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Oil-resin glands in Velloziaceae flowers: structure, ontogenesis and secretion

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Abstract

Many Velloziaceae flowers present conspicuous glands, whose taxonomic value has already been highlighted. However, until now, their micromorphology, anatomy and ultrastructure have not been investigated, nor have the natures and possible functions of their exudates. Our aim was to investigate distribution, ontogenesis, structure, and secretion mechanisms of glands of Barbacenia flava and Vellozia intermedia and to discuss their possible ecological functions. Samples were prepared according to standard methods for investigations of plant anatomy, scanning electron microscopy, and transmission electron microscopy. Histochemical tests were performed, and focal field observations were made in the study site. The capitate stalked glands on the pedicel, tepals and hypanthium are covered by a sticky secretion that is released in the gland head through the outer periclinal cell walls and cuticle. Secretions are produced in the epidermal and subepidermal cells that contain structural components typical of mixed, mainly lipophilic secretions. Bacteria were found inside the oil-resin gland cells of both species. The Meliponina bees Trigona spinipes and Tetragonisca angustula were observed collecting resin from both species, but were not involved in pollination. Our observations clearly indicate that flower glands of B. flava and V. intermedia are oil-resin secreting and remain active in secretion from very young buds, through to immature fruit. New, smaller glands replace senescent glands by divisions near the base of the original stalk cells. Oil-resin glands have a number of different, but important functions, including the interaction with Meliponina bees, protection against water loss and high temperatures by ultraviolet screening, and anti-desiccant properties.

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References

  • Altenburger R, Matile P (1990) Further observations on rhythmic emission of fragrance in flowers. Planta 180:194–197

    Article  CAS  PubMed  Google Scholar 

  • Alves RJV, Silva NG, Oliveira JA, Medeiros D (2014a) Circumscribing campo rupestre—megadiverse Brazilian rocky montane savannas. Braz J Biol 74:355–362

    Article  CAS  PubMed  Google Scholar 

  • Alves RJV, Guimarães AR, Rezende CM, Braga LS, Silva NGA (2014b) New giant Vellozia (Velloziaceae) from Minas Gerais, Brazil with comments on the V. compacta complex and conservation. Phytotaxa 172:13–21

    Article  Google Scholar 

  • Amaral LIV, Pereira MF, Cortelazzo AL (2001) Formação das substâncias de reserva durante o desenvolvimento de sementes de urucum (Bixa orellana L.—Bixaceae). Acta Bot Brasil 15:125–132

    Article  Google Scholar 

  • Armbruster WS (1984) The role of resin in angiosperm pollination: ecological and chemical considerations. Amer J Bot 71:1149–1160

    Article  Google Scholar 

  • Armbruster WS, Webster GL (1979) Pollination of two species of Dalechampia (Euphorbiaceae) in Mexico by euglossine bees. Biotropica 11:278–283

    Article  Google Scholar 

  • Ascensão L, Marques N, Pais MS (1997) Peltate glandular trichomes of Leonotis leonurus leaves: ultrastructure and histochemical characterization of secretions. Int J Pl Sci 158:249–258

    Article  Google Scholar 

  • Beltran-Garcia MJ, White JF Jr, Prado FM, Prieto KR, Yamaguchi LF, Torres MS, Di Mascio P (2014) Nitrogen acquisition in Agave tequilana from degradation of endophytic bacteria. Sci Rep 4:6938. doi:10.1038/srep06938

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cheniclet C, Carde JP (1985) Presence of leucoplasts in secretory cells and of monoterpenes in the essential oil: a correlative study. Israel J Bot 34:219–238

    Google Scholar 

  • Cortelazzo AL, Vidal BC (1991) Soybean seed proteins: detection in situ and mobilization during germination. Braz J Bot 14:27–34

    CAS  Google Scholar 

  • Dafni A, Keavan PG, Husband BC (2005) Practical pollination biology. Enviroquest Ltda, Cambridge

