全缘叶绿绒蒿黄色花形成关键基因的挖掘

doi:10.3969/j.issn.1004-1524.20230535

浙江农业学报 ›› 2024, Vol. 36 ›› Issue (4): 811-824.DOI: 10.3969/j.issn.1004-1524.20230535

全缘叶绿绒蒿黄色花形成关键基因的挖掘

陈晓涓¹(), 罗军¹, 王富敏¹, 李拓键¹, 屈燕¹^,²^,³^,^*()

1.西南林业大学园林园艺学院,云南昆明 650224
2.国家林业和草原局西南风景园林工程技术研究中心,云南昆明 650224
3.云南省功能性花卉资源及产业化技术工程研究中心,云南昆明 650224

收稿日期:2023-04-26 出版日期:2024-04-25 发布日期:2024-04-29
作者简介:陈晓涓(1998—),女,云南大理人,硕士研究生,研究方向为园林植物资源开发与利用研究。E-mail: 359911018@qq.com
通讯作者: *屈燕,E-mail: quyan@swfu.edu.cn
基金资助:
国家自然科学基金(32160404);国家自然科学基金(31460218);云南省“万人计划”青年拔尖人才项目(YNWR-QNBJ-2019-211)

Excavation of key genes for yellow flower formation in Meconopsis integrifolia

CHEN Xiaojuan¹(), LUO Jun¹, WANG Fumin¹, LI Tuojian¹, QU Yan¹^,²^,³^,^*()

1. College of Landscape Architecture and Horticulture, Southwest Forestry University, Kunming 650224, China
2. Southwest Engineering and Technology Research Center of Landscape Architecture (National Forestry and Grassland Administration), Kunming 650224, China
3. Yunnan Engineering Research Center for Functional Flower Resources and Industrialization, Kunming 650224, China

Received:2023-04-26 Online:2024-04-25 Published:2024-04-29
Contact: QU Yan

摘要/Abstract

摘要：

为挖掘全缘叶绿绒蒿黄色花形成的关键基因,探讨其花色形成在转录水平上的调控机制,选取全缘叶绿绒蒿 3 个花发育时期的花瓣组织进行转录组测序,并对盛花期花瓣组织的黄酮类化合物进行了绝对定量。结果表明:(1)LC-MS/MS 共检测到 38 种黄酮类化合物,其中以槲皮素及其衍生物为主,其含量超过黄酮类化合物总含量的 80%;(2)转录组测序共获得 171 902 条单基因,筛选后得到 14 906 个差异表达基因,这些差异基因在 48 条 KEGG 通路中显著富集(P<0.05),其中苯丙烷生物合成通路与类黄酮生物合成通路在 3 个花发育时期都显著富集(P<0.05);(3)同时还发现与黄酮类化合物合成相关的基因在 3 个花发育时期中差异表达,同一时期 MiFLSs(Cluster-28469.86、Cluster-28469.89、Cluster-28469.91)的表达量是 MiDFR(Cluster-49617.1)的 1.2~4.7 倍;与槲皮素衍生物合成相关的 MiFG3(Cluster-15071.0)呈现逐渐上调的表达趋势;转录因子 MiMYB4 表达量也逐渐上升,且与 MiMYB38、MiMYB39、MiDFR(Cluster-49617.1)和 MiANS(Cluster-29740.1)呈强负相关关系;(4)所选基因 qRT-PCR 结果与 RNA-seq 相关性较好(R²=0.820 4,P<0.05),表明转录组数据可靠。综上所述,全缘叶绿绒蒿黄色花瓣的主要成分可能是槲皮素及其衍生物;MiFLSs 相较于 MiDFR 更强的竞争力促使更多底物流向黄酮醇合成,为大量合成黄酮醇类化合物提供了前体物,MiFG3 消耗前体物促进槲皮素衍生物的大量合成;同时,转录因子 MiMYB4 可能通过抑制与花青素合成相关的结构基因和转录因子,间接促进底物流向黄酮醇合成,这些结构基因与转录因子共同调控全缘叶绿绒蒿的花色形成过程。研究筛选出了6个调控全缘叶绿绒蒿花色形成的关键基因,初步探讨了其黄色花形成的分子机制,为进一步研究全缘叶绿绒蒿花色变异提供了理论参考。

关键词: 全缘叶绿绒蒿, 花色, 黄酮醇, 关键基因

Abstract:

