谷子β-胡萝卜素异构酶家族基因的表达与变异分析

doi:10.11983/CBB22171

摘要/Abstract

摘要： 株型是影响谷类作物产量的重要性状, 株型改良对提高作物产量具有重要意义。独脚金内酯(strigolactones, SLs)作为一种最新被鉴定的植物激素, 其通过抑制腋芽的伸长调控分枝/分蘖的形成。β-胡萝卜素异构酶(D27s)是SLs合成途径的关键酶, 通过对谷子(Setaria italica) β-胡萝卜素异构酶典型结构域Pfam:DUF4033进行分析, 鉴定到3个谷子D27s基因家族成员(Seita.8G168400、Seita.6G088800和Seita.3G050900)。蛋白质特性分析显示, 谷子D27s蛋白由271-277个氨基酸残基组成, 分子量为30.1-30.4 kDa, 等电点为5.85-9.31, 不稳定系数介于38.48-74.47之间, 且均定位于叶绿体; 系统进化分析发现, 谷子D27s家族成员位于3个不同进化分支; 顺式作用元件预测显示, SiD27-1 (Seita.8G168400)可能参与调控生物节律、生长素介导的生长发育以及干旱和低温等胁迫应答过程。基因表达分析显示, SiD27-1在谷子多分蘖材料中表达下调, 在低磷胁迫处理下, D27s基因均能产生不同程度的响应, 并且SiD27-1的响应较其它成员更快速。单倍型分析结果表明, SiD27-1的H001单倍型为优异单倍型, 对谷子的株高、抽穗期和产量改良具有重要应用价值。综上, 推测SiD27-1极可能在SLs合成中发挥关键作用并对谷子株型产生影响。研究结果为深入揭示D27s对谷子分蘖形成的调控机制奠定了基础, 也为谷子株型分子设计育种提供了优异的等位变异位点。

关键词: β-胡萝卜素异构酶, 基因家族, 表达, 单倍型变异, 谷子

Abstract: Plant architecture is of great importance for yield improvement of cereal crops, and improvement of plant architecture is of great significance for improving crop yield potential. As a newly identified plant hormone, strigolactones is one of plant hormones regulating branching and tillering by inhibiting the elongation of axillary buds. β-carotene isomerase is the key enzyme for strigolactone synthesis. By the typical domain Pfam:DUF4033, all members in the β-carotene isomerase gene family in foxtail millet (Setaria italica) were identified (Seita.8G168400, Seita.6G088800, Seita.3G- 050900), encoding 271 to 277 amino acid residues with molecular weight ranging from 30.1 kDa to 30.4 kDa, isoelectric point ranging from 5.85 to 9.31, and instability coefficient ranging from 38.48 to 74.47. All members were subcellularly localized in chloroplast, and were grouped into three different evolutionary branches. Cis-element analysis revealed that SiD27-1 (Seita.8G168400) was involved in regulating circadian rhythm, auxin-mediated development, and response to drought and low temperature. Transcription of SiD27-1 was down-regulated in foxtail millet accessions with more tillers, and in low phosphorus treatment could respond to faster than all other members. Haplotype variation analysis revealed that H001 of SiD27-1 may contribute more to plant height, heading date and grain yield than other haplotypes. We inferred that SiD27-1 was involved in strigolactone synthesis and plant architecture in foxtail millet. It laid the foundation for in-depth analysis of regulatory mechanism of D27s on the formation of foxtail millet tillering, and provided allelic variation sites for molecular breeding of foxtail millet.

Key words: β-carotene isomerase, gene families, transcription, haplotype variation, foxtail millet

张慧, 梁红凯, 智慧, 张林林, 刁现民, 贾冠清. 谷子β-胡萝卜素异构酶家族基因的表达与变异分析. 植物学报, 2023, 58(1): 34-50.

