Integrated Transcriptomic and Targeted Metabolomic Analysis Reveals Regulation of Carotenoid Accumulation During Pepper Fruit Development

doi:10.16420/j.issn.0513-353x.2023-0374

Acta Horticulturae Sinica ›› 2024, Vol. 51 ›› Issue (8): 1773-1791.doi: 10.16420/j.issn.0513-353x.2023-0374

• Genetic & Breeding·Germplasm Resources·Molecular Biology • Previous Articles Next Articles

Integrated Transcriptomic and Targeted Metabolomic Analysis Reveals Regulation of Carotenoid Accumulation During Pepper Fruit Development

DUAN Minjie¹, LI Yifei¹, WANG Chunping², YANG Xiaomiao¹, HUANG Renzhong¹, HUANG Qizhong¹, ZHANG Shicai¹^,^*()

¹ Institute of Vegetables and Flowers，Chongqing Academy of Agricultural Sciences，Chongqing 401329，China
² Institute of Biotechnology，Chongqing Academy of Agricultural Sciences，Chongqing 401329，China

Received:2024-02-22 Revised:2024-05-20 Online:2024-08-25 Published:2024-08-21
Contact: ZHANG Shicai

Abstract

Abstract:

In this study，the fruit of pepper inbred line 1189 during different developmental stages was used to investigate the profiles of carotenoids by combination of metabolomic and transcriptomic analyses. Transcription factors that may be involved in regulating carotenoid biosynthesis in pepper were identified by weighted gene co-expression network analysis（WGCNA）. A total of 60 carotenoids were identified by targeted metabolome. After analysis，it was found that the main components at young fruit stage and mature green fruit stage were lutein（73.4% and 64.5%）and the lutein contents sharply decreased at color-changed fruit stage. The capsanthin content（32.5%）was highest at red ripe fruit stage and the lutei could not be detected. The 14 148 differentially expressed genes（DEGs）and 15 DEGs related to carotenoid metabolism were identified respectively by transcriptomic. The 12 286 DEGs screened were divided into 16 modules by WGCNA. It was found that MEdarkseagreen4，MElightcyan1 and MEbrown2 module were significantly correlated with 11 major carotenoids. The metabolic regulatory network was constructed based on carotenoid-related DEGs in the three modules，and ten transcription factors，including bHLH48，SEP3，CMB1，AGL27，YABBY2，GT-3B，NF-YA3，NAC2，HOX5 and GATA26，were obtained through promoter binding motif analysis，which may play important regulatory roles in carotenoid accumulation.

Key words: pepper, carotenoid, transcriptomic, targeted metabolomic, WGCNA, transcription factor

DUAN Minjie, LI Yifei, WANG Chunping, YANG Xiaomiao, HUANG Renzhong, HUANG Qizhong, ZHANG Shicai. Integrated Transcriptomic and Targeted Metabolomic Analysis Reveals Regulation of Carotenoid Accumulation During Pepper Fruit Development[J]. Acta Horticulturae Sinica, 2024, 51(8): 1773-1791.

