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Expanding the laticifer knowledge in Cannabaceae: distribution, morphology, origin, and latex composition

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Abstract

Cannabaceae is a known family because of the production of cannabinoids in laticifers and glandular trichomes of Cannabis sativa. Laticifers are latex-secreting structures, which in Cannabaceae were identified only in C. sativa and Humulus lupulus. This study aimed to expand the knowledge of laticifers in Cannabaceae by checking their structural type and distribution, and the main classes of substances in the latex of Celtis pubescens, Pteroceltis tatarinowii, and Trema micrantha. Such information is also updated for C. sativa. Samples of shoot apices, stems, leaves, and flowers were processed for anatomical, histochemical, ultrastructural, and cytochemical analyses. Laticifers are articulated unbranched in all species instead of non-articulated as previously described for the family. They occur in all sampled organs. They are thick-walled, multinucleate, with a large vacuole and a peripheral cytoplasm. The cytoplasm is rich in mitochondria, endoplasmic reticulum, dictyosomes, ribosomes, and plastids containing starch grains and oil drops. Pectinase and cellulase activities were detected in the laticifer wall and vacuole, confirming its articulated origin, described by first time in the family. These enzymes promote the complete dissolution of the laticifer terminal walls. The latex contains proteins, lipids, and polysaccharides in addition to phenolics (C. sativa) and terpenes (C. pubescens, T. micrantha). The presence of laticifers with similar distribution and morphology supports the recent insertion of Celtis, Pteroceltis, and Trema in Cannabaceae. The articulated type of laticifer found in Cannabaceae, Moraceae, and Urticaceae indicates that the separation of these families by having distinct laticifer types should be reviewed.

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References

  • Allen RD, Nessler CL (1984) Cytochemical localization of pectinase activity in laticifers of Nerium oleander L. Protoplasma 119:74–78

    CAS  Google Scholar 

  • Andre CM, Hausman J-F, Guerriero G (2016) Cannabis sativa: the plant of the thousand and one molecules. Front Plant Sci 7:1–17

    Google Scholar 

  • Arruda VLV, Sazima M (1988) Polinização e reprodução de Celtis iguanaea (Jacq.) Sarg. (Ulmaceae), uma espécie anemófila. Brazilian Journal Botany 11:113–122

  • Ashton CH (2001) Pharmacology and effects of Cannabis: a brief review. Br J Psychiatry 178:101–106

    CAS  PubMed  Google Scholar 

  • Bal AK (1974) Cellulase. In: Haya MA (ed) Electron microscopy of enzymes, vol 3. Van Nostrand Reinhold, New York, pp 68–79

    Google Scholar 

  • Barth O, Macieira E, Corte-Real S (1975) Morfologia do polen anemofilo alergisante no Brasil. Memorias Instituto Oswaldo Cruz 73:141–150

  • Cai X, Li W, Yin L (2009) Ultrastructure and cytochemical localization of acid phosphatase of laticifers in Euphorbia kansui Liou. Protoplasma 238:3–10

    CAS  PubMed  Google Scholar 

  • Canaveze Y, Machado SR (2016) The occurrence of intrusive growth associated with articulated laticifers in Tabernaemontana catharinensis a. DC., a new record for Apocynaceae. Int J Plant Sci 177:458–467

  • Croteau R, Kutchan TM, Lewis NG (2000) Natural products (secondary metabolites). In: Buchanan BB, Gruissem W, Jones RL (eds) Biochemistry and molecular biology of plants. Wiley, Hoboken, pp 1250–1318

    Google Scholar 

  • Culley TM, Weller SG, Sakai AK (2002) The evolution of wind pollintion in angiosperms. Trends Ecol Evol 17:361–369

    Google Scholar 

  • David R, Carde JP (1964) Coloration différentielle des inclusions lipidiques et terpeniques des pseudophylles du pin maritime au moyen du reactif Nadi. C R Acad Sci 258:1338–1340

    CAS  Google Scholar 

  • Demarco D, Castro MM (2008) Laticíferos articulados anastomosados em espécies de Asclepiadeae (Asclepiadoideae, Apocynaceae) e suas implicações ecológicas. Rev Bras Bot 31:701–713

    Google Scholar 

  • Demarco D, Kinoshita LS, Castro MM (2006) Laticíferos articulados anastomosados: novos registros para Apocynaceae. Rev Bras Bot 29:133–144

