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Differential regulation of fluorescent alkaloid metabolism between idioblast and lacticifer cells during leaf development in Catharanthus roseus seedlings

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Abstract

Bioactive specialized (secondary) metabolites are indispensable for plant development or adjustment to their surrounding environment. In many plants, these specialized metabolites are accumulated in specifically differentiated cells. Catharanthus roseus is a well-known medicinal plant known for producing many kinds of monoterpenoid indole alkaloids (MIAs). C. roseus has two types of specifically differentiated cells accumulating MIAs, so-called idioblast cells and laticifer cells. In this study, we compared each of the cells as they changed during seedling growth, and found that the fluorescent metabolites accumulated in these cells were differentially regulated. Analysis of fluorescent compounds revealed that the fluorescence observed in these cells was emitted from the compound serpentine. Further, we found that the serpentine content of leaves increased as leaves grew. Our findings suggest that idioblast cells and laticifer cells have different biological roles in MIA biosynthesis and its regulation.

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  • 12 March 2022

    Masami Yokota Hirai's ORCID number was missing and included in this version.

References

  • Asada K, Salim V, Masada-Atsumi S, Edmunds E, Nagatoshi M, Terasaka K, Mizukami H, De Luca V (2013) A 7-deoxyloganetic acid glucosyltransferase contributes a key step in Secologanin biosynthesis in Madagascar Periwinkle. Plant Cell 25:4123–4134

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Besseau S, Kellner F, Lanoue A, Thamm AMK, Salim V, Schneider B, Geu-Flores F, Höfer R, Guirimand G, Guihur A, Oudin A, Glevarec G, Foureau E, Papon N, Clastre M, Giglioli-Guivarc ’HN, St-Pierre B, Werck-Reichhart D, Burlat V, De Luca V, O’Connor SE, Courdavault V (2013) A pair of Tabersonine 16-Hydroxylases initiates the synthesis of Vindoline in an organ-dependent manner in Catharanthus roseus. Plant Physiol 163:1792–1803

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Brown RT, Leonard J, Sleigh SK (1978) The role of strictosidine in monoterpenoid indole alkaloid biosynthesis. Phytochemistry 17:899–900

    Article  CAS  Google Scholar 

  • Caputi L, Franke J, Farrow SC, Chung K, Payne RME, Nguyen TD, Dang TT, Soares Teto Carqueijeiro I, Koudounas K, Duge de Bernonville T, Ameyaw B, Jones DM, Vieira IJC, Courdavault V, O’Connor SE (2018) Missing enzymes in the biosynthesis of the anticancer drug vinblastine in Madagascar periwinkle. Science 360:1235–1239

    Article  CAS  PubMed  Google Scholar 

  • Carqueijeiro I, Guimaraes AL, Bettencourt S, Martinez-Cortes T, Guedes JG, Gardner R, Lopes T, Andrade C, Bispo C, Martins NP, Andrade P, Valentao P, Valente IM, Rodrigues JA, Duarte P, Sottomayor M (2016) Isolation of cells specialized in anticancer alkaloid metabolism by fluorescence-activated cell sorting. Plant Physiol 171:2371–2378

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Colinas M, Goossens A (2018) Combinatorial transcriptional control of plant specialized metabolism. Trends Plant Sci 23:324–336

    Article  CAS  PubMed  Google Scholar 

  • Das Gupta M, Nath U (2015) Divergence in patterns of leaf growth polarity is associated with the expression divergence of miR396. Plant Cell 27:2785–2799

    CAS  PubMed  PubMed Central  Google Scholar 

  • Dassonneville L, Bonjean K, De Pauw-Gillet M-C, Colson P, Houssier C, Quetin-Leclercq J, Angenot L, Bailly C (1999) Stimulation of topoisomerase II-mediated DNA cleavage by three DNA-intercalating plant alkaloids: Cryptolepine, Matadine, and Serpentine. Biochemistry 38:7719–7726

    Article  CAS  PubMed  Google Scholar 

  • De Luca V, Balsevich J, Tyler RT, Kurz WG (1987) Characterization of a novel N-methyltransferase (NMT) from Catharanthus roseus plants: Detection of NMT and other enzymes of the indole alkaloid biosynthetic pathway in different cell suspension culture systems. Plant Cell Rep 6:458–461

    Google Scholar 

  • Esau K (1965) Plant anatomy. John Wiley & Sons, Inc., New York, London, Sydney

    Google Scholar 

  • Foster AS (1956) Plant idioblasts: remarkable examples of cell specialization. Protoplasma 46:10