Figures/Tables 12

References 61

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基因 Gene	引物（5′-3′） Forward sequence	生物学功能 Biological function
CCS	F：AGCACCCACATCAAAGCCAG R：GTGGTGAAGGGTCAACGCAA	催化玉米黄质和紫黄质转化为辣椒红素和辣椒玉红素 Catalyzes the conversion of zeaxanthin and vioxanthin to capsanthin and capsorubin
PSY1	F：ACAGGCAGGTCTATCCGACGAAG R：ACAACAGCAGAGATGCCAACACAG	催化GGPP合成八氢番茄红素 Catalyzes the synthesis of phytoene by GGPP
CHYB	F：GCACGAGTCACACCATAGACCAAG R：CGTGAACGAACATGTAGGCCATCC	催化β-胡萝卜素转化为玉米黄质 Catalyzes the conversion of β-carotene to zeaxanthin
NCED1	F：GACATTCAGGGATAGCAAGGC R：TTGAAATAGACCAAACCAGCGT	催化紫黄质和新黄质裂解成ABA前体 Catalytic cleavage of vioxanthin and neoxanthin into ABA precursors
LCYB	F：GTTGTTGGAATTGGTGGCACAGC R：ATGGCATTGGCAACGACAGGAG	催化番茄红素生成β-胡萝卜素 Catalyzes the conversion of lycopene to β-carotene
ABA2	F：CCCCTTGTTCAAATATCCTCG R：ACAGACCCTGCTATACTGCCTAA	参与类胡萝卜素裂解及ABA的生物合成 Involved in carotenoid cleavage and ABA biosynthesis
PSY2	F：AGACAGAGGTGGAATTTTGGGTCT R：CAAATTCCCCGGAAGCACA	参与植物绿色器官色素积累 Involved in the accumulation of pigment in plant green organs
LCYE	F：ACCCTCGGTGTAAGAATTAAAG R：GAGTGATCTGACAACGGAATAA	催化番茄红素转化为δ-胡萝卜素 Catalyzes the conversion of lycopene to δ-carotene
CRTISO	F：CACGGCAGGCGTTCATACA R：TCAGCCAGCAACACCCCAT	催化八氢番茄红素转化为番茄红素 Catalyzes the conversion of phytoene to lycopene
CMB1	F：CTCTAGTCGTGGCAAGCTTTAT R：CTGATGGTTGGGTTCCTTCA	番茄：参与果实成熟及调控果实色素积累 Tomato：Involved in fruit ripening and regulating fruit pigment accumulation
SEP3	F：ATCATGGCATTCTGGGGAGC R：TTTCGGTAGCACGGCATCG	拟南芥：调控花器官发育 Arabidopsis：Regulates the development of floral organs
YABBY2	F：GCGTGTTCCTTCTGCCTACA R：TTGCCCTCCAGCTTGAGTC	番茄：调节果实心室数和内源赤霉素含量 Tomato：Regulates the number of ventricles and endogenous gibberellin content in the fruit
GT-3B	F：CGCAGATAGGTTCCCTCAATG R：TCAGGCTCCAGCGTTTCAC	拟南芥：调控耐盐相关基因表达 Arabidopsis：Regulation of salt tolerance-related gene expression
NF-YA3	F：AGAAGCCCCAAGAGTCCAAA R：CCGATGCACGATGAGAAGG	拟南芥：调控早期胚胎发育 Arabidopsis：Regulates early embryonic development
NAC2	F：TCACCCGACTGATGAAGAGC R：TCCCCATACAACGCCAAAT	拟南芥：调控胚胎发育 Arabidopsis：Regulates embryonic development
AGL27	F：AAACGAAGGAAAGGTCTGATGA R：TCTGCCACGATTGGAGATGAT	拟南芥：增强植物对环境胁迫的耐受性 Arabidopsis：Enhancing plant tolerance to environmental stresses
HOX5	F：AGGCAGGTGGCTGTATGGTT R：ATCGTTGTCTTTGCGAATGG	拟南芥：ABA响应的正向调节因子 Arabidopsis：A positive regulator of ABA response
GATA26	F：GCTGGATTCGTTGCGTTTT R：GCTGCTACTGGTGCTTGCTT	拟南芥：参与光依赖调节 Arabidopsis：Involved in light-dependent regulation
bHLH48	F：AATCCCTACAGCGACAAGTGG R：GTTTGTCCCTCGGTCCAGAT	拟南芥：与光敏色素互作调控下胚轴伸长 Arabidopsis：Interacts with photosensitizer pigments to regulate hypocotyl elongation

