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CC BY-NC-ND 4.0 · Planta Medica International Open 2022; 9(01): e23-e33
DOI: 10.1055/a-1712-7978
Original Papers

Biosynthesis and Chemopreventive Potential of Jute (Corchorus capsularis and C. olitorius) Flavonoids and Phylogeny of Flavonoid Biosynthesis Pathways

Pratik Satya
1   ICAR-Central Research Institute for Jute and Allied Fibres, Barrackpore, Kolkata, India
,
Debabrata Sarkar
1   ICAR-Central Research Institute for Jute and Allied Fibres, Barrackpore, Kolkata, India
,
Amitava Chatterjee
2   Faculty Centre of Integrated Rural Development & Management, Ramakrishna Mission Vivekananda Educational and Research Institute, Narendrapur, Kolkata, India
,
Srikumar Pal
3   Bidhan Chandra Krishi Viswavidyalaya, Mohanpur, Nadia, West Bengal, India
,
Soham Ray
1   ICAR-Central Research Institute for Jute and Allied Fibres, Barrackpore, Kolkata, India
,
Laxmi Sharma
1   ICAR-Central Research Institute for Jute and Allied Fibres, Barrackpore, Kolkata, India
,
Suman Roy
1   ICAR-Central Research Institute for Jute and Allied Fibres, Barrackpore, Kolkata, India
,
Amit Bera
1   ICAR-Central Research Institute for Jute and Allied Fibres, Barrackpore, Kolkata, India
,
Srinjoy Ghosh
1   ICAR-Central Research Institute for Jute and Allied Fibres, Barrackpore, Kolkata, India
,
Jiban Mitra
1   ICAR-Central Research Institute for Jute and Allied Fibres, Barrackpore, Kolkata, India
,
Gouranga Kar
1   ICAR-Central Research Institute for Jute and Allied Fibres, Barrackpore, Kolkata, India
,
Nagendra Kumar Singh
4   ICAR-National Institute for Plant Biotechnology, Pusa Campus, New Delhi, India
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Abstract

Flavonoids are valuable phytochemicals for human health and nutrition. Jute (Corchorus capsularis and C. olitorius), a vegetable rich in phenolics and flavonoids, is globally consumed for its health benefit, but the biosynthesis pathways and metabolic profiles of its flavonoids are poorly characterized. Elucidating the flavonoid biosynthesis pathways would augment the broader use of jute, including targeted synthesis of its specific flavonoids. We reconstructed the core flavonoid biosynthesis pathways in jute by integrating transcriptome mining, HPLC and flavonoid histochemistry. In C. capsularis (white jute), the flavonoid biosynthesis pathways’ metabolic flux was driven toward the biosynthesis of proanthocyanidins that mediate the acquisition of abiotic stress tolerance. However, higher levels of flavonols in C. olitorius (tossa jute) render it more suitable for nutritional and medicinal use. Jute flavonoid extract exhibited in vitro inhibition of matrix metalloproteinase-2, suggesting its potential chemopreventive and immunity-boosting roles. Using the flavonoid biosynthesis pathways profiles of 93 plant species, we reconstructed the flavonoid biosynthesis pathways phylogeny based on distance-based clustering of reaction paths. This reaction-path flavonoid biosynthesis pathways phylogeny was quite distinct from that reconstructed using individual gene sequences. Our flavonoid biosynthesis pathways-based classification of flavonoid groups corroborates well with their chemical evolution, suggesting complex, adaptive evolution of flavonoid biosynthesis pathways, particularly in higher plants.

Key words

Corchorus spp. - flavonoid - Malvaceae - MMP-2 - pathway - phylogeny

Supplementary Material



Publication History

Received: 10 July 2021
Received: 08 October 2021

Accepted: 18 November 2021

Article published online:
07 February 2022

© 2022. The Author(s). This is an open access article published by Thieme under the terms of the Creative Commons Attribution-NonDerivative-NonCommercial-License, permitting copying and reproduction so long as the original work is given appropriate credit. Contents may not be used for commercial purposes, or adapted, remixed, transformed or built upon. (https://creativecommons.org/licenses/by-nc-nd/4.0/).