    Article  Google Scholar 

  • Franceschi V (2001) Calcium oxalate in plants. Trends Plant Sci 6:331

    Article  CAS  PubMed  Google Scholar 

  • Geerlings A, Ibanez MM, Memelink J, van Der Heijden R, Verpoorte R (2000) Molecular cloning and analysis of strictosidine beta-D-glucosidase, an enzyme in terpenoid indole alkaloid biosynthesis in Catharanthus roseus. J Biol Chem 275:3051–3056

    Article  CAS  PubMed  Google Scholar 

  • Geu-Flores F, Sherden NH, Courdavault V, Burlat V, Glenn WS, Wu C, Nims E, Cui Y, O’Connor SE (2012) An alternative route to cyclic terpenes by reductive cyclization in iridoid biosynthesis. Nature 492:138–142

    Article  CAS  PubMed  Google Scholar 

  • Hao B (2000) Laticifer differentiation in Hevea brasiliensis: induction by exogenous jasmonic acid and linolenic acid. Ann Bot 85:37–43

    Article  CAS  Google Scholar 

  • Hara T, Kobayashi E, Ohtsubo K, Kumada S, Kanazawa M, Abe T, Itoh RD, Fujiwara MT (2015) Organ-level analysis of idioblast patterning in Egeria densa Planch. Leaves PLOS ONE 10:e0118965

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Hisiger S, Jolicoeur M (2007) Analysis of Catharanthus roseus alkaloids by HPLC. Phytochem Rev 6:207–234

    Article  CAS  Google Scholar 

  • Irmler S, Schröder G, St-Pierre B, Crouch NP, Hotze M, Schmidt J, Strack D, Matern U, Schröder J (2000) Indole alkaloid biosynthesis in Catharanthus roseus: new enzyme activities and identification of cytochrome P450 CYP72A1 as secologanin synthase. Plant J 24:797–804

    Article  CAS  PubMed  Google Scholar 

  • Kanazawa T, Morinaka H, Ebine K, Shimada TL, Ishida S, Minamino N, Yamaguchi K, Shigenobu S, Kohchi T, Nakano A, Ueda T (2020) The liverwort oil body is formed by redirection of the secretory pathway. Nature Commun 11(1):6152

    Article  CAS  Google Scholar 

  • Leete E, Ueda S (1966) Biosynthesis of the vinca alkaloids. The incorporation of geraniol-3-14C into catharanthine and vindoline. Tetrahedron Lett 7:4915–4918

    Article  Google Scholar 

  • Liscombe DK, Usera AR, O’Connor SE (2010) Homolog of tocopherol C methyltransferases catalyzes N methylation in anticancer alkaloid biosynthesis. Proc Natl Acad Sci U S A 107:18793–18798

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Luijendijk TJC, Stevens LH, Verpoorte R (1998) Purification and characterisation of strictosidine β-d-glucosidase from Catharanthus roseus cell suspension cultures. Plant Physiol Bioch 36:419–425

    Article  CAS  Google Scholar 

  • Mahlberg PG (1961) Embryogeny and histogenesis in Nerium oleander. II. Origin and development of the nonArticulated laticifer. Am J Bot 48:10

    Article  Google Scholar 

  • Mersey BG, Cutler AJ (1986) Differential distribution of specific indole alkaloids in leaves of Catharanthus-Roseus. Can J Bot 64:1039–1045

    Article  CAS  Google Scholar 

  • Miettinen K, Dong L, Navrot N, Schneider T, Burlat V, Pollier J, Woittiez L, van der Krol S, Lugan R, Ilc T, Verpoorte R, Oksman-Caldentey KM, Martinoia E, Bouwmeester H, Goossens A, Memelink J, Werck-Reichhart D (2014) The seco-iridoid pathway from Catharanthus roseus. Nat Commun 5:3606

    Article  PubMed  CAS  Google Scholar 

  • Monachino J (1954) Rauvolfia serpentina—its history, botany and medical use. Economic Bot 8:349–365

    Article  CAS  Google Scholar 

  • Noe W, Mollenschott C, Berlin J (1984) Tryptophan decarboxylase from Catharanthus roseus cell suspension cultures: purification, molecular and kinetic data of the homogenous protein. Plant Mol Biol 3:281–288

    Article  CAS  PubMed  Google Scholar 

  • Pan Q, Mustafa NR, Tang K, Choi YH, Verpoorte R (2015) Monoterpenoid indole alkaloids biosynthesis and its regulation in Catharanthus roseus: a literature review from genes to metabolites. Phytochem Rev 15:221–250