基因 Gene	引物（5′-3′） Forward sequence	生物学功能 Biological function
CCS	F：AGCACCCACATCAAAGCCAG R：GTGGTGAAGGGTCAACGCAA	催化玉米黄质和紫黄质转化为辣椒红素和辣椒玉红素 Catalyzes the conversion of zeaxanthin and vioxanthin to capsanthin and capsorubin
PSY1	F：ACAGGCAGGTCTATCCGACGAAG R：ACAACAGCAGAGATGCCAACACAG	催化GGPP合成八氢番茄红素 Catalyzes the synthesis of phytoene by GGPP
CHYB	F：GCACGAGTCACACCATAGACCAAG R：CGTGAACGAACATGTAGGCCATCC	催化β-胡萝卜素转化为玉米黄质 Catalyzes the conversion of β-carotene to zeaxanthin
NCED1	F：GACATTCAGGGATAGCAAGGC R：TTGAAATAGACCAAACCAGCGT	催化紫黄质和新黄质裂解成ABA前体 Catalytic cleavage of vioxanthin and neoxanthin into ABA precursors
LCYB	F：GTTGTTGGAATTGGTGGCACAGC R：ATGGCATTGGCAACGACAGGAG	催化番茄红素生成β-胡萝卜素 Catalyzes the conversion of lycopene to β-carotene
ABA2	F：CCCCTTGTTCAAATATCCTCG R：ACAGACCCTGCTATACTGCCTAA	参与类胡萝卜素裂解及ABA的生物合成 Involved in carotenoid cleavage and ABA biosynthesis
PSY2	F：AGACAGAGGTGGAATTTTGGGTCT R：CAAATTCCCCGGAAGCACA	参与植物绿色器官色素积累 Involved in the accumulation of pigment in plant green organs
LCYE	F：ACCCTCGGTGTAAGAATTAAAG R：GAGTGATCTGACAACGGAATAA	催化番茄红素转化为δ-胡萝卜素 Catalyzes the conversion of lycopene to δ-carotene
CRTISO	F：CACGGCAGGCGTTCATACA R：TCAGCCAGCAACACCCCAT	催化八氢番茄红素转化为番茄红素 Catalyzes the conversion of phytoene to lycopene
CMB1	F：CTCTAGTCGTGGCAAGCTTTAT R：CTGATGGTTGGGTTCCTTCA	番茄：参与果实成熟及调控果实色素积累 Tomato：Involved in fruit ripening and regulating fruit pigment accumulation
SEP3	F：ATCATGGCATTCTGGGGAGC R：TTTCGGTAGCACGGCATCG	拟南芥：调控花器官发育 Arabidopsis：Regulates the development of floral organs
YABBY2	F：GCGTGTTCCTTCTGCCTACA R：TTGCCCTCCAGCTTGAGTC	番茄：调节果实心室数和内源赤霉素含量 Tomato：Regulates the number of ventricles and endogenous gibberellin content in the fruit
GT-3B	F：CGCAGATAGGTTCCCTCAATG R：TCAGGCTCCAGCGTTTCAC	拟南芥：调控耐盐相关基因表达 Arabidopsis：Regulation of salt tolerance-related gene expression
NF-YA3	F：AGAAGCCCCAAGAGTCCAAA R：CCGATGCACGATGAGAAGG	拟南芥：调控早期胚胎发育 Arabidopsis：Regulates early embryonic development
NAC2	F：TCACCCGACTGATGAAGAGC R：TCCCCATACAACGCCAAAT	拟南芥：调控胚胎发育 Arabidopsis：Regulates embryonic development
AGL27	F：AAACGAAGGAAAGGTCTGATGA R：TCTGCCACGATTGGAGATGAT	拟南芥：增强植物对环境胁迫的耐受性 Arabidopsis：Enhancing plant tolerance to environmental stresses
HOX5	F：AGGCAGGTGGCTGTATGGTT R：ATCGTTGTCTTTGCGAATGG	拟南芥：ABA响应的正向调节因子 Arabidopsis：A positive regulator of ABA response
GATA26	F：GCTGGATTCGTTGCGTTTT R：GCTGCTACTGGTGCTTGCTT	拟南芥：参与光依赖调节 Arabidopsis：Involved in light-dependent regulation
bHLH48	F：AATCCCTACAGCGACAAGTGG R：GTTTGTCCCTCGGTCCAGAT	拟南芥：与光敏色素互作调控下胚轴伸长 Arabidopsis：Interacts with photosensitizer pigments to regulate hypocotyl elongation

