小肽调控植物分生组织发育的机制及其在作物改良中的研究进展

doi:10.13560/j.cnki.biotech.bull.1985.2024-0193

摘要/Abstract

摘要：

在高等植物的生长发育过程中，根尖分生组织和茎尖分生组织不断分裂分化产生根系、茎、叶和花等器官，分别形成植物的地上和地下部分。小肽是胞间通讯的关键信号分子之一，参与了植物生长发育、抗病抗逆等诸多生命活动，其中包括植物根尖和茎尖分生组织的干细胞活性调控，进而影响了植物器官的生成和发育。近年来，越来越多的研究揭示了小肽分子在分生组织维持和发育中的重要性，及其在多种作物农艺性状调控中的关键作用。本文综述了小肽及其受体在拟南芥和作物中维持分生组织稳态的分子机制，探讨了小肽对作物产量性状的影响及在作物改良中的应用策略，并对小肽领域的研究方向进行了分析和展望。

关键词: 小肽, 分生组织, 调控机制, 农艺性状, 作物改良

Abstract:

Throughout the growth and development of higher plants, the shoot apical meristem（SAM）and root apical meristem（RAM）continually differentiate to generate roots, stems, leaves and flowers, then forming above-ground and below-ground organs, respectively. As one of important intercellular signal transduction molecule, small peptides are involved in regulation of many physiological processes in plant development and resistance to biotic and abiotic stress. Particularly, they play crucial role in regulating the activity of SAM and RAM, which ultimately affect the origin and development of plant organs. In recent years, emerging evidences reveal the importance roles of small peptides in maintaining meristems homeostasis and regulating crop agronomic traits. This review highlights the biological functions and molecular mechanisms of small peptides and their receptors in maintaining the homeostasis of meristems in Arabidopsis and crop species. It also discusses the role of small peptides in regulating crop yield traits and their application in crop improvement. Additionally, the review proposes and prospects the potential interesting research direction of small peptides.

Key words: small peptides, meristems, regulatory mechanism, agronomic traits, crop improvement

刘文浩, 吴刘记, 徐芳. 小肽调控植物分生组织发育的机制及其在作物改良中的研究进展[J]. 生物技术通报, 2024, 40(7): 1-18.

LIU Wen-hao, WU Liu-ji, XU Fang. Regulatory Mechanisms of Small Peptides in Plant Meristem Development and Its Research Advances in Crop Improvement[J]. Biotechnology Bulletin, 2024, 40(7): 1-18.

图/表 4

图1 小肽参与拟南芥茎尖分生组织调控的分子机制拟南芥茎尖分生组织由组织中心、中央母细胞区、周缘分生组织区和肋状分生组织区组成，也可分为L1、L2、L3层。维持茎尖分生组织干细胞特性的关键转录因子WUS在组织中心特异性表达，并通过胞间连丝向中央母细胞区迁移，在转录因子HAM的限制下，促进中央母细胞区CLV3的表达。CLV3前肽表达后经修饰和剪切形成成熟肽并扩散至组织中心，反过来抑制WUS的表达，形成茎尖分生组织中的关键负反馈通路。CLV1，CLV2，CRN，RPK2，CIKs能够形成多种受体复合物，识别CLV3肽并向下游传递，抑制WUS的表达。CLE40与其受体BAM1在周缘分生组织区表达，与WUS建立了另一个负反馈调控通路。EPFL肽与其受体ERf在茎尖分生组织周边表达，将WUS和CLV3的表达限制在中心区域

Fig. 1 Molecular mechanisms involved in the regulation of shoot apical meristem（SAM）by small peptides in Arabidopsis In Arabidopsis, the shoot apical meristem（SAM）is composed of organizing center（OC）, central zone（CZ）, peripheral zone（PZ）, and rib zone（RZ）, which can also be divided into layer L1, L2, and L3. The key transcription factor WUS, which maintains stem cell characteristics in SAM, is specifically expressed in OC and migrates to the CZ through plasmodesmata. WUS promotes the expression of CLV3 in the CZ under the restriction of the transcription factor HAM. After being modified and cleaved, mature CLV3 peptides move to the OC and inhibits the expression of WUS, establishing a key negative feedback pathway in SAM regulation. CLV1, CLV2, CRN, RPK2, and CIKs form different receptor complexes that recognize CLV3 peptide and transmit signal to inhibit WUS expression. CLE40 and its receptor BAM1 are expressed in the PZ, forming an additional negative feedback pathway with WUS. EPFL and its receptor ERf are expressed in the PZ, restricting the expression of WUS and CLV3 to the CZ

图2 R类CLE、RGF、EPF/EPFL肽的翻译后修饰及序列特征以CLV3、RGF1和Stomagen/EPFL9为例展示R类CLE、RGF、EPF/EPFL肽的翻译后修饰及序列特征[16,63 -64]。在R类CLE、RGF、EPF/EPFL家族中完全一致的氨基酸用红色标注，相似性较高的氨基酸用蓝色标出。H类CLE的成熟肽的第一个氨基酸为His，包括TDIF（CLE41/44/42）和CLE46，其余CLE肽为R类CLE肽，成熟肽的第一个氨基酸为Arg[16,65]

