多组学联合解析红色玫瑰香型葡萄品种转色过程中单萜和花色苷积累规律

doi:10.3864/j.issn.0578-1752.2025.13.012

Abstract

Abstract:

【Objective】 The accumulation of anthocyanins and monoterpenes during grape berry color change at both metabolic and transcriptional levels were analyzed, to explore the spatio-temporal synthesis mechanisms of anthocyanins and monoterpenes, and provide a theoretical basis for the regulation of anthocyanin and monoterpene synthesis in table grape. 【Method】 The grape berries of Ruiduhongyu were used as materials, sampling was started at 5 days before the veraison and continued until 40 days after the initial color change. The contents of total soluble solids and titratable acid in the berry samples were determined by conventional methods; The changes in monoterpene components and content in berries were determined with headspace solid-phase microextraction combined with gas chromatography-mass spectrometry (HS-SPEME-GC-MS); The content of total flavonoids and total anthocyanins were detected using a spectrophotometer; The expression changes of key genes involved in monoterpenes and anthocyanins synthesis were analyzed by transcriptome sequencing and real-time fluorescence quantitative PCR. 【Result】 With the advancement of the coloration process, the main components of 25 free and bound monoterpenes in the Ruiduhongyu berries fluctuated. Most of the free monoterpenes began to be synthesized in large quantities from the 20th day of coloration and reached the highest level at the 35-40 th day of coloration. The content of bound monoterpenes reached the highest level at 30 days after coloration. The content of bound monoterpenes was higher than that of free monoterpenes. Flavonoids were synthesized and accumulated in large quantities before the fruit coloration; the synthesis of anthocyanins was initiated along with the fruit coloration and reached the highest level at 20 days after coloration, followed by a slight decrease. Based on transcriptome sequencing, a total of 5 836 differentially expressed genes were identified, and the number of differentially expressed genes varied significantly among different developmental stages. The differentially expressed genes were enriched in the pathways of phenylalanine synthesis, flavonoid synthesis, and monoterpene synthesis. Among them, 14 differentially expressed genes were related to the monoterpene synthesis pathway, and 11 were related to the anthocyanin synthesis pathway. The expression patterns of these genes were consistent with the accumulation of monoterpenes and anthocyanins. Further correlation analysis screened out 24 transcription factors that were significantly correlated with the expression of multiple genes involved in the monoterpene and anthocyanin synthesis pathways. 【Conclusion】 The synthesis of anthocyanins in red Muscat type grape berries initiates earlier than that of the aroma compound monoterpenes, and the synthesis of the two types of compounds is regulated in a spatio-temporal pattern. The accumulation of monoterpenes and anthocyanins is closely related to the expression of multiple key enzyme genes in their synthesis pathways, and their synthesis is regulated at the transcriptional level of various genes.

Key words: grapes, monoterpenes, anthocyanins, fruit development, transcriptional regulation

WANG HuiLing, ZHANG YingYing, YAN AiLing, WANG XiaoYue, LIU ZhenHua, REN JianCheng, XU HaiYing, SUN Lei. Multi-Omics Analysis Reveals the Changes of Monoterpenes and Anthocyanins Accumulation During Veraison in Red Muscat-Type Grape[J].Scientia Agricultura Sinica, 2025, 58(13): 2645-2662.

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Figures/Tables 12

Table 1

Table 2

Table 3

Table 4

Changes in the content of free monoterpenes in Ruiduhongyu at different development stage"