Georg Thieme Verlag KG
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  • References

  • 1 Falcone Ferreyra ML, Rius SP, Casati P. Flavonoids: biosynthesis, biological functions, and biotechnological applications. Front Plant Sci 2012; 3: 222
    CrossrefPubMedGoogle Scholar
  • 2 Kumar A, Kumar S, Bains S, Vaidya V, Singh B, Kaur R, Kaur J, Singh K. De novo transcriptome analysis revealed genes involved in flavonoid and vitamin c biosynthesis in Phyllanthus emblica (L.). Front Plant Sci 2016; 7: 1610
    CrossrefPubMedGoogle Scholar
  • 3 Raffa D, Maggio B, Raimondi MV, Plescia F, Daidone G. Recent discoveries of anticancer flavonoids. Eur J Med Chem 2017; 142: 213-228
    CrossrefPubMedGoogle Scholar
  • 4 Russo M, Moccia S, Spagnuolo C, Tedesco I, Russo GL. Roles of flavonoids against coronavirus infection. Chem-Biol Interac 2020; 328: 109211
    CrossrefPubMedGoogle Scholar
  • 5 Nyadanu D, AduAmoah R, Kwarteng AO, Akromah R, Aboagye LM, Adu-Dapaah H, Dansi A, Lotsu F, Tsama A. Domestication of jute mallow (Corchorus olitorius L.): ethnobotany, production constraints and phenomics of local cultivars in Ghana. Genet Resour Crop Evol 2017; 64: 1313-1329
    CrossrefPubMedGoogle Scholar
  • 6 Azuma K, Nakayama M, Koshioka M, Ippoushi K, Yamaguchi Y, Kohata K, Yamauchi Y, Ito H, Higashio H. Phenolic antioxidants from the leaves of Corchorus olitorius L. J Agric Food Chem 1999; 47: 3963-3966
    CrossrefPubMedGoogle Scholar
  • 7 Maeda G, Takara K, Wada K, Oki T, Masuda M, Ichiba T, Chuda Y, Ono H, Suda I. Evaluation of antioxidant activity of vegetables from Okinawa prefecture and determination of some antioxidative compounds. Food Sci Technol Res 2006; 12: 8-14
    CrossrefPubMedGoogle Scholar
  • 8 Park HY, Oh MJ, Kim Y, Choi I. Immunomodulatory activities of Corchorus olitorius leaf extract: Beneficial effects in macrophage and NK cell activation immunosuppressed mice. J Funct Foods 2018; 46: 220-226
    CrossrefPubMedGoogle Scholar
  • 9 Ola SS, Catia G, Marzia I, Francesco FV, Afolabi AA, Nadia M. HPLC/DAD/MS characterisation and analysis of flavonoids and cynnamoil derivatives in four Nigerian green-leafy vegetables. Food Chem 2009; 115: 1568-1574
    CrossrefPubMedGoogle Scholar
  • 10 Yakoub ARB, Abdehedi O, Jridi M, Elfalleh W, Nasri M, Ferchichi A. Flavonoids, phenols, antioxidant, and antimicrobial activities in various extracts from Tossa jute leave (Corchorus olitorius L.). Ind Crops Prod 2018; 118: 206-213
    CrossrefPubMedGoogle Scholar
  • 11 Robinson AR, Gheneim R, Kozak RA, Ellis DD, Mansfield SD. The potential of metabolite profiling as a selection tool for genotype discrimination in Populus . J Exp Bot 2005; 56: 2807-2819
    CrossrefPubMedGoogle Scholar
  • 12 Stushnoff C, Ducreux LJM, Hancock RD, Hedley PE, Holm DG, McDougall GJ, McNicol JW, Morris J, Morris WL, Sungurtas JA, Verrall SR, Zuber T, Taylor MA. Flavonoid profiling and transcriptome analysis reveals new gene-metabolite correlations in tubers of Solanum tuberosum L. J Exp Bot 2010; 61: 1225-1238
    CrossrefPubMedGoogle Scholar
  • 13 Satya P, Sarkar D, Vijayan J, Ray S, Ray DP, Mandal NA, Roy S, Sharma S, Bera A, Kar CS, Mitra J, Singh NK. Pectin biosynthesis pathways are adapted to higher rhamnogalacturonan formation in lignocellulosic jute (Corchorus spp.). Plant Growth Regul 2020; 93: 131-147
    CrossrefPubMedGoogle Scholar
  • 14 Furumoto T, Wang R, Okazaki K, Hasan AFMF, Ali MI, Kondo A, Fukui H. Antitumor promoters in leaves of jute (Corchorus capsularis and Corchorus olitorius). Food Sci Technol Res 2002; 8: 239-243
