Colleters in the vegetative axis of Aechmea blanchetiana (Bromeliaceae): anatomical, ultrastructural and functional aspects
Igor Ballego-Campos A B and Elder Antônio Sousa Paiva AA Departamento de Botânica, Instituto de Ciências Biológicas, Universidade Federal de Minas Gerais, Belo Horizonte, 31270-901, MG, Brazil.
B Corresponding author. Email: igorballego@gmail.com
Australian Journal of Botany 66(5) 379-387 https://doi.org/10.1071/BT18095
Submitted: 4 May 2018 Accepted: 12 August 2018 Published: 4 September 2018
Abstract
Colleters are common among eudicotyledons, but few records exist for monocotyledons and other groups of plants. For Bromeliaceae, mucilage secretions that protect the young portions of the plant have been observed only in the reproductive axis, and little is known about the secretory systems behind this or even other kind of secretions in the family. We aimed to describe, for the first time, the occurrence of colleters associated with the vegetative shoot of Aechmea blanchetiana (Baker) L.B.Sm., and elucidate aspects of their structure, ultrastructure and secretory activity. Samples of various portions of the stem axis were prepared according to standard methods for light and electron microscopy. Colleters were found compressed in the axillary portion of leaves and in all leaf developmental stages. Secretory activity, however, was found to be restricted to young and unexpanded leaves. The colleters displayed a flattened hand-like shape formed by a multiseriate stalk and an expanded secretory portion bearing elongated marginal cells. Ultrastructural data confirmed that the secretory role of the colleters is consistent with mucilaginous secretion. The functional roles of the colleters are discussed with regard to environmental context and intrinsic features of the plant, such as the presence of a water-impounding tank.
Additional keywords: bromeliads, desiccation, mucilage, plant–environment interactions, plant secretion.
References
Ballego-Campos I, Paiva EAS (2018) Mucilage secretion in the inflorescences of Aechmea blanchetiana: evidence of new functions of scales in Bromeliaceae. Flora 246–247, 1–9.| Mucilage secretion in the inflorescences of Aechmea blanchetiana: evidence of new functions of scales in Bromeliaceae.Crossref | GoogleScholarGoogle Scholar |
Benzing DH (1970) Foliar permeability and the absorption of minerals and organic nitrogen by certain tank bromeliads. Botanical Gazette 131, 23–31.
| Foliar permeability and the absorption of minerals and organic nitrogen by certain tank bromeliads.Crossref | GoogleScholarGoogle Scholar |
Benzing DH (1976) Bromeliad trichomes: structure, function, and ecological significance. The Journal of the Marie Selby Botanical Gardens 1, 330–348.
Benzing DH (2000) ‘Bromeliaceae: profile of an adaptive radiation’. (Cambridge University Press: New York)
Benzing DH, Givnish TJ, Bermudes D (1985) Absorptive trichomes in Brocchinia reducta (Bromeliaceae) and their evolutionary and systematic significance. Systematic Botany 10, 81–91.
| Absorptive trichomes in Brocchinia reducta (Bromeliaceae) and their evolutionary and systematic significance.Crossref | GoogleScholarGoogle Scholar |
Brundrett MC, Kendrick B, Peterson CA (1991) Efficient lipid staining in plant material with Sudan Red 7B or Fluoral Yellow 088 in polyethylene glycol-glycerol. Biotechnic & Histochemistry 66, 111–116.
| Efficient lipid staining in plant material with Sudan Red 7B or Fluoral Yellow 088 in polyethylene glycol-glycerol.Crossref | GoogleScholarGoogle Scholar |
Cardoso-Gustavson P, Campbell LM, Mazzoni-Viveiros SC, Barros F (2014) Floral colleters in Pleurothallidinae (Epidendroideae: Orchidaceae). American Journal of Botany 101, 587–597.
| Floral colleters in Pleurothallidinae (Epidendroideae: Orchidaceae).Crossref | GoogleScholarGoogle Scholar |
Carvalho JDT, Essi L, Oliveira JMS (2017) Flower and floral trichome morphology of species of Dyckia Schult. f. (Bromeliaceae, Pitcairnioideae), and their importance to species characterization and genus taxonomy. Acta Botanica Brasílica 31, 29–41.