编号 Code	化合物 Compound	转色天数Days after veraison (d)
编号 Code	化合物 Compound	-5	0	5	10	15	20	25	30	35	40
M1	β-月桂烯 β-myrcene	2.60±0.35f	1.30±0.22f	2.82±0.34f	2.54±0.20f	7.29±1.06f	16.92±7.17e	38.66±1.55d	74.09±2.91c	108.39±27.40b	178.44±13.15a
M2	柠檬烯 Limonene	5.56±2.06g	2.09±0.02h	2.03±0.40h	6.93±0.42g	12.12±1.49f	24.16±1.89e	39.77±6.41d	94.18±2.24b	124.84±32.18a	80.30±11.58c
M3	水芹烯 Phellandrene	2.40±0.50de	1.11±0.33e	0.20±0.01f	2.77±0.06de	2.07±0.78de	3.80±0.67d	5.64±2.40c	13.75±3.88b	20.52±4.78a	23.36±13.01a
M4	β-trans-罗勒烯 β-trans-ocimene	2.50±0.38g	3.96±0.10f	1.27±0.45h	2.06±0.45g	5.54±0.21e	11.42±0.67d	18.37±3.75c	40.77±9.48b	61.15±10.73a	46.23±7.99b
M5	γ-松油烯 γ-terpinen	39.04±4.23a	22.94±2.69c	0.26±0.04e	31.82±1.62b	10.07±0.52d	9.66±0.24d	8.96±1.97d	26.14±5.04c	30.73±1.05b	24.48±1.70c
M6	β-cis-罗勒烯 β-cis-ocimene	5.02±2.21e	2.27±0.57f	2.34±0.95f	3.72±0.49f	7.87±0.62e	18.87±2.09d	31.23±1.07c	77.18±2.27b	123.07±24.11a	102.41±34.07a
M7	异松油烯 Terpinolen	27.83±2.16f	15.09±1.69g	5.26±0.44h	27.13±0.77f	29.82±3.73f	67.28±5.11e	85.46±9.71d	236.50±6.25b	307.25±17.54a	134.64±3.72c
M8	cis-氧化玫瑰 cis-rose oxide	0.06±0.01e	0.14±0.09d	0.05±0.01e	0.23±0.04c	0.32±0.09c	0.45±0.06c	0.89±0.07bc	3.64±1.13ab	3.49±0.85ab	4.11±0.38a
M9	trans-氧化玫瑰 trans-rose oxide	tr	tr	tr	0.01±0.00e	0.12±0.01d	0.26±0.08c	0.50±0.04b	0.42±0.03b	0.52±0.03b	1.41±0.93a
M10	别罗勒烯 Allo-ocimene	0.51±0.06ef	0.23±0.05g	0.23±0.10g	0.39±0.02f	0.73±0.05e	1.51±0.09d	3.10±0.67c	5.96±0.82b	9.87±2.05a	9.62±1.18a
M11	（E,Z）-别罗勒烯 (E,Z)-allo-ocimene	0.07±0.01d	0.10±0.05d	0.07±0.01d	0.08±0.01d	0.13±0.02d	0.07±0.01	0.46±0.08c	0.85±0.05b	3.61±0.89a	3.48±0.84a
M12	cis-呋喃型氧化里那醇 cis-furan linalool oxide	53.53±7.36d	28.46±7.19e	8.69±1.47f	137.06±4.14c	53.90±6.79d	114.12±8.85c	73.56±8.32d	355.45±14.61a	388.61±11.61a	261.67±4.96b
M13	trans-呋喃型氧化锂 trans-furan linalool oxide	22.23±3.11ef	16.89±1.77f	11.92±1.70f	51.54±1.24d	30.79±1.10e	77.88±3.00d	138.38±7.31c	372.01±11.36b	455.65±13.61a	392.81±17.64b
M14	橙花醚 Nerol oxide	59.85±9.59c	34.08±3.69d	5.58±1.38e	123.02±3.22a	45.24±2.42cd	63.16±4.75c	48.00±5.58cd	128.91±45.36a	111.53±4.52b	32.10±1.38d
M15	里那醇 Linalool	33.78±9.91g	27.38±0.46g	36.57±2.52g	35.43±6.51g	94.09±5.18f	215.72±9.69e	423.10±18.52d	721.67±21.95c	1171.90±30.92b	1681.14±10.29a
M16	脱氢里那醇 Hortrineol	207.67±7.24cd	120.13±4.19d	21.69±6.52e	425.52±17.53b	180.12±8.21d	339.03±25.02c	249.76±40.37cd	824.44±18.52a	848.21±26.92a	268.17±13.84bc
M17	4-松油烯醇 4-terpineol	6.98±1.39c	3.35±0.97d	0.74±0.22e	8.40±0.20c	2.86±0.38d	90.97±14.34a	5.42±0.83cd	18.74±0.86b	24.37±1.65b	6.28±1.08c
M18	橙花醛 Neral	0.60±0.01c	0.59±0.01c	0.60±0.01c	0.59±0.01c	0.59±0.01c	0.59±0.01c	0.59±0.01c	0.99±0.07b	1.25±0.14a	1.00±0.37b
M19	α-萜品醇 α-terpineol	13.71±3.84f	7.59±0.26g	8.95±2.03g	18.15±2.36f	31.28±1.57e	79.86±5.54d	91.13±2.33d	309.53±7.91b	432.38±10.32a	162.71±3.98c
M20	香叶醛 Geranial	0.56±0.01d	0.65±0.15d	0.62±0.08d	0.57±0.02d	0.82±0.04cd	1.12±0.09c	1.96±0.05b	2.12±0.61b	3.11±0.77a	3.60±0.62a
M21	β-香茅醇 β-citronellol	tr	tr	tr	tr	tr	tr	tr	0.19±0.02c	7.52±0.38b	23.55±4.78a
M22	γ-香叶醇 γ-geraniol	9.62±0.03c	9.70±0.11c	9.60±0.01c	9.60±0.01c	9.69±0.05c	9.67±0.07c	9.75±0.15b	9.84±0.07b	9.98±0.13b	10.68±0.23a
M23	橙花醇 Nerol	1.26±0.13e	1.22±0.16e	1.24±0.19e	1.25±0.21e	2.69±0.52e	5.99±0.26d	9.45±0.39c	24.61±7.93b	39.14±8.73a	26.89±1.74b
M24	香叶醇 Geraniol	12.06±1.69e	12.57±3.50e	15.85±2.41e	11.62±1.73e	15.63±2.13e	26.81±1.05d	36.67±2.00c	89.12±2.63b	130.10±26.25a	95.13±3.36b
M25	香叶酸 Geranic acid	133.91±7.91c	62.51±3.47d	286.98±6.28bc	197.28±7.48c	144.51±2.96c	111.57±6.58cd	315.79±19.39b	244.17±10.13c	321.73±11.41b	1079.00±13.53a

