蒺藜苜蓿SMXL基因家族全基因组鉴定及表达分析

doi:10.13560/j.cnki.biotech.bull.1985.2025-0481

摘要/Abstract

摘要：

目的 SMXLs（SUPPRESSOR of MAX2 1-LIKE）是重要植物激素独角金内酯信号转导通路中的抑制因子及烟素（karrikins, KARs）信号通路的主要成员。在全基因组水平鉴定蒺藜苜蓿SMXL基因家族成员并分析其在非生物胁迫下的表达模式变化，为豆科植物相关基因家族的研究提供理论支持，为未来深入研究MtSMXL基因的功能奠定基础。方法运用生物信息学方法，基于已报道植物SMXL家族编码氨基酸序列，对蒺藜苜蓿SMXL家族成员进行全基因组鉴定，利用TBtools等工具对MtSMXL成员进行进化和功能分析，同时利用转录组数据进行成员不同组织内表达分析及钾、氮、磷、硫营养缺乏胁迫处理和在冷害、干旱、高盐胁迫下的表达量分析。结果依据进化分析，共筛选鉴定出17个MtSMXL成员。参考基因结构和保守结构域将它们分为G1-G3三个组群；MtSMXLs上游启动子区域存在多种参与响应植物激素和非生物胁迫的顺式作用元件，各成员中类型和数量有一定差异；共线性分析表明，豆科植物WGD事件对MtSMXL基因家族的扩张有重要作用；家族成员在不同组织部位及响应各种胁迫的过程中其表达模式均存在明显差异，通过分析选出参与不同胁迫响应功能候选基因。结论蒺藜苜蓿SMXL基因不同组群在进化中结构和功能差异较大，成员及不同胁迫下响应模式不同，其中MtSMXL2/7/11可用于K/N/S/P元素缺乏胁迫；而MtSMXL7/8/13/14/16可用于干旱、冷、高盐胁迫响应通路研究。

关键词: MtSMXL, 基因组, 蒺藜苜蓿, 全基因组鉴定, 系统发育, 基因特征

Abstract:

Objective SMXLs (SUPPRESSOR of MAX2 1-LIKE) are key repressors in the signal transduction pathway of the important plant hormone strigolactones (SLs) and major components of the karrikin (KARs) signaling pathway. The genome-wide identification of SMXL gene family members in Medicago truncatula and analysis of their expression pattern changes under abiotic stresses were conducted to provide theoretical support for the study of related gene families in legumes and lay a foundation for in-depth research on the functions of MtSMXL genes in the future. Method Employing bioinformatics methods, based on the reported amino acid sequences encoded by the SMXL family in plants, the genome-wide identification of SMXL family members in M. truncatula was performed. Tools such as TBtools were used for evolutionary and functional analyses of MtSMXL members. Meanwhile, transcriptome data were utilized to analyze the expressions of these members in different tissues, as well as their expressions under nutrient deficiency stress treatments (potassium, nitrogen, phosphorus, and sulfur deficiency) and abiotic stress treatments (cold,drought,and high salt). Result Through evolutionary analysis, a total of 17 MtSMXL members were identified. They were divided into three groups (G1-G3) with reference to gene structure and conserved domains. The upstream promoter regions of MtSMXLs contained a variety of cis-acting elements involved in responding to plant hormones and abiotic stresses, with differences in the type and number of these elements among different members. Synteny analysis revealed that WGD events in legumes play a crucial role in the expansion of the MtSMXL gene family. Significant differences were observed in the expression patterns of family members across different tissues and in response to various stresses. Functional candidate genes involved in responses to various stresses were selected through analysis. Conclusion Different groups of SMXL genes in M. truncatula present significant differences in structure and function during evolution, and the expression patterns of members vary under different stresses. Among them, MtSMXL2/7/11 can be used for the study of K/N/S/P element deficiency stress response pathways, while MtSMXL7/8/13/14/16 can be applied to the studies on the response pathways to drought, cold, and high salt stress.

Key words: MtSMXL, genome, Medicago truncatula, genome-wide identification, phylogeny, gene characteristics

庄娜, 贺红利, 张兴政. 蒺藜苜蓿SMXL基因家族全基因组鉴定及表达分析[J]. 生物技术通报, 2026, 42(2): 250-266.

ZHUANG Na, HE Hong-li, ZHANG Xing-zheng. Genome-wide Identification and Expression Analysis of the SMXL Gene Family in Medicago truncatula[J]. Biotechnology Bulletin, 2026, 42(2): 250-266.