Hui Zhang, Hongkai Liang, Hui Zhi, Linlin Zhang, Xianmin Diao, Guanqing Jia. Analyses on the Transcription and Structure Variation of β-carotene Isomerase Gene Family in Foxtail Millet. Chinese Bulletin of Botany, 2023, 58(1): 34-50.

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链接本文: https://www.chinbullbotany.com/CN/10.11983/CBB22171

https://www.chinbullbotany.com/CN/Y2023/V58/I1/34

图/表 12

表1 引物列表

Table 1 List of primers

Primer name	Primer sequence (5'-3')
D27-8G-N-F	GCTGTACAAGACTAGTATGGAGGTC- GCGGCCACTTC
D27-8G-N-R	GGGGAAATTCGAGCTCTCAAATCAC- TTGACGATTCT
D27family-6G-N-F	GCTGTACAAGACTAGTATGGCAGCA- GCCCTGCCCAT
D27family-6G-N-R	GGGGAAATTCGAGCTCCTATGTCTG-AAGTTTGGGGC
D27family-3G-N-F	GCTGTACAAGACTAGTATGGCGACG- CCGCTCGCGAC
D27family-3G-N-R	GGGGAAATTCGAGCTCTCAAACTTG-GGGGCAACCGA
QRT-8G-F	ATGAAACGAAGCTACTACACGA
QRT-8G-R	CAGATTGTCGAACCAGTTGTC
QRT-6G-F	GATGGGGGAGAAGACGGAGTA
QRT-6G-R	TTCTTCTTCTTCTCCAACTCCG
QRT-3G-F	CGCCTCTATTGCTTGTCCTATA
QRT-3G-R	AACTGAACATGTGCCCATTAAC
Culin-F	TATGGGTCATCAACAGCTTGTC
Culin-R	GTAGTCCCTCGTGATGAGATCC

表2 不同物种D27s基因基本特征

Table 2 Characteristics of D27s genes from different plant species

Gene ID	Species	Primary structure				GRAVY	Subcellular location	Secondary structure
Gene ID	Species	Length of amino acids	Molecular weight (kDa)	Theoretical PI	Instability index (II)	GRAVY	Subcellular location	Alpha helix	Beta bridge	Exten- ded strand	Ran- dom coil
AT4G01995	Arabidopsis thaliana	258.00	28636.56	7.97	38.48	0.030	Chloroplast	0.34	0.03	0.15	0.49
AT1G03055	A. thaliana	264.00	29795.14	8.94	53.39	-0.358	Chloroplast	0.35	0.03	0.16	0.46
AT1G64680	A. thaliana	250.00	28162.63	8.52	51.89	-0.333	Chloroplast	0.33	0.03	0.12	0.52
BdiBd21-2.2G0489400	Brachypodium distachyon	268.00	29298.93	8.28	56.92	-0.093	Chloroplast	0.34	0.05	0.11	0.51
BdiBd21-4.4G0220000	B. distachyon	277.00	30715.66	8.76	52.53	-0.091	Chloroplast	0.34	0.02	0.11	0.54