| Flower and floral trichome morphology of species of Dyckia Schult. f. (Bromeliaceae, Pitcairnioideae), and their importance to species characterization and genus taxonomy.Crossref | GoogleScholarGoogle Scholar |
Chu EP, Tavares AR, Kanashiro S, Giampaoli P, Yokota ES (2010) Effects of auxins on soluble carbohydrates, starch and soluble protein content in Aechmea blanchetiana (Bromeliaceae) cultured in vitro. Scientia Horticulturae 125, 451–455.
| Effects of auxins on soluble carbohydrates, starch and soluble protein content in Aechmea blanchetiana (Bromeliaceae) cultured in vitro.Crossref | GoogleScholarGoogle Scholar |
Dickison WC (2000) ‘Integrative plant anatomy.’ (Academic Press: London)
Evans TM, Jabaily RS, Gelli De Faria AP, De Sousa LOF, Wendt T, Brown GK (2015) Phylogenetic relationships in Bromeliaceae subfamily Bromelioideae based on chloroplast DNA sequence data. Systematic Botany 40, 116–128.
| Phylogenetic relationships in Bromeliaceae subfamily Bromelioideae based on chloroplast DNA sequence data.Crossref | GoogleScholarGoogle Scholar |
Fahn A (1979) ‘Secretory tissues in plants.’ (Academic Press: London)
Fahn A (2000) Structure and function of secretory cells. Advances in Botanical Research 31, 37–75.
| Structure and function of secretory cells.Crossref | GoogleScholarGoogle Scholar |
Fernandes VF, Thadeo M, Dalvi VC, Meira RMSA (2017) Secretory structures in Casearia sylvestris Sw. (Salicaceae): diversity, mechanisms of secretion, and exudate complexity. International Journal of Plant Sciences 178, 288–301.
| Secretory structures in Casearia sylvestris Sw. (Salicaceae): diversity, mechanisms of secretion, and exudate complexity.Crossref | GoogleScholarGoogle Scholar |
Givnish TJ, Burkhardt EL, Happel RE, Weintraub JD (1984) Carnivory in the bromeliad Brocchinia reducta, with a cost/benefit model for the general restriction of carnivorous plants to sunny, moist, nutrient-poor habitats. American Naturalist 124, 479–497.
| Carnivory in the bromeliad Brocchinia reducta, with a cost/benefit model for the general restriction of carnivorous plants to sunny, moist, nutrient-poor habitats.Crossref | GoogleScholarGoogle Scholar |
Givnish TJ, Millam KC, Berry PE, Sytsma KJ (2007) Phylogeny, adaptive radiation, and historical biogeography of Bromeliaceae inferred from ndhF sequence data. Aliso 23, 3–26.
| Phylogeny, adaptive radiation, and historical biogeography of Bromeliaceae inferred from ndhF sequence data.Crossref | GoogleScholarGoogle Scholar |
Givnish TJ, Barfuss MHJ, Ee BV, Riina R, Schulte K, Horres R, Gonsiska PA, Jabaily RS, Crayn DM, Smith AC, Winter K, Brown GK, Evans TM, Holst BK, Luther H, Till W, Zizka G, Berry PE, Sytsma KJ (2011) Phylogeny, adaptive radiation, and historical biogeography in Bromeliaceae: insights from an eight-locus plastid phylogeny. American Journal of Botany 98, 872–895.
| Phylogeny, adaptive radiation, and historical biogeography in Bromeliaceae: insights from an eight-locus plastid phylogeny.Crossref | GoogleScholarGoogle Scholar |
Horner HT Horner HT (1968) Development, structure and function of secretory trichomes in Psychotria bacteriophila (Rubiaceae). American Journal of Botany 55, 1089–1099.
| Development, structure and function of secretory trichomes in Psychotria bacteriophila (Rubiaceae).Crossref | GoogleScholarGoogle Scholar |
Horres R, Schulte K, Weising K, Zizka G (2007) Systematics of Bromelioideae (Bromeliaceae) – evidence from molecular and anatomical studies. Aliso 23, 27–43.