    Google Scholar 

  • Dell B (1977) Distribution and function of resins and glandular hairs in Western Australian plants. J Roy Soc Western Australia 59:119–123

    Google Scholar 

  • Dell B, McComb AJ (1987) Plant resins—their formation, secretion and possible functions. Advances Bot Res 6:277–316

    Article  Google Scholar 

  • Evert RF (2006) Esau’s plant anatomy: meristems, cells, and tissues of the plant body: their structure, function, and development, 3rd edn. Wiley, Hoboken

    Book  Google Scholar 

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

    Google Scholar 

  • Fahn A (1988) Secretory tissues in vascular plants. New Phytol 108:229–257

    Article  Google Scholar 

  • Fahn A (2000) Structure and function of secretory cells. Advances Bot Res 31:37–75

    Article  CAS  Google Scholar 

  • Feder N, O’Brien TP (1968) Plant microtechnique: some principles and new methods. Amer J Bot 55:123–142

    Article  Google Scholar 

  • Feeny P (1976) Plant apparency and chemical defense. In: Wallace JW, Mansell RL (eds) Biochemical interaction between plants and insects. Recent advances in phytochemistry, vol 10. Plenum Press, New York, pp 1–40. doi:10.1007/978-1-4684-2646-5_1

  • Gabe M (1968) Techniques histologiques. Masson & Cie, Paris

    Google Scholar 

  • Gahan PB (1984) Plant histochemistry and cytochemistry—an introduction. Academic Press, London

    Google Scholar 

  • Giulietti AM, Pirani JR (1988) Patterns of geographic distribution of some plant species from the Espinhaço Range, Minas Gerais and Bahia, Brazil. In: Vanzolini PE, Heyer WR (eds) Proceedings of a Workshop on Neotropical Distribution Patterns. Academia Brasileira de Ciências, Rio de Janeiro, pp 39–69

    Google Scholar 

  • Gleizes M, Marpeau A, Pauly G, Bernard-Dagan C (1982) Role of acyclic compounds in monoterpene biosynthesis in Pinus pinaster. Phytochemistry 21:2641–2644

    Article  CAS  Google Scholar 

  • Gleizes M, Pauly G, Carde JP, Marpeau A, Bernard-Dagan C (1983) Monoterpene hydrocarbon biosynthesis by isolated leucoplasts of Citrofortunella mitis. Planta 159:373–381

    Article  CAS  PubMed  Google Scholar 

  • Gregory M, Baas P (1989) A survey of mucilage cells in vegetative organs of the dicotyledons. Israel J Bot 38:125–174

    Google Scholar 

  • Hammond CT, Mahlberg PG (1973) Morphology of glandular hairs of Cannabis sativa from scanning electron microscopy. Amer J Bot 60:524–528

    Article  Google Scholar 

  • Hansted L, Jakobsen HB, Olsen CE (1994) Influence of temperature on the rhythmic emission of volatiles from Ribes nigrum flowers in situ. Pl Cell Environ 17:1069–1072

    Article  CAS  Google Scholar 

  • Harborne JB (1997) Biochemical plant ecology. In: Dey PM, Harborne JB (eds) Plant Biochemistry. Academic Press, London, pp 503–516

    Chapter  Google Scholar 

  • Jacobi CM, Del Sarto MCL (2007) Pollination of two species of Vellozia (Velloziaceae) from high-altitude quartzitic grasslands, Brazil. Acta Bot Brasil 21:325–333

    Article  Google Scholar 

  • Jakobsen HB, Olsen CE (1994) Influence of climatic factors on emission of flower volatiles in situ. Planta 192:365–371

    CAS  Google Scholar 

  • Jensen WA (1962) Botanical histochemistry: principles and practice. WH Freeman & Co., San Francisco

    Google Scholar 

  • Johansen DA (1940) Plant microtechnique. McGraw-Hill Book Company, New York

    Google Scholar 

  • Kearns CA, Inouye DW (1993) Techniques for pollination biologists. University Press of Colorado, Niwot