图/表 18

表1 MtSMXL基因基础信息

Table 1 Basic information of MtSMXL genes

基因名称 Gene name	基因ID Gene ID	染色体定位 Location	基因链 Strand	外显子数 Exon	编码区长度 CDS （bp）
MtSMXL1	Medtr1g057150	chr1：25117416..25121709	+	3	2 427
MtSMXL2	Medtr1g090640	chr1：40585935..40589246	-	3	2 550
MtSMXL3	Medtr2g038200	chr2：16610767..16615642	+	3	3 030
MtSMXL4	Medtr3g461000	chr3：24065055..24068423	+	8	2 449
MtSMXL5	Medtr3g464150	chr3：25772408..25778862	+	3	3 243
MtSMXL6	Medtr3g070850	chr3：31780989..31785558	+	3	3 246
MtSMXL7	Medtr3g098310	chr3：44871095..44878208	-	13	2 859
MtSMXL8	Medtr3g498725	chr3：45109729..45116929	+	11	2 769
MtSMXL9	Medtr3g102830	chr3：47377876..47383774	+	10	2 784
MtSMXL10	Medtr3g106160	chr3：49006958..49015432	-	10	2 943
MtSMXL11	Medtr4g109450	chr4：45465442..45469308	+	5	2 739
MtSMXL12	Medtr4g127290	chr4：52803794..52807296	-	3	2 463
MtSMXL13	Medtr4g129230	chr4：53817793..53821564	+	3	3 126
MtSMXL14	Medtr5g071060	chr5：30105997..30111708	+	3	3 279
MtSMXL15	Medtr6g013660	chr6：4395062..4403563	-	10	2 925
MtSMXL16	Medtr7g012820	chr7：3513549..3521223	-	10	2 937
MtSMXL17	Medtr8g100040	chr8：40241178..40246683	+	10	2 781

图１蒺藜苜蓿SMXL基因家族成员染色体分布红色代表高基因密度，蓝色代表低基因密度

Fig. 1 Chromosome distribution of SMXL gene family in M. truncatulaRed indicates high gene density, and blue indicates low gene density

表2 MtSMXL蛋白理化性质预测

Table 2 Prediction of physical and chemical properties of MtSMXLproteins

基因名称 Gene name	氨基酸数 Peptide （aa）	分子质量 Mass of molecule （kD）	等电点 Theoretical pI	不稳定系数 Instability index	脂肪指数 Aliphatic index	平均亲水指数 GRAVY	亚细胞定位 Subcellular localization
MtSMXL1	808	90.50	5.74	46.88	82.86	-0.502	叶绿体
MtSMXL2	849	95.17	6.03	54.29	82.99	-0.362	叶绿体
MtSMXL3	1 009	113.46	6.41	51.71	78.12	-0.509	细胞核
MtSMXL4	810	90.80	7.33	37.38	97.32	-0.233	细胞质
MtSMXL5	1 080	120.931	6.27	50.68	85.24	-0.307	细胞核
MtSMXL6	1 081	119.74	6.34	50.45	84.38	-0.356	细胞核
MtSMXL7	963	107.09	7.04	47.16	89.41	-0.287	叶绿体
MtSMXL8	922	102.71	6.35	40.68	95.40	-0.341	叶绿体
MtSMXL9	927	103.07	6.41	40.14	93.50	-0.360	叶绿体
MtSMXL10	980	109.89	6.53	38.67	92.85	-0.385	线粒体
MtSMXL11	912	101.35	5.85	36.33	96.23	-0.402	细胞质
MtSMXL12	820	92.33	8.18	58.46	77.52	-0.524	叶绿体
MtSMXL13	1 027	112.90	6.34	46.61	83.50	-0.471	细胞质
MtSMXL14	1 092	120.61	6.05	43.61	81.12	-0.254	细胞核
MtSMXL15	974	109.96	6.65	42.89	89.30	-0.474	叶绿体
MtSMXL16	978	110.28	6.26	37.80	90.14	-0.455	线粒体
MtSMXL17	926	102.78	6.44	40.51	94.04	-0.357	叶绿体

图2 SMXL 基因家族系统发育树A：种间系统发育树；B：种内系统发育树

Fig. 2 Phylogenetic tree of SMXL gene familyA: Interspecific phylogenetic tree. B: Intraspecific phylogenetic tree

