Please wait a minute...
Journal of Integrative Agriculture  2024, Vol. 23 Issue (3): 876-887    DOI: 10.1016/j.jia.2023.11.022
Horticulture Advanced Online Publication | Current Issue | Archive | Adv Search |

Identification of key genes regulating the synthesis of quercetin derivatives in Rosa roxburghii through integrated transcriptomics and metabolomics

Liyao Su, Min Wu, Tian Zhang, Yan Zhong, Zongming (Max) Cheng#

State Key Laboratory of Crop Genetics and Germplasm Enhancement, College of Horticulture, Nanjing Agricultural University, Nanjing 210095, China

Download:  PDF in ScienceDirect  
Export:  BibTeX | EndNote (RIS)      
摘要  

刺梨果实富含黄酮类化合物,但对其生物合成途径知之甚少。在本研究中,我们采用转录组学和代谢组学研究了刺梨果实发育五个阶段黄酮类化合物的动态变化。黄酮类化合物及其生物合成相关基因在不同发育阶段的丰度发生显著变化,并鉴定出大量槲皮素衍生物。WGCNA结果中发现三个与刺梨中黄酮类化合物的丰度显著相关的基因表达模块,并在这些模块中鉴定了三个直接参与槲皮素衍生物合成的结构UDP-糖基转移酶基因。此外,我们发现RrBEH4RrLBD1RrIF8可以显著促进槲皮素衍生物生物合成下游基因的表达。总之,这些结果为刺梨中黄酮类化合物的代谢和槲皮素衍生物的积累提供了新的见解。



Abstract  

Rosa roxburghii fruit is rich in flavonoids, but little is known about their biosynthetic pathways.  In this study, we employed transcriptomics and metabolomics to study changes related to the flavonoids at five different stages of Rroxburghii fruit development.  Flavonoids and the genes related to their biosynthesis were found to undergo significant changes in abundance across different developmental stages, and numerous quercetin derivatives were identified.  We found three gene expression modules that were significantly associated with the abundances of the different flavonoids in Rroxburghii and identified three structural UDP-glycosyltransferase genes directly involved in the synthesis of quercetin derivatives within these modules.  In addition, we found that RrBEH4, RrLBD1 and RrPIF8 could significantly increase the expression of downstream quercetin derivative biosynthesis genes.  Taken together, these results provide new insights into the metabolism of flavonoids and the accumulation of quercetin derivatives in Rroxburghii.

Keywords:  Rosa roxburghii       Quercetin derivatives         Weighted gene co-expression network analysis         Transcription factor        Transcriptome         Metabolome
  
Received: 20 March 2023   Accepted: 25 June 2023
Fund: This research was supported in part by the Priority Academic Program Development of Jiangsu Higher Education Institutions and the State Key Laboratory of Crop Genetics and Germplasm Enhancement, China (ZW201813). 
About author:  Liyao Su, E-mail: 2020204001@stu.njau.edu.cn; #Correspondence Zongming (Max) Cheng, E-mail: zcheng@utk.edu

Cite this article: 

Liyao Su, Min Wu, Tian Zhang, Yan Zhong, Zongming (Max) Cheng. 2024.

Identification of key genes regulating the synthesis of quercetin derivatives in Rosa roxburghii through integrated transcriptomics and metabolomics . Journal of Integrative Agriculture, 23(3): 876-887.

Aburto N J, Ziolkovska A, Hooper L, Elliott P, Cappuccio F P, Meerpohl J J. 2013. Effect of lower sodium intake on health: Systematic review and meta-analyses. British Medical Journal, 346, f1326.

Boots A W, Haenen G R M M, Bast A. 2008. Health effects of quercetin: From antioxidant to nutraceutical. European Journal of Pharmacology, 585, 325–337.

Borghi L, Bureau M, Simon R. 2007. Arabidopsis JAGGED LATERAL ORGANS is expressed in boundaries and coordinates KNOX and PIN activity. The Plant Cell, 19, 1795–1808.