    Google Scholar 

  • Dickison W (2000) Integrative plant anatomy. Academic Press, San Diego

    Google Scholar 

  • Evert RF (2006) Esau’s plant anatomy: meristems, cells, and tissues of the plant body: their structure, function, and development. Wiley, Hoboken

    Google Scholar 

  • Fahn A (1979) Secretory tissues in plants. Academic Press, London

    Google Scholar 

  • Fahn A (1990) Plant Anatomy. Butterworth-Heinemann, London

    Google Scholar 

  • Friedman J, Barrett SCH (2009) Wind of change: new insights on the ecology and evolution of pollination and mating in wind-pollinated plants. Ann Bot 103:1515–1527

    PubMed  PubMed Central  Google Scholar 

  • Furr M, Mahlberg PG (1981) Histochemical analyses of laticifers and glandular trichomes in Cannabis sativa. J Nat Prod 44:153–159

    Google Scholar 

  • Gagne SJ, Stout JM, Liu E, Boubakir Z, Clark SM, Page JE (2012) Identification of olivetolic acid cyclase from Cannabis sativa reveals a unique catalytic route to plant polyketides. PNAS 31:12811–12816

    Google Scholar 

  • Giordani R (1980) Dislocation du plasmalemme et libération de vésicules pariétales lors de la degradation des parois terminales durant la différenciation des laticifères articulés. Biol Cell 38:231–236

    CAS  Google Scholar 

  • Hagel JM, Yeung EC, Facchini PJ (2008) Got milk? The secret life of laticifers. Trends Plant Sci:1360–1385

  • Happyana N, Agnolet S, Muntendam R, Van Dam A, Schneider B, Kayser O (2013) Analysis of cannabinoids in laser-microdissected trichomes of medicinal Cannabis sativa using LCMS and cryogenic NMR. Phytochemistry 87:51–59

    CAS  PubMed  Google Scholar 

  • Heinrich G (1970) Elektronenmikroskopische Untersuchung der Milchrohren von Ficus elastica. Protoplasma 70:317–323

    Google Scholar 

  • Hill MN, Patel S, Campolongo P, Tasker JG, Wotjak CT, Bains JS (2010) Functional interactions between stress and the endocannabinoid system: from synaptic signaling to behavioral output. J Neurosci 30:14980–14986

    CAS  PubMed  PubMed Central  Google Scholar 

  • Honório KM, Arroio A, Silva ABF (2006) Aspectos terapêuticos de compostos da planta Cannabis sativa. Química Nova 29:318–325

  • Jacomassi E, Moscheta IS, Machado SR (2007) Morfoanatomia e histoquímica de Brosimum gaudichaudii Trécul (Moraceae). Acta Bot Bras 21:575–597

    Google Scholar 

  • Jacomassi E, Moscheta IS, Machado SR (2010) Morfoanatomia e histoquímica de órgãos reprodutivos de Brosimum gaudichaudii (Moraceae). Braz J Bot 33:115–129

    Google Scholar 

  • Jensen WE (1962) Botanical histochemistry: principles and practice. W. H. Freeman and Co, San Francisco

    Google Scholar 

  • Johansen DA (1940) Plant Microtechnique. McGraw-Hill Book Co. Inc, New York

    Google Scholar 

  • Judd WS, Campbell CS, Kellogg EA, Stevens PF, Donoghue MJ (2009) Sistemática vegetal: um enfoque filogenético, 3ª edn. Artmed, Porto Alegre

    Google Scholar 

  • Karnovsky MJ (1965) A formaldehyde-glutaraldehyde fixative of hight osmolality for use in electron microscopy. J Cell Biol 27:137–138

    Google Scholar 

  • Kim E-S, Mahlberg PG (1991) Secretory cavity development glandular trichomes of Cannabis sativa L. (Cannabaceae). Am J Bot 78:220–229

    Google Scholar 

  • Kim E-S, Mahlberg PG (1997) Immunochemical localization of tetrahydrocannabinol of (THC) in cryofixed glandular trichomes of Cannabis (Cannabaceae). Am J Bot 84:336–342

    CAS  PubMed  Google Scholar 

  • Kitajima S, Taira T, Oda K, Yamato KT, Inukai Y, Hori Y (2012) Comparative study of gene expression and major proteins function of laticifers in lignified and unlignified organs of mulberry. Planta 235:589–601

    CAS  PubMed  Google Scholar 

  • Liang S, Wang H, Yang M, Wu H (2009) Sequential actions of pectinases and cellulases during secretory cavity formation in Citrus fruits. Trees 23:19–27

