药学学报

Family	Number	Member	GenBank accession	Bioinformation	Tissue expression	Elicitor	Reference
AP2/ERF	179	SmERF72	-	699 bp	Periderm	-	[25, 28]
		SmERF98	-	891 bp	Xylem	-	[25]
		SmERF73	QRQ89295.1	780 bp ORF, 259 aa	Root	YE+Ag⁺, MeJA	[20]
		SmERF128	MG897156	633 bp, 210 aa	Periderm	-	[29]
		SmERF1L1	MH006594	741 bp ORF, 246 aa	Stem	MeJA, YE, SA, ET	[30]
		SmERF2	-	741 bp ORF, 246 aa	Stem	YE, MeJA, ET, SA	[31]
		SmERF6	KY988300	561 bp ORF, 186 aa	Root	ET	[32]
		SmERF8	MH006600	654 bp ORF, 217 aa	Root head	ET	[33]
		SmAP2/ERF82	-	582 bp CDS, 193 aa	Root	-	[26]
		SmERF1	KC405081.1	549 bp ORF, 182 aa	-	YE, MeJA	[34]
bHLH	127	SmbHLH61	-	1 008 bp ORF, 335 aa	Root	MeJA, SA	[35, 36]
		SmbHLH74	KP257507.1	696 bp CDS, 231 aa	Root	MeJA	[37]
		SmbHLH92	KP257525.1	681 bp ORF, 226 aa	Root	-	[38]
		SmbHLH7	-	1 911 bp ORF, 636 aa	Xylem	MeJA, GA	[39]
		SmbHLH10	-	972 bp ORF, 323 aa	Flower	GA, ABA	[39]
		SmbHLH130	-	1 185 bp ORF, 394 aa	Leaf	MeJA, GA, ABA	[39]
		SmbHLH148	-	675 bp ORF, 224 aa	Fibrous root	MeJA, GA, ABA	[39]
		SmbHLH3	-	1 476 bp ORF, 491 aa	Fibrous root	MeJA	[39]
		SmbHLH59	KP257492	1 146 bp CDS, 381 aa	Leaf	MeJA	[22]
MYB	110	SmMYB9b	JX113685	1 207 bp	Blooming flowers	ABA, GA, MeJA	[40, 41]
		SmMYB98	AGN52122.1	699 bp ORF, 232 aa	Lateral roots	-	[42]
		SmMYB1	-	1 071 bp full length, 356 aa	Leaf	MeJA, SA	[43]
		SmMYB36	KF059390.1	160 aa	-	-	[44]
		SmMYB4	-	696 bp ORF	-	-	[21]
		SmMYB97	KF059451	825 bp, 274 aa	Leaf	MeJA	[45]
bZIP	70	SmbZIP1	-	474 bp ORF	Periderm	ABA, YE, ET, SA	[46, 47]
		SmbZIP3	-	807 bp ORF, 268 aa	-	ABA	[48]
		SmHY5	MT408030	474 bp ORF, 157 aa	Leaf	-	[49]
WRKY	61	SmWRKY1	-	789 bp ORF, 262 aa	Stem	MeJA, SA, NO	[50, 51]
		SmWRKY2	-	1 476 bp ORF, 491 aa	Leaf	MeJA	[52]
		SmWRKY14	KM823137	732 bp CDS, 243 aa	Root	MeJA	[22]
		SmWRKY44	KM823167.1	798 bp CDS, 265 aa	Stem	MeJA, SA, 4℃, PEG, NaCl	[53]
		SmWRKY40	-	1 059 bp CDS, 352 aa	Root	MeJA, SA	[54]
		SmWRKY34	-	930 bp ORF, 309 aa	Stem	ABA	[48]
		SmWRKY54	-	861 bp ORF	Taproot	SA, ABA, MeJA, GA3, ET, YE	[55]
		SmWRKY61	-	507 bp full length	-	MeJA	[56]
LBD	51	SmLBD44	-	687 bp CDS, 228 aa	-	MeJA	[57, 58]
GRAS	35	SmGRAS1	KY435886	1 470 bp ORF, 489 aa	Periderm	GA, SA, NAA, MeJA, ABA	[24]
		SmGRAS2	KY435887	1 380 bp ORF, 459 aa	Periderm	GA, SA, NAA, MeJA, ABA	[24, 59]
		SmGRAS3	KY435888	2 247 bp ORF, 748 aa	Periderm	GA, SA, NAA, MeJA, ABA	[24]
		SmGRAS4	KY435889	1 581 bp ORF, 526 aa	Periderm	GA, SA, NAA, MeJA, ABA	[24]
		SmGRAS5	KY435890	1 041 bp ORF, 346 aa	Periderm	GA, SA, NAA, MeJA, ABA	[24]
JAZ	9	SmJAZ1	-	543 bp ORF, 180 aa	Stem	ABA, ET, GA, YE, MeJA	[27, 60]
		SmJAZ2	-	642 bp ORF, 213 aa	Leaf	ABA, SA, ET, GA, YE, NAA, PEG, MeJA	[27, 60]
		SmJAZ5	-	825 bp ORF, 274 aa	Leaf	ABA, SA, ET, GA, YE, NAA, Ag⁺, MeJA	[27, 60]
		SmJAZ6	-	720 bp ORF, 239 aa	Leaf	ABA, SA, GA, YE, NAA, PEG, Ag⁺, MeJA	[27, 60]
		SmJAZ9	-	921 bp ORF, 306 aa	Leaf	ABA, GA, SA, YE, NAA, PEG, Ag⁺, MeJA	[27, 60]
		SmJAZ3	-	1 011 bp ORF, 336 aa	Periderm	ABA, SA, ET, GA, YE, NAA, PEG, MeJA	[60]
		SmJAZ4	-	945 bp ORF, 314 aa	Root	ABA, SA, GA, YE, NAA, PEG, Ag⁺, MeJA	[27, 60]
		SmJAZ8	-	372 bp ORF, 123 aa	Leaf	ABA, SA, ET, GA, YE, NAA, PEG, Ag⁺, MeJA	[61]
		SmJAZ10	-	540 bp ORF, 179 aa	Stem	ABA, SA, ET, GA, YE, NAA, PEG, Ag⁺, MeJA	[27]
WD40	225	SmWD40-170	-	972 bp full length, 323 aa	Root	Mechanical damage, MeJA, GA	[62]
EIL		SmEIN3	-	1 797 bp ORF, 598 aa	Leaf	ABA, GA, SA, MeJA, YE	[63]