Chen S, Zhou Y, Chen Y, Gu J. 2018. fastp: An ultra-fast all-in-one FASTQ preprocessor. Bioinformatics, 34, i884–i890.

Fan W, Pan X, He C, Chen H, Zhou Y. 2021. Accumulation of sugar and flavonoids as well as their association with changes of light intensity during fruit development of Rosa roxburghii. Scientia Agricultura Sinica, 54, 5277–5289. (in Chinese)

Grabherr M G, Haas B J, Yassour M, Levin J Z, Thompson D A, Amit I, Adiconis X, Fan L, Raychowdhury R, Qiandong Z, Zehua C, Mauceli E, Hacohen N, Gnirke A, Rhind N, Palma F D, Birren B W, Nusbaum C, Lindblad-Toh K, Friedman N, et al. 2013. Trinity: Reconstructing a full-length transcriptome without a genome from RNA-Seq data. Nature Biotechnology, 29, 644–652.

Havsteen B H. 2002. The biochemistry and medical significance of the flavonoids. Pharmacol Therapeut, 96, 67–202.

He J, Zhang Y, Ma N, Zhang X, Liu M, Fu W. 2016. Comparative analysis of multiple ingredients in Rosa roxburghii and R. sterilis fruits and their antioxidant activities. Journal of Functional Foods, 27, 29–41.

Heim K E, Tagliaferro A R, Bobilya D J. 2002. Flavonoid antioxidants: Chemistry, metabolism and structure-activity relationships. The Journal of Nutritional Biochemistry, 13, 572–584.

Huang M, Xu Q, Deng X. 2014. L-Ascorbic acid metabolism during fruit development in an ascorbate-rich fruit crop chestnut rose (Rosa roxburghii Tratt). Journal of Plant Physiology, 171, 1205–1216.

Jeong S, Kang M, Choi H, Kim J, Kim J. 2012. Quercetin ameliorates hyperglycemia and dyslipidemia and improves antioxidant status in type 2 diabetic db/db mice. Nutrition Research and Practice, 6, 201–207.

Jones P, Messner B, Nakajima J, Schäffner A R, Saito K. 2003. UGT73C6 and UGT78D1, glycosyltransferases involved in flavonol glycoside biosynthesis in Arabidopsis thaliana. Journal of Biological Chemistry, 278, 43910–43918.

Kim D, Langmead B, Salzberg S L. 2015. HISAT: A fast spliced aligner with low memory requirements. Nature Methods, 12, 357–360.

Langfelder P, Horvath S. 2008. WGCNA: An R package for weighted correlation network analysis. BMC Bioinformatics, 9, 559–572.

Lee J, Mitchell A E. 2011. Quercetin and isorhamnetin glycosides in onion (Allium cepa L.): varietal comparison, physical distribution, coproduct evaluation, and long-term storage stability. Journal of Agricultural and Food Chemistry, 59, 857–863.

Li H, Fang W, Wang Z, Chen Y. 2022. Physicochemical, biological properties, and flavour profile of Rosa roxburghii Tratt, Pyracantha fortuneana, and Rosa laevigata Michx fruits: A comprehensive review. Food Chemistry, 366, 130509.

Li Z B, Li C F, Li J, Zhang Y S. 2014. Molecular cloning and functional characterization of two divergent 4-coumarate: Coenzyme A ligases from Kudzu (Pueraria lobata). Biological and Pharmaceutical Bulletin, 37, 113–122.

Lim E, Doucet C J, Li Y, Elias L, Worrall D, Spencer S P, Ross J, Bowles D J. 2002. The activity of Arabidopsis glycosyltransferases toward salicylic acid, 4-hydroxybenzoic acid, and other benzoates. The Journal of Biological Chemistry, 277, 586–592.