表3 MtSMXLs蛋白质二级结构预测

Table 3 Secondary structure prediction of the MtSMXLs protein

蛋白质 Protein	α螺旋 Alpha helix		延伸链 Extended strand		β转角 β-turn		无规则卷曲 Random coil
蛋白质 Protein	长度 Length （aa）	所占比例 Proportion （%）	长度 Length （aa）	所占比例 Proportion （%）	长度 Length （aa）	所占比例 Proportion （%）	长度 Length （aa）	所占比例 Proportion （%）
MtSMXL1	382	47.28	68	8.42	21	2.60	358	44.31
MtSMXL2	366	43.11	53	6.24	13	1.53	430	50.65
MtSMXL3	440	43.61	77	7.63	17	1.68	492	48.76
MtSMXL4	417	51.48	87	10.74	51	6.30	306	37.78
MtSMXL5	443	41.02	88	8.15	14	1.30	549	50.83
MtSMXL6	406	37.56	99	9.16	19	1.76	576	53.28
MtSMXL7	506	52.54	86	8.93	51	5.30	371	38.53
MtSMXL8	496	53.80	87	9.44	51	5.53	339	36.77
MtSMXL9	523	56.42	85	9.17	50	5.39	319	34.41
MtSMXL10	563	57.45	82	8.37	44	4.49	335	34.18
MtSMXL11	550	60.31	84	9.21	45	4.93	278	30.48
MtSMXL12	363	44.27	53	6.46	7	0.85	404	49.27
MtSMXL13	512	49.85	70	6.82	20	1.95	445	43.33
MtSMXL14	471	43.13	84	7.69	16	1.47	537	49.18
MtSMXL15	554	56.88	84	8.62	46	4.72	336	34.50
MtSMXL16	545	55.73	86	8.79	45	4.60	347	35.48
MtSMXL17	507	54.75	92	9.94	49	5.29	327	35.31

表4 MtSMXLs保守基序序列鉴定

Table 4 Conserved motifs identification of MtSMXLs

基序 Motif	Sites	长度 Length （aa）	序列 Sequence
1	9	50	MSEYMERHTVSRLIGAPPGYVGYEEGGQLTEAVRRRPYTVVLFDEIEKAH
2	9	50	GATTLDEYRKHIEKDPALERRFQPVKVPEPSVEDTISILKGLRERYEJHH
3	9	50	GKLDPVIGRDEZIERVIQILSRRTKNNPVLIGEPGVGKTAIAEGLAQRIV
4	17	41	NPNRPIASFMFLGPTGVGKTELAKALAEYVFGSEEALIRJD
5	15	35	LQIJEDGRLTDSQGRTVSFKNTIIIMTSNVGSSVI
6	17	38	QZELTEEAAKVJKLAVEVARRRGHAQVTPLHIASALLS
7	9	50	KVRYTDDALVAAAELSDRYISDRFLPDKAIDLIDEAGSKVRLZHASKPEE
8	7	50	VLKEVTESSGZIILFIDEIHTVIGAGATEGAMDAANJLKPMLARGELRCI
9	9	49	WTGIPVSKLSQDERERLLKLEDTLHKRVIGQDEAVEAIARAIRRSRVGL
10	9	50	KDSSYNRIKSLVMEELRQYFRPEFLNRLDEMIVFRPLTKLZVKEIADJML
11	9	50	VTERARDLVVDEGYBPSYGARPLRRAIQRLVEBELAEKMLRREIKEGDSV
12	8	29	VKVELEQLIJSILDDPSVSRVMREAGFSS
13	9	24	PPVSNALMAAJKRAQAHQRRGPIE
14	17	29	DVPETLHPLQLIALDLGLLVALAKYPGEF
15	4	50	ARQLGHNYIGSEHLLLGLLREGEGVAARVLENLGADPTNIRTQVIRMVGE

图3 蒺藜苜蓿SMXL成员保守基序、蛋白保守结构域和基因结构A：MtSMXL蛋白的保守基序，不同的方形代表不同的基序；B：MtSMXL蛋白保守结构域，不同的方形代表不同的蛋白质结构域；C：MtSMXLs基因结构

Fig. 3 Conserved motifs, protein conserved domains, and gene structure of MtSMXLs in M. truncatulaA: Conserved motif of MtSMXL protein, different squares indicate different motif. B: MtSMXL protein domain, different squares indicate different protein domains. C: Gene structure of MtSMXL genes