| Systematics of Bromelioideae (Bromeliaceae) – evidence from molecular and anatomical studies.Crossref | GoogleScholarGoogle Scholar |
Johansen DA (1940) ‘Plant microtechnique.’ (McGraw-Hill Book Co: New York)
Judd WS, Campbell CS, Kellogg EA, Stevens PF (2009) Taxonomic evidence: structural and biochemical characters. In ‘Plant systematics: a phylogenetic approach’. (Eds WS Judd, CS Campbell, EA Kellogg, PF Stevens) pp. 53–102. (Sinnauer Associates: Sunderland, MA, USA)
Kanashiro S, Ribeiro RDCS, Gonçalves AN, Dias CTDS, Jocys T (2007) Efeitos de diferentes concentrações de nitrogênio no crescimento de Aechmea blanchetiana (Baker) L.B.Sm. cultivada in vitro. Hoehnea 34, 59–66.
| Efeitos de diferentes concentrações de nitrogênio no crescimento de Aechmea blanchetiana (Baker) L.B.Sm. cultivada in vitro.Crossref | GoogleScholarGoogle Scholar |
Karnovsky MJ (1965) A formaldehyde-glutaraldehyde fixative of high osmolarity for use in electron microscopy. Journal of Cell Biology 27, 137A
Krauss BH (1949) Anatomy of the vegetative organs of the pineapple, Ananas comosus (L.) Merr. (Continued) II. The leaf. Botanical Gazette 110, 333–404.
| Anatomy of the vegetative organs of the pineapple, Ananas comosus (L.) Merr. (Continued) II. The leaf.Crossref | GoogleScholarGoogle Scholar |
Kristen U, Lockhausen J (1985) The leaf glands of Veronica beccabunga L.: ultrastructure and a possible pathway of secretion. Israel Journal of Botany 34, 147–156.
Leitão CAE, Cortelazzo AL (2008) Structural and histochemical characterisation of the colleters of Rodriguezia venusta (Orchidaceae). Australian Journal of Botany 56, 161–165.
| Structural and histochemical characterisation of the colleters of Rodriguezia venusta (Orchidaceae).Crossref | GoogleScholarGoogle Scholar |
Lersten NR (1974a) Colleter morphology in Pavetta, Neorosea and Tricalysia (Rubiaceae) and its relationship to the bacterial leaf nodule symbiosis. Botanical Journal of the Linnean Society 69, 125–136.
| Colleter morphology in Pavetta, Neorosea and Tricalysia (Rubiaceae) and its relationship to the bacterial leaf nodule symbiosis.Crossref | GoogleScholarGoogle Scholar |
Lersten NR (1974b) Morphology and distribution of colleters and crystals in relation to the taxonomy and bacterial leaf nodule symbiosis of Psychotria (Rubiaceae). American Journal of Botany 61, 973–981.
| Morphology and distribution of colleters and crystals in relation to the taxonomy and bacterial leaf nodule symbiosis of Psychotria (Rubiaceae).Crossref | GoogleScholarGoogle Scholar |
Lersten NR (1975) Colleter types in Rubiaceae, especially in relation to the bacterial leaf nodule symbiosis. Botanical Journal of the Linnean Society 71, 311–319.
| Colleter types in Rubiaceae, especially in relation to the bacterial leaf nodule symbiosis.Crossref | GoogleScholarGoogle Scholar |
Lüttge U (1971) Structure and function of plant glands. Annual Review of Plant Physiology 22, 23–44.
| Structure and function of plant glands.Crossref | GoogleScholarGoogle Scholar |
Machado SR, Gregório EA, Guimarães E (2006) Ovary peltate trichomes of Zeyheria montana (Bignoniaceae): developmental ultrastructure and secretion in relation to function. Annals of Botany 97, 357–369.