    Google Scholar 

  • Kleinig H (1989) The role of plastids in isoprenoid biosynthesis. Annual Rev. Pl Physiol Pl Molec Biol 40:39–59

    Article  CAS  Google Scholar 

  • Langenheim JH (2003) Plant resins: chemistry, evolution, ecology and ethnobotany. Timber Press, Portland

    Google Scholar 

  • Langeron M (1949) Precis de microscopie. Masson & Cie, Paris

    Google Scholar 

  • Loughrin JN, Hamilton-Kemp TR, Andersen RA, Hildebrand DF (1990) Volatiles from flowers of Nicotiana sylvestris, N. otophora and Malus domestica: headspace components and day/night changes in their relative concentrations. Phytochemistry 29:2473–2477

    Article  CAS  Google Scholar 

  • Machado SR, Gregório EA, Guimarães E (2006) Ovary peltate trichomes of Zeyheria montana (Bignoniaceae): developmental ultrastructure in relation to function. Ann Bot (Oxford) 97:357–369

    Article  Google Scholar 

  • Machado SR, Barreiro DP, Rocha JF, Rodrigues TM (2012) Dendroid colleters on vegetative and reproductive apices in Alibertia sessilis (Rubiaceae) differ in ultrastructure and secretion. Flora Morphol Distrib Funct Ecol Pl 207:868–877

    Article  Google Scholar 

  • Machado SR, Teixeira SP, Rodrigues TM (2014) Bacterial leaf glands in Styrax camporum (Styracaceae): first report for the family. Bot Int J Pl Biol 92:403–411

    Google Scholar 

  • Machado SR, Paleari LM, Paiva EAS, Rodrigues TM (2015) Colleters on the inflorescence axis of Croton glandulosus (Euphorbiaceae): structural and functional characterization. Int J Pl Sci 176:86–93

    Article  Google Scholar 

  • Maclean RC, Ivemey-Cook WR (1952) Textbook of practical botany. Longmans Greenands Co., London

    Google Scholar 

  • Majetic CJ, Raguso RA, Ashman TL (2009) The sweet smell of success: floral scent affects pollinator attraction and seed fitness in Hesperis matronalis. Funct Ecol 23:480–487

    Article  Google Scholar 

  • Matile P, Altenburger R (1988) Rhythms of fragrance emission in flowers. Planta 174:242–247

    Article  CAS  PubMed  Google Scholar 

  • Mello-Silva R (1995) Aspectos Taxonômicos, Biogeográficos, Morfológicos e Biológicos das Velloziaceae de Grão-Mogol, Minas Gerais, Brasil. Bol Bot Univ São Paulo 14:49–79

    Google Scholar 

  • Mello-Silva R (2004) Velloziaceae. In: Smith N, Mori SA, Henderson A, Stevenson DW, Heald SV (eds) Flowering plants of the neotropics. Princeton University Press, Princeton, pp 490–491

    Google Scholar 

  • Mello-Silva R (2005) Morphological analysis, phylogenies and classification in Velloziaceae. Bot J Linn Soc 148:157–173

    Article  Google Scholar 

  • Menezes NL (1973) Natureza dos apêndices petalóides em Barbacenioideae (Velloziaceae). Bol Zool Biol Mar NS 30:713–755

    Google Scholar 

  • Menezes NL (1980) Evolution in Velloziaceae, with special reference to androecial characters. In: Brickell CD, Cutler DF, Gregory M (eds) Petaloid monocotyledons. Linnean society symposium serries, vol 8. Academic Press, London, pp 117–139

    Google Scholar 

  • Menezes NL (1988) Evolution of the anther in the family Velloziaceae. Bol Bot Univ São Paulo 10:33–41