To find out the key genes of yellow flower formation in Meconopsis integrifolia and to study the regulatory mechanism of flower color formation at the transcriptional level, in this study, the petal tissues of M. integrifolia were selected for RNA sequencing at three flower developmental stages, and the absolute quantification of flavonoids in petal tissue were measured at blooming period. The results showed that: (1) A total of 38 flavonoids were detected in LC-MS/MS, among which quercetin and its derivatives were the main ones, and their content exceeded 80% of the total content of flavonoids. (2) A total of 171 902 Unigenes were obtained from RNA sequencing, and 14 906 DEGs were obtained after screening, which were significantly enriched in 48 KEGG pathways (P<0.05), among which the phenylpropanoid biosynthesis and flavonoid biosynthesis were significantly enriched in the three flower development stages (P<0.05). (3) At the same time, it was also found that genes related to flavonoid synthesis were expressed differently in the three flower development periods, and the expression of MiFLSs (Cluster-28469.86, Cluster-28469.89, Cluster-28469.91) was 1.2-4.7 times higher than that of MiDFR(Cluster-49617.1) in the same period. The expression of MiFG3 (Cluster-15071.0) related to the synthesis of quercetin derivatives showed a gradual up-regulation trend. The expression of transcription factor MiMYB4 also increased gradually, and it showed a strong negative correlation with MiMYB38, MiMYB39, MiDFR(Cluster-49617.1) and MiANS(Cluster-29740.1). (4) The qRT-PCR results of the selected genes correlated well with RNA-seq (R²=0.820 4, P<0.05), indicating that the transcriptome data was reliable. In summary, the main component of the yellow petals of M. integrifolia may be quercetin and its derivatives. The stronger competitiveness of MiFLSs compare with MiDFR drives more substrates toward flavonol synthesis, providing precursors for the bulk synthesis of flavonols, and MiFG3 consumption of precursors promotes the bulk synthesis of quercetin derivatives. Meanwhile, the transcription factor MiMYB4 may indirectly promote substrate flow toward flavonol synthesis by repressing structural genes and transcription factors associated with anthocyanin synthesis, which together with transcription factors regulate the process of flower color formation in M. integrifolia. In this study, 6 key genes regulating the flower color formation of M. integrifolia are screened, and the molecular mechanism of its yellow flower formation is preliminarily explored, which provides a theoretical reference for further research on the flower color variation of Meconopsis.

Key words: Meconopsis integrifolia, flower color, flavonol, key gene

中图分类号:

S681.9

陈晓涓, 罗军, 王富敏, 李拓键, 屈燕. 全缘叶绿绒蒿黄色花形成关键基因的挖掘[J]. 浙江农业学报, 2024, 36(4): 811-824.

CHEN Xiaojuan, LUO Jun, WANG Fumin, LI Tuojian, QU Yan. Excavation of key genes for yellow flower formation in Meconopsis integrifolia[J]. Acta Agriculturae Zhejiangensis, 2024, 36(4): 811-824.

图/表 14

图1 全缘叶绿绒蒿3个发育时期的花朵 A,自然采摘状态下的花朵;B,去除萼片后的花朵。

Fig.1 Flowers in 3 developmental stages of M. integrifolia A, Flowers in a naturally picked state; B, Flowers after sepal removal.

表1 全缘叶绿绒蒿花瓣采集信息表

Table 1 M. integrifolia petal collection information table

实验材料 Experimental materials	开花时期 Flowering period	编号 Number	皇家比色卡色号 Royal color card number	采集地 Collection location	经纬度 Latitude and Longitude
全缘叶绿绒蒿	花蕾期Budding period	P1	YELLOW-GREEN 145D	云南省丽江市玉龙雪山	27°0'10″N,
M. integrifolia	初开期Initial opening period	P2	YELLOW-GREEN 150D	Jade Dragon Snow Mountain,	100°10'56″E
	盛花期Blooming period	P3	YELLOW-GREEN 150B	Lijiang City, Yunnan Province

图2 全缘叶绿绒蒿P3期花瓣中6种黄酮类化合物的含量不同字母表示在0.05水平上差异显著。

Fig.2 Content of 6 flavonoids in the petals of M. integrifolia P3 stage Different letters mean significant difference at 0.05 level.

