Full Text:   <1697>

Summary:  <459>

Suppl. Mater.: 

CLC number: 

On-line Access: 2024-08-27

Received: 2023-10-17

Revision Accepted: 2024-05-08

Crosschecked: 2022-04-19

Cited: 0

Clicked: 1925

Citations:  Bibtex RefMan EndNote GB/T7714

 ORCID:

Haoru TANG

https://orcid.org/0000-0001-6008-2747

-   Go to

Article info.
Open peer comments

Journal of Zhejiang University SCIENCE B 2022 Vol.23 No.4 P.300-314

http://doi.org/10.1631/jzus.B2100806


Comparative metabolomics provides novel insights into the basis of petiole color differences in celery (Apium graveolens L.)


Author(s):  Mengyao LI, Jie LI, Haohan TAN, Ya LUO, Yong ZHANG, Qing CHEN, Yan WANG, Yuanxiu LIN, Yunting ZHANG, Xiaorong WANG, Haoru TANG

Affiliation(s):  College of Horticulture, Sichuan Agricultural University, Chengdu 611130, China; more

Corresponding email(s):   htang@sicau.edu.cn

Key Words:  Celery, Metabolite, Anthocyanin, Chlorophyll, Petiole color


Mengyao LI, Jie LI, Haohan TAN, Ya LUO, Yong ZHANG, Qing CHEN, Yan WANG, Yuanxiu LIN, Yunting ZHANG, Xiaorong WANG, Haoru TANG. Comparative metabolomics provides novel insights into the basis of petiole color differences in celery (Apium graveolens L.)[J]. Journal of Zhejiang University Science B, 2022, 23(4): 300-314.

@article{title="Comparative metabolomics provides novel insights into the basis of petiole color differences in celery (Apium graveolens L.)",
author="Mengyao LI, Jie LI, Haohan TAN, Ya LUO, Yong ZHANG, Qing CHEN, Yan WANG, Yuanxiu LIN, Yunting ZHANG, Xiaorong WANG, Haoru TANG",
journal="Journal of Zhejiang University Science B",
volume="23",
number="4",
pages="300-314",
year="2022",
publisher="Zhejiang University Press & Springer",
doi="10.1631/jzus.B2100806"
}

%0 Journal Article
%T Comparative metabolomics provides novel insights into the basis of petiole color differences in celery (Apium graveolens L.)
%A Mengyao LI
%A Jie LI
%A Haohan TAN
%A Ya LUO
%A Yong ZHANG
%A Qing CHEN
%A Yan WANG
%A Yuanxiu LIN
%A Yunting ZHANG
%A Xiaorong WANG
%A Haoru TANG
%J Journal of Zhejiang University SCIENCE B
%V 23
%N 4
%P 300-314
%@ 1673-1581
%D 2022
%I Zhejiang University Press & Springer
%DOI 10.1631/jzus.B2100806

TY - JOUR
T1 - Comparative metabolomics provides novel insights into the basis of petiole color differences in celery (Apium graveolens L.)
A1 - Mengyao LI
A1 - Jie LI
A1 - Haohan TAN
A1 - Ya LUO
A1 - Yong ZHANG
A1 - Qing CHEN
A1 - Yan WANG
A1 - Yuanxiu LIN
A1 - Yunting ZHANG
A1 - Xiaorong WANG
A1 - Haoru TANG
J0 - Journal of Zhejiang University Science B
VL - 23
IS - 4
SP - 300
EP - 314
%@ 1673-1581
Y1 - 2022
PB - Zhejiang University Press & Springer
ER -
DOI - 10.1631/jzus.B2100806


