基于转录组测序的苦瓜皂苷合成相关基因的鉴定和分析

doi:10.3864/j.issn.0578-1752.2024.09.012

中国农业科学 ›› 2024, Vol. 57 ›› Issue (9): 1779-1793.doi: 10.3864/j.issn.0578-1752.2024.09.012

基于转录组测序的苦瓜皂苷合成相关基因的鉴定和分析

戚仁洁¹^,²(), 宁宇³(), 刘静³, 刘之洋³, 徐海³, 罗志丹¹^,²(), 陈龙正³()

¹ 江苏海洋大学药学院/江苏省海洋生物资源与环境重点实验室/江苏省海洋药物化合物筛选重点实验室，江苏连云港 222005
² 江苏海洋大学/江苏海洋生物产业技术协同创新中心，江苏连云港 222005
³ 江苏省农业科学院蔬菜研究所/江苏省高效园艺作物遗传改良重点实验室，南京 210014

收稿日期:2023-09-29 接受日期:2023-12-18 出版日期:2024-05-01 发布日期:2024-05-09
通信作者:
罗志丹，E-mail：lzd@jou.edu.cn。
陈龙正，E-mail：longzhengchen@qq.com。
联系方式: 戚仁洁，E-mail：13956705571@163.com。宁宇，E-mail：20190022@jaas.ac.cn。戚仁洁和宁宇为同等贡献作者。
基金资助:
国家自然科学基金(32102392); 江苏省重点研发计划(Be2022339); 江苏省自然科学基金(BK20200279); 江苏省自然科学基金(3027)

Identification and Analysis of Genes Related to Bitter Gourd Saponin Synthesis Based on Transcriptome Sequencing

QI RenJie¹^,²(), NING Yu³(), LIU Jing³, LIU ZhiYang³, XU Hai³, LUO ZhiDan¹^,²(), CHEN LongZheng³()

¹ College of Pharmacy/Jiangsu Key Laboratory of Marine Biological Resources and Environment/Jiangsu Key Laboratory of Marine Pharmaceutical Compound Screening, Jiangsu Ocean University, Lianyungang 222005, Jiangsu
² Co-Innovation Center of Jiangsu Marine Bio-industry Technology/Jiangsu Ocean University, Lianyungang 222005, Jiangsu
³ Institute of Vegetable Crops, Jiangsu Academy of Agricultural Sciences /Jiangsu Key Laboratory for Horticultural Crop Genetic Improvement, Nanjing 210014

Received:2023-09-29 Accepted:2023-12-18 Published:2024-05-01 Online:2024-05-09

摘要/Abstract

摘要：

【目的】皂苷是苦瓜果实苦味的主要来源，具有降血糖、抗癌等多种药用价值。鉴定和挖掘参与调控苦瓜皂苷生物合成的代谢通路及基因，为进一步深入解析苦瓜皂苷形成的分子机制提供参考。【方法】以苦瓜高代自交系GK24为试验材料，分别在子房期（T1）、幼果期（T2）、商品果期（T3）和完全成熟期（T4）取果实组织，通过香草醛-冰醋酸法测定不同时期的苦瓜皂苷含量，利用转录组测序的方法鉴定差异表达基因。【结果】从T1到T4，苦瓜内源皂苷含量随着果实发育而呈现显著下降的趋势。转录组测序共鉴定到17 504个基因，在T1-vs-T2、T2-vs-T3和T3-vs-T4三组比较中，下调表达基因数量均高于上调表达基因数量。GO富集分析表明含磷复合物代谢过程、驱动蛋白复合体和2-琥珀酰-6-羟基-环己二烯-1-羧酸合成酶活性分别是生物过程、细胞组分及分子功能模块最显著富集的条目。KEGG分析显示全局与概述图谱、碳水化合物代谢和氨基酸代谢是3组比较中共同的最显著富集的代谢通路。根据表达模式可将基因划分为20个模块，其中profile 0中基因的表达量从T1到T4逐渐降低，与苦瓜果实发育过程中皂苷含量变化规律一致。从profile 0中鉴定出与苦瓜皂苷生物合成相关的基因14个，包括萜类骨架生物合成通路上的基因AAT1、HMG1、MVK、PMK、MVD2和FPS1，倍半萜与三萜生物合成途径中的基因SS12、SQE1和CPQ及后修饰酶基因CYP97A3、CYP71AN24、UGT94E5及UGT73C6。实时荧光定量PCR（qRT-PCR）结果与RNA-seq结果一致。【结论】苦瓜果实中皂苷含量随着果实不断成熟而逐渐降低。苦瓜皂苷生物合成首先通过上游的萜类骨架生物合成（ko00900）代谢途径完成萜类皂苷骨架的积累，随后通过倍半萜与三萜生物合成（ko00909）代谢途径以及下游的氧化还原酶、糖基转移酶的修饰最终生成皂苷，本研究通过转录组测序共鉴定到14个与苦瓜皂苷生物合成相关的基因。