表2 全缘叶绿绒蒿转录组数据质量信息

Table 2 Transcriptome data quality information for M. integrifolia

样本 Sample	原始序列 Raw reads	过滤后序列 Clean reads	过滤后的碱基 Clean bases/GB	错误率 Error rate/%	Q20/%	Q30/%	GC/%
QYY-P1-1	46 105 634	45 312 642	6.80	0.03	97.27	92.42	41.41
QYY-P1-2	46 446 078	45 552 808	6.83	0.03	97.53	93.02	41.65
QYY-P1-3	46 078 118	45 182 696	6.78	0.03	97.26	92.44	41.62
QYY-P2-1	44 529 162	43 227 950	6.48	0.03	97.30	92.56	41.13
QYY-P2-2	47 350 222	46 244 742	6.94	0.03	97.30	92.42	41.16
QYY-P2-3	48 324 836	47 314 210	7.10	0.03	97.72	93.41	40.90
QYY-P3-1	48 823 172	47 635 926	7.15	0.03	97.34	92.59	41.23
QYY-P3-2	46 197 126	44 753 484	6.71	0.03	97.21	92.39	41.18
QYY-P3-3	48 061 136	46 960 540	7.04	0.03	97.51	92.97	41.03

表3 七大数据库对转录本的注释情况

Table 3 Annotations to transcripts in the seven major databases

数据库 Database	注释到的基因数量 Number of genes	占比 Percentage/%
KEGG	76 662	44.60
Nr	97 732	56.85
SwissProt	70 402	40.95
TrEMBL	103 886	60.43
KOG	61 267	35.64
GO	87 982	51.18
Pfam	51 596	30.01
Annotated in at least	106 907	62.19
one Database
Total Unigenes	171 902	100

图3 全缘叶绿绒蒿不同发育时期花瓣差异表达基因分析

Fig.3 Analysis of DEGs in petals of M. integrifolia at different developmental stages

图4 全缘叶绿绒蒿不同发育时期花瓣所有差异表达基因热图

Fig.4 Heat map of all DEGs in the petals of M. integrifolia at different developmental stages

图5 全缘叶绿绒蒿DEGs显著富集(P<0.05)的KEGG分类

Fig.5 KEGG classification of DEGs of significant enrichment (P<0.05) of M. integrifolia

图6 类黄酮及黄酮醇生物合成通路中关键差异表达基因及相关代谢物红色虚线框为黄酮醇合成部分通路图。CHS,查尔酮合成酶;CHI,查尔酮异构酶;F3H,柚皮素 3-双加氧酶;FLS,黄酮醇合酶;F3'H,类黄酮3'-羟化酶;DFR,二氢黄酮醇 4-还原酶;ANS,花青素合酶;FG3,半乳糖苷葡萄糖基转移酶。

Fig.6 Key DEGs and associated metabolites in flavonoid and flavonol biosynthetic pathway The red dotted box shows the partial pathway of flavonol biosynthesis. CHS, Chalcone synthase; CHI, Chalcone isomerase; F3H, Naringenin 3-dioxygenase; FLS, Flavonol synthase; F3'H, Flavonoid 3'-hydroxylase; DFR, Flavanone 4-reductase; ANS, Anthocyanidin synthase; FG3, Galactoside glucosyltransferase.

