Abstract
Floral secretory structures have been reported for Gentianaceae; however, morphoanatomical studies of these glands are rare. We described the development and secretory activity of the colleters and nectaries throughout the floral development of Chelonanthus viridiflorus. We collected flower buds, flowers at anthesis, and fruits to be investigated using light and scanning electron microscopy. We performed histochemical tests on the secretion of colleters and used glycophyte to confirm the presence of glucose in nectar. Colleters are located on the ventral surface of sepals and nectaries occur in four regions: (i) the dorsal and (ii) ventral surfaces of sepals; (iii) apex of petals; and (iv) base of ovary. The colleters have a short peduncle and a secretory portion with homogeneous cells. They are active in flower buds and secrete polysaccharides and proteins. In flowers at anthesis, they begin to senescence presenting protoplast retraction, cell collapse, and lignification; these characteristics are intensified in fruit. The nectaries of sepals and petals have two to five cells surrounding a central cell through which the secretion is released. Nectaries are numerous, forming a nectariferous area on the dorsal surface of sepals, like that observed on petals, and can form isolated units on the ventral surface of sepals. They are active from flower buds to fruits. A region with secretory activity was identified at the base of the ovary. The secretion of colleters acts in the protection of developing organs, while nectaries are related to defenses against herbivores and the supply of nectar to potential robbers or pollinators.
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References
Baillon HE (1889) Histoire des plantes. Libraire Hachette & Co, Paris
Baker HG, Baker I (1983) Floral nectar sugar constituents in relation to pollinator type. In: Jones CE, Little RJ (eds) Handbook of experimental pollination biology. Van Nostrand Reinhold Company Inc., New York, pp 117–141
Barreiro DP, Machado SR (2007) Coléteres dendróides em Alibertia sessilis (Vell.) K. Schum., uma espécie não-nodulada de Rubiaceae. Braz J Bot 30:389–399. https://doi.org/10.1590/S0100-84042007000300005
Barros TC, Marinho CR, Pedersoli GD, Paulino JV, Teixeira SP (2017) Beyond pollination: diversity of secretory structures during flower development in diferente legume lineages. Acta Bot Bras 31:358–373. https://doi.org/10.1590/0102-33062016abb0291
Bernadello G (2007) A systematic survey of floral nectaries. In: Nicolson SW, Nepi M, Pacini E (eds) Nectaries and nectar, 1st edn. Springer, Dordrecht, pp 19–128
Calió MFA (2009) Sistemática de Helieae Gilg (Gentianaceae). Dissertation, Universidade de São Paulo
Caspary R (1848) De nectariis. PhD Thesis. Bonn: Elverfeldae
Costa ISC, Lucena EMP, Bonilla OH, Guesdon IR, Coutinho IAC (2020) Seasonal variation in colleter exudates in Myrcia splendens (Myrtaceae). Aust J Bot 68:403–412. https://doi.org/10.1071/BT20020
Dalvi VC, Meira RMSA, Azevedo AA (2013) Extrafloral nectaries in neotropical Gentianaceae: occurrence, distribution patterns, and anatomical characterization. Am J Bot 100:1779–1789. https://doi.org/10.3732/ajb.1300130
Dalvi VC, Meira RMA, Francino DMT, Silva LC, Azevedo AA (2014a) Anatomical characteristics as taxonomic tools for the species of Curtia and Hockinia (Saccifolieae-Gentianaceae Juss.). Plant Syst Evol 300:99–112. https://doi.org/10.1007/s00606-013-0863-1
Dalvi VC, Cardinelli LS, Meira RMSA, Azevedo AA (2014b) Foliar colleters in Macrocarpaea obtusifolia (Gentianaceae): anatomy, ontogeny, and secretion. Botany 92:59–67. https://doi.org/10.1139/cjb-2013-0203
Dalvi VC, Meira RMSA, Azevedo AA (2017) Are stem nectaries common in Gentianaceae Juss.? Acta Bot Bras 31:403–410. https://doi.org/10.1590/0102-33062016abb0404
Dalvi VC, de Faria GS, Azevedo AA (2020) Calycinal secretory structures in Calolisianthus pedunculatus (Cham. & Schltdl) Gilg (Gentianaceae): anatomy, histochemistry and functional aspects. Protoplasma 257:275–284. https://doi.org/10.1007/s00709-019-01436-5
Dejean A, Corbara B, Leroy C, Delabie JHC, Rossi V, Céréghino R (2011) Inherited biotic protection in a neotropical pioneer plant. PLoS One 6:1–11. https://doi.org/10.1371/journal.pone.0018071
Delgado MN, Silva LC, Báo SN, Morais HC, Azevedo AA (2011a) Distribution, structural and ecological aspects of the unusual leaf nectaries of Calolisianthus species (Gentianaceae). Flora 206:676–683. https://doi.org/10.1016/j.flora.2010.11.016