| Ovary peltate trichomes of Zeyheria montana (Bignoniaceae): developmental ultrastructure and secretion in relation to function.Crossref | GoogleScholarGoogle Scholar |
Machado SR, Paleari LM, Paiva EAS, Rodrigues TM (2015) Colleters on the inflorescence axis of Croton glandulosus (Euphorbiaceae): structural and functional characterization. International Journal of Plant Sciences 176, 86–93.
| Colleters on the inflorescence axis of Croton glandulosus (Euphorbiaceae): structural and functional characterization.Crossref | GoogleScholarGoogle Scholar |
Mayer JLS, Cardoso-Gustavson P, Appezzato-da-Glória B (2011) Colleters in monocots: new record for Orchidaceae. Flora 206, 185–190.
| Colleters in monocots: new record for Orchidaceae.Crossref | GoogleScholarGoogle Scholar |
Mercadante-Simões MO, Paiva EAS (2013) Leaf colleters in Tontelea micrantha (Celastraceae, Salacioideae): ecological, morphological and structural aspects. Comptes Rendus Biologies 336, 400–406.
| Leaf colleters in Tontelea micrantha (Celastraceae, Salacioideae): ecological, morphological and structural aspects.Crossref | GoogleScholarGoogle Scholar |
Monteiro RF, Macedo MV (2014) First report on the diversity of insects trapped by a sticky exudate of the inflorescences of Vriesea bituminosa Wawra (Bromeliaceae: Tillandsioideae). Arthropod-Plant Interactions 8, 519–523.
| First report on the diversity of insects trapped by a sticky exudate of the inflorescences of Vriesea bituminosa Wawra (Bromeliaceae: Tillandsioideae).Crossref | GoogleScholarGoogle Scholar |
O’Brien TP, Feder N, McCully ME (1964) Polychromatic staining of plant cell walls by toluidine blue O. Protoplasma 59, 368–373.
| Polychromatic staining of plant cell walls by toluidine blue O.Crossref | GoogleScholarGoogle Scholar |
Oliveira CS, Salino A, Paiva EAS (2017) Colleters in Thelypteridaceae: unveiling mucilage secretion and its probable role in ferns. Flora 228, 65–70.
| Colleters in Thelypteridaceae: unveiling mucilage secretion and its probable role in ferns.Crossref | GoogleScholarGoogle Scholar |
Paiva EAS (2009) Occurrence, structure and functional aspects of the colleters of Copaifera langsdorffii Desf. (Fabaceae, Caesalpinioideae). Comptes Rendus Biologies 332, 1078–1084.
| Occurrence, structure and functional aspects of the colleters of Copaifera langsdorffii Desf. (Fabaceae, Caesalpinioideae).Crossref | GoogleScholarGoogle Scholar |
Paiva EAS (2012) Colleters in Cariniana estrellensis (Lecythidaceae: structure, secretion and evidences for young leaf protection. The Journal of the Torrey Botanical Society 139, 1–8.
| Colleters in Cariniana estrellensis (Lecythidaceae: structure, secretion and evidences for young leaf protection.Crossref | GoogleScholarGoogle Scholar |
Paiva EAS (2016) How do secretory products cross the plant cell wall to be released? A new hypothesis involving cyclic mechanical actions of the protoplast. Annals of Botany 117, 533–540.
| How do secretory products cross the plant cell wall to be released? A new hypothesis involving cyclic mechanical actions of the protoplast.Crossref | GoogleScholarGoogle Scholar |
Roland AM (1978) General preparations and staining of thin sections. In ‘Electron microscopy and cytochemistry of plant cells’. (Ed. JL Hall) pp. 1–62. (Elsevier: New York)
Santa-Rosa S, Souza F, Vidal Á (2013) Micropropagation of the ornamental vulnerable bromeliads Aechmea blanchetiana and Aechmea distichantha. Horticultura Brasileira 31, 112–118.
| Micropropagation of the ornamental vulnerable bromeliads Aechmea blanchetiana and Aechmea distichantha.Crossref | GoogleScholarGoogle Scholar |
Sass C, Specht CD (2010) Phylogenetic estimation of the core Bromelioids with an emphasis on the genus Aechmea (Bromeliaceae). Molecular Phylogenetics and Evolution 55, 559–571.