关键词: 苦瓜, 转录组, 差异表达基因, 皂苷, 合成调控

Abstract:

【Objective】As the main source of bitterness in bitter gourd fruit, saponin possesses various medicinal values including hypoglycemic and anticancer properties. This paper aimed at identifying the metabolic pathways and genes involved in the regulation of bitter gourd saponin biosynthesis, so as to provide the theoretical basis for further analysis of the molecular mechanism of bitter gourd saponin formation.【Method】Using the bitter gourd high-generation inbred line GK24 as the test material, fruit tissues were sampled at the ovary stage (T1), young fruit stage (T2), commodity fruit stage (T3), and maturity fruit stage (T4). The saponin content of bitter gourd at different periods were determined by the vanillin-glacial acetic acid method, and the differentially expressed genes (DEGs) were identified using the method of transcriptome sequencing. 【Result】From T1 to T4, the endogenous saponin content of bitter gourd showed significant decrease with fruit development. A total of 17 504 genes were identified by transcriptome sequencing, and the number of down-regulated genes was higher than that of up-regulated genes in the comparison of the three groups of T1-vs-T2, T2-vs-T3, and T3-vs-T4. GO enrichment analysis showed that phosphorus-containing complex metabolic process, kinesin complex and 2-succinyl-6-hydroxy-cyclohexadiene-1-carboxylic acid synthetase activity were the most significantly enriched terms in biological process, cellular component and molecular function, respectively. KEGG analysis showed that global and overview mapping, carbohydrate metabolism, and amino acid metabolism were the most significantly enriched pathways in all three comparative groups. The genes could be categorized into 20 profiles based on their expression patterns. Genes in profile 0 gradually decreased from T1 to T4, showing similar pattern of saponin content changes with bitter gourd fruit development. 14 genes related to bitter gourd saponin biosynthesis were identified from profile 0, including AAT1, HMG1, MVK, PMK, MVD2, and FPS1 in the terpene skeleton biosynthesis pathway, SS12, SQE1, and CPQ in the sesquiterpene and triterpene biosynthesis pathway, and the postmodifying enzyme genes CYP97A3, CYP71AN24, UGT94E5 and UGT73C6. The results of RNA-seq were validated by qRT-PCR method.【Conclusion】The saponin content of bitter gourd decreased with the fruit development. Bitter gourd saponin was synthesized through the terpenoid bone biosynthesis (ko00900) metabolic pathway to accumulate terpenoid saponin skeleton in the first, and then produce saponins through the sesquiterpene and triterpene biosynthesis (ko00909) metabolic pathway and the modification of oxidoreductase and glycosyltransferase successively. A total of 14 genes related to the saponin biosynthesis of bitter gourd have been identified in the present study.

Key words: bitter gourd, transcriptome, differentially expressed genes, saponin, regulation of synthesis

戚仁洁, 宁宇, 刘静, 刘之洋, 徐海, 罗志丹, 陈龙正. 基于转录组测序的苦瓜皂苷合成相关基因的鉴定和分析[J]. 中国农业科学, 2024, 57(9): 1779-1793.

QI RenJie, NING Yu, LIU Jing, LIU ZhiYang, XU Hai, LUO ZhiDan, CHEN LongZheng. Identification and Analysis of Genes Related to Bitter Gourd Saponin Synthesis Based on Transcriptome Sequencing[J]. Scientia Agricultura Sinica, 2024, 57(9): 1779-1793.