Family	Number	Member	GenBank accession	Bioinformation	Tissue expression	Elicitor	Reference
AP2/ERF	179	SmERF72	-	699 bp	Periderm	-	[25, 28]
		SmERF98	-	891 bp	Xylem	-	[25]
		SmERF73	QRQ89295.1	780 bp ORF, 259 aa	Root	YE+Ag⁺, MeJA	[20]
		SmERF128	MG897156	633 bp, 210 aa	Periderm	-	[29]
		SmERF1L1	MH006594	741 bp ORF, 246 aa	Stem	MeJA, YE, SA, ET	[30]
		SmERF2	-	741 bp ORF, 246 aa	Stem	YE, MeJA, ET, SA	[31]
		SmERF6	KY988300	561 bp ORF, 186 aa	Root	ET	[32]
		SmERF8	MH006600	654 bp ORF, 217 aa	Root head	ET	[33]
		SmAP2/ERF82	-	582 bp CDS, 193 aa	Root	-	[26]
		SmERF1	KC405081.1	549 bp ORF, 182 aa	-	YE, MeJA	[34]
bHLH	127	SmbHLH61	-	1 008 bp ORF, 335 aa	Root	MeJA, SA	[35, 36]
		SmbHLH74	KP257507.1	696 bp CDS, 231 aa	Root	MeJA	[37]
		SmbHLH92	KP257525.1	681 bp ORF, 226 aa	Root	-	[38]
		SmbHLH7	-	1 911 bp ORF, 636 aa	Xylem	MeJA, GA	[39]
		SmbHLH10	-	972 bp ORF, 323 aa	Flower	GA, ABA	[39]
		SmbHLH130	-	1 185 bp ORF, 394 aa	Leaf	MeJA, GA, ABA	[39]
		SmbHLH148	-	675 bp ORF, 224 aa	Fibrous root	MeJA, GA, ABA	[39]
		SmbHLH3	-	1 476 bp ORF, 491 aa	Fibrous root	MeJA	[39]
		SmbHLH59	KP257492	1 146 bp CDS, 381 aa	Leaf	MeJA	[22]
MYB	110	SmMYB9b	JX113685	1 207 bp	Blooming flowers	ABA, GA, MeJA	[40, 41]
		SmMYB98	AGN52122.1	699 bp ORF, 232 aa	Lateral roots	-	[42]
		SmMYB1	-	1 071 bp full length, 356 aa	Leaf	MeJA, SA	[43]
		SmMYB36	KF059390.1	160 aa	-	-	[44]
		SmMYB4	-	696 bp ORF	-	-	[21]
		SmMYB97	KF059451	825 bp, 274 aa	Leaf	MeJA	[45]
bZIP	70	SmbZIP1	-	474 bp ORF	Periderm	ABA, YE, ET, SA	[46, 47]
		SmbZIP3	-	807 bp ORF, 268 aa	-	ABA	[48]
		SmHY5	MT408030	474 bp ORF, 157 aa	Leaf	-	[49]
WRKY	61	SmWRKY1	-	789 bp ORF, 262 aa	Stem	MeJA, SA, NO	[50, 51]
		SmWRKY2	-	1 476 bp ORF, 491 aa	Leaf	MeJA	[52]
		SmWRKY14	KM823137	732 bp CDS, 243 aa	Root	MeJA	[22]
		SmWRKY44	KM823167.1	798 bp CDS, 265 aa	Stem	MeJA, SA, 4℃, PEG, NaCl	[53]
		SmWRKY40	-	1 059 bp CDS, 352 aa	Root	MeJA, SA	[54]
		SmWRKY34	-	930 bp ORF, 309 aa	Stem	ABA	[48]
		SmWRKY54	-	861 bp ORF	Taproot	SA, ABA, MeJA, GA3, ET, YE	[55]
		SmWRKY61	-	507 bp full length	-	MeJA	[56]
LBD	51	SmLBD44	-	687 bp CDS, 228 aa	-	MeJA	[57, 58]
GRAS	35	SmGRAS1	KY435886	1 470 bp ORF, 489 aa	Periderm	GA, SA, NAA, MeJA, ABA	[24]
		SmGRAS2	KY435887	1 380 bp ORF, 459 aa	Periderm	GA, SA, NAA, MeJA, ABA	[24, 59]
		SmGRAS3	KY435888	2 247 bp ORF, 748 aa	Periderm	GA, SA, NAA, MeJA, ABA	[24]
		SmGRAS4	KY435889	1 581 bp ORF, 526 aa	Periderm	GA, SA, NAA, MeJA, ABA	[24]
		SmGRAS5	KY435890	1 041 bp ORF, 346 aa	Periderm	GA, SA, NAA, MeJA, ABA	[24]
JAZ	9	SmJAZ1	-	543 bp ORF, 180 aa	Stem	ABA, ET, GA, YE, MeJA	[27, 60]
		SmJAZ2	-	642 bp ORF, 213 aa	Leaf	ABA, SA, ET, GA, YE, NAA, PEG, MeJA	[27, 60]
		SmJAZ5	-	825 bp ORF, 274 aa	Leaf	ABA, SA, ET, GA, YE, NAA, Ag⁺, MeJA	[27, 60]
		SmJAZ6	-	720 bp ORF, 239 aa	Leaf	ABA, SA, GA, YE, NAA, PEG, Ag⁺, MeJA	[27, 60]
		SmJAZ9	-	921 bp ORF, 306 aa	Leaf	ABA, GA, SA, YE, NAA, PEG, Ag⁺, MeJA	[27, 60]
		SmJAZ3	-	1 011 bp ORF, 336 aa	Periderm	ABA, SA, ET, GA, YE, NAA, PEG, MeJA	[60]
		SmJAZ4	-	945 bp ORF, 314 aa	Root	ABA, SA, GA, YE, NAA, PEG, Ag⁺, MeJA	[27, 60]
		SmJAZ8	-	372 bp ORF, 123 aa	Leaf	ABA, SA, ET, GA, YE, NAA, PEG, Ag⁺, MeJA	[61]
		SmJAZ10	-	540 bp ORF, 179 aa	Stem	ABA, SA, ET, GA, YE, NAA, PEG, Ag⁺, MeJA	[27]
WD40	225	SmWD40-170	-	972 bp full length, 323 aa	Root	Mechanical damage, MeJA, GA	[62]
EIL		SmEIN3	-	1 797 bp ORF, 598 aa	Leaf	ABA, GA, SA, MeJA, YE	[63]

Family	Member	Positive/negative	Target gene	Reference		Family	Member	Positive/negative	Target gene	Reference
AP2/ERF	SmERF72	Positive	HMGR, CYP76AH3, KSL1, IDI1	[25]		WRKY	SmWRKY1	Positive	DXR	[51]
	SmERF98	Positive	CYP76AH3, KSL1, IDI1	[25]		SmWRKY2	Positive	CPS	[52]
	SmERF73	Positive	DXR1, CPS1, KSL1, CYP76AH3	[20]		SmWRKY14	Positive	CPS1	[22]
	SmERF128	Positive	CYP76AH1, CPS1, KSL1	[29]		SmWRKY44	Positive	CPS1, CPS5, KSL1	[53]
	SmERF1L1	Positive	DXR	[30]		SmWRKY40	Negative	CPS1, CPS5	[54]
	SmERF2	Positive	CPS1	[31]		SmWRKY34	Negative	GGPPS	[48]
	SmERF6	Positive	KSL1, CPS1	[32]		SmWRKY54	Positive	KSL	[55]
	SmERF8	Positive	KSL1	[33]		SmWRKY61	Positive	-	[56]
	SmAP2/ ERF82	Positive	IDI1, CPS1, CYP76AH3	[26]	LBD	SmLBD44	Negative	KSL1	[58]
	SmERF1	Positive	-	[34]	GRAS	SmGRAS1	Positive	KSL1	[24]
bHLH	SmbHLH61	Positive	-	[36]		SmGRAS2	Positive	-	[24, 59]
	SmbHLH74	Negative	HMGR1, GGPPS1, CYP76AH1	[37]		SmGRAS3	Positive	KSL1	[24]
	SmbHLH92	Positive/ negative	DXR, HMGR4	[38]		SmGRAS4	Positive	KSL1	[24]
	SmbHLH7	Positive	DXS2, CPS1, KSL1, CYP76AH1	[39]		SmGRAS5	Positive	KSL1	[24]
	SmbHLH10	Positive	DXS2, CPS1, CPS5	[39]	JAZ	SmJAZ1	Positive	-	[27, 60]
	SmbHLH130	Positive	CPS1, DXS2, KSL1, CYP76AH1	[39]		SmJAZ2	Positive	-	[27, 60]
	SmbHLH3	Negative	KSL1, CYP76AH1	[39]		SmJAZ5	Positive	-	[27, 60]
	SmbHLH148	Positive	DXS2, CPS1, CYP76AH1	[39]		SmJAZ6	Positive	-	[27, 60]
	SmbHLH59	Positive	CPS1, KSL1	[22]		SmJAZ9	Positive	-	[27, 60]
MYB	SmMYB9b	Positive	-	[41]		SmJAZ3	Negative	-	[60]
	SmMYB98	Positive	GGPPS1	[42]		SmJAZ4	Negative	-	[27, 60]
	SmMYB1	Positive	-	[43]		SmJAZ8	Negative	-	[61]
	SmMYB36	Positive	HMGS1, GGPPS, DXR, CMK, MCT	[44]	WD40	SmWD40-170	Positive	-	[62]
	SmMYB4	Negative	-	[21]	EIL	SmEIN3	Positive	HMGR, DXS2	[63]
	SmMYB39	Negative	-	[39]
	SmMYB97	Positive	CPS1, KSL1	[45]
bZIP	SmbZIP1	Negative	GGPPS	[47]
	SmbZIP3	Positive	-	[48]
	SmHY5	Positive	-	[49]