    CrossrefPubMedGoogle Scholar
  • 15 Taiwo BJ, Taiwo GO, Olubiyi OO, Fatokun AA. Polyphenolic compounds with anti-tumour potential from Corchorus olitorius (L.) Tiliaceae, a Nigerian leaf vegetable. Bioorganic Med Chem Lett 2016; 26: 3404-3410
    CrossrefPubMedGoogle Scholar
  • 16 Roy R, Yang J, Moses MA. Matrix metalloproteinases as novel biomarkers and potential therapeutic targets in human cancer. J Clin Oncol 2009; 27: 5287-5297
    CrossrefPubMedGoogle Scholar
  • 17 Demeule M, Brossard M, Pagé M, Gingras D, Béliveau R. Matrix metalloproteinase inhibition by green tea catechins. Biochim Biophys Acta 2000; 1478: 51-60
    CrossrefPubMedGoogle Scholar
  • 18 Markham KR. Distribution of flavonoids in the lower plants and its evolutionary significance. In: Harborne JB, ed. The Flavonoids. Advances in Research Since 1980. London: Chapman and Hall; 1988: 427-468
    CrossrefGoogle Scholar
  • 19 Campanella JJ, Smalley JV, Dempsey ME. A phylogenetic examination of the primary anthocyanin production pathway of the Plantae. Bot Stud 2014; 55: 10
    CrossrefPubMedGoogle Scholar
  • 20 Rausher MD, Miller RE, Tiffin P. Patterns of evolutionary rate variation among genes of the anthocyanin biosynthetic pathway. Mol Biol Evol 1999; 16: 266-274
    CrossrefPubMedGoogle Scholar
  • 21 Weißenborn S, Walther D. Metabolic pathway assignment of plant genes based on phylogenetic profiling – a feasibility study. Front Plant Sci 2017; 8: 1831
    CrossrefPubMedGoogle Scholar
  • 22 Hong SH, Kim TY, Lee SY. Phylogenetic analysis based on genome-scale metabolic pathway reaction content. Appl Microbiol Biotechnol 2004; 65: 203-210
    PubMedGoogle Scholar
  • 23 Forst CV, Schulten K. Phylogenetic analysis of metabolic pathways. J Mol Evol 2001; 52: 471-489
    CrossrefPubMedGoogle Scholar
  • 24 Heymans M, Singh AK. Deriving phylogenetic trees from the similarity analysis of metabolic pathways. Bioinformatics 2003; 19: i138-i146
    CrossrefPubMedGoogle Scholar
  • 25 Basak SL. Quantitative genetics of fibre yield and its components. In: Denton IR, ed. Review on the Genetics and Breeding of Jute. Dhaka: International Jute Organization; 1993: 51-95
    CrossrefGoogle Scholar
  • 26 Roy S, Lutfar LB. Bast fibres: jute. In: Kozlowski RM, ed. Handbook of Natural Fibres: Volume 1 Types, Properties and Factors Affecting Breeding and Cultivation. Cambridge: Woodhead Publishing Limited; 2012: 24-46
    CrossrefGoogle Scholar
  • 27 Arai Y, Watanabe S, Kimira M, Shimoi K, Mochizuki R, Kinae N. Dietary intakes of flavonols, flavones and isoflavones by Japanese women and the inverse correlation between quercetin intake and plasma LDL cholesterol concentration. J Nutr 2000; 130: 2243-2250
    CrossrefPubMedGoogle Scholar
  • 28 Jiang X, Shi Y, Fu Z, Li WW, Lai S, Wu Y, Wang Y, Liu Y, Gao L, Xia T. Functional characterization of three flavonol synthase genes from Camellia sinensis: roles in flavonol accumulation. Plant Sci 2020; 300: 11632
    CrossrefPubMedGoogle Scholar
  • 29 Kong CS, Kim YA, Kim MM, Park JS, Kim JA, Kim SK, Lee BJ, Nam TJ, Seo Y. Flavonoid glycosides isolated from Salicornia herbacea inhibit matrix metalloproteinase in HT1080 cells. Toxicol in Vitro 2008; 22: 1742-1748
    CrossrefPubMedGoogle Scholar
  • 30 Pereira SC, Parente JM, Belo VA, Mendes AS, Gonzaga NA, do Vale GT, Ceron CS, Tanus-Santos JE, Tirapelli CR, Castro MM. Quercetin decreases the activity of matrix metalloproteinase-2 and ameliorates vascular remodeling in renovascular hypertension. Atherosclerosis 2018; 270: 146e153