图4 SMXL基因启动子的顺式作用元件A：MtSMXL基因启动子区顺式作用元件分布，不同颜色的椭圆代表不同的元件；B：M启动子区域顺式作用元件数量热图；C：MtSMXL基因启动子区域各类顺式作用元件堆积统计图。由于启动子位置重合和篇幅原因，启动子位置图A和热图B中不展示光响应元件和一些与本研究无关的生长发育相关元件

Fig. 4 Cis-acting elements in the promoter of the SMXL genesA: Distribution of cis-acting element in the promoter region of the MtSMXL gene, with different colored ovals representing different cis-elements. B: Heatmap of the number of cis-acting elements in the promoter region of M . C: Stacked statistical chart of various cis-acting elements in the promoter region of the MtSMXL gene. Due to the overlap of promoter positions and space limitations, light-responsive elements and some growth- and development-related elements irrelevant to this study are not shown in the promoter position map A and the heatmap B

图5 MtSMXL基因物种内共线性图灰色线代表基因组中具有共线性的基因对，绿色线表示具有共线关系的MtSMXL基因对；图中内圈和中圈皆表示蒺藜苜蓿基因组基因密度，最外圈表示染色体；图例表示内圈中基因密度情况，黄色表示高基因密度，蓝色表示低基因密度

Fig. 5 Intraspecific collinearity of the MtSMXL genesThe gray lines indicate collinearity gene pairs in the genome, and the green lines indicate gene pairs ofcollinear MtSMXL. The inner and middle circles indicate the gene density of the M. truncatula genome, and the outermost circle indicates the chromosomes. The legend indicates the gene density in the inner circle, where yellow shows high gene density and blue shows low gene density

表5 MtSMXL基因对分离时间估算

Table 5 Estimated separation time of MtSMXL gene pairs

基因对Gene pairs		Ka	Ks	Ka/Ks	分离时间Estimated time（Mya）
MtSMXL3	MtSMXL12	0.253	0.919	0.275	75.3
MtSMXL5	MtSMXL14	0.255	0.721	0.354	59.08
MtSMXL8	MtSMXL17	0.056	0.68	0.082	55.74

图6 蒺藜苜蓿与其他物种SMXL家族基因的共线性分析A：蒺藜苜蓿与大豆和菜豆的SMXL共线性分析；B：蒺藜苜蓿与玉米和拟南芥的SMXL共线性分析。蒺藜苜蓿和其他物种基因组中的共线由灰线显示，与其他物种之间的共线SMXL基因对用亮色线条突出显示

Fig. 6 Collinearity analysis of SMXL genes between M. truncatula and other speciesA: Collinearity analysis of SMXL family genes in M. truncatula, Glycine max and common bean. B: Collinearity analysis of SMXL family genes in M. truncatula, Z. mays and Arabidopsis. The collinear regions in the genomes of M. truncatula and other species are shown by gray lines, and the collinear SMXL gene pairs with other species are highlighted by bright lines

表6 MtSMXLs和AtSMXLs、GmSMXLs、PvSMXLs、ZmSMXLs基因的同线性分析

Table 6 Synteny analysis of MdSMXLs and AtSMXLs, GmSMXLs, PvSMXLs, and ZmSMXLs gene