Family	Member	Positive/negative	Target gene	Reference		Family	Member	Positive/negative	Target gene	Reference
AP2/ERF	SmERF72	Positive	HMGR, CYP76AH3, KSL1, IDI1	[25]		WRKY	SmWRKY1	Positive	DXR	[51]
	SmERF98	Positive	CYP76AH3, KSL1, IDI1	[25]		SmWRKY2	Positive	CPS	[52]
	SmERF73	Positive	DXR1, CPS1, KSL1, CYP76AH3	[20]		SmWRKY14	Positive	CPS1	[22]
	SmERF128	Positive	CYP76AH1, CPS1, KSL1	[29]		SmWRKY44	Positive	CPS1, CPS5, KSL1	[53]
	SmERF1L1	Positive	DXR	[30]		SmWRKY40	Negative	CPS1, CPS5	[54]
	SmERF2	Positive	CPS1	[31]		SmWRKY34	Negative	GGPPS	[48]
	SmERF6	Positive	KSL1, CPS1	[32]		SmWRKY54	Positive	KSL	[55]
	SmERF8	Positive	KSL1	[33]		SmWRKY61	Positive	-	[56]
	SmAP2/ ERF82	Positive	IDI1, CPS1, CYP76AH3	[26]	LBD	SmLBD44	Negative	KSL1	[58]
	SmERF1	Positive	-	[34]	GRAS	SmGRAS1	Positive	KSL1	[24]
bHLH	SmbHLH61	Positive	-	[36]		SmGRAS2	Positive	-	[24, 59]
	SmbHLH74	Negative	HMGR1, GGPPS1, CYP76AH1	[37]		SmGRAS3	Positive	KSL1	[24]
	SmbHLH92	Positive/ negative	DXR, HMGR4	[38]		SmGRAS4	Positive	KSL1	[24]
	SmbHLH7	Positive	DXS2, CPS1, KSL1, CYP76AH1	[39]		SmGRAS5	Positive	KSL1	[24]
	SmbHLH10	Positive	DXS2, CPS1, CPS5	[39]	JAZ	SmJAZ1	Positive	-	[27, 60]
	SmbHLH130	Positive	CPS1, DXS2, KSL1, CYP76AH1	[39]		SmJAZ2	Positive	-	[27, 60]
	SmbHLH3	Negative	KSL1, CYP76AH1	[39]		SmJAZ5	Positive	-	[27, 60]
	SmbHLH148	Positive	DXS2, CPS1, CYP76AH1	[39]		SmJAZ6	Positive	-	[27, 60]
	SmbHLH59	Positive	CPS1, KSL1	[22]		SmJAZ9	Positive	-	[27, 60]
MYB	SmMYB9b	Positive	-	[41]		SmJAZ3	Negative	-	[60]
	SmMYB98	Positive	GGPPS1	[42]		SmJAZ4	Negative	-	[27, 60]
	SmMYB1	Positive	-	[43]		SmJAZ8	Negative	-	[61]
	SmMYB36	Positive	HMGS1, GGPPS, DXR, CMK, MCT	[44]	WD40	SmWD40-170	Positive	-	[62]
	SmMYB4	Negative	-	[21]	EIL	SmEIN3	Positive	HMGR, DXS2	[63]
	SmMYB39	Negative	-	[39]
	SmMYB97	Positive	CPS1, KSL1	[45]
bZIP	SmbZIP1	Negative	GGPPS	[47]
	SmbZIP3	Positive	-	[48]
	SmHY5	Positive	-	[49]

转录因子对丹参酮类物质调控作用及机制研究进展

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白艳红 ¹ , 辛林林 ¹ , 曾婷 ¹^,² , 韩凤霞 ¹ , 张永清 ¹ , 蒲高斌 ¹ , 陈雪 ¹^,^* , 刘谦 ¹^,²^,^*

药学学报 | 综述 2024,59(5): 1218-1228

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药学学报 | 综述 2024, 59(5): 1218-1228

转录因子对丹参酮类物质调控作用及机制研究进展

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白艳红¹, 辛林林¹, 曾婷¹^,², 韩凤霞¹, 张永清¹, 蒲高斌¹, 陈雪¹^,^*, 刘谦¹^,²^,^*

作者信息

1.山东中医药大学药学院, 山东济南 250355

2.黄冈师范学院李时珍中医学院, 湖北黄冈 438000

通讯作者:

^*陈雪, E-mail: xchenaylli@sina.com;

刘谦, E-mail: cleanlq@163.com

Research progress in regulation and mechanism of transcription factors on tanshinones

Yan-hong BAI¹, Lin-lin XIN¹, Ting ZENG¹^,², Feng-xia HAN¹, Yong-qing ZHANG¹, Gao-bin PU¹, Xue CHEN¹^,^*, Qian LIU¹^,²^,^*

Affiliations

1. College of Pharmacy, Shandong University of Chinese Medicine, Jinan 250355, China

2. LiShizhen College of Traditional Chinese Medicine, Huanggang Normal University, Huanggang 438000, China

出版时间: 2024-05-12 doi: 10.16438/j.0513-4870.2023-1110

文章导航

摘要

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丹参是临床常用的活血化瘀药, 主要用于心脑血管疾病的治疗, 其关键活性物质丹参酮的合成和调控机制一直为研究热点。本文对近年来有关转录因子(AP2/ERF、bHLH、MYB、bZIP、WRKY等) 调节丹参酮类成分生物合成的研究成果进行了归纳总结, 指出了丹参转录调控研究存在的问题, 探讨了转录因子在丹参酮类活性成分生物合成调控中的研究方向, 为进一步发现和利用丹参酮类活性物质调控功能基因提供理论依据。

关键词

转录因子 / 丹参酮 / 调控作用 / 分子机制

Abstract

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Salvia miltiorrhiza, a commonly used traditional Chinese medicine, has been widely recognized for its blood-activating and stasis-removing properties in the clinical treatment of cardiovascular and cerebrovascular diseases. The synthesis and regulatory mechanism of tanshinones, the key active constituents of Salvia miltiorrhiza, have been a hot topic of research. The paper summarized the research findings on the regulation of tanshinone biosynthesis by transcription factors such as AP2/ERF, bHLH, MYB, bZIP, and WRKY in recent years. The review identifies the existing issues in the transcriptional regulation studies of Salvia miltiorrhiza and discusses the research direction of transcription factors in the regulation of tanshinone biosynthesis, providing a theoretical basis for the further discovery and utilization of functional genes involved in the regulation of tanshinone bioactive constituents.

Key words

transcription factor / tanshinone / regulation / molecular mechanism

引用本文

白艳红, 辛林林, 曾婷, 韩凤霞, 张永清, 蒲高斌, 陈雪, 刘谦. 转录因子对丹参酮类物质调控作用及机制研究进展. 药学学报, 2024 , 59 (5) : 1218 -1228 . DOI: 10.16438/j.0513-4870.2023-1110

Yan-hong BAI, Lin-lin XIN, Ting ZENG, Feng-xia HAN, Yong-qing ZHANG, Gao-bin PU, Xue CHEN, Qian LIU. Research progress in regulation and mechanism of transcription factors on tanshinones[J]. Acta Pharmaceutica Sinica, 2024 , 59 (5) : 1218 -1228 . DOI: 10.16438/j.0513-4870.2023-1110

正文

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丹参为唇形科植物丹参(Salvia miltiorrhiza Bunge) 的干燥根及根茎, 具有活血祛瘀、通经止痛、清心除烦、凉血消痈等功效, 主要用于心脑血管疾病的治疗, 是临床常用的活血化瘀药^[1-3]。丹参主要包含两类生物活性成分: 丹参酮类成分和酚酸类成分^{[4, 5]}, 其中丹参酮类成分, 如隐丹参酮、二氢丹参酮Ⅰ、丹参酮Ⅰ和丹参酮Ⅱ_A, 具有抗炎、抗肿瘤、抗心肌纤维化等药理作用^{[6, 7]}。天然资源中丹参酮类化合物含量较低, 丹参酮是决定丹参药材发挥临床疗效的关键活性成分, 其合成积累备受广泛关注。转录因子可以通过激活或抑制一条或多条代谢途径中多个关键酶基因的表达, 实现丹参酮类成分高效合成和定向积累。关于转录因子对丹参酮类成分生物合成调控的研究一直受到国内外学者的广泛关注, AP2/ERF、bHLH、MYB、bZIP、WRKY等转录因子家族已被证实参与此过程, 本文就这些转录因子对丹参酮类物质调控作用及机制研究进行了综述, 旨在为相关研究提供参考。

1 丹参酮类物质生物合成途径

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丹参酮代谢途径以萜类化合物共同合成前体异戊烯基焦磷酸(isopentenyl pyrophosphate, IPP) 及其异构体二甲基烯丙基焦磷酸(dimethylallyl pyrophosphate, DMAPP) 为起始, 通过两个独立的途径合成: 位于细胞质中的甲羟戊酸(mevalonate, MVA) 途径和位于质体中的2-C-甲基-D-赤藓糖醇-4-磷酸(2-C-methyl-D-derythritol 4-phosphate, MEP) 途径^{[8, 9]} (图 1)。