    CrossrefPubMedGoogle Scholar
  • 31 APG III. An update of the Angiosperm Phylogeny Group classification for the orders and families of flowering plants: APG III. Bot J Linn Soc 2009; 161: 105-121
    CrossrefPubMedGoogle Scholar
  • 32 Rausher MD. The evolution of flavonoids and their genes. In: Grotewold E, ed. The Science of Flavonoids. Springer; 2006: 175-211
    CrossrefGoogle Scholar
  • 33 Piatkowski BT, Imwattana K, Tripp EA, Weston DJ, Healey A, Schmutz J, Shaw AJ. Phylogenomics reveals convergent evolution of red-violet coloration in land plants and the origins of the anthocyanin biosynthetic pathway. Mol Phylogenet Evol 2020; 151: 106904
    CrossrefPubMedGoogle Scholar
  • 34 Wright KM, Rausher MD. The evolution of control and distribution of adaptive mutations in a metabolic pathway. Genetics 2010; 184: 483-502
    CrossrefPubMedGoogle Scholar
  • 35 Chakraborty A, Sarkar D, Satya P, Karmakar PG, Singh NK. Pathways associated with lignin biosynthesis in lignomaniac jute fibres. Mol Genet Genomics 2015; 290: 1523-1542
    CrossrefPubMedGoogle Scholar
  • 36 Satya P, Chakraborty A, Sarkar D, Karan M, Das D, Mandal NA, Saha D, Datta S, Ray S, Kar CS, Karmakar PG, Singh NK. Transcriptome profiling uncovers β-galactosidases of diverse domain classes influencing hypocotyl development in jute (Corchorus capsularis L.). Phytochemistry 2018; 156: 20-32
    CrossrefPubMedGoogle Scholar
  • 37 Moriya Y, Itoh M, Okuda S, Yoshizawa AC, Kanehisa M. KAAS: An automatic genome annotation and pathway reconstruction server. Nucleic Acids Res 2007; 35: W182-W185
    CrossrefPubMedGoogle Scholar
  • 38 Untergasser A, Cutcutache I, Koressaar T, Ye J, Faircloth BC, Remm M, Rozen SG. Primer3-new capabilities and interfaces. Nucleic Acids Res 2012; 40: e115
    CrossrefPubMedGoogle Scholar
  • 39 Peer WA, Brown DE, Tague BW, Muday GK, Taiz L, Murphy AS. Flavonoid accumulation patterns of transparent testa mutants of Arabidopsis . Plant Physiol 2001; 126: 536-548
    CrossrefPubMedGoogle Scholar
  • 40 Bhattacharyya N, Mondal S, Ali MN, Mukherjee R, Adhikari A, Chatterjee A. Activated salivary MMP-2 – a potential breast cancer marker. Open Confer Proc J 2017; 8: 22-32
    CrossrefPubMedGoogle Scholar
  • 41 Toth M, Fridman R. Assessment of gelatinases (MMP-2 and MMP-9) by gelatin zymography. Methods Mol Med 2001; 57: 163-174
    PubMedGoogle Scholar
  • 42 Mondal S, Bardhan K, Dutta A, Chatterjee A. Identification of vertebrate MMP-2 and MMP-9 like molecules in the aqueous extract of nasturtium (Tropaeolum majus) flowers, Bambusa balcooa Leaves and nayantara (Catharanthus roseus) flowers. J Tumor 2018; 6: 540-544
    PubMedGoogle Scholar
  • 43 Hammer Ø, Harper DAT, Ryan PD. Past: Paleontological Statistics Software Package for Education and Data Analysis. Palaeontologia Electronica 2001; 4: 1-9
    PubMedGoogle Scholar
  • 44 Lemoine F, Domelevo Entfellner JB, Wilkinson E, Correia D, Dávila Felipe M, De Oliveira T, Gascuel O. Renewing Felsenstein’s phylogenetic bootstrap in the era of big data. Nature 2018; 556: 452-456
    CrossrefPubMedGoogle Scholar
  • 45 Robinson O, Dylus D, Dessimoz C. Phylo.io: Interactive viewing and comparison of large phylogenetic trees on the web. Mol Biol Evol 2016; 33: 2163-2166
    CrossrefPubMedGoogle Scholar
  • 46 Robinson DF, Foulds LR. Comparison of phylogenetic trees. Math Biosci 1981; 53: 131-147
    CrossrefPubMedGoogle Scholar