    Google Scholar 

  • Miller IM, Reporter M (1987) Bacterial leaf symbiosis in Dioscorea sansibarensis: morphology and ultrastructure of the acuminate leaf glands. Pl Cell Environ 10:413–424

    Google Scholar 

  • Miller IM, Scott A, Gardner IC (1983) Leaf nodule development in Psychotria kirkii Hiern (Rubiaceae). Ann Bot (Oxford) 52:791–802

    Google Scholar 

  • Miller IM, Gardner IC, Scott A (1984) Structure and function of trichomes in the shoot tip of Ardisia crispa (Thunb.) A.DC. (Myrsinaceae). Bot J Linn Soc 88:223–236

    Article  Google Scholar 

  • Montserrat L, Mello-Silva R (2013) Velloziaceae do Parque Estadual de Ibitipoca, Minas Gerais, Brasil. Bol Bot Univ São Paulo 31:131–139

    Google Scholar 

  • Paiva EAS (2009) Ultrastructure and post-floral secretion of the pericarpial nectaries of Erythrina speciosa (Fabaceae). Ann Bot (Oxford) 104:937–944

    Article  Google Scholar 

  • Porto ALM, Machado SMF, Oliveira CMA, Bittrich V, Amaral MCA, Marsaioli AJ (2000) Polyisoprenylated benzophenones from Clusia floral resins. Phytochemistry 55:755–768

    Article  CAS  PubMed  Google Scholar 

  • Possobom CCF, Guimarães E, Machado SR (2015) Structure and secretion mechanisms of floral glands in Diplopterys pubipetala (Malpighiaceae) a neotropical species. Flora Morphol Distrib Funct Ecol Pl 211:26–39

    Article  Google Scholar 

  • Reinhold-Hurek B, Hurek T (2011) Living inside plants: bacterial endophytes. Curr Opin Pl Biol 14:435–443

    Article  Google Scholar 

  • Renner S (1983) The widespread occurrence of anther destruction by Trigona bees in Melastomataceae. Biotropica 15:251–256

    Article  Google Scholar 

  • Reynolds ES (1963) The use of lead citrate at high pH as an electron-opaque stain in electron microscopy. J Cell Biol 17:208

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Rodella LG, Tarifa JR (2002) Clima da Serra do Ibitipoca, MG. GEOUSP—Espaço e. Tempo 11:101–113

    Google Scholar 

  • Rodrigues TM, Teixeira SP, Machado SR (2011) The oleoresin secretory system in seedlings and adult plants of copaíba (Copaifera langsdorffii Desf., Leguminosae–Caesalpinioideae). Flora Morphol Distrib Funct Ecol Pl 206:585–594

    Article  Google Scholar 

  • Rosenblueth M, Martínez-Romero E (2006) Bacterial endophytes and their interactions with hosts. Molec Pl Microbe Interact 19:827–837

    Article  CAS  Google Scholar 

  • Sá-Haiad B, Silva CP, Paula RCV, Rocha JF, Machado SR (2015) Androecia in two Clusia species: development, structure and resin secretion. Pl Biol (Stuttgart) 17:816–824

    Article  Google Scholar 

  • Sajo MG, Mello-Silva R, Rudall PJ (2010) Homologies of floral structures in Velloziaceae with particular reference to the corona. Int J Pl Sci 171:595–606

    Article  Google Scholar 

  • Sazima M (1978) Biologia floral de espécies de Velloziaceae na Serra do Cipó, Minas Gerais. PhD Thesis, Universidade de São Paulo, São Paulo

  • Sazima M, Sazima I (1990) Hummingbird pollination in two species of Vellozia (Liliiflorae: Velloziaceae) in southeastern Brazil. Bot Acta 103:83–86

    Article  Google Scholar 

  • Schindelin J, Arganda-Carreras I, Frise E, Kaynig V, Longair M, Pietzsch T, Preibisch S, Rueden C, Saalfeld S, Schmid B, Tinevez JY, White DJ, Hartenstein V, Eliceiri K, Tomancak P, Cardona A (2012) Fiji: an open-source platform for biological-image analysis. Nat Meth 9:676–682