Table 4

Table 5

Changes in the content of bound monoterpenes in Ruiduhongyu at different development stage"

编号 Code	化合物 Compound	转色天数Days after veraison (d)
编号 Code	化合物 Compound	-5	0	5	10	15	20	25	30	35	40
CM1	β-月桂烯 β-Myrcene	0.92±0.70d	0.45±0.25d	1.77±0.55d	0.59±0.07d	1.18±0.50d	5.51±0.48c	5.66±1.60c	43.67±2.28a	29.63±6.93b	32.36±8.12b
CM2	柠檬烯 Limonene	tr	tr	tr	tr	tr	2.11±0.49c	2.17±0.36c	12.11±6.00a	8.95±2.29b	8.71±1.48b
CM3	水芹烯 Phellandrene	1.04±0.07d	1.12±0.24d	1.37±0.05d	1.05±0.17d	1.18±0.25d	1.98±0.29c	2.15±0.33c	8.31±1.29a	5.77±1.11b	5.86±1.79b
CM4	β-trans-罗勒烯 β-trans-Ocimene	3.93±0.13c	4.01±0.36c	4.27±0.11c	3.88±0.10c	3.98±0.01c	4.54±0.10c	4.42±0.06c	12.58±4.23a	10.20±2.58a	8.80±2.59b
CM5	γ-松油烯 γ-terpinen	0.89±0.02c	0.88±0.02c	0.98±0.15c	0.92±0.07c	0.87±0.01c	1.10±0.01c	1.19±0.25c	3.51±1.11a	2.72±0.63b	2.20±0.67b
CM6	β-cis-罗勒烯 β-cis-ocimene	0.41±0.16e	0.34±0.17e	0.83±0.16d	0.25±0.12e	0.25±0.02e	0.92±0.02d	0.80±0.08d	16.38±1.94a	12.16±1.14b	8.76±1.67c
CM7	异松油烯 Terpinolen	2.85±0.03c	2.84±0.02c	2.93±0.09c	2.94±0.19c	2.93±0.10c	3.36±0.03c	3.24±0.03c	14.30±3.84a	9.43±1.62b	8.06±1.58b
CM8	cis-氧化玫瑰 cis-rose oxide	0.05±0.03e	0.02±0.01e	0.24±0.09d	0.45±0.14c	0.18±0.02d	0.67±0.13c	0.24±0.03d	8.05±1.09a	4.35±0.49b	3.19±1.28b
CM9	trans-氧化玫瑰 trans-rose oxide	tr	tr	0.05±0.02d	0.20±0.12c	0.15±0.03c	0.36±0.02c	0.15±0.03c	2.69±1.03a	1.47±0.18b	1.15±0.66b
CM10	别罗勒烯 Allo-ocimene	0.32±0.01c	0.32±0.01c	0.31±0.01c	0.32±0.01c	0.31±0.01c	0.35±0.01c	0.37±0.05c	1.31±0.48a	1.16±0.35b	1.09±0.41b
CM11	（E,Z）-别罗勒烯 (E,Z)-allo-ocimene	0.32±0.01b	0.32±0.01b	0.32±0.01b	0.33±0.01b	0.32±0.01b	0.32±0.01b	0.36±0.08b	0.32±0.01b	0.32±0.01b	0.80±0.32a
CM12	cis-呋喃型氧化里那醇 cis-furan linalool oxide	tr	tr	tr	25.32±0.64f	35.03±7.97f	99.83±10.63d	53.86±15.73e	271.65±10.41a	123.31±6.14c	207.24±10.93b