BdiBd21-3.3G0180800	B. distachyon	275.00	30152.06	9.16	58.90	-0.147	Chloroplast	0.33	0.03	0.11	0.53
Seita.6G088800	Setaria italica	271.00	30429.45	8.93	54.85	-0.380	Chloroplast	0.37	0.03	0.09	0.52
Seita.3G050900	S. italica	277.00	30185.83	8.66	58.84	-0.170	Chloroplast	0.32	0.05	0.12	0.51
Seita.8G168400	S. italica	277.00	30185.83	8.66	58.84	-0.170	Chloroplast	0.36	0.03	0.13	0.48
LOC_Os08g02210	Oryza sativa	261.00	28906.58	8.88	49.96	-0.244	Chloroplast	0.35	0.05	0.10	0.50
LOC_Os05g04090	O. sativa	118.00	13355.34	5.85	56.27	-0.186	Cytoplasm	0.23	0.04	0.17	0.56
LOC_Os05g04070	O. sativa	270.00	29343.02	7.94	58.60	-0.047	Chloroplast	0.31	0.04	0.13	0.51
LOC_Os11g37650	O. sativa	365.00	40864.68	8.52	55.08	0.024	Chloroplast	0.34	0.00	0.16	0.45
Sobic.009G030800	Sorghum bicolor	277.00	30225.93	8.51	64.68	-0.182	Chloroplast	0.31	0.05	0.09	0.55
Sobic.005G168200	So. bicolor	292.00	32325.36	8.72	54.69	-0.216	Chloroplast	0.37	0.03	0.13	0.47
Sobic.007G016600	So. bicolor	369.00	30202.19	8.79	62.57	-0.383	Chloroplast	0.33	0.03	0.10	0.54
Sevir.6G087800	Setaria viridis	271.00	30483.49	8.83	55.49	-0.403	Chloroplast	0.38	0.03	0.09	0.49
Sevir.8G177900	Se. viridis	289.00	32243.38	8.82	54.93	-0.187	Chloroplast	0.36	0.03	0.13	0.48
Sevir.3G051400	Se. viridis	277.00	30185.83	8.66	58.84	-0.170	Chloroplast	0.32	0.05	0.12	0.51
Zm00008a034103	Zea mays	202.00	22824.65	9.31	65.45	-0.249	Chloroplast	0.34	0.04	0.18	0.44
Zm00008a023158	Z. mays	155.00	17878.49	8.22	56.01	-0.370	Chloroplast	0.46	0.07	0.14	0.33
Zm00008a023504	Z. mays	235.00	26224.37	8.93	67.47	-0.340	Chloroplast	0.36	0.03	0.12	0.49
HORVU1Hr1G015940	Hordeum vulgare	307.00	33309.59	9.29	65.88	-0.191	Chloroplast	0.34	0.04	0.10	0.52
HORVU7Hr1G076030	H. vulgare	294.00	33156.27	8.63	65.27	-0.413	Chloroplast	0.34	0.05	0.12	0.49
HORVU7Hr1G096970	H. vulgare	275.00	30372.12	8.89	74.47	-0.130	Chloroplast	0.38	0.03	0.13	0.45