Fig. 2 Post-translational modifications and sequence characteristics of R-type CLE, RGF, EPF/EPFL peptides CLV3, RGF1 and Stomagen/EPFL9 were used as examples to demonstrate the post-translational modifications and sequence characteristics of R-type CLE, RGF, EPF/EPFL peptides[16,63 -64]. Identical amino acid residues are highlighted in red, and similar amino acid residues are highlighted in blue. The first amino acid of the mature peptides of H-type CLE is His, including TDIF（CLE41/44/42）and CLE46. The other CLE peptides are R-type CLE peptides, and the first amino acid of the mature peptides R-type is Arg[16,65]

图3 小肽参与拟南芥根尖分生组织调控的分子机制 A：拟南芥根尖分生组织由静止中心、远端分生组织和近端分生组织组成。远端分生组织即小柱干细胞，近端分生组织包括静止中心上方的一层干细胞及其后代细胞。近端分生组织中的初生韧皮部由筛管-原形成层干细胞经多次垂周和平周分裂产生。B：CLE40-CLV1/ACR4通过抑制WUS促进小柱干细胞的分化，CLE45通过BAM1/3，CIKs，CLV2/CRN，RPK2组成的多种受体复合物抑制初生韧皮部分化，其下游组分包括MAKR5和PBL34/35/36等。OPS和BRX、BR信号和pH梯度均参与了CLE45信号通路，调控初生韧皮部分化。RGF1-RGFR通过MAPK级联和ROS上调PLT1/2，维持根分生组织细胞增殖活性。RGF1的酪氨酸硫酸化由TPST酶催化，生长素信号通过上调TPST间接调控RGF1信号通路

Fig. 3 Molecular mechanisms involved in the regulation of root apical meristem（RAM）by small peptides in Arabidopsis A：In Arabidopsis, the root apical meristem（RAM）comprises of the quiescent center（QC）, distal meristem（DM）, and proximal meristem（PM）. The DM consists of columella stem cells（CSCs）and the PM includes a layer of stem cells adjacent to QC and its progeny cells. Protophloem in the PM is produced by Sieve Element（SE）-Procambium Stem Cell（SPSC）after multiple periclinal and anticlinal divisions. B：CLE40-CLV1/ACR4 inhibits WUS to promote the differentiation of CSCs, and CLE45 inhibits the differentiation of the protophloem through different receptor complexes composed of BAM1/3, CIKs, CLV2/CRN, and RPK2, with downstream components including MAKR5 and PBL34/35/36. OPS, BRX, BR signals, and pH gradient are all involved in the CLE45 signaling pathway, regulating protophloem differentiation. RGF1-RGFR upregulates PLT1/2 through MAPK cascades and ROS to maintain meristem proliferation activity in RAM. The tyrosine sulfation of RGF1 is catalyzed by TPST, and auxin signals indirectly regulate the RGF1 signaling pathway by upregulating TPST

表1 小肽分子在顶端分生组织调控中的功能

Table 1 Function of small peptides in apical meristem regulation

定位 Location	家族 Family	物种 Species	小肽 Peptide	受体 Receptor	下游组分 Downstream components	功能 Functions	参考文献 References
SAM	CLE	拟南芥	CLV3	CLV1，CLV2，CRN，RPK2，CIKs	PBL34/35/36，MAPK级联，Ca²⁺，KAPP，POL/PLL，AGB1，WUS	抑制WUS的表达，抑制茎尖、花序、花分生组织干细胞活性，调控器官产生	[16,19,23,25,36 -37,46,48,51,53⇓⇓ -56,58 -59,61 -62]
			CLE40	BAM1	WUS	作为来自周缘分生组织区的信号，微调WUS的表达和干细胞活性	[26,40]
		水稻	FON2 （FON4）	FON1		抑制花分生组织干细胞活性，调控枝梗、花器官和雌蕊数量等产量性状	[113-114,117]
			FOS1			与FON2-FON1冗余性地调控花分生组织干细胞活性	[118]
			FCP1/2		OsWOX4	抑制OsWOX4的表达，抑制茎尖分生组织干细胞活性	[115,119]
		玉米	ZmFCP1	FEA2，FEA3	ZmCRN	抑制茎尖、花序分生组织干细胞活性，调控玉米果穗大小、穗行数、行粒数等产量性状	[61,112,122,124]
			ZmCLE7	FEA2	CT2	抑制茎尖、花序分生组织干细胞活性，调控玉米果穗大小、穗行数、行粒数等产量性状	[61,112,122,124]
			ZmCLE1E5			与ZmCLE7冗余性地调控花序分生组织干细胞活性，调控玉米果穗大小、穗行数、行粒数等产量性状	[112]
		番茄	SlCLV3	FAB	SLWUS	抑制SlWUS的表达，抑制茎尖、花序、花分生组织干细胞活性，调控花、花心皮数量，影响果实大小	[32,43,128]
			SlCLE9	FAB	SLWUS	与SlCLV3冗余性地调控分生组织干细胞活性，调控花、花心皮数量，影响果实大小	[32,126]
	EPF/ EPFL	拟南芥	EPFL1/2/4/6	ERf	WUS，CLV3	限制WUS和CLV3的表达区域，调控茎尖分生组织稳态	[68⇓-70]
		水稻	GAD1（OsEPFL1）			调控水稻每穗粒数、粒形和芒的发育	[129-130]
			OsEPFL6/7/8/9	OsER1	MAPK级联	调节水稻每穗粒数	[131]
RAM	CLE	拟南芥	CLE40/16/ 17	ACR4，CLV1，CIKs	WOX5	抑制WOX5表达，促进小柱干细胞的分化，调控根远端分生组织稳态	[34,74⇓ -76]
			CLE25/26/33/45	BAM1/3，CLV2，CRN，CIKs	PBL34/35/36，BRX，OPS	抑制初生韧皮部分化，调控根近端分生组织稳态	[12,53,77,79 -80,82,87]
			CLE14	CLV2，PEPR2	SCR，SHR，PIN	通过调控根分生组织活性参与低磷胁迫响应	[108]
	RGF	拟南芥	RGF1/2/3	RGFR1/2/3/4/5	RITF1，MAPK级联，PLT1/2，WOX5	响应生长素信号，通过下游PLT1/PLT2和WOX5调控根近端和远端分生组织稳态，并参与低磷胁迫响应	[91,93 -94,96,100,104]

