Abstract
This study aims to investigate colleters’ secretory function, on cellular level, in Rubiaceae species from contrasting environments looking to explore the association between secretion and environment. We collected samples from eight species of Rubiaceae growing in forest and savanna having standard-type colleters with diverse histochemistry (hydrophilic, lipophilic and mixed secretions) and processed for both conventional and cytochemical study under transmission electron microscopy (TEM). The standard colleters, although similar in morphology and anatomy, exhibited marked differences on cellular level, especially in the abundance and topology of Golgi bodies, endoplasmic reticulum and plastids when comparing forest and savanna species. These differences were clearly aligned with the chemical nature of the secretions they produce, with predominance of hydrophilic secretions in forest species and lipophilic or mixed secretions in savanna species. The combination of methods in electron microscopy revealed the sites of synthesis and intracellular compartmentation of substances, the mechanisms of their secretion from the protoplast and confirmed the involvement of the outer walls of the epithelial cells in the elimination of exudates to the gland surface. Our study suggests a potential environment-associated plasticity of the secretory cells of standard-type colleters in modulating their secretory function performance.
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References
Angermüller S, Fahimi DH (1982) Imidazole-buffered osmium tetroxide: an excellent stain for visualization of lipids in transmission electron microscopy. Histochem J 14:823–825
Appezzato-da-Glória B, Estelita MEM (2000) Development, structure and distribution of colleters in Mandevilla illustris and M. velutina (Apocynaceae). Braz J Bot 23:113–120. doi:10.1590/S0100-84042000000200001
Benayoun J, Fahn A (1979) Intracellular transport and elimination of resin from epithelial duct-cells of Pinus halepensis. Ann Bot 43:179–181. doi:10.1093/oxfordjournals.aob.a085622
Carvalho WA, Panoso LA, Moraes MH (1991) Levantamento semidetalhado dos solos da Fazenda experimental Edgardia-Município de Botucatu. UNESP/FCA Boletim Científico, Botucatu, p 2
Coelho VPM, Leite JPV, Fietto LG, Ventrella MC (2013) Colleters in Bathysa cuspidate (Rubiaceae): development, ultrastructure and chemical composition of the secretion. Flora 208:579–590. doi:10.1016/j.flora.2012.08.005
Coutinho LM (2002) O bioma do cerrado. In: Klein AL (ed) Eugen warming e o cerrado brasileiro: um século depois. Editora da Unesp, São Paulo, pp 77–91
Cunha AR, Martins D (2009) Classificação climática para os municípios de Botucatu e São Manuel-SP. Irriga 14:1–11
Davis AP, Govaerts R, Bridson DM, Ruhsam M, Moat J, Brummitt NA (2009) A global assessment of distribution, diversity, endemism, and taxonomic effort in the Rubiaceae. Ann Missouri Bot Gard 96:68–78. doi:10.3417/2006205
Delvaux B, Brahy V (2014) Mineral soils conditioned by a wet (Sub) tropical climate . FAO. Retrieved 30 September 2016
Déstro GFG, Campos S (2006) SIG-SPRING na caracterização do uso dos solos a partir de imagens do satélite CBERS. Energia 21:28–35
Empresa Brasileira de Pesquisa Agropecuária (EMBRAPA) (1999) Sistema brasileiro de classificação de solo. Centro Nacional de Pesquisa de Solos, Rio de Janeiro
Evert RF (2006) Esau’s plant anatomy. John Wiley & Sons, New Jersey
Fahn A (1979) Secretory tissues in plants. Academic Press, London
Fahn A (2000) Structure and function of secretory cells. Adv Bot Res 31:37–75. doi:10.1016/S0065-2296(00)31006-0
Fakan S (2004) Ultrastructural cytochemical analyses of nuclear functional architecture. Eur J Histochem 48:5–14
Hall LJ, Flowers TJ, Roberts RM (1981) Plant cell structure and metabolism, 2nd edn. Longman Group Limited, New York
Horner HT, Lersten NR (1968) Development, structure and function of secretory trichomes in Psychotria bacteriophila (Rubiaceae). Am J Bot 55:1089–1099
Jeffree CE (1996) Structure and ontogeny of plant cuticles. In: Plant cuticles: an integrated functional approach. BIOS Scientific Publishers, Oxford, pp 33–82
Juneja A, Ceballos RM, Murthy GS (2013) Effects of environmental factors and nutrient availability on the biochemical composition of algae for biofuels production: a review. Energies 6:4607–4638. doi:10.3390/en6094607
Kakani VG, Reddy KR, Zhao D, Sailaja K (2003) Field crop response to ultraviolet-B radiation: a review. Agric For Meteorol 120:191–218. doi:10.1016/j.agrformet.2003.08.015
Klein DE, Gomes VM, Silva-Neto SJ, Da Cunha M (2004) The structure of colleters in several species of Simira (Rubiaceae). Ann Bot 94:733–740. doi:10.1093/aob/mch198
Kronestedt-Robards E, Robards A (1991) Exocytosis in gland cells. In: Hawea C, Coleman J, Evans D (eds) Endocytosis, exocytosis and vesicle traffic in plants. Cambridge University Press, Cambridge, pp 199–232
Kroon H, Huber H, Stuefer JF, van Groenedael JM (2005) A modular concept of phenotypic plasticity in plants. New Phytol 166:73–82. doi:10.1111/j.1469-8137.2004.01310.x
Lacchia APS, Tölke EEAD, Carmello-Guerreiro SM, Ascensão L, Demarco D (2016) Foliar colleters in Anacardiaceae: first report for the family. Botany 94:337–346. doi:10.1139/cjb-2015-0236