表2 不同物种D27s基因基本特征

Table 2 Characteristics of D27s genes from different plant species

Gene ID	Species	Primary structure				GRAVY	Subcellular location	Secondary structure
Gene ID	Species	Length of amino acids	Molecular weight (kDa)	Theoretical PI	Instability index (II)	GRAVY	Subcellular location	Alpha helix	Beta bridge	Exten- ded strand	Ran- dom coil
AT4G01995	Arabidopsis thaliana	258.00	28636.56	7.97	38.48	0.030	Chloroplast	0.34	0.03	0.15	0.49
AT1G03055	A. thaliana	264.00	29795.14	8.94	53.39	-0.358	Chloroplast	0.35	0.03	0.16	0.46
AT1G64680	A. thaliana	250.00	28162.63	8.52	51.89	-0.333	Chloroplast	0.33	0.03	0.12	0.52
BdiBd21-2.2G0489400	Brachypodium distachyon	268.00	29298.93	8.28	56.92	-0.093	Chloroplast	0.34	0.05	0.11	0.51
BdiBd21-4.4G0220000	B. distachyon	277.00	30715.66	8.76	52.53	-0.091	Chloroplast	0.34	0.02	0.11	0.54
BdiBd21-3.3G0180800	B. distachyon	275.00	30152.06	9.16	58.90	-0.147	Chloroplast	0.33	0.03	0.11	0.53
Seita.6G088800	Setaria italica	271.00	30429.45	8.93	54.85	-0.380	Chloroplast	0.37	0.03	0.09	0.52
Seita.3G050900	S. italica	277.00	30185.83	8.66	58.84	-0.170	Chloroplast	0.32	0.05	0.12	0.51
Seita.8G168400	S. italica	277.00	30185.83	8.66	58.84	-0.170	Chloroplast	0.36	0.03	0.13	0.48
LOC_Os08g02210	Oryza sativa	261.00	28906.58	8.88	49.96	-0.244	Chloroplast	0.35	0.05	0.10	0.50
LOC_Os05g04090	O. sativa	118.00	13355.34	5.85	56.27	-0.186	Cytoplasm	0.23	0.04	0.17	0.56
LOC_Os05g04070	O. sativa	270.00	29343.02	7.94	58.60	-0.047	Chloroplast	0.31	0.04	0.13	0.51
LOC_Os11g37650	O. sativa	365.00	40864.68	8.52	55.08	0.024	Chloroplast	0.34	0.00	0.16	0.45
Sobic.009G030800	Sorghum bicolor	277.00	30225.93	8.51	64.68	-0.182	Chloroplast	0.31	0.05	0.09	0.55
Sobic.005G168200	So. bicolor	292.00	32325.36	8.72	54.69	-0.216	Chloroplast	0.37	0.03	0.13	0.47
Sobic.007G016600	So. bicolor	369.00	30202.19	8.79	62.57	-0.383	Chloroplast	0.33	0.03	0.10	0.54
Sevir.6G087800	Setaria viridis	271.00	30483.49	8.83	55.49	-0.403	Chloroplast	0.38	0.03	0.09	0.49
Sevir.8G177900	Se. viridis	289.00	32243.38	8.82	54.93	-0.187	Chloroplast	0.36	0.03	0.13	0.48
Sevir.3G051400	Se. viridis	277.00	30185.83	8.66	58.84	-0.170	Chloroplast	0.32	0.05	0.12	0.51
Zm00008a034103	Zea mays	202.00	22824.65	9.31	65.45	-0.249	Chloroplast	0.34	0.04	0.18	0.44
Zm00008a023158	Z. mays	155.00	17878.49	8.22	56.01	-0.370	Chloroplast	0.46	0.07	0.14	0.33
Zm00008a023504	Z. mays	235.00	26224.37	8.93	67.47	-0.340	Chloroplast	0.36	0.03	0.12	0.49
HORVU1Hr1G015940	Hordeum vulgare	307.00	33309.59	9.29	65.88	-0.191	Chloroplast	0.34	0.04	0.10	0.52
HORVU7Hr1G076030	H. vulgare	294.00	33156.27	8.63	65.27	-0.413	Chloroplast	0.34	0.05	0.12	0.49
HORVU7Hr1G096970	H. vulgare	275.00	30372.12	8.89	74.47	-0.130	Chloroplast	0.38	0.03	0.13	0.45

图1 不同作物D27s基因的系统进化树使用邻接法, 利用8个物种中鉴定的D27s蛋白质的氨基酸序列构建系统进化树。

Figure 1 Phylogenetic trees of D27s genes in different crops The phylogenetic tree was constructed by using amino acid sequences of D27 proteins from 8 crop species, and the neighbor-joining method.

图2 不同物种D27s的三级结构根据系统进化树对拟南芥、二穗短柄草、大麦、水稻、谷子、青狗尾草、高粱和玉米不同分支成员三级结构进行可视化, 其中Class1、Class2和Class3分别对应系统进化树中的第一、二和三分支。

Figure 2 Tertiary structure of D27s in different species The tertiary structure of D27s in Arabidopsis thaliana, Brachypodium distachyon, Hordeum vulgare, Oryza sativa, Setaria italica, Se. viridis, Sorghum bicolor and Zea mays are visualized according to the phylogenetic tree. Class1, Class2 and Class3 correspond to the first, second and third clades of the phylogenetic tree, respectively.