MVA合成途径鉴定到的关键酶有乙酰乙酰基辅酶A硫解酶(aceto-acetyl-CoA thiolase, AACT)、3-羟基-3-甲基戊二酰辅酶A合成酶(3-hydroxy-3-methylglutaryl CoA synthase, HMGS)、3-羟基-3-甲基戊二酰辅酶A还原酶(3-hydroxy-3-methylglutaryl CoA reductase, HMGR) 等; MEP合成途径鉴定到的关键酶有1-脱氧-D-木酮糖合成酶(1-deoxy-D-xylulose 5-phosphate synthase, DXS)、1-脱氧-D-木酮糖-5-磷酸还原酶(1-deoxy-D-xylulose 5-phosphate reductoisomerase, DXR)、1-羟基-2-甲基-2-(E)-丁烯基-4-二磷酸还原酶[1-hydroxy-2-methyl-2-(E)-butenyl-4-diphosphate reductase, HDR] 等; 下游合成途径鉴定到的关键酶有牻牛儿基牻牛儿基焦磷酸合酶(geranylgeranyl diphosphate synthase, GGPPS)、柯巴基焦磷酸合酶(copalyl diphosphate synthase, CPS)、类贝壳杉烯合酶(kaurene synthase-like, KSL) 以及CYP450家族成员。其中, HMGR是MVA途径第一个限速酶^[10], 目前已经从丹参基因组中鉴定出HMGR1、HMGR2、HMGR3、HMGR4^[8], SmHMGR2基因过表达可以提高丹参酮含量^[11]。DXS是MEP途径第一个限速酶^[12], 在丹参基因组中已鉴定到5个DXS, SmDXS2在根中表达水平高于其他基因, 该基因过表达可提高丹参酮含量^{[13, 14]}。

在下游途径中, 二萜类化合物前体牻牛儿基牻牛儿基焦磷酸(geranylgeranyl diphosphate, GGPP) 是由GGPPS催化IPP和DMAPP生成的, GGPPS是联系丹参酮上游和下游途径的关键酶, SmGGPPS1和SmGGPPS3启动子内的转录因子结合位点的变异与丹参酮类成分含量之间具有显著相关性^[15]。另外, 丹参酮积累与SmCPS、SmKSL关键酶基因表达呈正相关^[16]。已被鉴定的CYP76AH1、CYP76AH3、CYP76AK1参与到丹参酮类化合物结构修饰, 丹参酮二烯在CYP76AH1催化作用下生成铁锈醇(ferruginol), 进一步在CYP76AH3和CYP76AK1作用下催化形成11, 20-二羟基铁锈醇(11, 20-dihydroxy ferruginol, 11, 20-HF) 和11, 20-二羟基柳杉酚(11, 20-dihydroxy sugiol, 11, 20-HS)^[17-19]。最后, 丹参酮类成分在CYP450家族作用下催化合成, 但其具体的催化反应步骤仍不清楚, 有待进一步研究。

2 调节丹参酮类成分生物合成的转录因子

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转录因子作为一类重要调控因子, 在调节次级代谢产物合成网络中起关键作用。转录因子调控丹参酮合成主要在两方面起作用, 一是转录因子通过激活或抑制丹参酮生物合成途径中单个或者多个基因的表达, 进而正向或负向调控丹参酮生物合成, 比如SmERF73通过激活DXR1、CPS1、KSL1、CYP76AH3基因表达正调控丹参酮合成^[20], SmMYB4通过激活GGPPS3基因表达负调控丹参酮合成^[21]。二是单个转录因子可以与其他转录因子形成复合物共同发挥作用, 调节靶基因表达, 比如JAZ蛋白与SmbHLH59或SmMYB97发生相互作用, 抑制靶基因表达, 进而抑制丹参酮合成^[22]。目前已经报道了多个转录因子家族参与调控丹参酮类成分生物合成, AP2/ERF、bHLH、MYB、bZIP、WRKY等转录因子与关键酶基因之间的转录调控网络如图 2所示。

2.1 转录因子的组织特异性

丹参以皮色红者为佳, 皮部红色物质主要为丹参酮类次生代谢产物, 尤其是周皮木栓层, 红色越深, 丹参酮含量越高^[23]。根据目前研究表明, 丹参GRAS在根周皮的表达量均显著高于其他部位, 说明GRAS转录因子在丹参酮的合成调控中发挥重要作用^[24]。其他类型的转录因子大多也在丹参根中表达较高, 比如属于ERF亚家族SmERF73^[20]、SmERF72^[25]、SmAP2/ERF82^[26]等在根中表达量最高(表 1^{[20-22, 24-63]})。因此, 挖掘具有组织特异性的转录因子, 可能揭示其在丹参酮合成积累方面的作用。

2.2 诱导子对转录因子的调控

AP2/ERF、bHLH、MYB、bZIP、WRKY等转录因子家族受茉莉酸甲酯(methyl jasmonate, MeJA)、水杨酸(salicylic acid, SA)、脱落酸(abscisic acid, ABA)、赤霉素(gibberellins, GA)、茉莉酸(jasmonic acid, JA)、酵母提取物(yeast extract, YE) 等诱导子的诱导, 表现出对丹参酮合成的调控能力(表 1)。比如外源施加MeJA, 毛状根中SmJAZ表达水平被显著诱导或抑制^[27]; GRAS转录因子作为GA信号通路的关键调控因子, GA诱导后SmGRAS表达量显著上调或下调^[24]。因此, 系统分析转录因子家族受诱导表达模式, 有助于了解其对丹参酮合成的调控能力。

2.3 转录因子对丹参酮合成的调控作用

表 2^{[20-22, 24-27, 29-34, 36-39, 41-45, 47-49, 51-56, 58-63]}总结了转录因子对丹参酮正向或负向调控以及调控丹参酮合成途径上的目标基因。

2.3.1 AP2/ERF转录因子

AP2/ERF转录因子是一类主要存在于植物中被认为是最大的转录因子家族之一, 包含长约60个氨基酸的AP2结构域, 可直接与顺式元件相互作用。根据AP2结构域数量及结合序列, 可分为AP2、ERF、DREB、RAV、Soloist五个亚家族^[64], 其中响应乙烯信号通路的ERF亚族对丹参酮的调控研究较为深入。Ji等^[28]从丹参基因组中鉴定出179个AP2/ERF转录因子, 根据AP2结构域数量和序列特征可分为5个亚家族, 结合基因表达分析、共表达网络分析、顺式调控元件分析, 推测SmERF128和SmERF152调节丹参酮的生物合成。

目前研究表明, ERF类转录因子对丹参酮的调控多为正向调控, 比如: SmERF72^[25]、SmERF98^[25]、SmERF73^[20]、SmERF128^[29]、SmERF1L1^[30]、SmERF2^[31]、SmERF6^[32]、SmERF8^[33]、SmAP2/ERF82^[26]、SmERF1^[34]。进一步机制研究表明, SmERF72结合靶基因HMGR、KSL1、CYP76AH3、IDI1启动子序列中的GCC-box, SmERF98结合靶基因KSL1、CYP76AH3、IDI1启动子序列中的GCC-box^[25], SmERF73结合DXR1、CPS1、KSL1、CYP76AH3启动子序列中的GCC-box^[20], 从而激活靶基因的转录。SmERF128则是通过结合GCC-box、CBF2、RAA基序激活SmCPS1、SmKSL1、SmCYP76AH1的表达正调控丹参酮合成^[29]。SmERF1L1以SmDXR为靶点正向调控丹参酮生物合成^[30]。另外, SmERF2过表达显著提高毛状根中丹参酮含量, SmERF2干扰株系与对照株系相比丹参酮含量没有明显变化, 但SmDXS2、SmDXR、SmHMGS、SmKSL基因表达显著上调, 说明SmERF2对丹参酮的合成起一定的正调控作用^[31]。

ERF类转录因子不仅正向调控丹参酮的合成, 而且在生长发育和非生物胁迫方面发挥重要作用。SmERF6/8与SmKSL1、SmCPS1启动子的乙烯反应元件GCC-box结合并激活转录正调节丹参酮生物合成, 过表达SmERF6、SmERF8会抑制丹参毛状根生长^{[32, 33]}。SmAP2/ERF82通过调控丹参酮生物合成途径中关键酶基因IDI1、CPS1、CYP76AH3表达正向调控丹参酮类化合物的生物合成。此外, SmAP2/ERF82过表达株系生长矮小, 根系稀疏, RNAi株系生长健壮, 根系发达, 这可能是由于SmAP2/ERF82负向调控GA的生物合成^[26]。SmERF1虽然对丹参酮类物质合成的调节效果较弱, 但能提高丹参的耐盐性^[34]。