    Article  CAS  Google Scholar 

  • Pfitzner A, Stockigt J (1982) Partial-purification and characterization of Geissoschizine dehydrogenase from suspension-cultures of Catharanthus-Roseus. Phytochemistry 21:1585–1588

    Article  CAS  Google Scholar 

  • Power R, Kurz WGW, De Luca V (1990) Purification and characterization of acetylcoenzyme A: deacetylvindoline 4-O-acetyltransferase from Catharanthus roseus. Archives Biochem Biophys 279:370–376

    Article  CAS  Google Scholar 

  • Qu Y, Easson ML, Froese J, Simionescu R, Hudlicky T, De Luca V (2015) Completion of the seven-step pathway from tabersonine to the anticancer drug precursor vindoline and its assembly in yeast. Proc Natl Acad Sci U S A 112:6224–6229

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Qu Y, Easson MEAM, Simionescu R, Hajicek J, Thamm AMK, Salim V, De Luca V (2018) Solution of the multistep pathway for assembly of corynanthean, strychnos, iboga, and aspidosperma monoterpenoid indole alkaloids from 19E-geissoschizine. Proc Natl Acad Sci USA 115:3180–3185

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Renaudin JP (1985) Extraction and fluorimetric detection after high-performance liquid-chromatography of Indole alkaloids from cultured-cells of Catharanthus-Roseus. Physiol Veg 23:381–388

    CAS  Google Scholar 

  • Salim V, Yu F, Altarejos J, De Luca V (2013) Virus-induced gene silencing identifies Catharanthus roseus7-deoxyloganic acid-7-hydroxylase, a step in iridoid and monoterpene indole alkaloid biosynthesis. Plant J 76:754–765

    Article  CAS  PubMed  Google Scholar 

  • Salim V, Wiens B, Masada-Atsumi S, Yu F, De Luca V (2014) 7-Deoxyloganetic acid synthase catalyzes a key 3 step oxidation to form 7-deoxyloganetic acid in Catharanthus roseus iridoid biosynthesis. Phytochemistry 101:23–31

    Article  CAS  PubMed  Google Scholar 

  • Schneider CA, Rasband WS, Eliceiri KW (2012) NIH Image to ImageJ: 25 years of image analysis. Nat Methods 9:671–675

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Stavrinides A, Evangelos Foureau E, Caputi L, Kellner F, Courdavault V, Sarah, (2015) Unlocking the diversity of alkaloids in Catharanthus roseus: nuclear localization suggests metabolic channeling in secondary metabolism. Chem Biol 22:336–341

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Stöckigt J, Zenk MH (1977) Strictosidine (isovincoside): the key intermediate in the biosynthesis of monoterpenoid indole alkaloids. J Chem Soc Chem Commun 18:646–648

    Article  Google Scholar 

  • St-Pierre B, De Luca V (1995) A Cytochrome P-450 Monooxygenase catalyzes the first step in the conversion of Tabersonine to Vindoline in Catharanthus roseus. Plant Physiol 109:131–139

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • St-Pierre B, Laflamme P, Alarco A-M, Luca DV E (1998) The terminal O-acetyltransferase involved in vindoline biosynthesis defines a new class of proteins responsible for coenzyme A-dependent acyl transfer. Plant J 14:703–713

    Article  CAS  PubMed  Google Scholar 

  • St-Pierre B, Vazquez-Flota FA, Luca VD (1999) Multicellular compartmentation of Catharanthus roseus alkaloid biosynthesis predicts intercellular translocation of a pathway intermediate. Plant Cell 11:14

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Suire C (2000) A comparative, transmission-electron microscopic study on the formation of oil-bodies in liverworts. J Hattori Bot Lab:209–232

  • Svoboda GH, Gorman M, Neuss N, Barnes AJ (1961) Alkaloids of Vinca rosea Linn. (Catharanthus roseus G. Don.) VIII. J Pharm Sci 50:409–413

    Article  CAS  Google Scholar 

  • Tan D, Hu X, Fu L, Kumpeangkeaw A, Ding Z, Sun X, Zhang J (2017) Comparative morphology and transcriptome analysis reveals distinct functions of the primary and secondary laticifer cells in the rubber tree. Sci Rep 7(1):3126