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链接本文: https://www.chinaagrisci.com/CN/10.3864/j.issn.0578-1752.2024.09.012

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图/表 12

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表3

表4

Profile 0中ko00900和ko00909通路中的基因"

基因编号 Gene number	基因注释 Gene function	通路 Pathway	T1 FPKM	T2 FPKM	T3 FPKM	T4 FPKM
evm.TU.chr1.608	法尼基半胱氨酸裂解酶异构体 Farnesylcysteine lyase isoform	ko00900	38.15	28.42	17.24	10.65
evm.TU.chr10.805	2-甲基-D-赤藓糖醇2,4-环二磷酸合酶 2-C-methyl-D-erythritol 2,4-cyclodiphosphate synthase	ko00900	115.94	71.18	43.36	26.32
evm.TU.chr2.34	香叶基香叶基二磷酸还原酶样异构体 Geranylgeranyl diphosphate reductase-like isoform	ko00900	30.58	17.55	16.44	7.16
evm.TU.chr3.1930	羟基-3-甲基丁-2-烯-1-基二磷酸合酶 4-hydroxy-3-methylbut-2-en-1-yl diphosphate synthase	ko00900	433.17	194.37	106.87	85.58
evm.TU.chr3.2317	法尼基焦磷酸合酶1 Farnesyl pyrophosphate synthase 1	ko00900	358.50	164.00	51.39	7.70
evm.TU.chr4.352	乙酰辅酶A乙酰转移酶 Acetyl-CoA acetyltransferae	ko00900	439.08	95.24	57.25	34.89
evm.TU.chr4.613	4-羟基-3-甲基丁-2-烯基二磷酸还原酶 4-hydroxy-3-methylbut-2-enyl diphosphate reductase	ko00900	1091.57	439.96	370.39	217.45
evm.TU.chr6.140	1-脱氧-D-酮糖5-磷酸还原异构酶 1-deoxy-D-xylulose 5-phosphate reductoisomerase	ko00900	239.29	131.64	82.92	76.05
evm.TU.chr6.518	脱氧-D-酮糖-5-磷酸合成酶Deoxy-D-xylulose-5-phosphate synthase	ko00900	637.07	42.68	19.10	0.17
evm.TU.chr4.378	HMG-CoA合成酶 3-hydroxy-3-methyl glutaryl coenzyme A synthesis	ko00900	1274.61	1010.52	91.31	2.87
evm.TU.chr8.4201	甲羟戊酸激酶 Mevalonate kinase	ko00900	105.59	52.77	31.46	14.07
evm.TU.chr9.3672	焦磷酸甲羟戊酸脱羧酶Pyrophosphomethylvalerate decarboxylase	ko00900	671.59	131.25	53.80	28.02
evm.TU.chr10.2918	磷酸甲羟戊酸激酶 Phosphomevalonate kinase	ko00900	85.10	58.17	9.86	3.75
evm.TU.chr6.363	磷酸甲羟戊酸激酶 Phosphomevalonate kinase	ko00900	41.95	20.49	13.08	12.38
evm.TU.chr2.1021	角鲨烯合成酶 Squalene synthase	ko00909	437.66	285.81	89.01	48.19
evm.TU.chr3.2797	橙花内酯合成酶 Nerolidol synthase	ko00909	15.85	9.29	0.69	0.07
evm.TU.chr7.10	葫芦二烯醇合酶 Cucurbitadienol synthase	ko00909	981.27	444.87	79.12	4.09
evm.TU.chr8.588	角鲨烯环氧酶 Squalene epoxidase 1	ko00909	1030.32	506.37	76.82	1.14