蒺藜苜蓿 M. truncatula	拟南芥 A. thaliana	玉米 Z. mays	菜豆 P. vulgaris	大豆 G. max	蒺藜苜蓿 M. truncatula	拟南芥 A. thaliana	玉米 Z. mays	菜豆 P. vulgaris	大豆 G. max
MtSMXL1			ESW17795	Glyma.02G198000.1	MtSMXL11	AT1G74310.1			Glyma.05G022200.1
MtSMXL1				Glyma.10G079000.1					Glyma.06G202200.2
MtSMXL2			ESW16225	Glyma.10G121542.2					Glyma.17G077500.1
				Glyma.10G196300.1	MtSMXL12	AT4G29920.2		ESW10759	Glyma.09G060500.1
				Glyma.20G193900.1		AT5G57130.1		ESW26697	Glyma.13G101300.1
MtSMXL3	AT4G29920.2		ESW10759	Glyma.09G060500.1					Glyma.15G167000.1
	AT5G57130.1		ESW26697	Glyma.13G101300.1					Glyma.17G058400.1
				Glyma.15G167000.1	MtSMXL13	AT4G30350.1	Zm00001eb412800_T002	ESW26813	Glyma.13G092700.1
				Glyma.17G058400.1	MtSMXL13	AT5G57710.1	Zm00001eb257430_T002		Glyma.17G067700.1
MtSMXL4					MtSMXL14	AT2G29970.1		ESW14200	Glyma.02G226900.6
MtSMXL5	AT1G07200.2		ESW14200	Glyma.02G226900.6				ESW18766	Glyma.11G174500.4
	AT2G29970.1		ESW18766	Glyma.11G174500.4					Glyma.14G193900.2
				Glyma.14G193900.2					Glyma.18G062300.1
				Glyma.18G062300.1	MtSMXL15
MtSMXL6	AT2G40130.2		ESW13755	Glyma.11G230700.1	MtSMXL16	AT5G15450.1		ESW11501	Glyma.08G242100.1
			ESW18766	Glyma.18G026600.3				ESW23286	Glyma.13G058600.1
			ESW35546	Glyma.18G062300.1					Glyma.18G264400.1
MtSMXL7	AT5G51070.1	Zm00001eb084420_T004	ESW09825	Glyma.04G203300.1					Glyma.19G027900.1
MtSMXL7				Glyma.06G162200.1	MtSMXL17	AT3G48870.3	Zm00001eb084890_T001	ESW09858	Glyma.04G200400.8
MtSMXL8						AT5G50920.1		ESW31965	Glyma.05G201100.4
MtSMXL9									Glyma.06G165200.6
MtSMXL10	AT2G25140.1	Zm00001eb234160_T001	ESW08954	Glyma.04G062200.1					Glyma.08G008400.1

图7 MtSMXLs互作蛋白预测网络

Fig. 7 Putative network for MtSMXLs interacting proteins M. truncatula

图8 蒺藜苜蓿SMXL家族基因不同组织部位表达分析右上角显示MtSMXL基因在不同组织中的表达量变化范围，红色越深代表表达量越高，蓝色越深代表表达量越低；图中adj指距离，dap指授粉后日数

Fig. 8 Expression analysis of SMXL family genes indifferent tissues of M. truncatulaThe upper right corner shows the expression range of the MtSMXL gene in different tissues. Darker red indicates higher expression， and darker blue indicates lower expression. In the figure， adj refers to distance， and dap refers to days after pollination

图9 蒺藜苜蓿MtSMXL成员在N、P、K和S元素缺乏条件下基因表达分析A：MtSMXLs基因响应低钾处理在根及芽中的表达水平热图；B：MtSMXLs基因响应低氮处理在根及芽中的表达水平热图；C：MtSMXLs基因响应低磷处理在根及芽中的表达水平热图；D：MtSMXLs基因响应低硫处理在根及芽中的表达水平热图

Fig. 9 Expression analysis of SMXL family genes of M. truncatula under conditions of N, P, K and S deficiencyA: Heatmap of the expressions of MtSMXLs genes in response to low potassium treatment in the roots and shoots. B: Heatmap of the expressions of MtSMXLs genes in response to low nitrogen treatment in the roots and shoots. C: Heatmap of the expressions of MtSMXLs genes in response to low phosphorus treatment in the roots and shoots. D: Heatmap of the expressions of MtSMXLs gene in response to low sulfur treatment in the roots and shoots

图10 候选互作蛋白编码基因在N、P、K和S处理下基因表达分析依据GraphPad Prism 5.0分析，*P<0.05，**P<0.005

Fig. 10 Gene expression analysis of candidate genes encoding interacting proteins under N, P, K and S treatmentsBased on GraphPad Prism 5.0 analysis, *P<0.05, **P<0.005

图11 候选互作蛋白编码基因在干旱、冷、盐处理条件下基因表达分析

Fig. 11 Gene expression analysis of candidate genes encoding interacting proteins under drought, cold and salt treatment conditions

图12 蒺藜苜蓿MtSMXL成员在干旱、冷、盐处理条件下基因表达分析A：MtSMXLs基因在干旱处理下在幼苗中的表达水平热图；B：MtSMXLs基因在冷处理下在幼苗中的表达水平热图；C：MtSMXLs基因在盐处理下在幼苗中的表达水平热图

Fig. 12 Analysis of the gene expression patterns of SMXL family genes under drought, cold and salt treatmentA: Heatmap of the expression levels of MtSMXLs gene under drought treatment in seedlings. B: Heatmap of the expression levels of MtSMXLs gene under cold treatment in seedlings. C: Heatmap of the expression levels of MtSMXLs gene under salt treatment in seedlings

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