Liu J, Osbourn A, Ma P. 2015. MYB transcription factors as regulators of phenylpropanoid metabolism in plants. Molecular Plant, 8, 689–708.

Liu Y, Lv J, Liu Z, Wang J, Yang B, Chen W, Ou L, Dai X, Zhang Z, Zou X. 2020. Integrative analysis of metabolome and transcriptome reveals the mechanism of color formation in pepper fruit (Capsicum annuum L.). Food Chemistry, 306, 125629.

Luca S V, Macovei I, Bujor A, Miron A, Skalicka-Woźniak K, Aprotosoaie A C, Trifan A. 2020. Bioactivity of dietary polyphenols: The role of metabolites. Critical Reviews in Food Science and Nutrition, 60, 626–659.

Ma D, Reichelt M, Yoshida K, Gershenzon J, Constabel C P. 2018. Two R2R3-MYB proteins are broad repressors of flavonoid and phenylpropanoid metabolism in poplar. The Plant Journal, 96, 949–965.

Mehrtens F, Kranz H, Bednarek P, Weisshaar B. 2005. The Arabidopsis transcription factor MYB12 is a flavonol-specific regulator of phenylpropanoid biosynthesis. Plant Physiology, 138, 1083–1096.

Nakajima O, Akiyama T, Hakamatsuka T, Shibuya M, Noguchi H, Ebizuka Y, Sankawa U. 1991. Isolation, sequence and bacterial expression of a cDNA for chalcone synthase from the cultured cells of Pueraria lobata. Chemical & Pharmaceutical Bulletin, 39, 1911–1913.

Oh J, Park E, Song K, Bae G, Choi G. 2020. PHYTOCHROME INTERACTING FACTOR8 inhibits phytochrome A-mediated far-red light responses in Arabidopsis. The Plant Cell, 32, 186–205.

Ralston L, Subramanian S, Matsuno M, Yu O. 2005. Partial reconstruction of flavonoid and isoflavonoid biosynthesis in yeast using soybean type I and type II chalcone isomerases. Plant Physiology, 137, 1375–1388.

Shen N, Wang T, Gan Q, Liu S, Wang L, Jin B. 2022. Plant flavonoids: Classification, distribution, biosynthesis, and antioxidant activity. Food Chemistry, 383, 132531.

Song B, Tang Z, Li X, Li J, Zhang M, Zhao K, Liu H, Zhang S, Wu J. 2020. Mining and evolution analysis of lateral organ boundaries domain (LBD) genes in Chinese white pear (Pyrus bretschneideri). BMC Genomics, 21, 644–661.

Soyano T, Thitamadee S, Machida Y, Chua N. 2008. ASYMMETRIC LEAVES2-LIKE19/LATERAL ORGAN BOUNDARIES DOMAIN30 and ASL20/LBD18 regulate tracheary element differentiation in Arabidopsis. The Plant Cell, 20, 3359–3373.

Stracke R, Ishihara H, Huep G, Barsch A, Mehrtens F, Niehaus K, Weisshaar B. 2007. Differential regulation of closely related R2R3-MYB transcription factors controls flavonol accumulation in different parts of the Arabidopsis thaliana seedling. The Plant Journal, 50, 660–677.

Umer M J, Bin Safdar L, Gebremeskel H, Zhao S, Yuan P, Zhu H, Kaseb M O, Anees M, Lu X, He N, Gong C, Liu W. 2020. Identification of key gene networks controlling organic acid and sugar metabolism during watermelon fruit development by integrating metabolic phenotypes and gene expression profiles. Horticulture Research, 7, 193–206.

Wang G, Wang Y, Yao L, Gu W, Zhao S, Shen Z, Lin Z, Liu W, Yan T. 2022. Pharmacological activity of quercetin: An updated review. Evidence-Based Complementary and Alternative Medicine, 2022, 3997190.