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Tatsis EC, Carqueijeiro I, Duge de Bernonville T, Franke J, Dang TT, Oudin A, Lanoue A, Lafontaine F, Stavrinides AK, Clastre M, Courdavault V, O’Connor SE (2017) A three enzyme system to generate the Strychnos alkaloid scaffold from a central biosynthetic intermediate. Nat Commun 8:316

    Article  PubMed  PubMed Central  CAS  Google Scholar 

  • Treimer JF, Zenk MH (1979) Purification and properties of strictosidine synthase, the key enzyme in indole alkaloid formation. Eur J Biochem 101:225–233

    Article  CAS  PubMed  Google Scholar 

  • Vazquez-Flota F, De Carolis E, Alarco AM, De Luca V (1997) Molecular cloning and characterization of desacetoxyvindoline-4-hydroxylase, a 2-oxoglutarate dependent-dioxygenase involved in the biosynthesis of vindoline in Catharanthus roseus (L.) G. Don. Plant Mol Biol 34:935–948

    Article  CAS  PubMed  Google Scholar 

  • Warsi SAR (2017) Phytochemical screening and antioxidant activity of ethanolic extract and ethyl acetate fraction from basil leaf (Ocimum basilicum L.) by DPPH radical scavenging method. In: IOP conference series: materials science engineering, vol 259, p 012008

  • Yamamoto K, Takahashi K, Mizuno H, Anegawa A, Ishizaki K, Fukaki H, Ohnishi M, Yamazaki M, Masujima T, Mimura T (2016) Cell-specific localization of alkaloids in Catharanthus roseus stem tissue measured with Imaging MS and Single-cell MS. Proc Natl Acad Sci USA 113:3891–3896

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yamamoto K, Takahashi K, Caputi L, Mizuno H, Rodriguez-Lopez CE, Iwasaki T, Ishizaki K, Fukaki H, Ohnishi M, Yamazaki M, Masujima T, O’Connor SE, Mimura T (2019) The complexity of intercellular localisation of alkaloids revealed by single-cell metabolomics. New Phytol 224:848–859

    Article  CAS  PubMed  Google Scholar 

  • Yamamoto K, Grzech D, Koudounas K, Stander EA, Caputi L, Mimura T, Courdavault V, O’Connor SE (2021) Improved virus-induced gene silencing allows discovery of a serpentine synthase gene in Catharanthus roseus. Plant Physiol 187(2):846–857

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yoder LR, Mahlberg PG (1976) Reactions of alkaloid and histochemical indicators in laticifers and specialized parenchyma cells of Catharanthus roseus (Apocynaceae). Am J Bot 63:7

    Article  Google Scholar 

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Acknowledgements

We greatly appreciate Dr. Ryosuke Munakata (Kyoto University, Japan) and Dr. Shuichi Sakaguchi (Nara women’s University, Japan) for detailed discussion, MSc. Ryoko Kusakabe (Kobe University, Japan), Prof. Masaaki Miyamoto (Kobe University, Japan), Mr. Muneo Sato (RIKEN Center for Sustainable Resource Science), Dr. Aya Anegawa (Agilent Technology Japan), MSc. Delia Ayled Serna Guerrero (Max Planck Institute for Chemical Ecology) and Dr. Maritta Kunert (Max Planck Institute for Chemical Ecology) for the support with MS measurement, MSc. Ayuko Kuwahara (RIKEN Center for Sustainable Resource Science) for the support for experiments, Greenhouse staff (Max Planck Institute for Chemical Ecology), particularly Ms. Eva Rothe for the support on preparing many cultivars of C. roseus plants, Dr. Sarah O’Connor (Max Planck Institute for Chemical Ecology) for supporting experiments, and Prof. Hiroshi Matsufuji (Nihon University, Japan) for the support with fluorescent measurement. We also would like to offer our special thanks to Prof. Rob Reid (University of Adelaide, Australia) for his kind discussion and correction of this manuscript.

Funding

This work was supported by a Grant-in-Aid for Scientific Research of Innovative Areas from the Japanese Ministry of Education, Sports, Culture, Science, and Technology on ‘‘Perceptive plants (22120006)’’ and “Plant-structure-opt (18H05493)”, and JSPS KAKENHI grant Number 16H04807 to TM. This work was also supported by RIKEN Junior Research Associate Program.

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Uzaki, M., Yamamoto, K., Murakami, A. et al. Differential regulation of fluorescent alkaloid metabolism between idioblast and lacticifer cells during leaf development in Catharanthus roseus seedlings. J Plant Res 135, 473–483 (2022). https://doi.org/10.1007/s10265-022-01380-1

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