表1 小肽分子在顶端分生组织调控中的功能

Table 1 Function of small peptides in apical meristem regulation

定位 Location	家族 Family	物种 Species	小肽 Peptide	受体 Receptor	下游组分 Downstream components	功能 Functions	参考文献 References
SAM	CLE	拟南芥	CLV3	CLV1，CLV2，CRN，RPK2，CIKs	PBL34/35/36，MAPK级联，Ca²⁺，KAPP，POL/PLL，AGB1，WUS	抑制WUS的表达，抑制茎尖、花序、花分生组织干细胞活性，调控器官产生	[16,19,23,25,36 -37,46,48,51,53⇓⇓ -56,58 -59,61 -62]
			CLE40	BAM1	WUS	作为来自周缘分生组织区的信号，微调WUS的表达和干细胞活性	[26,40]
		水稻	FON2 （FON4）	FON1		抑制花分生组织干细胞活性，调控枝梗、花器官和雌蕊数量等产量性状	[113-114,117]
			FOS1			与FON2-FON1冗余性地调控花分生组织干细胞活性	[118]
			FCP1/2		OsWOX4	抑制OsWOX4的表达，抑制茎尖分生组织干细胞活性	[115,119]
		玉米	ZmFCP1	FEA2，FEA3	ZmCRN	抑制茎尖、花序分生组织干细胞活性，调控玉米果穗大小、穗行数、行粒数等产量性状	[61,112,122,124]
			ZmCLE7	FEA2	CT2	抑制茎尖、花序分生组织干细胞活性，调控玉米果穗大小、穗行数、行粒数等产量性状	[61,112,122,124]
			ZmCLE1E5			与ZmCLE7冗余性地调控花序分生组织干细胞活性，调控玉米果穗大小、穗行数、行粒数等产量性状	[112]
		番茄	SlCLV3	FAB	SLWUS	抑制SlWUS的表达，抑制茎尖、花序、花分生组织干细胞活性，调控花、花心皮数量，影响果实大小	[32,43,128]
			SlCLE9	FAB	SLWUS	与SlCLV3冗余性地调控分生组织干细胞活性，调控花、花心皮数量，影响果实大小	[32,126]
	EPF/ EPFL	拟南芥	EPFL1/2/4/6	ERf	WUS，CLV3	限制WUS和CLV3的表达区域，调控茎尖分生组织稳态	[68⇓-70]
		水稻	GAD1（OsEPFL1）			调控水稻每穗粒数、粒形和芒的发育	[129-130]
			OsEPFL6/7/8/9	OsER1	MAPK级联	调节水稻每穗粒数	[131]
RAM	CLE	拟南芥	CLE40/16/ 17	ACR4，CLV1，CIKs	WOX5	抑制WOX5表达，促进小柱干细胞的分化，调控根远端分生组织稳态	[34,74⇓ -76]
			CLE25/26/33/45	BAM1/3，CLV2，CRN，CIKs	PBL34/35/36，BRX，OPS	抑制初生韧皮部分化，调控根近端分生组织稳态	[12,53,77,79 -80,82,87]
			CLE14	CLV2，PEPR2	SCR，SHR，PIN	通过调控根分生组织活性参与低磷胁迫响应	[108]
	RGF	拟南芥	RGF1/2/3	RGFR1/2/3/4/5	RITF1，MAPK级联，PLT1/2，WOX5	响应生长素信号，通过下游PLT1/PLT2和WOX5调控根近端和远端分生组织稳态，并参与低磷胁迫响应	[91,93 -94,96,100,104]

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