2 双加氧酶（HGDs）
			—	谷氨酸脱氢酶（GDHs）	Pavona decussata、 Stylophora pistillata	南海；红海	分解代谢谷氨酸以推动 TCA 循环	温度升高表达量升高	Zhang et al ^[80] Rädecker et al ^[81]
			—	谷氨酰胺合成酶（GS）	Stylophora pistillata	红海		温度升高表达量降低	Rädecker et al ^[81]
			—	谷氨酸合酶 (GOGAT)	Stylophora pistillata	红海		温度升高表达量降低	Rädecker et al ^[81]
	共生微生物	宏基因组测序	—	糖基转移酶（GT）	Favites sp.	南海	合成多糖/糖蛋白	温度升高表达量升高	Sun F et al ^[82]
			—	糖苷水解酶（GH）			降解和转化碳水化合物	温度升高表达量降低
			代谢相关基因	共生微生物			降解和转化碳水化合物	温度升高表达量降低		宏基因组测序	—	碳水化合物酯酶（CE）	Favites sp.	南海	降解和转化碳水化合物	温度升高表达量降低	Sun F et al ^[82]
		光保护蛋白相关基因	虫黄藻	RNA-Seq	—	PsaA	Pocillopora woodjones、 Pocillopora kelleheri、 Pocillopora verrucose、 Galaxea astreata、 Acropora tenuis	南海	修复虫黄藻光系统结构；增强光合能力	温度升高表达量升高	Sun et al ^[83] 沈城等^[84] Gong et al ^[85]
PsaC					—
—	PsbA
	PsbB
	PsbC
	PsbD
	PsbO
珊瑚宿主	RNA-Seq ；RNAi；cDNA 微阵列分析		DR987865	GFP	Montastraea faveolata； Acropora yongei； Acropora millepora、 Acropora digitifera、 Montipora digitata； Goniopora lobata、 Goniopora norfolkensis	加勒比海；西太平洋；大堡礁；南海	能量传递受体；光保护；抗氧化与珊瑚颜色相关	随光照的增加减少而快速变化；温度升高表达量降低	Desalvo et al ^[39] Roth et al ^[86] Smith-Keune ^[87] Conaco et al ^[88] 黄文靖^[89]
	RNA-Seq ；cDNA 微阵列分析		—	RFP	Acropora digitifera、 Montipora digitata、 Favites colemani、 Seriatopora caliendrum； Goniopora lobata、 Goniopora norfolkensis	大堡礁；南海			Conaco et al ^[88] 黄文靖^[89]
	RNA-Seq ；cDNA 微阵列分析		—	CFP		大堡礁；南海			Conaco et al ^[88] 黄文靖^[89]
钙离子通道蛋白相关基因	珊瑚宿主	RNA-Seq ；cDNA 微阵列分析	DR987851	Similar to EF-hand domain protein	Montastraea faveolata	加勒比海	Ca²⁺ 结合区域	温度升高表达量降低	Desalvo et al ^[39]
			DR987178	CaM	Montastraea faveolata； Galaxea astreata、 Acropora muricata	加勒比海；南海	视紫红素介导的信号调节；维持Ca²⁺平衡	高温下表达量降低	Desalvo et al ^[39] Huang et al ^[90] 黄元佳^[91] Chiou et al ^[92]
			NW018149378	CRT	Montastraea faveolata； Galaxea astreata； Acropora tenuis	加勒比海、墨西哥湾；南海；琉球群岛	维持 Ca²⁺ 稳态；内质网 ER Ca²⁺ 容量的调节	温度升高表达量降低	Desalvo et al ^[39] 黄元佳^[91] Huang et al ^[93] Voolstra et al ^[76] Yuyama et al ^[27]
			DR987943	Galaxin	Montastraea faveolata、 Galaxea fascicularis	加勒比海	有机基质可溶性蛋白；作为分子伴侣协助维持细胞内Ca²⁺稳态水平		Desalvo et al ^[39]
			NW018148627	TnC	Acropora muricata	南海、东大西洋	有机基质可溶性蛋白；作为分子伴侣协助维持细胞内Ca²⁺稳态水平		Chiou et al Weston et al ^[94]