Lüttge U (1971) Structure and function of plant glands. Ann Rev Plant Physiol 22:23–44. doi:10.1146/annurev.pp.22.060171.000323
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 207:868–877. doi:10.1016/j.flora.2012.09.013
MacRae EK, Meetz GD (1970) Electron microscopy of the ammoniacal silver reaction for histones in the erythropoietic cells of the chick. J Cell Biol 45:235–245
Miguel EC, Gomes VM, Oliveira MA, Da Cunha M (2006) Colleters in Bathysa nicholsonii K. Schum. (Rubiaceae): ultrastructure, secretion protein composition, and antifungal activity. Plant Biol 8:715–722. doi:10.1055/s-2006-924174
Miguel EM, Klein DE, Oliveira MA, Da Cunha M (2010) Ultrastructure of secretory and senescence phase in colleters of Bathysa gymnocarpa and B. stipulata (Rubiaceae). Braz J Bot 33:425–436. doi:10.1590/S0100-84042010000300006
Nicotra AB, Atkin OK, Bonser SP et al (2010) Plant phenotypic plasticity in a changing climate. Trends in Plant Sci 15:684–692. doi:10.1016/j.tplants.2010.09.008
Possobom CF, Guimarães E, Machado SR (2015) Structure and secretion mechanisms of floral glands in Diplopterys pubipetala (Malpighiaceae), a neotropical species. Flora 211:26–39. doi:10.1016/j.flora.2015.01.002
Reinecke M, Walther C (1978) Aspects of turnover and biogenesis of synaptic vesicles at locust neuromuscular junctions as revealed by iodide-osmium tetroxide (ZIO) reacting with intravesicular sh-groups. J Cell Biol 21:839–855
Ren B, Cui H, Camberato JJ, Dong S, Liu P, Zhao B, Zhang J (2016) Effects of shading on the photosynthetic characteristics and mesophyll cell ultrastructure of summer maize. Sci Nat 103:67. doi:10.1007/s00114-016-1392-x
Reynolds ES (1963) The use of lead citrate at high pH as an electron-opaque stain in electron microscopy. J Cell Biol 17:208–212
Rios-Estepa R, Turner GW, Lee JM, Croteau RB, Lange BM (2008) A systems biology approach identifies the biochemical mechanisms regulating monoterpenoid essential oil composition in peppermint. Proc Natl Acad Sci U S A 105:2818–2013. doi:10.1073/pnas.0712314105
Roshchina VV, Roshchina VD (1993) Excretory function of higher plants. Springer-Verlag, Berlin
Sá-Haiad B, Silva CP, Paula RCV, Rocha JF, Machado SR (2015) Androecia in two Clusia species: development, structure and resin secretion. Plant Biol (Stuttg) 17:816–824. doi:10.1111/plb.12314
Sheue C-R, Chen YJ, Yang YP (2012) Stipules and colleters of the mangrove Rhizophoraceae: morphology, structure and comparative significance. Bot Stud 53:243–254
Sheue C-R, Chesson P, Chen Y-J et al (2013) Comparative systematic study of colleters and stipules of Rhizophoraceae with implications for adaptation to challenging environments. Bot J Linn Soc 172:449–464. doi:10.1111/boj.12058
Taiz L, Zeiger E (2013) Plant physiology, 5th edn. Sinauer Associates, Massachusetts
Thiéry JP (1967) Mise en evidence des polysaccharides sur coupes fines en microscopie eletronique. J Microsc 6:987–1017
Thomas V (1991) Structural, functional and phylogenetic aspects of the colleter. Ann Bot 68:287–305
Tresmondi F, Nogueira A, Guimarães E, Machado SR (2015) Morphology, secretion composition, and ecological aspects of stipular colleters in Rubiaceae species from tropical forest and savanna. Naturwissenschaften 102(11–12):73. doi:10.1007/s00114-015-1320-5
Turner GW, Croteau R (2004) Organization of monoterpene biosynthesis in Mentha: Immunocytochemical localization of geranyl diphosphate synthase, limonene-6-hydroxylase, isopiperitenol dehydrogenase, and pulegone reductase. Plant Physiol 136:4215–4227. doi:10.1104/pp.104.050229
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. Plant Physiol 120:879–886
Vassilyev AE (2000) Quantitative ultrastructural data of secretory duct epithelial cells in Rhus Toxicodendron. Int J Plant Sci 161(4):615–630
Wiermann R (1981) Secondary plant products and cell and tissue differentiation. In: Stumpf PK, Conn EE (eds) The biochemistry of plants; a comprehensive treatise, vol 7. Academic Press, New York, pp 85–116
Wilkinson HP (1979) The plant surface; the cuticle. In: Metcalfe CR, Chalk L (eds) Anatomy of the dicotyledons, vol 1. Clarendon Press, Oxford, pp 140–148
Acknowledgements
This article is part of the doctoral thesis of F. Tresmondi. We acknowledge the financial support of the National Council for Scientific and Technological Development (CNPq—financial support Proc. 473289/2010 and grants to the SR Machado Proc. 302657/2011-8) and the São Paulo Council for Research (FAPESP—financial support Thematic Project Proc. 2008/55434-7 and grants to the first author—Proc. 2011/02488-5). Thanks to the Electron Microscopy Centre (CME) IBB, UNESP and its technicians for assistance with sample preparations.
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Communicated by: Sven Thatje
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Tresmondi, F., Canaveze, Y., Guimarães, E. et al. Colleters in Rubiaceae from forest and savanna: the link between secretion and environment. Sci Nat 104, 17 (2017). https://doi.org/10.1007/s00114-017-1444-x
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DOI: https://doi.org/10.1007/s00114-017-1444-x