| Phylogenetic estimation of the core Bromelioids with an emphasis on the genus Aechmea (Bromeliaceae).Crossref | GoogleScholarGoogle Scholar |
Scarano FR (2002) Structure, function and floristic relationships of plant communities in stressful habitats marginal to the Brazilian Atlantic rainforest. Annals of Botany 90, 517–524.
| Structure, function and floristic relationships of plant communities in stressful habitats marginal to the Brazilian Atlantic rainforest.Crossref | GoogleScholarGoogle Scholar |
Scarano FR, Duarte HM, Ribeiro KT, Rodrigues PJFP, Barcellos EMB, Franco AC, Brulfert J, Deleéns E, Lüttge U (2001) Four sites with contrasting environmental stress in southeastern Brazil: relations of species, life form diversity, and geographic distribution to ecophysiological parameters. Botanical Journal of the Linnean Society 136, 345–364.
| Four sites with contrasting environmental stress in southeastern Brazil: relations of species, life form diversity, and geographic distribution to ecophysiological parameters.Crossref | GoogleScholarGoogle Scholar |
Schulte K, Barfuss MHJ, Zizka G (2009) Phylogeny of Bromelioideae (Bromeliaceae) inferred from nuclear and plastid DNA loci reveals the evolution of the tank habit within the subfamily. Molecular Phylogenetics and Evolution 51, 327–339.
| Phylogeny of Bromelioideae (Bromeliaceae) inferred from nuclear and plastid DNA loci reveals the evolution of the tank habit within the subfamily.Crossref | GoogleScholarGoogle Scholar |
Silva MDS, Coutinho IAC, Araújo MN, Meira RMSA (2017) Colleters in Chamaecrista (L.) Moench sect. Chamaecrista and sect. Caliciopsis (Leguminosae-Caesalpinioideae): anatomy and taxonomic implications. Acta Botanica Brasílica 31, 382–391.
| Colleters in Chamaecrista (L.) Moench sect. Chamaecrista and sect. Caliciopsis (Leguminosae-Caesalpinioideae): anatomy and taxonomic implications.Crossref | GoogleScholarGoogle Scholar |
Solereder H, Scott DH (1908) ‘Systematic anatomy of the dicotyledons: a handbook for laboratories of pure and applied botany. Vol. 2.’ (Clarendon Press: Oxford, UK)
Spurr AR (1969) A low-viscosity epoxy resin embedding medium for electron microscopy. Journal of Ultrastructure Research 26, 31–43.
| A low-viscosity epoxy resin embedding medium for electron microscopy.Crossref | GoogleScholarGoogle Scholar |
Tavares AR, Giampaoli P, Machado J, Kanashiro S, Chu EP (2015) Structural analysis of the foliar epidermis during acclimatization of Aechmea blanchetiana (Bromeliaceae) in vitro cultured. Horticultura Brasileira 33, 45–50.
| Structural analysis of the foliar epidermis during acclimatization of Aechmea blanchetiana (Bromeliaceae) in vitro cultured.Crossref | GoogleScholarGoogle Scholar |
Thomas V (1991) Structural, functional and phylogenetic aspects of the colleter. Annals of Botany 68, 287–305.
| Structural, functional and phylogenetic aspects of the colleter.Crossref | GoogleScholarGoogle Scholar |
Tomlinson PB (1969) ‘Anatomy of the monocotyledons: III Commelinales-Zingiberales.’ (Claredon Press: London, UK)
Zampieri MCT, Saiki M, Tavares AR, Pinna GFdAMd (2012) Acúmulo de minerais em Aechmea blanchetiana (Baker) L.B. Smith. Hoehnea 39, 379–385.
| Acúmulo de minerais em Aechmea blanchetiana (Baker) L.B. Smith.Crossref | GoogleScholarGoogle Scholar |
Zotz G, Thomas V (1999) How much water is in the tank? Model calculations for two epiphytic bromeliads. Annals of Botany 83, 183–192.
| How much water is in the tank? Model calculations for two epiphytic bromeliads.Crossref | GoogleScholarGoogle Scholar |