CM13	trans-呋喃型氧化里那醇 trans-furan linalool oxide	0.68±0.06f	13.72±0.89e	13.89±0.92e	74.96±9.73cd	58.69±5.42d	111.21±6.56c	147.48±6.89b	189.59±8.23a	59.87±2.64d	54.76±10.07d
CM14	橙花醚 Nerol oxide	5.73±0.21c	5.89±0.24c	6.04±0.18c	7.71±1.00c	7.23±0.21c	9.17±0.27c	7.45±0.15c	42.73±2.38a	21.14±2.19b	14.26±5.82b
CM15	里那醇 Linalool	74.38±0.94d	74.34±0.22d	74.08±0.28d	75.48±1.22d	85.82±5.58d	129.29±8.93c	124.43±1.56c	573.48±15.88a	491.72±12.85b	479.38±12.96b
CM16	脱氢里那醇 Hortrineol	tr	tr	tr	tr	tr	1.60±0.23c	0.59±0.16c	13.09±1.87a	4.63±1.01b	3.85±1.08b
CM17	4-松油烯醇 4-terpineol	0.01±0.01e	0.07±0.01e	tr	0.51±0.03c	0.15±0.06d	0.42±0.07c	0.09±0.03	1.88±0.09a	0.91±0.34b	0.25±0.17d
CM18	橙花醛 Neral	3.75±0.41d	4.33±0.76d	5.84±0.87d	7.18±0.92d	4.63±0.40d	7.15±1.01d	5.91±0.42d	72.96±6.41a	45.43±9.07b	33.34±2.49c
CM19	α-萜品醇 α-Terpineol	15.71±0.82c	17.26±1.79c	15.37±0.07c	17.72±0.92c	16.63±0.23c	17.60±0.12c	16.88±0.19c	34.62±7.86a	24.72±2.75b	25.00±5.44b
CM20	香叶醛 Geranial	6.69±0.41d	5.98±0.78d	9.26±1.34d	6.21±2.17d	4.39±0.12d	7.34±0.78d	5.13±0.18d	73.46±8.27a	41.28±8.21b	24.94±6.29c
CM21	β-香茅醇 β-citronellol	13.93±0.95c	12.26±1.07c	38.29±5.65b	3.48±0.82d	1.24±0.33d	3.57±0.12d	2.67±0.07d	61.64±2.32a	69.47±1.74a	43.93±8.31b
CM22	γ-香叶醇 γ-geraniol	48.41±0.18b	48.46±0.13b	48.81±0.11b	48.40±0.27b	48.14±0.01b	48.30±0.02b	48.25±0.02b	52.58±1.66a	52.13±1.11a	50.26±1.53a
CM23	橙花醇 Nerol	11.97±3.24d	11.14±3.95d	23.04±2.47c	12.83±4.71d	10.13±0.79d	13.65±0.35d	15.12±0.72d	167.79±9.75a	189.67±7.69a	84.789±6.46b
CM24	香叶醇 Geraniol	73.19±9.26d	68.61±7.84d	94.70±7.36c	57.93±6.71e	52.16±0.54e	58.05±0.41e	54.94±0.68e	204.72±12.03a	172.01±2.40b	109.69±5.42c
CM25	香叶酸 Geranic acid	408.62±4.38d	533.26±24.91d	1166.52±26.38c	549.90±13.00d	331.97±2.15e	488.75±40.30d	358.36±22.79	5316.57±20.97a	2687.36±64.58b	1062.64±61.19c