表4

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图8

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基因名 Gene name	正向引物Forward primer (5′-3′)	反向引物Reverse primer (5′-3′)
CPQ	GTTGAAAGAGGGGGAAGAGG	CACCAGACCCGGAAGTAAAA
FSP1	GCGGATCTCAGGTCAACATT	TCCAGGCACATTGTAGTCCA
CYP97A3	GGGAGATATGGCGTGTAAGAAGAC	CTAAAGTCAGACGAGAGAACAGGG
CYP71AN24	GAACACAAGGCCAAGATGAGAG	CAGTTGTGTCAGTTCCAGCTAC
UGT73C6	TGCCTCCAGAGCTGAAACAT	TCCCATGAATCCAGCCACTT
UGT94E5	TCATCACACAACCAAAGGCC	ATCGGAATGTTGAGCGATGC
SQE1	AGCAAGGGACGGTTACTTCA	TGAGAAGCAGCCATCACAGA
MVK	GCAGTCGTTCATGGATCCAC	TGGCCACGAAAACTCCAATG
PMK	GGGACCATGAGAGGACTGAG	AGGGTCAGACTTTTGCCACT
Actin	GGCAAACCCTAAAGTTTTCTTCG	GATGAGCCCTTGTAATGAAGTGG

样品 Sample	原始数据 Raw reads	过滤后数据 Clean reads	Q30含量 Q30 content (%)	GC含量 GC content (%)	单一比对率 Unique mapped (%)	总比对率 Total mapped (%)
T1-1	46878594	46673674	92.28	46.80	93.74	96.88
T1-2	55531244	55302940	92.51	46.59	93.74	96.89
T1-3	65068774	64756962	91.96	46.30	93.49	96.61
T2-1	53923956	53678084	91.97	46.70	93.42	96.63
T2-2	46863574	46589694	92.55	47.09	93.61	96.87
T2-3	51548340	51304488	92.54	47.04	93.43	96.74
T3-1	44171240	43942622	92.37	46.84	93.10	95.88
T3-2	44849744	44668862	92.68	47.20	94.17	97.07
T3-3	55212924	54973380	92.20	47.14	93.68	96.43
T4-1	69720780	69450220	92.42	47.30	93.73	96.46
T4-2	66405070	66157562	92.94	46.67	94.16%	96.82
T4-3	64248114	63979034	92.29	46.69	92.75	96.29

通路名称 Pathway name	通路ID Pathway ID	基因数目 Number of genes	所有基因数 Number of all genes	P值 P value
核糖体 Ribosome	ko03010	83	305	3.36E-13
同源重组 Homologous recombination	ko03440	20	58	1.03E-05
DNA复制 DNA replication	ko03030	16	46	7.03E-05
氨基酸的生物合成 Biosynthesis of amino acids	ko01230	44	202	9.41E-05
错配修复 Mismatch repair	ko03430	14	39	0.000135124
缬氨酸、亮氨酸和异亮氨酸生物合成 Valine, leucine and isoleucine biosynthesis	ko00290	8	18	0.000748137
真核生物核糖体的生物合成 Ribosome biogenesis in eukaryotes	ko03008	19	77	0.002133956
嘧啶代谢 Pyrimidine metabolism	ko00240	15	58	0.00377061
2-氧代羧酸代谢 2-Oxocarboxylic acid metabolism	ko01210	14	53	0.004117066
糖鞘脂生物合成 Glycosphingolipid biosynthesis	ko00604	3	4	0.006896205
精氨酸生物合成 Arginine biosynthesis	ko00220	10	35	0.008097428
碱基切除修复 Base excision repair	ko03410	13	52	0.009192653
核质运输 Nucleocytoplasmic transport	ko03013	20	98	0.01563779
赖氨酸生物合成 Lysine biosynthesis	ko00300	5	13	0.01582533
萜类骨架生物合成 Terpenoid backbone biosynthesis	ko00900	14	62	0.0173777
糖胺聚糖降解 Glycosaminoglycan degradation	ko00531	6	18	0.01771733
氨酰基tRNA生物合成 Aminoacyl-tRNA biosynthesis	ko00970	13	57	0.0198342
不同类型的N-聚糖生物合成 Various types of N-glycan biosynthesis	ko00513	8	30	0.02599519
组氨酸代谢 Histidine metabolism	ko00340	5	16	0.03922549

基于转录组测序的苦瓜皂苷合成相关基因的鉴定和分析

Identification and Analysis of Genes Related to Bitter Gourd Saponin Synthesis Based on Transcriptome Sequencing

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