Regulatory Mechanisms of Small Peptides in Plant Meristem Development and Its Research Advances in Crop Improvement

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

Abstract

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

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.

Figures/Tables 4

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

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]

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

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]

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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