Wang L, Lv M, An J, Fan X, Dong M, Zhang S, Wang J, Wang Y, Cai Z, Fu Y. 2021. Botanical characteristics, phytochemistry and related biological activities of Rosa roxburghii Tratt fruit, and its potential use in functional foods: A review. Food and Function, 12, 1432–1451.

Wang R, Shu P, Zhang C, Zhang J, Chen Y, Zhang Y, Du K, Xie Y, Li M, Ma T, Zhang Y, Li Z, Grierson D, Pirrello J, Chen K, Bouzayen M, Zhang B, Liu M. 2022. Integrative analyses of metabolome and genome-wide transcriptome reveal the regulatory network governing flavor formation in kiwifruit (Actinidia chinensis). New Phytologist, 233, 373–389.

Wang W, Sun C, Mao L, Ma P, Liu F, Yang J, Gao Y. 2016. The biological activities, chemical stability, metabolism and delivery systems of quercetin: A review. Trends in Food Science and Technology, 56, 21–38.

Wang Z, Jian X, Zhao Y, Li S, Luo J. 2020. Functional characterization of cinnamate 4-hydroxylase from Helianthus annuus Linn using a fusion protein method. Gene, 758, 144950.

Wang Z, Nakano T, Gendron J, He J, Chen M, Vafeados D, Yang Y, Fujioka S, Yoshida S, Asami T, Chory J. 2002. Nuclear-localized BZR1 mediates brassinosteroid-induced growth and feedback suppression of brassinosteroid biosynthesis. Developmental Cell, 2, 505–513.

Wu S, Wu D, Song J, Zhang Y, Tan Q, Yang T, Yang J, Wang S, Xu J, Xu W, Liu A. 2022. Metabolomic and transcriptomic analyses reveal new insights into the role of abscisic acid in modulating mango fruit ripening. Horticulture Research, 9, c102.

Xu F, Ning Y, Zhang W, Liao Y, Li L, Cheng H, Cheng S. 2014. An R2R3-MYB transcription factor as a negative regulator of the flavonoid biosynthesis pathway in Ginkgo biloba. Functional and Integrative Genomics, 14, 177–189.

Yang Q, Zhang D, Farha A K, Yang X, Li H, Kong K, Zhang J, Chan C, Lu W, Corke H, Gan R. 2020. Phytochemicals, essential oils, and bioactivities of an underutilized wild fruit Cili (Rosa roxburghii). Industrial Crops and Products, 143, 111928.

Yin Y, Vafeados D, Tao Y, Yoshida S, Asami T, Chory J. 2005. A new class of transcription factors mediates brassinosteroid-regulated gene expression in Arabidopsis. Cell, 120, 249–259.

Yordanov Y S, Regan S, Busov V. 2010. Members of the LATERAL ORGAN BOUNDARIES DOMAIN transcription factor family are involved in the regulation of secondary growth in Populus. The Plant Cell, 22, 3662–3677.

Zhang C, Liu X, Qiang H, Li K, Wang J, Chen D, Zhuang Y. 2001. Inhibitory effects of rosa roxburghii tratt juice on in vitro oxidative modification of low density lipoprotein and on the macrophage growth and cellular cholesteryl ester accumulation induced by oxidized low density lipoprotein. Clinica Chimica Acta, 313, 37–43.

Zhou H, Lin-Wang K, Wang F, Espley R V, Ren F, Zhao J, Ogutu C, He H, Jiang Q, Allan A C, Han Y. 2019. Activator-type R2R3-MYB genes induce a repressor-type R2R3-MYB gene to balance anthocyanin and proanthocyanidin accumulation. The New Phytologist, 221, 1919–1934.

Zhu Q, Xie X, Lin H, Sui S, Shen R, Yang Z, Lu K, Li M, Liu Y. 2015. Isolation and functional characterization of a phenylalanine ammonia-lyase gene (SsPAL1) from Coleus (Solenostemon scutellarioides (L.) Codd). Molecules, 20, 16833–16851.

No related articles found!
No Suggested Reading articles found!