2.3.2 bHLH转录因子

bHLH转录因子家族是真核转录因子中最大的家族之一, 具有高度保守的碱性/螺旋环-螺旋特殊结构域, 总共约有50~60个氨基酸, 由两部分组成, 一部分是碱性氨基酸区, 另一部分是螺旋-环-螺旋区, 这两部分在功能上完全不同。碱性氨基酸区位于N端, 主要功能是识别并特异性结合靶基因启动子的DNA序列; 螺旋-环-螺旋区域位于C端, 主要功能是促进蛋白质的相互作用并形成同二聚体或异二聚体复合物控制基因转录^{[65, 66]}。Zhang等^[35]在丹参基因组中鉴定出127个bHLH转录因子, 根据系统发育分为25个亚家族, MeJA处理后, 发现7个bHLH基因(SmbHLH37/51/53/60/74/92/103) 可能参与丹参酮代谢调控。

bHLH转录因子可正负双向参与调节丹参酮类成分合成。首先, SmbHLH61^[36]、SmbHLH7^[39]、SmbHLH10^[39]、SmbHLH130^[39]、SmbHLH148^[39]、SmbHLH59^[22]参与丹参酮正向调控。Xing^[39]研究发现SmbHLH7、SmbHLH10、SmbHLH130、SmbHLH148通过结合丹参酮类物质合成途径中关键酶基因启动子区E/G-box元件调节基因的转录; SmbHLH59结合启动子区内的E/G-box元件激活CPS1、KSL1表达^[22]。其次, SmbHLH3^[39]、SmbHLH74^[37]负向调控丹参酮合成, SmbHLH3结合KSL1、CYP76AH1启动子区元件抑制丹参酮类物质的代谢^[39]; SmbHLH74直接抑制SmHMGR1、SmGGPPS1、SmCYP76AH1的转录负调控丹参酮生物合成^[37]。另外, SmbHLH92对丹参酮积累具有双重调节作用, 负调控二氢丹参酮I和隐丹参酮, 正调控丹参酮I和丹参酮II_A, 进一步转录组数据结果表明, SmbHLH92可能通过直接结合SmHMGR4、SmGPPS.LSU、SmGPPS.SUII.2、SmDXR启动子的G-box调控基因表达^[38]。

bHLH受其他转录因子的调控, 动态调节丹参酮类成分的合成, 比如SmMYC2直接抑制SmbHLH74的转录, 削弱了SmbHLH74对丹参酮积累的抑制作用^[37]; SmJAZ1/8蛋白抑制SmbHLH59的转录活性, 从而抑制丹参酮生物合成^[22]。SmbHLH7和SmMYB39调控丹参酮类物质代谢的靶基因具有重叠, 竞争性结合靶基因, 当二者形成复合体时, 使得SmbHLH7与其他正调控的MYB转录因子无法形成复合体, 进而协同调控丹参中次生代谢的动态平衡^[39]。

2.3.3 MYB转录因子

MYB转录因子家族数量庞大、功能多样, 是植物生长发育过程中重要的调控因子, N端是高度保守DNA结合域, 具有1~3个重复序列(R1、R2、R3), 每个重复序列由51~52个氨基酸残基组成, 折叠成三个α-螺旋, 第二螺旋和第三螺旋可形成螺旋-转角-螺旋结构。根据结构域数量和位置, MYB家族分为1R (R1/2, R3-MYB)、2R (R2R3-MYB)、3R (R1R2R3-MYB)、4R (R1R2R2R1/2-MYB), 大多数MYB蛋白属于R2R3-MYB亚家族^{[67, 68]}。Li等^[40]从丹参基因组中鉴定分析出110个R2R3-MYB转录因子, 基于系统发育和拟南芥的研究结果, 分为37个亚组, 预测亚组4、5、20中的成员是丹参萜类化合物合成的潜在调控因子。

MYB转录因子不仅对丹参酮的积累起正向调控作用, 而且影响丹参根系的发育, 比如SmMYB9b^[41]、SmMYB98^[42]、SmMYB1^[43]。SmMYB9b通过激活丹参MEP通路相关基因SmDXS2、SmDXR、SmGGPPS、SmKSL1转录水平发挥正向调控作用, SmMYB9b过表达毛状根比对照组长得更细、侧根更少、更易形成愈伤组织^[41]。SmMYB98过表达后毛状根相对于对照组长得更短更粗, GA含量降低, 丹参酮含量增加, 说明SmMYB98影响丹参毛状根生长, 负向调控GA生物合成, 正向调控丹参酮合成^[42]。SmMYB1作为重要的反馈调节因子, 促进了丹参毛状根的生长和毛状根中丹参酮类物质的积累^[43]。SmMYB36通过提高DSX1、DXS2、DXR、MCT、MDS、HDS、CMK、HDR1、GGPPS1、CPS1、CYP76AH1、KSL1转录水平促进丹参酮积累^[44]。MYB类转录因子也可负调控丹参酮合成。相比于对照, SmMYB4过表达株系隐丹参酮和丹参酮Ⅱ_A含量下降, SmMYB4干扰株系中隐丹参酮和丹参酮Ⅱ_A含量增加, 丹参酮合成途径下游关键酶基因GGPPS3表达受显著影响, 推测SmMYB4通过调控GGPPS3负调控丹参酮合成^[21]。

另外, MYB转录因子会和bHLH及WD40蛋白形成MBW蛋白复合体协同调控次生代谢。Xing^[39]研究发现SmMYB39过表达抑制毛状根中丹参酮类物质含量和丹参酮生物合成途径基因DXS2、DXR、HMGR1、GGPPS、KSL1表达。SmMYB39和SmbHLH7相互作用, 过表达SmbHLH7促进SmMYB39的转录, 沉默SmbHLH7后SmMYB39的转录受到抑制, 二者协同调控丹参酮积累的动态平衡。Li等^[45]研究发现SmMYB97过表达增加了丹参酮含量, 上调丹参酮合成路径基因SmDXS1、SmHMGR1、SmFPPS、SmGPPS、SmGGPPS、SmCPS1、SmKSL1、SmCYP76AH1表达。酵母单杂交和瞬时转录活性测定表明, SmMYB97结合CPS1和KSL1启动子区域激活表达。酵母双杂交和双分子荧光互补实验表明, SmMYB97与SmJAZ8相互作用, 共同抑制SmCPS1和SmKSL1的表达, 说明SmMYB97与SmJAZ8参与丹参酮积累过程。

2.3.4 bZIP转录因子

bZIP转录因子也是一个庞大而多样的家族, 包含一个由60~80个氨基酸残基组成的bZIP结构域, N端为碱性区域相对保守, 含有一个核定位信号和一个N-X7-R/K基序; C端为亮氨酸拉链区域, 由亮氨酸或其他疏水氨基酸组成, 可形成同源或异源二聚体发挥作用^{[69, 70]}。Zhang等^[46]首次对丹参bZIP基因家族进行全基因组分析, 根据与拟南芥的系统发育关系, 共鉴定出70个SmbZIP转录因子, 分为11个亚群, SmbZIP7、SmbZIP20可能参与丹参酮生物合成的调控。

bZIP转录因子通过不同的途径直接或者间接地影响丹参酮的生物合成, 比如ABA处理丹参毛状根后, bZIP3/6/10/18/19/36/37/68/71与丹参酮生物合成途径上的一个或多个关键酶基因显著相关, 推测bZIP转录因子可能通过与丹参酮生物合成途径中基因启动子结合激活基因转录, 进而调控丹参有效成分的生物合成^[71]; SmbZIP1与G-Box元件结合直接抑制GGPPS基因表达降低丹参酮含量^[47]。SmbZIP3通过调节转录因子SmERF128和SmMYB9b间接促进丹参酮生物合成^[48]。另外, SmHY5对丹参根系形态发育和有效成分积累多重调控作用, 过表达SmHY5降低丹参的一级侧根数、二级侧根数和鲜重, 增加了丹参的一级侧根直径、根长, 提高丹参酮含量, 沉默SmHY5基因结果相反^[49]。

2.3.5 WRKY转录因子

WRKY家族是高等植物中最大的转录因子家族之一, 其DNA结合域包含大约1个或2个由60个氨基酸组成的WRKY结构, N端含七肽序列WRKYGQK的保守区, C端为C2H2型或C2HC型的锌指结构^[72]。WRKY蛋白质通过特异性结合靶基因启动子的W-box实现生物学功能, W-box的特定序列为(C/T)TGAC(C/T), TGAC是其核心序列^[73]。Li等^{[50, 74]}从丹参基因组中鉴定出61个SmWRKY转录因子, 多重序列比对表明, SmWRKY可分为3个类群, 有42个响应YE和Ag⁺胁迫, 推测SmWRKY1/3/7/9/12/19/25/29/30/35/42/52/56/58/63/68参与丹参酮合成。