Abstract: 
Plant metabolites are important for plant development and human health. Plants of celery (Apium graveolens L.) with different-colored petioles have been formed in the course of long-term evolution. However, the composition, content distribution, and mechanisms of accumulation of metabolites in different-colored petioles remain elusive. Using ultra-high performance liquid chromatography-tandem mass spectrometry (UHPLC-MS/MS), 1159 metabolites, including 100 lipids, 72 organic acids and derivatives, 83 phenylpropanoids and polyketides, and several alkaloids and terpenoids, were quantified in four celery cultivars, each with a different petiole color. There were significant differences in the types and contents of metabolites in celery with different-colored petioles, with the most striking difference between green celery and purple celery, followed by white celery and green celery. Annotated analysis of metabolic pathways showed that the metabolites of the different-colored petioles were significantly enriched in biosynthetic pathways such as anthocyanin, flavonoid, and chlorophyll pathways, suggesting that these metabolic pathways may play a key role in determining petiole color in celery. The content of chlorophyll in green celery was significantly higher than that in other celery cultivars, yellow celery was rich in carotenoids, and the content of anthocyanin in purple celery was significantly higher than that in the other celery cultivars. The color of the celery petioles was significantly correlated with the content of related metabolites. Among the four celery cultivars, the metabolites of the anthocyanin biosynthesis pathway were enriched in purple celery. The results of quantitative real-time polymerase chain reaction (qRT-PCR) suggested that the differential expression of the chalcone synthase (CHS) gene in the anthocyanin biosynthesis pathway might affect the biosynthesis of anthocyanin in celery. In addition, HPLC analysis revealed that cyanidin is the main pigment in purple celery. This study explored the differences in the types and contents of metabolites in celery cultivars with different-colored petioles and identified key substances for color formation. The results provide a theoretical basis and technical support for genetic improvement of celery petiole color.

比较代谢组学为芹菜叶柄颜色差异的形成提供了新的见解

目的:对四种不同颜色芹菜的呈色物质进行比较分析,探讨芹菜叶柄颜色形成的机理。
创新点:明确了芹菜叶柄颜色形成的主要差异代谢物的调控途径。
方法:以四个叶柄颜色差异明显的芹菜品种(白色、黄色、绿色和紫色)为材料,利用非靶代谢组学分析,探讨了叶柄的代谢物成分,对四个品种的花青素、叶绿素、类胡萝卜素含量进行测定,研究不同品种富含的代谢物进而探讨不同颜色形成的机理,进一步运用高效液相色谱技术(HPLC)进行代谢物验证,并结合基因表达揭示了芹菜叶柄颜色呈色的差异代谢物调控途径。
结论:不同颜色芹菜叶柄中叶绿素、花青素、类胡萝卜素含量差异显著,花青素和叶绿素分别在紫色和绿色品种中大量积累,表明花青素与叶绿素可能在芹菜叶柄颜色中起关键作用。利用非靶代谢组学在四个品种中检测到647种差异代谢物,不同颜色芹菜代谢物质种类和含量存在显著差异,绿色芹菜富含与叶绿素生物合成途径相关的代谢物,紫色芹菜富含与花青素生物合成途径的代谢物。进一步采用HPLC验证显示矢车菊素是紫芹的主要色素。为探究代谢物和基因表达的相关性,采用实时定量聚合酶链反应(qRT-PCR)进行表达量分析,结果与代谢物积累趋势一致。此外,不同颜色的芹菜富含不同的营养物质,例如,具有生物活性的代谢物如芹菜素和儿茶素被发现在绿芹中显著富集。本研究鉴定出丰富的代谢产物不仅为研究芹菜的生物活性物质提供了信息,也为挖掘不同颜色植物的代谢产物提供参考。

关键词:芹菜;代谢物;花青素;叶绿素;叶柄颜色

Darkslateblue:Affiliate; Royal Blue:Author; Turquoise:Article

Reference

[1]BealeSI, 2005. Green genes gleaned. Trends Plant Sci, 10(7):309-312.

[2]ChenC, ZhouG, ChenJ, et al., 2021. Integrated metabolome and transcriptome analysis unveils novel pathway involved in the formation of yellow peel in cucumber. Int J Mol Sci, 22(3):1494.

[3]CotterD, MaerA, GudaC, et al., 2006. LMPD: LIPID MAPS proteome database. Nucleic Acids Res, 34(S1):D507-D510.

[4]DongT, HanRP, YuJW, et al., 2019. Anthocyanins accumulation and molecular analysis of correlated genes by metabolome and transcriptome in green and purple asparaguses (Asparagus officinalis, L.). Food Chem, 271:18-28.

[5]EckhardtU, GrimmB, HörtensteinerS, 2004. Recent advances in chlorophyll biosynthesis and breakdown in higher plants. Plant Mol Biol, 56(1):1-14.

[6]FengK, LiuJX, XingGM, et al., 2019. Selection of appropriate reference genes for RT-qPCR analysis under abiotic stress and hormone treatment in celery. PeerJ, 7:e7925.

[7]FengerJA, RouxH, RobbinsRJ, et al., 2021. The influence of phenolic acyl groups on the color of purple sweet potato anthocyanins and their metal complexes. Dyes Pigments, 185:108792.

[8]FerreyraMLF, RiusSP, CasatiP, 2012. Flavonoids: biosynthesis, biological functions, and biotechnological applications. Front Plant Sci, 3:222.