表4 全缘叶绿绒蒿R2R3 MYB基因信息

Table 4 Information of R2R3 MYB genes in M. integrifolia

基因 Gene name	基因ID Gene ID	蛋白长度 Protein length/aa	等电点 Isoelectric point	分子量 Molecular weight/u	所属拟南芥亚族 The subgroup of Arabidopsis to which the gene belongs
MiMYB1	Cluster-13873.16	1 185	9.35	131 836.98	—
MiMYB2	Cluster-73976.7	570	6.33	63 623.76	—
MiMYB3	Cluster-74122.1	501	5.89	55 023.13	—
MiMYB4	Cluster-46647.219	271	8.59	30 734.68	S4
MiMYB5	Cluster-176.1	257	9.20	29 366.95	—
MiMYB6	Cluster-24930.0	352	7.76	39 557.77	S9
MiMYB7	Cluster-26024.6	371	9.37	42 556.11	—
MiMYB8	Cluster-26024.7	354	9.32	40 353.59	—
MiMYB9	Cluster-26960.10	357	6.01	39 008.3	—
MiMYB10	Cluster-28521.4	297	5.58	33 656.54	S11
MiMYB11	Cluster-29061.0	355	5.70	40 225.53	S11
MiMYB12	Cluster-41024.1	255	9.00	28 447.39	—
MiMYB13	Cluster-42663.2	429	9.35	47 588.58	—
MiMYB14	Cluster-43725.2	130	6.17	14 861.21	S19
MiMYB15	Cluster-43725.4	209	6.59	23 973.62	S19
MiMYB16	Cluster-74557.6	791	5.47	86 693.98	—
MiMYB17	Cluster-48749.21	294	8.85	32 860.93	—
MiMYB18	Cluster-54127.0	165	4.38	18 843.61	—
MiMYB19	Cluster-54127.1	250	4.90	28 578.83	—
MiMYB20	Cluster-54127.5	165	4.38	18 843.61	—
MiMYB21	Cluster-56396.9	514	6.76	52 138.66	S13
MiMYB22	Cluster-56419.0	414	4.87	45 932.63	—
MiMYB23	Cluster-58089.0	220	9.97	24 934.41	—
MiMYB24	Cluster-59054.5	629	6.47	71 492.12	—
MiMYB25	Cluster-59054.7	583	5.65	66 005.51	—
MiMYB26	Cluster-60970.0	420	8.72	41 583.2	S22
MiMYB27	Cluster-61134.0	209	8.36	23 333.70	—
MiMYB28	Cluster-73421.2	310	5.28	34 749.97	—
MiMYB29	Cluster-61134.9	137	5.61	14 979.42	—
MiMYB30	Cluster-61178.1	266	5.13	30 023.11	S16
MiMYB31	Cluster-64347.0	244	8.38	27 986.6	S18
MiMYB32	Cluster-6447.11	115	5.88	13 429.9	S20
MiMYB33	Cluster-6447.2	349	5.00	40 058.43	S20
MiMYB34	Cluster-6447.5	115	5.88	13 429.90	S20
MiMYB35	Cluster-66523.6	508	9.27	56 339.69	—
MiMYB36	Cluster-67045.0	479	9.15	53 421.65	—
MiMYB37	Cluster-67577.0	265	7.22	30 531.08	—
MiMYB38	Cluster-67577.1	372	9.30	42 471.57	S6
MiMYB39	Cluster-67577.2	243	9.72	28 100.98	S6
MiMYB40	Cluster-69149.2	144	4.67	16 543.61	—
MiMYB41	Cluster-69645.1	278	9.30	31 487.15	—
MiMYB42	Cluster-69645.5	277	9.37	31 357.03	—
MiMYB43	Cluster-70083.7	208	9.27	22 811.18	—
MiMYB44	Cluster-69949.7	302	7.20	32 368.05	—
MiMYB45	Cluster-70083.0	208	9.42	22 879.34	—