WRKY转录因子通过结合丹参酮合成途径的关键酶编码基因启动子中W-box元件调控靶基因转录, 比如SmWRKY1^[51]、SmWRKY2^[52]、SmWRKY14^[22]、SmWRKY44^[53]、SmWRKY40^[54]。Cao等^[51]研究发现SmWRKY1过表达显著提高MEP途径中关键酶基因表达, 尤其是SmDXR, 双荧光素酶实验证明SmWRKY1通过直接结合启动子区域转录激活SmDXR表达, 正调控丹参酮生物合成。SmWRKY2结合SmCPS^[52]、SmWRKY14结合SmCPS1^[22]、SmWRKY44结合SmCPS1、SmCPS5、SmKSL1基因启动子中的W-box元件激活基因的转录促进丹参酮生物合成^[53], 另一个成员SmWRKY40结合SmCPS1和SmCPS5启动子中的W-box, 抑制丹参酮合成^[54]。SmWRKY54与SmKSL结合增加丹参酮产量的同时, 还通过W-box与SA信号转导途径中的相关基因相互作用, 增强拟南芥抗旱性^[55]。SmWRKY61对丹参酮的积累具有较强的调节作用, 主要通过调控MEP通路(DXS2、CMK、HMGS2) 和下游通路(CPS、KSL、KSL2、CYP76AH1、CYP76AK3) 基因表达, 促进丹参酮积累^[56]。SmWRKY34则是通过直接调控SmGGPPS负调控丹参酮合成^[48]。

2.3.6 其他转录因子

LBD转录因子由N端的LOB结构域和可变C端组成, 可分为class Ⅰ和class Ⅱ^[75]。MeJA对class Ⅱ成员SmLBD44有明显的诱导作用, SmLBD44对丹参酮合成起抑制作用。进一步研究证明SmLBD44抑制了SmKSL1的活性, 但SmJAZ1可以消除SmLBD44对SmKSL1抑制作用, 表明SmLBD44可能参与JA信号通路介导的丹参酮合成调控过程^[58]。

GRAS蛋白含有一个N端保守性较低的可变区和一个C端保守GRAS结构域, 典型的GRAS结构域包含5个保守序列基序: LHRI、VHIID、LHRII、PFYRE、SAW^[76]。SmGRAS1/2/3/4/5作为正调节剂影响丹参酮合成, 其作用机制有所不同, SmGRAS1/3/4/5通过直接与SmKSL1启动子中的GARE-motif结合激活基因表达促进丹参酮合成, SmGRAS2可能通过与SmGRAS1相互作用调节丹参酮合成^{[24, 59]}。

JAZ抑制因子是JA途径中的一类阻遏蛋白, 响应JA刺激, 可与其他转录因子互作发挥调控作用, 是JA信号途径调控次级代谢产物合成的关键环节之一^[77]。在MeJA处理下, SmJAZ1/2/5/6/9过表达显著增加毛状根中丹参酮的积累, 而SmJAZ3/4/8过表达降低毛状根中丹参酮的积累。另外, SmJAZs可与SmMYC2a、SmMYC2b、SmMYB39、SmPAP1形成复杂的调控网络, 在JA诱导的丹参酮合成中表现出功能多效性、多样性和冗余性^{[27, 61]}。

除上述转录因子, SmWD40-170过表达提高了丹参酮Ⅱ_A和隐丹参酮含量, 显著上调关键酶基因SmDXS、SmHMGR、SmFPPS、SmGGPPS、SmCPS、SmKSL表达水平^[62]。SmEIN3 (乙烯信号途径的关键转录因子) 通过直接激活SmHMGR、SmDXS2等关键酶基因的表达, 正调控丹参酮合成。此外, SmEIN3还可与SmMYC2 (JA信号途径的关键转录因子) 互作, 将乙烯信号通路和JA信号通路联系起来, 共同调节丹参酮合成^[63]。目前关于丹参WD40、EIL家族转录因子参与丹参酮类成分生物合成的研究报道较少, 其调控作用及机制有待深入研究。

3 总结与展望

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转录因子作为丹参酮生物合成途径中的高效调节因子, 可以同时激活或抑制一条或多条合成途径中的多个基因, 其功能受到研究者的广泛关注。本综述讨论了AP2/ERF、bHLH、MYB、bZIP、WRKY等转录因子家族在提高丹参酮含量方面的潜力和局限性, 并对未来研究方向做出展望。

转录因子是基因表达调控网络中的一部分, 调控机制通常是复杂的, 涉及到多个转录因子、共调控因子和底物基因。在研究转录因子对丹参酮类物质调控时, 很难完全了解所有调控因素之间的相互作用和调控网络的整体机制。首先, 转录因子家族数量庞大, 但只有家族中少数转录因子被证实参与丹参酮的生物合成, 且有正负调控之分; 其次, 植物中存在大量的转录因子家族和亚家族, 它们在功能上可能存在重叠和互补性, 这使得确定特定的转录因子在丹参酮类物质调控中的作用变得更加复杂, 需要进行更多功能基因组学研究; 最后, 丹参中转录因子数量众多、同一转录因子家族成员功能是否相同、转录因子之间是否互作、不同类型的转录因子是否在转录层面发挥作用等问题增加了调控机制研究的难度。目前, 关于转录因子对丹参酮类物质调控关系的认识还不完全, 需要更多研究来揭示其详细的调控网络。

在今后的研究中, 一方面, 通过整合转录组学、代谢组学、蛋白质组学等技术, 全面鉴定和分析参与丹参酮类物质合成调控的转录因子家族, 利用外源激素诱导转录因子的表达、比对与已报道植物中转录因子的同源性等方法来筛选调控丹参酮关键转录因子。最近, 单细胞组学技术在基因网络中筛选关键作用的核心转录因子、解析转录因子对植物组织成分等方面拥有巨大潜力^[78], 随着该技术的发展应用, 将会加快筛选在丹参酮合成方面起作用的转录因子。另一方面, 对挖掘到的核心转录因子, 结合基因过表达、CRISPR/Cas9基因编辑等技术, 对丹参酮类物质合成调控的转录因子进行功能验证和定点突变, 深入解析其调控机制, 增加对丹参酮合成转录调控网络的认识。这些研究方向有望提供更多关于丹参酮类物质合成调控的重要信息, 为植物次生代谢工程等领域的发展提供理论和实践指导。

丹参酮的主要来源是从丹参中直接提取, 培育丹参酮含量高的丹参新品种仍是未来的研究目标。转录因子作为丹参酮合成的高效调控因子, 具有调控关键酶基因表达和根系生长发育等作用, 在提高丹参酮含量和产量方面显示出广阔的发展前景。转录因子对丹参酮类物质调控作用机制大多集中在分析与靶基因结合位点, 因此后续研究可以注重转录因子表观遗传研究, 进而为丹参等药用植物的栽培及分子育种提供新的思路与方法。此外, 利用异源宿主植物(烟草、小立碗藓) 作为生物反应器可以稳定地生产青蒿素^[79], 将此方法结合组织培养、代谢工程等技术应用到丹参酮的生物合成, 有助于提高丹参酮的含量, 获得优质的丹参药材, 这可能开启转录因子调控丹参酮生物合成途径研究的新领域。

总之, 通过多种方法构建丹参酮合成调控网络, 筛选提高丹参酮含量的核心转录因子, 有助于丰富丹参酮代谢调控理论, 加速分子育种进程, 完善丹参资源的可持续利用, 为丹参产业的发展提供技术支持。

致谢: 山东省高教厅青年创新团队和山东中医药大学可持续利用青年创新团队对本文提供了支持。

作者贡献: 白艳红负责参考文献的整理及完成初稿撰写; 辛林林、曾婷、韩凤霞负责表格和图片整理; 张永清、蒲高斌负责提供部分参考资料; 陈雪负责对文章的修改提供建议; 刘谦负责提出文章构思、修改及审核。所有作者都认可手稿的最终版本。

利益冲突: 所有作者均声明不存在利益冲突。

基金

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国家自然科学基金资助项目(82003892)
国家现代农业产业技术体系(CARS-21)
山东省自然科学基金资助项目(ZR2021QH202)

参考文献

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文献

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2024年第59卷第5期

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文章信息

doi: 10.16438/j.0513-4870.2023-1110

接收时间：2023-09-26
首发时间：2025-11-27
出版时间：2024-05-12

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出版历史

收稿日期：2023-09-26
修回日期：2023-12-14

基金

国家自然科学基金资助项目(82003892)

国家现代农业产业技术体系(CARS-21)

山东省自然科学基金资助项目(ZR2021QH202)