图3 D27s基因的结构及其编码蛋白质的保守基序分析 (A) D27s基因的结构及其编码蛋白的保守结构域分析(基于进化树分类(左侧), 对25个D27s基因的结构(中间)及其编码蛋白的保守结构域(右侧)进行了分析; 中间部分横线代表内含子, 右侧部分的不同颜色代表不同保守结构域; 下方比例尺代表基因或蛋白长度); (B) 25个D27s成员序列比对生成的保守基序logo。UTR: 非翻译区; CDS: 编码序列

Figure 3 A gene structures of D27s genes and conserved motifs in the D27s (A) Analysis of D27s gene structure and D27 protein conserved domains (based on evolutionary tree (left), 25 D27s genes were analyzed for gene structure (middle) and protein conserved domains (right); horizontal lines in the middle represent introns, different colors in the right part represent different conserved domains; the lower scale represents gene or protein length); (B) The conservative motif logo generated by comparison of amino acid sequences of 25 D27s members. UTR: Untranslated region; CDS: Coding sequence

图4 8个不同物种D27氨基酸序列的多重比对 8个物种的25个D27s成员蛋白序列均存在motif1、motif2、motif4和motif5, 其中motif1用黑色标注; motif2用绿色标注; motif4用蓝色标注; motif5用红色标注。

Figure 4 Alignment of amino acid sequences of D27s from 8 different species Motif1, motif2, motif4 and motif5 are found in 25 D27s sequences of 8 species, and motif1 is marked in black; motif2 is marked in green; motif4 is marked in blue; motif5 is marked in red.

图5 D27s顺式作用元件预测谷子D27基因上游2 000 bp启动子区顺式作用元件示意图。不同颜色的矩形框代表不同的顺式作用元件。

Figure 5 Prediction of D27s cis-element Diagram of cis-acting elements in the 2 000 bp upstream promoter regions of foxtail millet D27 genes. Rectangular boxes with different colors represent different cis-elements.

图6 D27s基因在不同分蘖材料中的全生育期表达谱 (A) D27s基因在豫谷1号不同组织中的表达模式; (B) SiD27-1在少分蘖材料豫谷1号全生育期不同组织中的表达; (C) SvD27-1在多分蘖材料A10全生育期不同组织中的表达。R代表根, S代表茎, Yl代表幼叶, Ol代表老叶, Sh代表叶鞘, P代表穗。

Figure 6 Expression of D27s genes throughout the reproductive period in different tiller materials (A) Expression patterns of D27s genes in different tissues of Yugu1; (B) Expression of SiD27-1 in different tissues of less tiller material Yugu1 reproductive period; (C) Expression of SvD27-1 in different tissues of multi-tiller material A10 reproductive period. R stand for root, S stand for stem, Yl stand for young leaf, Ol stand for old leaf, Sh stand for leaf sheath, and P stand for spike.

图7 D27s在缺磷条件下不同组织中的响应模式 (A) Seita.8G168400 (SiD27-1); (B) Seita.6G088800 (SiD27-2); (C) Seita.3G050900 (SiD27-3)。* P<0.05; ** P<0.01

Figure 7 Responsive pattern of D27s in different tissues under phosphorus (P) deficiency treatment (A) Seita.8G168400 (SiD27-1); (B) Seita.6G088800 (SiD27-2); (C) Seita.3G050900 (SiD27-3). * P<0.05; ** P<0.01

图8 D27s蛋白的亚细胞定位 GFP代表绿色荧光蛋白。Bars=5 μm

Figure 8 Subcellular localization of D27 proteins GFP represents green fluorescence protein. Bars=5 μm

图9 SiD27-1序列多态性分析 (A) SiD27-1的基因结构和单倍型分析; (B) 单倍型变异分析(圆的大小表示每个Hap中的品种数量; 导线表示2个Haps之间的变化程度)

Figure 9 Sequence polymorphism analysis of SiD27-1 (A) The gene structure of SiD27-1 and its haplotypes; (B) Haplotype variation analysis (circle size indicate the number of varieties in each Hap; traverse lines represent the extent of variation between two Haps)

图10 SiD27-1与不同年份表型数据关联的箱式图红框代表SiD27-1基因型与分蘖表型的关联分析

Figure 10 Box plot of SiD27-1 associated with phenotypic data in different years The red box represent the association analysis between SiD27-1 genotype and tiller phenotype

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