    CAS  Google Scholar 

  • Lillie RD (1965) Histopathologic technic and practical histochemistry. McGraw-Hill Book Company, New York

    Google Scholar 

  • Lopes KLB, Thadeo M, Azevedo AA, Soares AA, Meira RMSA (2009) Articulated laticifers in the vegetative organs of Mandevilla atroviolacea (Apocynaceae, Apocynoideae). Botany 87:202–209

    Google Scholar 

  • Mace M, Howell C (1974) Histochemistry and identification of condensed tannin precursors in roots of cotton seedlings. Can J Bot 52:2423–2426

    CAS  Google Scholar 

  • Machado AV, Santos M (2004) Morfo-anatomia foliar comparativa de espécies conhecidas como espinheira-santa: Maytenus ilicifolia (Celastraceae), Sorocea bonplandii (Moraceae) e Zollernia ilicifolia (Leguminosae). Insula 33:01–19

    Google Scholar 

  • Mahlberg PG (1993) Laticifers: an historical perspective. Bot Rev 59:1–23

    Google Scholar 

  • Mahlberg PG, Kim ES (2004) Accumulation of cannabinoids in glandular Trichomes of Cannabis (Cannabaceae). Journal Industrial Hemp 9(1):15–35

  • Marinho CR, Teixeira SP (2019a) Novel reports of laticifers in Moraceae and Urticaceae: revisiting synapomorphies. Plant Syst Evol 305(1):13–31

    CAS  Google Scholar 

  • Marinho CR, Teixeira SP (2019b) Cellulases and pectinases act together on the development of articulated laticifers in Ficus montana and Maclura tinctoria (Moraceae). Protoplasma 256:1093–1107

    CAS  PubMed  Google Scholar 

  • Marinho CR, Pereira RAS, Peng Y-Q, Teixeira SP (2018) Laticifer distribution in fig inflorescence and its potential role in the fig-fig wasp mutualism. Acta Oecol 90:160–167

    Google Scholar 

  • Mechoulam R, Gaoni Y (1967) Recent advances in the chemistry of hashish. Fortschr Chem Org Naturst 25:175–213

    CAS  PubMed  Google Scholar 

  • Meeuse ADJ (1942) A study of intercellular relationships among vegetable cells with special reference to sliding growth and to cell shape. Recueil des Travaux Botaniques Neerlandais 38:18–140

  • Mesquita JF (1969) Electron microscope study of the origin and development of the vacuoles in root-tip cells of Lupinus albus L. J Ultrastruct Res 26:242–250

    CAS  PubMed  Google Scholar 

  • Mesquita JF, Dias JDS (1984) Ultrastructural and cytochemical study of the laticifers of Cannabis sativa L. Bol Soc Brot 57:337–356

  • Metcalfe CR (1966) Distribution of latex in the plant kingdom. Econ Bot 21:115–127

    Google Scholar 

  • Milanez FR (1954) Sobre os laticíferos foliares de Ficus retusa. Rodriguésia 28(29):159–192

    Google Scholar 

  • Miller N (1970) The genera of Cannabaceae in the southeastern United States. Journal of the Arnold Arboretum 51:185–203

  • Nessler C, Mahlberg P (1977) Ontogeny and cytochemistry of alkaloidal vesicles in laticifers of Papaver somniferum L. (Papaveraceae). Am J Bot 64:541–551

    Google Scholar 

  • Nessler CL, Mahlberg PG (1981) Cytochemical localization of cellulase activity in articulated, anastomosing laticifers of Papaver somniferum L. (Papaveraceae). Am J Bot 68:730–732

    Google Scholar 

  • O’Brien TP, Feder N, McCully ME (1964) Polychromatic staining of plant cell walls by toluidine blue O. Protoplasma 59:368–373

    Google Scholar 

  • Pearse AGE (1985) Histochemistry: theoretical and applied. C. Livingstone, Edinburgh

    Google Scholar 

  • Pilatzke-Wunderlich I, Nessler CL (2001) Expression and activity of cell-wall-degrading enzymes in the latex of opium poppy, Papaver somniferum L. Plant Mol Biol 45:567–576

    CAS  PubMed  Google Scholar 

  • Quintanar A, Castrejón JLZ, Lopéz C, Salgado-Ugarte IH (2004) Anatomía e histoquímica de la corteza de cinco especies de Moraceae. Polibotánica:15–38