Delgado MN, Azevedo AA, Valente GE, Kasuya MCM (2011b) Comparative anatomy of Calolisianthus species (Gentianaceae-Helieae) from Brazil: taxonomic aspects. Edinb J Bot 68:139–155. https://doi.org/10.1017/S0960428610000284
Delpino F (1873) Ulteriori osservazioni e considerazioni sulla Dicogamia nel regno vegetale. Atti Soc Ital Sci Nat 16:151–349
Demarco D (2017) Floral glands in Asclepiads: structure, diversity and evolution. Acta Bot Bras 31:477–502. https://doi.org/10.1590/0102-33062016abb0432
Dobat K, Peikert-Holle T (1985) Blüten und Fledermäuse (Chiropterophilie). Kramer, Frankfurt am Main
Fahn A (1979) Secretory tissues in plants. Academic Press, London
Gabe M (1968) Techniques histologiques. Masson and Cie, Paris
Gahan PB (1984) Plant histochemistry and cytochemistry. Academic Press, Florida, An introduction
Johansen DA (1940) Plant microtechnique. McGraw-Hill Book Company, New York
Judd WS, Campbell CS, Kellog EA, Stevens PF (2009) Plant systematics: a phylogenetic approach. Massachusetts: Sinauer Associates, Sunderland
Kalisz S, Vogler DW (2003) Benefits of autonomous selfing under unpredictable pollinator environments. Ecology 84:2928–2942. https://doi.org/10.1890/02-0519
Kalisz S, Vogler DW, Hanley KM (2004) Context-dependent autonomous self-fertilization yields reproductive assurance and mixed mating. Nature 430:884–887. https://doi.org/10.1038/nature02776
Klein DE, Gomes VM, Silva-Neto SJ, Cunha M (2004) The structure of colleters in several species of Simira (Rubiaceae). Ann Bot 94:733–740. https://doi.org/10.1093/aob/mch198
Lepis K (2009) Evolution and systematics of Chelonanthus (Gentianaceae). Ph.D. dissertation, Rutgers University
Lersten NR (1974) Morphology and distribution of colleters and crystals in relation to the taxonomy and bacterial leaf nodule symbiosis of Psychotria (Rubiaceae). Am J Bot 61:973–981. https://doi.org/10.2307/2441988
Lindsey AA (1940) Floral anatomy in the Gentianaceae. Am J Bot 27:640–652
MacCall AC, Irwin RE (2006) Florivory: the intersection of pollination and herbivory. Ecol Lett 9:1351–1365. https://doi.org/10.1111/j.1461-0248.2006.00975.x
Machado ICS, Sazima I, Sazima M (1998) Bat pollination of the terrestrial herb Irlbachia alata (Gentianaceae) in northeastern Brazil. Pl Syst Evol 290:231–237. https://doi.org/10.1007/BF00985230
Machado SR, Souza CV, Guimarães E (2017) A reduced, yet functional, nectary disk integrates a complex system of floral nectar secretion in the genus Zeyheria (Bignoniaceae). Acta Bot Bras 31:344–357. https://doi.org/10.1590/0102-33062016abb0279
Marquis RJ (2012) Uma abordagem geral das defesas das plantas contra a ação de herbívoros. In: Del-Claro K, Torezan-Silingardi HM (eds) Ecologia das interações plantas-animais: uma abordagem ecológico-evolutiva. Technical Books, Rio de Janeiro, pp 55–66
Mayer JLS, Carmello-Guerreiro SM, Mazzafera P (2013) A functional role for the colleters of coffee flowers. AoB Plants 5:plt 029. https://doi.org/10.1093/aobpla/plt029
McManus JFA (1948) Histological and histochemical uses of periodic acid. Stain Technol 23:99–108. https://doi.org/10.3109/10520294809106232
Miguel EC, Gomes VM, Oliveira MA, Cunha MD (2006) Colleters in Bathysa nicholsonii K. Schum. (Rubiaceae): ultrastructure, secretion protein composition and antifungal activity. Plant Biol 200:715–722. https://doi.org/10.1055/s-2006-924174
Nemomissa S (1997) Floral character states of the Northeast and Tropical East African Swertia species (Gentianaceae). Nord J Bot 17:145–156. https://doi.org/10.1111/j.1756-1051.1997.tb00301.x
Nemomissa S (1998) A synopsis of Swertia (Gentianaceae) in East and Northeast Tropical Africa. Kew Bull 27:548–572. https://doi.org/10.2307/4114507
Nicolson SW, Nepi M, Pacini E (2007) Nectaries and nectar. Springer, Netherlands, Dordrecht
Nobel PS, Cavelier J, Andrade JL (1992) Mucilage in cacti: its apoplastic capacitance, associated solutes, and influence on tissue water relations. J Exp Bot 43:641–648. https://doi.org/10.1093/jxb/43.5.641
Norment CJ (1988) The effect of nectar-thieving ants on the reproductive success of Frasera speciosa (Gentianaceae). Am Midl Nat 120:331–336. https://doi.org/10.2307/2426005
O’Brien TP, McCully ME (1981) The study of plant structure principles and selected methods. Termarcaphi Ptey. Ltd., Melbourne
O’Brien TP, Feder N, McCully ME (1964) Polychromatic staining of plant cells walls by toluidine blue O. Protoplasma 59:368–373. https://doi.org/10.1007/BF01248568
Paiva EAS, Martins LC (2011) Calycinal trichomes in Ipomoea cairica (Convolvulaceae): ontogenesis, structure and functional aspects. Aust J Bot 59:91–98. https://doi.org/10.1071/BT10194