Table 5

Fig. 1

Fig. 2

Table 6

Fig. 3

Fig. 4

Fig. 5

Fig. 6

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取样日期 Sampling date (M/D)	06/26	06/30	07/04	07/09	07/13	07/18	07/22	07/27	08/02	08/07
转色天数 Days after veraison (d)	-5	0	5	10	15	20	25	30	35	40
果实表型 Grape berry phenotype
表型描述 Phenotype description	果实硬未着色 Berries hard and not coloured	个别果实着色Individual berries coloured	果实1/4 着色 1/4 of berreis coloured	果实1/2 着色 1/2 of berreis coloured	果实2/3 着色 2/3 of berreis coloured	全部果实着色 All of berreis coloured	果实已发甜淡香 Berries with light Muscat flavor	果实香气明显 Berries with obvious Muscat flavor	果实香甜 Berries sweet and with strong Muscat flavor	果实香甜 Berries sweet and with strong Muscat flavor

基因Gene	基因ID	引物序列Primers sequence (5′-3′)
CHS	Vitvi14g01449	F：GAAGATGGGAATGGCTGCTG R：AAGGCACAGGGACACAAAAG
CHS	Vitvi05g01044	F：TCGGCTGAGGAAGGGCTGAA R：GGCAAGTAAAGTGGAAACAG
DFR	Vitvi18g00988	F：GAAACCTGTAGATGGCAGGA R：GGCCAAATCAAACTACCAGA
ANS	Vitvi02g00435	F：AGGGAAGGGAAAACAAGTAG R：ACTCTTTGGGGATTGACTGG
UFGT	Vitvi16g00156	F：GGGATGGTAATGGCTGTGG R：ACATGGGTGGAGAGTGAGTT
DXS	Vitvi04g00438	F：GAAGGCTCTGTTGGAGGGTTT R：TCCTCTGGTGATGCCTGTTCT
DXR	Vitvi17g00816	F：ATTGCTTATGGCAGGCGAAA R：CCGTTCCGATCTTACCAATCAC
HDR	Vitvi03g00374	F：ATTGCTTATGGCAGGCGAAA R：CCGTTCCGATCTTACCAATCAC
TPS	Vitvi10g02129	F：TGAAGGGAATGCTCTGCTTGT R：TGTTTTGCTCAAGGCCCTTT
TPS	Vitvi12g00574	F：TGGGATTCTCTCCTGCCTTTT R：GCAGTAGGCACAAGCACAACA
VvGAPDH	--	F：TTCTCGTTGAGGGCTATTCCA R：CCACAGACTTCATCGGTGACA

理化指标 Physical and chemical indicators	转色天数Days after veraison (d)
理化指标 Physical and chemical indicators	-5	0	5	10	15	20	25	30	35	40
可溶性固形物 Soluble solids (Brix°)	4.33±0.81	6.13±1.00	7.23±1.04	10.63±0.49	13.30±0.26	14.33±0.90	15.03±0.57	16.63±0.95	17.93±0.15	18.13±1.01
可滴定酸含量 Titrable acid content (g·L^-1)	31.11±4.92	29.53±4.64	20.22±2.15	16.57±1.44	14.56±1.00	13.48±1.24	12.72±1.69	9.85±0.86	9.43±1.30	6.27±0.13

样本Sample	干净读数 Clean data (Gb)	测序准确度 Q20 (%)	测序准确度 Q30 (%)	GC含量 GC content (%)	总比对 Total map (%)	特异比对率 Unique map (%)
5_1	6.71	97.00	91.90	46.72	94.51	82.38
5_2	7.74	97.34	92.46	46.75	98.54	86.19
5_3	8.18	97.32	92.38	46.87	92.65	80.54
20_1	7.17	97.08	92.18	46.45	97.80	86.99
20_2	7.14	96.76	91.47	46.60	95.11	82.46
20_3	7.04	97.08	91.78	46.64	92.02	89.53
30_1	7.23	97.08	92.12	46.24	95.02	85.76
30_2	6.52	97.25	92.20	46.35	95.84	82.88
30_3	7.46	96.99	91.95	46.17	97.56	84.45
40_1	7.28	97.05	92.09	46.24	90.92	87.58
40_2	6.91	97.07	92.04	46.37	96.18	86.33
40_3	7.21	97.28	92.46	46.36	98.34	86.70

Multi-Omics Analysis Reveals the Changes of Monoterpenes and Anthocyanins Accumulation During Veraison in Red Muscat-Type Grape

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