  • Rachmilevitz T, Fahn A (1982) Ultrastructure and development of the laticifers of Ficus carica L. Ann Bot 49:13–22

    Google Scholar 

  • Ramos MV, Demarco D, Souza ICC, Freitas CDT (2019) Laticifers, Latex, and Their Role in Plant Defense. Trends Plant Sci 24(6): 553–567

  • Sheldrake AR (1969) Cellulase in latex and its possible significance in cell differentiation. Planta 89:82–84

    CAS  PubMed  Google Scholar 

  • Sirikantaramas S, Taura F (2017) Cannabinoids: biosynthesis and biotechnological applications. In: Chandra S, Lata H, ElSohly M (eds) Cannabis sativa L. Botany and Biotechnology. Springer, Cham, pp 183–206

    Google Scholar 

  • Smith FH, Smith EC (1942) Anatomy of the inferior ovary of Darbya. Am J Bot 29(6):464–471

    Google Scholar 

  • Sytsma KJ, Morawetz J, Pires JC, Nepokroeff M, Conti E, Zjhra M, Hall JC, Chase MW (2002) Urticalean Rosids: circumscription, Rosid ancestry, and phylogenetics based on rbcL, trnL-F, and ndhF sequences. Am J Bot 89(9):1531–1546

    CAS  PubMed  Google Scholar 

  • Topper SMC, Koek-Noorman J (1980) The occurrence of axial latex tubes in the secondary xylem of some species of Artocarpus J.R. & G. Forster (Moraceae). IAWA Journal 1:113–119

  • Van Veenendaal WLH, Den Outer RW (1990) Distribution and development of the non-articulated branched laticifers on Morus nigra L. (Moraceae). Acta Botanica Neerlandica 39:285–296

  • Vidal BC (1970) Dichroism in collagen bundles stained with xylidine-Ponceau 2R. Ann Histochim 15:289–296

    Google Scholar 

  • Wang XY, Guo GQ, Nie XW, Zheng GC (1998) Cytochemical localization of cellulase activity in pollen mother cells of David lily during meiotic prophase I and its relation to secondary formation of plasmodesmata. Protoplasma 204:128–138

    CAS  Google Scholar 

  • Williamson EM, Evans FJ (2000) Cannabinoids in clinical practice. Drugs 60:1303–1314

    CAS  PubMed  Google Scholar 

  • Wilson K, Mahlberg P (1978) Ultrastructure of non-articulated laticifers in mature embryos and seedlings of Asclepias syriaca L. (Asclepiadaceae). Am J Bot 65:98–109

    Google Scholar 

  • Wilson KJ, Nessler CL, Mahlberg PG (1976) Pectinase in Asclepias latex and its possible role in Laticifer growth and development. Am J Bot 63(8):1140–1144

    CAS  Google Scholar 

  • Yang M-Q, Van Velzen R, Bakker FT, Sattarian A, Li D, Yi T (2013) Molecular phylogenetics and character evolution of Cannabaceae. Taxon 62:473–485

    Google Scholar 

  • Yu CH, Guo GQ, Nie XW, Zheng GC (2004) Cytochemical localization of pectinase activity in pollen mother cells of tobacco during meiotic prophase I and its relation to the formation of secondary plasmodesmata and cytoplasmic channels. Acta Bot Sin 46:1443–1453

    Google Scholar 

  • Zhang Q, Wang D, Zhang H, Wang M, Li P, Fang X, Cai X (2018) Detection of autophagy processes during the development of nonarticulated laticifers in Euphorbia kansui Liou. Planta 247:845–861

    CAS  PubMed  Google Scholar 

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Acknowledgments

The authors thank Edimárcio da Silva Campos (FCFRP/USP), Maria Dolores Seabra Ferreira, and José Augusto Maulin (FMRP/USP) for technical assistance and Elettra Greene for English review.

Funding

This work was supported by Sao Paulo Research Foundation (FAPESP) (process number 2014/07453-3, 2018/03691-8), National Council for Scientific and Technological Development (CNPq) (process number 303493/2015-1; 156,025/2017-5), and Coordenação de Aperfeiçoamento de Pessoal de Nível Superior (CAPES) (code number 001).

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Correspondence to Simone Pádua Teixeira.

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Leme, F.M., Borella, P.H., Marinho, C.R. et al. Expanding the laticifer knowledge in Cannabaceae: distribution, morphology, origin, and latex composition. Protoplasma 257, 1183–1199 (2020). https://doi.org/10.1007/s00709-020-01500-5

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