[9]FiehnO, 2002. Metabolomics—the link between genotypes and phenotypes. Plant Mol Biol, 48(1-2):155-171.

[10]GrotewoldE, 2006. The genetics and biochemistry of floral pigments. Annu Rev Plant Biol, 57:761-780.

[11]HanXY, LuoYT, LinJY, et al., 2021. Generation of purple-violet chrysanthemums via anthocyanin B-ring hydroxylation and glucosylation introduced from Osteospermum hybrid F3'5'H and Clitoria ternatea A3'5'GT. Ornament Plant Res, 1:4.

[12]JanR, AsafS, PaudelS, et al., 2021. Discovery and validation of a novel step catalyzed by OsF3H in the flavonoid biosynthesis pathway. Biology, 10(1):32.

[13]JewettMC, HofmannG, NielsenJ, 2006. Fungal metabolite analysis in genomics and phenomics. Curr Opin Biotechnol, 17(2):191-197.

[14]JiaLD, WangJS, WangR, et al., 2021. Comparative transcriptomic and metabolomic analyses of carotenoid biosynthesis reveal the basis of white petal color in Brassica napus. Planta, 253:8.

[15]JiangSK, ZhangXJ, XuZJ, et al., 2010. Comparison between QTLs for chlorophyll content and genes controlling chlorophyll biosynthesis and degradation in Japonica rice. Acta Agronom Sin, 36(3):376-384.

[16]LiMY, HouXL, WangF, et al., 2018. Advances in the research of celery, an important Apiaceae vegetable crop. Crit Rev Biotechnol, 38(2):172-183.

[17]LiSP, DengBL, TianS, et al., 2021. Metabolic and transcriptomic analyses reveal different metabolite biosynthesis profiles between leaf buds and mature leaves in Ziziphus jujuba Mill. Food Chem, 347:129005.

[18]LiXB, WangY, JinL, et al., 2021. Development of fruit color in Rubus chingii Hu (Chinese raspberry): a story about novel offshoots of anthocyanin and carotenoid biosynthesis. Plant Sci, 311:110996.

[19]LiuHN, SuJ, ZhuYF, et al., 2019. The involvement of PybZIPa in light-induced anthocyanin accumulation via the activation of PyUFGT through binding to tandem G-boxes in its promoter. Hortic Res, 6:134.

[20]LiuY, TikunovY, SchoutenRE, et al., 2018. Anthocyanin biosynthesis and degradation mechanisms in Solanaceous vegetables: a review. Front Chem, 6:52.

[21]LiuY, ShaoYR, LiXY, et al., 2020. Analysis of nicotine-induced metabolic changes in Blakeslea trispora by GC-MS. J Zhejiang Univ-Sci B (Biomed & Biotechnol), 21(2): 172-177.

[22]MaY, FengYH, DiaoTW, et al., 2020. Experimental and theoretical study on antioxidant activity of the four anthocyanins. J Mol Struct, 1204:27509.

[23]Masoudi-NejadA, GotoS, JaureguiR, et al., 2007. EGENES: transcriptome-based plant database of genes with metabolic pathway information and expressed sequence tag indices in KEGG. Plant Physiol, 144(2):857-866.

[24]NagellaP, AhmadA, KimSJ, et al., 2012. Chemical composition, antioxidant activity and larvicidal effects of essential oil from leaves of Apium graveolens. Immunopharm Immunot, 34(2):205-209.

[25]NakabayashiR, Yonekura-SakakibaraK, UranoK, et al., 2014. Enhancement of oxidative and drought tolerance in Arabidopsis by overaccumulation of antioxidant flavonoids. Plant J, 77(3):367-379.

[26]OliverMJ, GuoLN, AlexanderDC, et al., 2011. A sister group contrast using untargeted global metabolomic analysis delineates the biochemical regulation underlying desiccation tolerance in Sporobolus stapfianus. Plant Cell, 23(4):1231-1248.

[27]PatilRH, BabuRL, NaveenKM, et al., 2015. Apigenin inhibits PMA-induced expression of pro-inflammatory cytokines and AP-1 factors in A549 cells. Mol Cell Biochem, 403(1-2):95-106.

[28]PengYY, Lin-WangK, CooneyJM, et al., 2019. Differential regulation of the anthocyanin profile in purple kiwifruit (Actinidia species). Hortic Res, 6:3.

[29]PfafflMW, 2001. A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res, 29(9):e45.