表4 全缘叶绿绒蒿R2R3 MYB基因信息

Table 4 Information of R2R3 MYB genes in M. integrifolia

基因 Gene name	基因ID Gene ID	蛋白长度 Protein length/aa	等电点 Isoelectric point	分子量 Molecular weight/u	所属拟南芥亚族 The subgroup of Arabidopsis to which the gene belongs
MiMYB1	Cluster-13873.16	1 185	9.35	131 836.98	—
MiMYB2	Cluster-73976.7	570	6.33	63 623.76	—
MiMYB3	Cluster-74122.1	501	5.89	55 023.13	—
MiMYB4	Cluster-46647.219	271	8.59	30 734.68	S4
MiMYB5	Cluster-176.1	257	9.20	29 366.95	—
MiMYB6	Cluster-24930.0	352	7.76	39 557.77	S9
MiMYB7	Cluster-26024.6	371	9.37	42 556.11	—
MiMYB8	Cluster-26024.7	354	9.32	40 353.59	—
MiMYB9	Cluster-26960.10	357	6.01	39 008.3	—
MiMYB10	Cluster-28521.4	297	5.58	33 656.54	S11
MiMYB11	Cluster-29061.0	355	5.70	40 225.53	S11
MiMYB12	Cluster-41024.1	255	9.00	28 447.39	—
MiMYB13	Cluster-42663.2	429	9.35	47 588.58	—
MiMYB14	Cluster-43725.2	130	6.17	14 861.21	S19
MiMYB15	Cluster-43725.4	209	6.59	23 973.62	S19
MiMYB16	Cluster-74557.6	791	5.47	86 693.98	—
MiMYB17	Cluster-48749.21	294	8.85	32 860.93	—
MiMYB18	Cluster-54127.0	165	4.38	18 843.61	—
MiMYB19	Cluster-54127.1	250	4.90	28 578.83	—
MiMYB20	Cluster-54127.5	165	4.38	18 843.61	—
MiMYB21	Cluster-56396.9	514	6.76	52 138.66	S13
MiMYB22	Cluster-56419.0	414	4.87	45 932.63	—
MiMYB23	Cluster-58089.0	220	9.97	24 934.41	—
MiMYB24	Cluster-59054.5	629	6.47	71 492.12	—
MiMYB25	Cluster-59054.7	583	5.65	66 005.51	—
MiMYB26	Cluster-60970.0	420	8.72	41 583.2	S22
MiMYB27	Cluster-61134.0	209	8.36	23 333.70	—
MiMYB28	Cluster-73421.2	310	5.28	34 749.97	—
MiMYB29	Cluster-61134.9	137	5.61	14 979.42	—
MiMYB30	Cluster-61178.1	266	5.13	30 023.11	S16
MiMYB31	Cluster-64347.0	244	8.38	27 986.6	S18
MiMYB32	Cluster-6447.11	115	5.88	13 429.9	S20
MiMYB33	Cluster-6447.2	349	5.00	40 058.43	S20
MiMYB34	Cluster-6447.5	115	5.88	13 429.90	S20
MiMYB35	Cluster-66523.6	508	9.27	56 339.69	—
MiMYB36	Cluster-67045.0	479	9.15	53 421.65	—
MiMYB37	Cluster-67577.0	265	7.22	30 531.08	—
MiMYB38	Cluster-67577.1	372	9.30	42 471.57	S6
MiMYB39	Cluster-67577.2	243	9.72	28 100.98	S6
MiMYB40	Cluster-69149.2	144	4.67	16 543.61	—
MiMYB41	Cluster-69645.1	278	9.30	31 487.15	—
MiMYB42	Cluster-69645.5	277	9.37	31 357.03	—
MiMYB43	Cluster-70083.7	208	9.27	22 811.18	—
MiMYB44	Cluster-69949.7	302	7.20	32 368.05	—
MiMYB45	Cluster-70083.0	208	9.42	22 879.34	—

图7 全缘叶绿绒蒿R2R3-MYB功能预测及其表达量热图 A,全缘叶绿绒蒿和拟南芥 R2R3-MYB 基因家族系统进化分析;B,全缘叶绿绒蒿 R2R3-MYB 表达量热图。

Fig.7 Functional prediction of M. Integrifolia R2R3-MYB and its expression heat map A, Phylogenetic analysis of the R2R3-MYB gene families in M. integrifolia and A. thaliana; B, Heat map of R2R3-MYB expression of M. integrifolia.

图8 候选R2R3-MYB转录因子多序列比较 A,MiMYB4 与其他 MYB 蛋白氨基酸序列同源比较;B,MiMBY38、MiMYB39与其他 MYB 蛋白氨基酸序列同源比较。

Fig.8 Comparison of candidate R2R3-MYB transcription factors in multiple sequences A. Comparison of amino acid sequence homology of MiMYB4 with other MYB proteins; B. Comparison of amino acid sequence homology of MiMBY38, MiMYB39 with other MYB proteins.

图9 全缘叶绿绒蒿中花色相关结构基因与转录因子表达分析 A,全缘叶绿绒蒿中花色相关结构基因与转录因子相关性分析;B,全缘叶绿绒蒿中花色相关结构基因与转录因子之间的相互作用网络。红色是转录因子,蓝色是结构基因,实线代表正相关,虚线代表负相关,圈越大、节点越多则相关性越强。

Fig.9 Correlation analysis of flower color-related structural genes and transcription factors in M. integrifolia. A, Correlation analysis of flower color-related structural genes and transcription factors in M. integrifolia; B, Interaction network between flower color-related structural genes and transcription factors in M. integrifolia. Red is transcription factors, blue is structural genes, solid lines represent positive correlations, dashed lines represent negative correlations, and the larger the circle and the more nodes, the stronger the correlation.

图10 五个差异表达基因qRT-PCR和RNA-seq相关性分析

Fig.10 qRT-PCR and RNA-seq correlation analysis of 5 DEGs

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全缘叶绿绒蒿黄色花形成关键基因的挖掘

Excavation of key genes for yellow flower formation in Meconopsis integrifolia

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