作者信息

1.山东中医药大学药学院, 山东济南 250355

2.黄冈师范学院李时珍中医学院, 湖北黄冈 438000

通讯作者:

^*陈雪, E-mail: xchenaylli@sina.com;

刘谦, E-mail: cleanlq@163.com

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2种不同金属材料的力学参数

科 Family	属数 Number of genus	种数 Number of species	占总种数比例 Percentage of total species (%)	属 Genus	种数 Number of species	占总种数比例 Percentage of total species (%)
鹅膏菌科Amanitaceae	2	11	5.26	鹅膏菌属 Amanita	10	4.78
小菇科 Mycenaceae	2	12	5.74	丝盖伞属 Inocybe	5	2.39
多孔菌科 Polyporaceae	8	14	6.70	蜡蘑属 Laccaria	5	2.39
红菇科 Russulaceae	3	23	11.00	小皮伞属 Marasmius	6	2.87
				小菇属 Mycena	11	5.26
				光柄菇属 Pluteus	5	2.39
				红菇属 Russula	17	8.13
				栓菌属 Trametes	5	2.39

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Family	Number	Member	GenBank accession	Bioinformation	Tissue expression	Elicitor	Reference
AP2/ERF	179	SmERF72	-	699 bp	Periderm	-	[25, 28]
		SmERF98	-	891 bp	Xylem	-	[25]
		SmERF73	QRQ89295.1	780 bp ORF, 259 aa	Root	YE+Ag⁺, MeJA	[20]
		SmERF128	MG897156	633 bp, 210 aa	Periderm	-	[29]
		SmERF1L1	MH006594	741 bp ORF, 246 aa	Stem	MeJA, YE, SA, ET	[30]
		SmERF2	-	741 bp ORF, 246 aa	Stem	YE, MeJA, ET, SA	[31]
		SmERF6	KY988300	561 bp ORF, 186 aa	Root	ET	[32]
		SmERF8	MH006600	654 bp ORF, 217 aa	Root head	ET	[33]
		SmAP2/ERF82	-	582 bp CDS, 193 aa	Root	-	[26]
		SmERF1	KC405081.1	549 bp ORF, 182 aa	-	YE, MeJA	[34]
bHLH	127	SmbHLH61	-	1 008 bp ORF, 335 aa	Root	MeJA, SA	[35, 36]
		SmbHLH74	KP257507.1	696 bp CDS, 231 aa	Root	MeJA	[37]
		SmbHLH92	KP257525.1	681 bp ORF, 226 aa	Root	-	[38]
		SmbHLH7	-	1 911 bp ORF, 636 aa	Xylem	MeJA, GA	[39]
		SmbHLH10	-	972 bp ORF, 323 aa	Flower	GA, ABA	[39]
		SmbHLH130	-	1 185 bp ORF, 394 aa	Leaf	MeJA, GA, ABA	[39]
		SmbHLH148	-	675 bp ORF, 224 aa	Fibrous root	MeJA, GA, ABA	[39]
		SmbHLH3	-	1 476 bp ORF, 491 aa	Fibrous root	MeJA	[39]
		SmbHLH59	KP257492	1 146 bp CDS, 381 aa	Leaf	MeJA	[22]
MYB	110	SmMYB9b	JX113685	1 207 bp	Blooming flowers	ABA, GA, MeJA	[40, 41]
		SmMYB98	AGN52122.1	699 bp ORF, 232 aa	Lateral roots	-	[42]
		SmMYB1	-	1 071 bp full length, 356 aa	Leaf	MeJA, SA	[43]
		SmMYB36	KF059390.1	160 aa	-	-	[44]
		SmMYB4	-	696 bp ORF	-	-	[21]
		SmMYB97	KF059451	825 bp, 274 aa	Leaf	MeJA	[45]
bZIP	70	SmbZIP1	-	474 bp ORF	Periderm	ABA, YE, ET, SA	[46, 47]
		SmbZIP3	-	807 bp ORF, 268 aa	-	ABA	[48]
		SmHY5	MT408030	474 bp ORF, 157 aa	Leaf	-	[49]
WRKY	61	SmWRKY1	-	789 bp ORF, 262 aa	Stem	MeJA, SA, NO	[50, 51]
		SmWRKY2	-	1 476 bp ORF, 491 aa	Leaf	MeJA	[52]
		SmWRKY14	KM823137	732 bp CDS, 243 aa	Root	MeJA	[22]
		SmWRKY44	KM823167.1	798 bp CDS, 265 aa	Stem	MeJA, SA, 4℃, PEG, NaCl	[53]
		SmWRKY40	-	1 059 bp CDS, 352 aa	Root	MeJA, SA	[54]
		SmWRKY34	-	930 bp ORF, 309 aa	Stem	ABA	[48]
		SmWRKY54	-	861 bp ORF	Taproot	SA, ABA, MeJA, GA3, ET, YE	[55]
		SmWRKY61	-	507 bp full length	-	MeJA	[56]
LBD	51	SmLBD44	-	687 bp CDS, 228 aa	-	MeJA	[57, 58]
GRAS	35	SmGRAS1	KY435886	1 470 bp ORF, 489 aa	Periderm	GA, SA, NAA, MeJA, ABA	[24]
		SmGRAS2	KY435887	1 380 bp ORF, 459 aa	Periderm	GA, SA, NAA, MeJA, ABA	[24, 59]
		SmGRAS3	KY435888	2 247 bp ORF, 748 aa	Periderm	GA, SA, NAA, MeJA, ABA	[24]
		SmGRAS4	KY435889	1 581 bp ORF, 526 aa	Periderm	GA, SA, NAA, MeJA, ABA	[24]
		SmGRAS5	KY435890	1 041 bp ORF, 346 aa	Periderm	GA, SA, NAA, MeJA, ABA	[24]
JAZ	9	SmJAZ1	-	543 bp ORF, 180 aa	Stem	ABA, ET, GA, YE, MeJA	[27, 60]
		SmJAZ2	-	642 bp ORF, 213 aa	Leaf	ABA, SA, ET, GA, YE, NAA, PEG, MeJA	[27, 60]
		SmJAZ5	-	825 bp ORF, 274 aa	Leaf	ABA, SA, ET, GA, YE, NAA, Ag⁺, MeJA	[27, 60]
		SmJAZ6	-	720 bp ORF, 239 aa	Leaf	ABA, SA, GA, YE, NAA, PEG, Ag⁺, MeJA	[27, 60]
		SmJAZ9	-	921 bp ORF, 306 aa	Leaf	ABA, GA, SA, YE, NAA, PEG, Ag⁺, MeJA	[27, 60]
		SmJAZ3	-	1 011 bp ORF, 336 aa	Periderm	ABA, SA, ET, GA, YE, NAA, PEG, MeJA	[60]
		SmJAZ4	-	945 bp ORF, 314 aa	Root	ABA, SA, GA, YE, NAA, PEG, Ag⁺, MeJA	[27, 60]
		SmJAZ8	-	372 bp ORF, 123 aa	Leaf	ABA, SA, ET, GA, YE, NAA, PEG, Ag⁺, MeJA	[61]
		SmJAZ10	-	540 bp ORF, 179 aa	Stem	ABA, SA, ET, GA, YE, NAA, PEG, Ag⁺, MeJA	[27]
WD40	225	SmWD40-170	-	972 bp full length, 323 aa	Root	Mechanical damage, MeJA, GA	[62]
EIL		SmEIN3	-	1 797 bp ORF, 598 aa	Leaf	ABA, GA, SA, MeJA, YE	[63]

Family

Number

Member

GenBank accession

Bioinformation

Tissue expression

Elicitor

Reference

AP2/ERF

179

SmERF72

699 bp

Periderm

[25, 28]

SmERF98

891 bp

Xylem

[25]

SmERF73

QRQ89295.1

780 bp ORF, 259 aa

Root

YE+Ag⁺, MeJA

[20]

SmERF128

MG897156

633 bp, 210 aa

Periderm

[29]

SmERF1L1

MH006594

741 bp ORF, 246 aa

Stem

MeJA, YE, SA, ET

[30]

SmERF2

741 bp ORF, 246 aa

Stem

YE, MeJA, ET, SA

[31]

SmERF6

KY988300

561 bp ORF, 186 aa

Root

[32]

SmERF8

MH006600

654 bp ORF, 217 aa

Root head

[33]

SmAP2/ERF82

582 bp CDS, 193 aa

Root

[26]

SmERF1

KC405081.1

549 bp ORF, 182 aa

YE, MeJA

[34]

bHLH

127

SmbHLH61

1 008 bp ORF, 335 aa

Root

MeJA, SA

[35, 36]