    Article  CAS  Google Scholar 

  • Simpson BB, Neff JL (1983) Evolution and diversity of floral rewards. In: Jones CE, Little RJ (eds) Handbook of experimental pollination biology. Van Nostrand Reinhold Company Inc, New York, pp 142–159

    Google Scholar 

  • Subramaniam S, Marti T, Khorana HG (1990) Protonation state of Asp (Glu)-85 regulates the purple-to-blue transition in bacteriorhodopsin mutants Arg-82 → Ala and Asp-85 → Glu: the blue form is inactive in proton translocation. Proc Natl Acad Sci USA 87:1013–1017

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Swain T (1979) Tannins and lignins. In: Rosenthal GA, Janzen DH (eds) Herbivores: their interactions with secondary plant metabolites. Academic Press, London, pp 3–19

    Google Scholar 

  • Taboga SR, Vilamaior PSL (2013) Citoquímica. In: Carvalho HF, Recco-Pimentel SM (eds) A célula. Editora Manole, Barueri

    Google Scholar 

  • Turner GW, Croteau R (2004) Organization of monoterpene biosynthesis in Mentha. Immunocytochemical localizations of geranyl diphosphate synthase, limonene-6-hydroxylase, isopiperitenol dehydrogenase, and pulegone reductase. Pl Physiol (Lancaster) 136:4215–4227

    Article  CAS  Google Scholar 

  • Turner G, Gershenzon J, Nielson EE, Froehlich JE, Croteau RB (1999) Limonene synthase, the enzyme responsible for monoterpene biosynthesis in peppermint, is localized in oil gland secretory cells. Pl Physiol (Lancaster) 120:879–886

    Article  CAS  Google Scholar 

  • Van Oevelen S, De Wachter R, Robbrecht E, Prinsen E (2003) Induction of a crippled phenotype in Psychotria (Rubiaceae) upon loss of the bacterial endophyte. Bulg J Pl Physiol 3–4(Special Issue):242–247

    Google Scholar 

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Acknowledgments

We thank the editors and the anonymous reviewers for their helpful comments on an earlier version of this paper. We also thank Dr. Renato de Mello-Silva for plant identification and Dr. Felipe Vivallo for bee identification. We also thank the Electron Microscopy Centre (CME) IBB, UNESP and its technicians for assistance with the ultrastructural analyses. This study forms part of the master’s thesis of R. S. C., which was carried out in the Postgraduate Program in Biological Sciences (Botany) of the Universidade Federal do Rio de Janeiro (UFRJ), Museu Nacional, and was supported by CAPES (Coordenação de Aperfeiçoamento de Pessoal de Nível Superior). B. S. H. was supported by research Grants from FAPERJ APQ1 (Proc. E-26/111.207/2014) and MCTI/CNPQ/Universal (Proc. 447624/2014-8) and S. R. M. received Grants from CNPq.

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  1. Departamento de Botânica, Quinta da Boa Vista, Universidade Federal do Rio de Janeiro, Museu Nacional, Rio de Janeiro, RJ, 22940-040, Brazil

    Rachel Sadala-Castilho, Bárbara Sá-Haiad & Heloisa A. Lima

  2. Departamento de Botânica, Instituto de Biociências, Universidade Estadual Paulista, Caixa Postal 510, Botucatu, SP, 18618-000, Brazil

    Silvia R. Machado

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  1. Rachel Sadala-Castilho
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  2. Silvia R. Machado
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Correspondence to Rachel Sadala-Castilho.

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Sadala-Castilho, R., Machado, S.R., Sá-Haiad, B. et al. Oil-resin glands in Velloziaceae flowers: structure, ontogenesis and secretion. Plant Syst Evol 302, 585–599 (2016). https://doi.org/10.1007/s00606-016-1287-5

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