[30]ShiQQ, DuJT, ZhuDJ, et al., 2020. Metabolomic and transcriptomic analyses of anthocyanin biosynthesis mechanisms in the color mutant Ziziphus jujuba cv. Tailihong. J Agric Food Chem, 68(51):15186-15198.

[31]SongXM, SunPC, YuanJQ, et al., 2021. The celery genome sequence reveals sequential paleo-polyploidizations, karyotype evolution and resistance gene reduction in apiales. Plant Biotechnol J, 19(4):731-744.

[32]SowbhagyaHB, 2014. Chemistry, technology, and nutraceutical functions of celery (Apium graveolens L.): an overview. Crit Rev Food Sci Nutr, 54(3):389-398.

[33]SunTH, YuanH, CaoHB, et al., 2018. Carotenoid metabolism in plants: the role of plastids. Mol Plant, 11(1):58-74.

[34]TanGF, MaJ, ZhangXY, et al., 2017. AgFNS overexpression increase apigenin and decrease anthocyanins in petioles of transgenic celery. Plant Sci, 263:31-38.

[35]WangLY, TianYC, ShiW, et al., 2020. The miR396-GRFs module mediates the prevention of photo-oxidative damage by brassinosteroids during seedling de-etiolation in Arabidopsis. Plant Cell, 32(8):2525-2542.

[36]WangM, ChenL, LiangZJ, et al., 2020. Metabolome and transcriptome analyses reveal chlorophyll and anthocyanin metabolism pathway associated with cucumber fruit skin color. BMC Plant Biol, 20:386.

[37]WantEJ, MassonP, MichopoulosF, et al., 2013. Global metabolic profiling of animal and human tissues via UPLC-MS. Nat Protoc, 8(1):17-32.

[38]WeiK, ZhangYZ, WuLY, et al., 2016. Gene expression analysis of bud and leaf color in tea. Plant Physiol Biochem, 107:310-318.

[39]WenB, MeiZL, ZengCW, et al., 2017. metaX: a flexible and comprehensive software for processing metabolomics data. BMC Bioinformatics, 18:183.

[40]WishartDS, TzurD, KnoxC, et al., 2007. HMDB: the human metabolome database. Nucleic Acids Res, 35(S1):D521-D526.

[41]WuYQ, GuoJ, WangTL, et al., 2020. Metabolomic and transcriptomic analyses of mutant yellow leaves provide insights into pigment synthesis and metabolism in Ginkgo biloba. BMC Genomics, 21:858.

[42]XiaY, ChenWW, XiangWB, et al., 2021. Integrated metabolic profiling and transcriptome analysis of pigment accumulation in Lonicera japonica flower petals during colour-transition. BMC Plant Biol, 21:98.

[43]XuZS, YangQQ, FengK, et al., 2020. DcMYB113, a root-specific R2R3-MYB, conditions anthocyanin biosynthesis and modification in carrot. Plant Biotechnol J, 18(7):1585-1597.

[44]ZengZQ, LinTZ, ZhaoJY, et al., 2020. OsHemA gene, encoding glutamyl-tRNA reductase (GluTR) is essential for chlorophyll biosynthesis in rice (Oryza sativa). J Integr Agr, 19(3):612-623.

[45]ZhangLY, YuYB, YuRZ, 2020. Analysis of metabolites and metabolic pathways in three maize (Zea mays L.) varieties from the same origin using GC-MS. Sci Rep, 10:17990.

[46]ZhangWJ, LiuC, YangRJ, et al., 2019. Comparison of volatile profiles and bioactive components of sun-dried Pu-erh tea leaves from ancient tea plants on Bulang Mountain measured by GC-MS and HPLC. J Zhejiang Univ-Sci B (Biomed & Biotechnol), 20(7):563-575.

[47]ZhouDD, LiR, ZhangH, et al., 2020. Hot air and UV-C treatments promote anthocyanin accumulation in peach fruit through their regulations of sugars and organic acids. Food Chem, 309:125726.

[48]ZhuT, WangX, XuZM, et al., 2020. Screening of key genes responsible for Pennisetum setaceum ‘Rubrum’ leaf color using transcriptome sequencing. PLoS ONE, 15(11):e0242618.

Open peer comments: Debate/Discuss/Question/Opinion

<1>

Please provide your name, email address and a comment





Journal of Zhejiang University-SCIENCE, 38 Zheda Road, Hangzhou 310027, China
Tel: +86-571-87952783; E-mail: cjzhang@zju.edu.cn
Copyright © 2000 - 2024 Journal of Zhejiang University-SCIENCE