SmbHLH74

KP257507.1

696 bp CDS, 231 aa

Root

MeJA

[37]

SmbHLH92

KP257525.1

681 bp ORF, 226 aa

Root

[38]

SmbHLH7

1 911 bp ORF, 636 aa

Xylem

MeJA, GA

[39]

SmbHLH10

972 bp ORF, 323 aa

Flower

GA, ABA

[39]

SmbHLH130

1 185 bp ORF, 394 aa

Leaf

MeJA, GA, ABA

[39]

SmbHLH148

675 bp ORF, 224 aa

Fibrous root

MeJA, GA, ABA

[39]

SmbHLH3

1 476 bp ORF, 491 aa

Fibrous root

MeJA

[39]

SmbHLH59

KP257492

1 146 bp CDS, 381 aa

Leaf

MeJA

[22]

MYB

110

SmMYB9b

JX113685

1 207 bp

Blooming flowers

ABA, GA, MeJA

[40, 41]

SmMYB98

AGN52122.1

699 bp ORF, 232 aa

Lateral roots

[42]

SmMYB1

1 071 bp full length, 356 aa

Leaf

MeJA, SA

[43]

SmMYB36

KF059390.1

160 aa

[44]

SmMYB4

696 bp ORF

[21]

SmMYB97

KF059451

825 bp, 274 aa

Leaf

MeJA

[45]

bZIP

SmbZIP1

474 bp ORF

Periderm

ABA, YE, ET, SA

[46, 47]

SmbZIP3

807 bp ORF, 268 aa

ABA

[48]

SmHY5

MT408030

474 bp ORF, 157 aa

Leaf

[49]

WRKY

SmWRKY1

789 bp ORF, 262 aa

Stem

MeJA, SA, NO

[50, 51]

SmWRKY2

1 476 bp ORF, 491 aa

Leaf

MeJA

[52]

SmWRKY14

KM823137

732 bp CDS, 243 aa

Root

MeJA

[22]

SmWRKY44

KM823167.1

798 bp CDS, 265 aa

Stem

MeJA, SA, 4℃, PEG, NaCl

[53]

SmWRKY40

1 059 bp CDS, 352 aa

Root

MeJA, SA

[54]

SmWRKY34

930 bp ORF, 309 aa

Stem

ABA

[48]

SmWRKY54

861 bp ORF

Taproot

SA, ABA, MeJA, GA3, ET, YE

[55]

SmWRKY61

507 bp full length

MeJA

[56]

LBD

SmLBD44

687 bp CDS, 228 aa

MeJA

[57, 58]

GRAS

SmGRAS1

KY435886

1 470 bp ORF, 489 aa

Periderm

GA, SA, NAA, MeJA, ABA

[24]

SmGRAS2

KY435887

1 380 bp ORF, 459 aa

Periderm

GA, SA, NAA, MeJA, ABA

[24, 59]

SmGRAS3

KY435888

2 247 bp ORF, 748 aa

Periderm

GA, SA, NAA, MeJA, ABA

[24]

SmGRAS4

KY435889

1 581 bp ORF, 526 aa

Periderm

GA, SA, NAA, MeJA, ABA

[24]

SmGRAS5

KY435890

1 041 bp ORF, 346 aa

Periderm

GA, SA, NAA, MeJA, ABA

[24]

JAZ

SmJAZ1

543 bp ORF, 180 aa

Stem

ABA, ET, GA, YE, MeJA

[27, 60]

SmJAZ2

642 bp ORF, 213 aa

Leaf

ABA, SA, ET, GA, YE, NAA, PEG, MeJA

[27, 60]

SmJAZ5

825 bp ORF, 274 aa

Leaf

ABA, SA, ET, GA, YE, NAA, Ag⁺, MeJA

[27, 60]

SmJAZ6

720 bp ORF, 239 aa

Leaf

ABA, SA, GA, YE, NAA, PEG, Ag⁺, MeJA

[27, 60]

SmJAZ9

921 bp ORF, 306 aa

Leaf

ABA, GA, SA, YE, NAA, PEG, Ag⁺, MeJA

[27, 60]

SmJAZ3

1 011 bp ORF, 336 aa

Periderm

ABA, SA, ET, GA, YE, NAA, PEG, MeJA

[60]

SmJAZ4

945 bp ORF, 314 aa

Root

ABA, SA, GA, YE, NAA, PEG, Ag⁺, MeJA

[27, 60]

SmJAZ8

372 bp ORF, 123 aa

Leaf

ABA, SA, ET, GA, YE, NAA, PEG, Ag⁺, MeJA

[61]

SmJAZ10

540 bp ORF, 179 aa

Stem

ABA, SA, ET, GA, YE, NAA, PEG, Ag⁺, MeJA

[27]

WD40

225

SmWD40-170

972 bp full length, 323 aa

Root

Mechanical damage, MeJA, GA

[62]

EIL

SmEIN3

1 797 bp ORF, 598 aa

Leaf

ABA, GA, SA, MeJA, YE

[63]

Family	Member	Positive/negative	Target gene	Reference		Family	Member	Positive/negative	Target gene	Reference
AP2/ERF	SmERF72	Positive	HMGR, CYP76AH3, KSL1, IDI1	[25]		WRKY	SmWRKY1	Positive	DXR	[51]
	SmERF98	Positive	CYP76AH3, KSL1, IDI1	[25]		SmWRKY2	Positive	CPS	[52]
	SmERF73	Positive	DXR1, CPS1, KSL1, CYP76AH3	[20]		SmWRKY14	Positive	CPS1	[22]
	SmERF128	Positive	CYP76AH1, CPS1, KSL1	[29]		SmWRKY44	Positive	CPS1, CPS5, KSL1	[53]
	SmERF1L1	Positive	DXR	[30]		SmWRKY40	Negative	CPS1, CPS5	[54]
	SmERF2	Positive	CPS1	[31]		SmWRKY34	Negative	GGPPS	[48]
	SmERF6	Positive	KSL1, CPS1	[32]		SmWRKY54	Positive	KSL	[55]
	SmERF8	Positive	KSL1	[33]		SmWRKY61	Positive	-	[56]
	SmAP2/ ERF82	Positive	IDI1, CPS1, CYP76AH3	[26]	LBD	SmLBD44	Negative	KSL1	[58]
	SmERF1	Positive	-	[34]	GRAS	SmGRAS1	Positive	KSL1	[24]
bHLH	SmbHLH61	Positive	-	[36]		SmGRAS2	Positive	-	[24, 59]
	SmbHLH74	Negative	HMGR1, GGPPS1, CYP76AH1	[37]		SmGRAS3	Positive	KSL1	[24]
	SmbHLH92	Positive/ negative	DXR, HMGR4	[38]		SmGRAS4	Positive	KSL1	[24]
	SmbHLH7	Positive	DXS2, CPS1, KSL1, CYP76AH1	[39]		SmGRAS5	Positive	KSL1	[24]
	SmbHLH10	Positive	DXS2, CPS1, CPS5	[39]	JAZ	SmJAZ1	Positive	-	[27, 60]
	SmbHLH130	Positive	CPS1, DXS2, KSL1, CYP76AH1	[39]		SmJAZ2	Positive	-	[27, 60]
	SmbHLH3	Negative	KSL1, CYP76AH1	[39]		SmJAZ5	Positive	-	[27, 60]
	SmbHLH148	Positive	DXS2, CPS1, CYP76AH1	[39]		SmJAZ6	Positive	-	[27, 60]
	SmbHLH59	Positive	CPS1, KSL1	[22]		SmJAZ9	Positive	-	[27, 60]
MYB	SmMYB9b	Positive	-	[41]		SmJAZ3	Negative	-	[60]
	SmMYB98	Positive	GGPPS1	[42]		SmJAZ4	Negative	-	[27, 60]
	SmMYB1	Positive	-	[43]		SmJAZ8	Negative	-	[61]
	SmMYB36	Positive	HMGS1, GGPPS, DXR, CMK, MCT	[44]	WD40	SmWD40-170	Positive	-	[62]
	SmMYB4	Negative	-	[21]	EIL	SmEIN3	Positive	HMGR, DXS2	[63]
	SmMYB39	Negative	-	[39]
	SmMYB97	Positive	CPS1, KSL1	[45]
bZIP	SmbZIP1	Negative	GGPPS	[47]
	SmbZIP3	Positive	-	[48]
	SmHY5	Positive	-	[49]

Family

Member

Positive/negative

Target gene

Reference

Family

Member

Positive/negative

Target gene

Reference

AP2/ERF

SmERF72