Pearse AGE (1985) Histochemistry theoretical and applied: preparative and optical technology. Churchill Livingston, Edinburgh
Renobales G, Diego E, Urcelay B, López-Quintana A (2001) Secretory hairs in Gentiana and allied genera (Gentianaceae, subtribe Gentianinae) from the Iberian Peninsula. Bot J Linn Soc 136:119–129. https://doi.org/10.1111/j.1095-8339.2001.tb00560.x
Ribeiro JC, Ferreira MJP, DeMarco D (2017) Colleters in Asclepiadoideae (Apocynaceae): protection of meristems against desiccation and new functions assigned. Int J Plant Sci 178:465–477. https://doi.org/10.1086/692295
Rudgers JA (2004) Enemies of herbivores can shape plants traits: selection in a facultative ant-plant mutualism. Ecology 85:192–205. https://doi.org/10.1890/02-0625
Silva MS, Coutinho IAC, Araújo MN, Meira RMSA (2017) Colleters in Chamaecrista (L.) Moench sect. Chamaecrista and sect. Caliciopsis (Leguminosae-Caesalpinioidae): anatomy and taxonomic implications. Acta Bot Bras 31:382–391. https://doi.org/10.1590/0102-33062016abb0339
Simões AO, Castro MM, Kinoshita LS (2006) Calycine colleters of seven species of Apocynaceae (Apocynoideae) from Brazil. Bot J Linn Soc 152:387–398. https://doi.org/10.1111/j.1095-8339.2006.00572.x
Struwe L, Albert VA, Bremer B (1994) Cladistics of the family level classification of the Gentianales. Cladistics 10:175–206. https://doi.org/10.1006/clad.1994.1011
Struwe L, Kadereit JW, Klackenberg J, Nilsson S, Thiv M, Von-Hagen KB, Albert VA (2002) Systematics, character evolution, and biogeography of Gentianaceae, including a new tribal and subtribal classification. In: Struwe L, Albert VA (eds) Gentianaceae: systematics and natural history. Cambridge University Press, Cambridge
Thomas V (1991) Structural, functional and phylogenetic aspects of the colleter. Ann Bot 68:287–305. https://doi.org/10.1093/oxfordjournals.aob.a088256
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. Sci Nat 102:73. https://doi.org/10.1007/s00114-015-1320-5
Tresmondi F, Canaveze Y, Guimarães E, Machado SR (2017) Colleters in Rubiaceae from forest and savanna: the link between secretion and environment. Sci Nat 104:17. https://doi.org/10.1007/s00114-017-1444-x
Vogel S (1998) Remarkable nectaries: structure, ecology, organophyletic perspectives II Nectarioles. Flora 193:1–29. https://doi.org/10.1016/S0367-2530(17)30812-5
Wolff D (2006) Nectar sugar composition and volumes of 47 species of Gentianales from a Southern Ecuadorian montane forest. Ann Bot 97:767–777. https://doi.org/10.1093/aob/mcl033
Zangerl AR, Bazzaz FA (1992) Theory and pattern in plant defense allocation. In: Fritz R Simms EL (eds) Plant resistance to herbivores and pathogens: ecology, evolution, and genetics. Chicago University Press, Chicago, pp 363-391
Zanotti A (2018) Estruturas secretoras em Calolisianthus specious (Cham. & Schltdl.) Gilg. (Gentianaceae): ontogenia e biologia da secreção. Dissertation, Universidade Federal de Viçosa
Zimmermann JG (1932) Über die extrafloralen nektarien der angiospermen. Beih Bot Zentralb 49:99–196
Acknowledgements
We thank the Instituto Chico Mendes de Conservação da Biodiversidade for the collection licenses; the Laboratório de Anatomia Vegetal of the Instituto Federal Goiano (IF Goiano, Rio Verde campus) for the anatomical analysis; and the Laboratório Multiusuário de Microscopia de Alta Resolução (LabMic) of the Universidade Federal de Goiás (UFG) for allowing the preparation and analysis of scanning electron microscopy samples.
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Financial support was received from Conselho Nacional de Desenvolvimento Científico e Tecnológico (CNPq; Brasília, Brazil) for project development (grant number 406824/2016–9 to VCD), and for the scientific initiation scholarship to BEAO.
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VCD designed the research project; VCD and DMTF collected the samples; BEAO, VCD, and DMTF carried out the light microscopy and histochemical analyses; VCD performed the scanning microscopy analyses; and all authors wrote the paper.
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El Ajouz, B., Valentin-Silva, A., Francino, D.M.T. et al. A flower with several secretions: anatomy, secretion composition, and functional aspects of the floral secretory structures of Chelonanthus viridiflorus (Helieae—Gentianaceae). Protoplasma 259, 427–437 (2022). https://doi.org/10.1007/s00709-021-01652-y
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DOI: https://doi.org/10.1007/s00709-021-01652-y