			DR987097	SCRiP3A	Montastraea faveolata	加勒比海、墨西哥湾	分泌肽；细胞凋亡相关		黄晖等^[14] Desalvo et al ^[39] Reyes-Bermudez et al ^[95]
			DR987884	SCRiP5
			DR987486	SCRiP8
			DR987831	SCRiP1
			DR987097	SCRiP2
			DR987965	SCRiP7
细胞生长调控基因	珊瑚宿主	RNA-Seq ；cDNA 微阵列分析	NW018148815	DNA replication licensing factor mcm7-A	Montastraea faveolata； Acropora tenuis	加勒比海、墨西哥湾；琉球群岛	DNA 复制许可因子	温度升高表达量降低	Desalvo et al ^[39] Yuyama et al ^[27] Voolstra et al ^[76]
			NW018150375	DNAJ （Hsp40）	Montastraea faveolata； Acropora tenuis	加勒比海、墨西哥湾；琉球群岛	参与内质网未折叠蛋白反应	温度升高表达量升高	Desalvo et al ^[39] Yuyama et al ^[27] Voolstra et al ^[76]
			DR986717	RPL3	Montastraea faveolata； Acropora pruinosa、 Acropora nasuta	加勒比海；南海	蛋白质合成；核糖体的结构成分	温度升高表达量升高	Desalvo et al ^[39] Tian and W ^[96]
			DR986615	RPL9
			细胞生长调控基因	珊瑚宿主						RNA-Seq ；cDNA 微阵列分析	DR988078	RPL14	Montastraea faveolata； Acropora pruinosa、 Acropora nasuta	加勒比海；南海	蛋白质合成；核糖体的结构成分	温度升高表达量升高	Desalvo et al ^[39] Tian and W ^[96]
											AXP85384	RPL16
											DR987703	RPL23
											DR987703	RPL26
											DR986615	RPS2
											DR988446	RP S3
											DR988446	RP S5
											DR988266	RPS7
											DR986825	RPS25
					NW018148536	细胞周期基因（CDK2）	Montastraea faveolata	加勒比海、墨西哥湾	调控G1/S期		温度升高表达量降低	Desalvo et al ^[39] Voolstra et al ^[76]
其他基因	珊瑚宿主	RNA-Seq ；cDNA 微阵列	DR988150	凝胶素Gelsolin （GSN）	Montastraea faveolata； Pocillopora astreoides、 Acropora cervicornis	加勒比海；西大西洋	钙调节的肌动蛋白切断蛋白	温度升高表达量降低	Desalvo et al ^[39] Vollmer et al ^[97] Kenkel et al ^[98]
			DR986355	原肌球蛋白（TPM）			肌动蛋白结合细胞骨架成分
			FE039783	Lethal giant larvae homologue 2 （LGL2）			细胞骨架组织；半桥体组装
			DR988233	肌球蛋白 9A （MYO9A）			肌动蛋白依赖性ATP酶活性	温度升高表达量升高
			DR987650	肌球蛋白 7A （MYO7A）			肌动蛋白依赖性ATP酶活性	温度升高表达量升高
	珊瑚宿主	RNA-Seq ；cDNA 微阵列	DR986515	泛素偶联酶 E2S	Montastraea faveolata； Galaxea fascicularis、 Montipora capricornis	加勒比海；东大西洋	蛋白质的去泛素化；膜转运	温度升高表达量降低	Desalvo et al ^[39] Yohann et al ^[99]
	珊瑚宿主	RNA-Seq ；cDNA 微阵列	DR987159	泛素特异性蛋白酶 24 （USP24）		加勒比海；东大西洋	蛋白质的去泛素化	温度升高表达量升高	Desalvo et al ^[39] Yohann et al ^[99]

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