目标基因 Target gene	候选转录因子 Transcription factor candidate	缩写 Abbreviation	蛋白ID Protein ID	启动子基序结合位点 Promoter motif union sites	拟南芥同源基因 Arabidopsis locus name
CCS	预测：核转录因子Y亚基A-3-like亚型X1 Predicted：Nuclear transcription factor Y subunit A-3-like isoform X1	NF-YA3	XP_016562508.1	93	AT1G72830
	含NAC结构域的蛋白2 -like NAC domain-containing protein 2-like	NAC2	XP_016569664.1	1	AT3G15510
	SEPALLATA-like MADS-box蛋白3 SEPALLATA-like MADS-box protein 3	SEP3	AYA60475.1	12	AT1G24260
	预测：GATA转录因子26亚型X1 Predicted：GATA transcription factor 26 isoform X1	GATA26	XP_016575075.1	44	AT4G17570
PSY	预测：MADS-box蛋白CMB -like Predicted：MADS-box protein CMB1-like	CMB1	XP_016547230.1	1	AT2G03710
NCED1	三螺旋转录因子GT-3b Trihelix transcription factor GT-3b	GT-3B	XP_016542034.1	45	AT5G01380
CHYB	预测：无性生殖类似MADS-box蛋白AGL27亚型X5 Predicted：Agamous-like MADS-box protein AGL27 isoform X5	AGL27	XP_016551041.1	2	AT1G77080
CHYB	预测：GATA转录因子26亚型X1 Predicted：GATA transcription factor 26 isoform X1	GATA26	XP_016575075.1	78	AT4G17570
PSY2	预测：转录因子bHLH48亚型X2 Predicted：Transcription factor bHLH48 isoform X2	bHLH48	XP_016543852.1	16	AT2G42300
CRTISO	假定的轴向调节YABBY 2亚型X1 Putative axial regulator YABBY 2 isoform X1	YABBY2	XP_016548878.1	2	AT2G26580
CRTISO	同源框亮氨酸拉链蛋白HOX5 Homeobox-leucine zipper protein HOX5	HOX5	KAF3660217.1	3	AT5G65310

目标基因 Target gene	候选转录因子 Transcription factor candidate	缩写 Abbreviation	蛋白ID Protein ID	启动子基序结合位点 Promoter motif union sites	拟南芥同源基因 Arabidopsis locus name
CCS	预测：核转录因子Y亚基A-3-like亚型X1 Predicted：Nuclear transcription factor Y subunit A-3-like isoform X1	NF-YA3	XP_016562508.1	93	AT1G72830
	含NAC结构域的蛋白2 -like NAC domain-containing protein 2-like	NAC2	XP_016569664.1	1	AT3G15510
	SEPALLATA-like MADS-box蛋白3 SEPALLATA-like MADS-box protein 3	SEP3	AYA60475.1	12	AT1G24260
	预测：GATA转录因子26亚型X1 Predicted：GATA transcription factor 26 isoform X1	GATA26	XP_016575075.1	44	AT4G17570
PSY	预测：MADS-box蛋白CMB -like Predicted：MADS-box protein CMB1-like	CMB1	XP_016547230.1	1	AT2G03710
NCED1	三螺旋转录因子GT-3b Trihelix transcription factor GT-3b	GT-3B	XP_016542034.1	45	AT5G01380
CHYB	预测：无性生殖类似MADS-box蛋白AGL27亚型X5 Predicted：Agamous-like MADS-box protein AGL27 isoform X5	AGL27	XP_016551041.1	2	AT1G77080
CHYB	预测：GATA转录因子26亚型X1 Predicted：GATA transcription factor 26 isoform X1	GATA26	XP_016575075.1	78	AT4G17570
PSY2	预测：转录因子bHLH48亚型X2 Predicted：Transcription factor bHLH48 isoform X2	bHLH48	XP_016543852.1	16	AT2G42300
CRTISO	假定的轴向调节YABBY 2亚型X1 Putative axial regulator YABBY 2 isoform X1	YABBY2	XP_016548878.1	2	AT2G26580
CRTISO	同源框亮氨酸拉链蛋白HOX5 Homeobox-leucine zipper protein HOX5	HOX5	KAF3660217.1	3	AT5G65310

Integrated Transcriptomic and Targeted Metabolomic Analysis Reveals Regulation of Carotenoid Accumulation During Pepper Fruit Development

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