Register      Login
Australian Journal of Botany Australian Journal of Botany Society
Southern hemisphere botanical ecosystems
RESEARCH ARTICLE

Secretory and ecological function of petiolar glands in Solanum fernandesii: first description of resin glands in the genus Solanum

Valéria da Silva Sampaio https://orcid.org/0000-0002-6551-8877 A * , Ítalo Antônio Cotta Coutinho A , Tiina Särkinen B and Maria Iracema Bezerra Loiola A
+ Author Affiliations
- Author Affiliations

A Universidade Federal do Ceará, Departamento de Biologia, Programa de Pós-Graduação em Ecologia e Recursos Naturais, Bloco 906, Campus do Pici Prof. Prisco Bezerra, 60440-900, Fortaleza, Ceará, Brazil.

B Royal Botanic Garden Edinburgh, 20A Inverleith Row, Edinburgh EH3 5LR, UK.

* Correspondence to: valeriasampaiobio@gmail.com

Handling Editor: Noushka Reiter

Australian Journal of Botany 70(1) 32-41 https://doi.org/10.1071/BT21001
Submitted: 1 January 2021  Accepted: 15 August 2021   Published: 23 November 2021

© 2022 The Author(s) (or their employer(s)). Published by CSIRO Publishing

Abstract

Extrafloral nectaries are known from many plant groups but have rarely been recorded in the large genus Solanum or, in fact, in the family Solanaceae. This study set out to explore the functional role of the extrafloral nectaries recently described in Solanum fernandesii, a species endemic to north-eastern Brazil. Light and scanning electron microscopy was used to study the morphoanatomical structure of the nectaries and histochemical analyses were performed to study the chemical composition of the exudates recovered from the glands on the basis of field studies. Light and scanning electron microscopy show that although the petiolar glands in S. fernandesii appear sessile to the naked eye, the glands are short stalked. The epidermis of the glands is composed of short, tightly packed multicellular trichomes. The gland secretions contain a mixture of polysaccharides, pectins, mucilage, proteins, lipids, essential oils, resins, and phenolic compounds on the basis of histochemical tests performed. These findings confirm that the petiolar glands in S. fernandesii are in fact resin glands and not extrafloral nectaries as previously claimed. Our study is the first report of resin glands in the large genus Solanum and we confirm that the glands found in S. fernandesii are unique in the genus.

Keywords: secretory structures, Solanoideae, trichomes.


References

Alvares CA, Stape JL, Sentelhas PC, Moraes Gonçalves JL, Sparovek G (2013) Köppen’s climate classification map for Brazil. Meteorologische Zeitschrift 22, 711–728.
Köppen’s climate classification map for Brazil.Crossref | GoogleScholarGoogle Scholar |

Anderson GJ, Symon DE (1985) Extrafloral nectaries in Solanum. Biotropica 17, 40–45.
Extrafloral nectaries in Solanum.Crossref | GoogleScholarGoogle Scholar |

Anil Kumar VS, Sunila AV, Murugan K (2017) Foliar trichomes and their systematic relevance in Solanum (Solanaceae) species from southern Western Ghats, Kerala. Rheedea 27, 119–131.
Foliar trichomes and their systematic relevance in Solanum (Solanaceae) species from southern Western Ghats, Kerala.Crossref | GoogleScholarGoogle Scholar |

Armbruster WS (1984) The role of resin in angiosperm pollination: ecological and chemical considerations. American Journal of Botany 71, 1149
The role of resin in angiosperm pollination: ecological and chemical considerations.Crossref | GoogleScholarGoogle Scholar |

Buchmann SL (1983) Buzz pollination in Angiosperms. In ‘Handbook of experimental pollination biology’. (Eds CE Jones, RJ Little) pp. 73–113. (Scientific and Academic Editions, Van Nostrand Reinhold)

Cardoso-Gustavson P, Andreazza NL, Sawaya ACHF, Castro MM (2013) Only attract ants? The versatility of petiolar extrafloral nectaries in Passiflora. American Journal of Plant Sciences 4, 460–469.
Only attract ants? The versatility of petiolar extrafloral nectaries in Passiflora.Crossref | GoogleScholarGoogle Scholar |

Caspary R (1848) ‘De nectariis.’ (Elverfeld: Bonnae)

Castro MM, Demarco D (2008) Phenolic compounds produced by secretory structures in plants: a brief review. Natural Product Communications 3, 1273–1284.

Costa ISC, Lucena EMP, Bonilla OH, Guesdon IR, Coutinho ÍAC (2020) Seasonal variation in colleter exudates in Myrcia splendens (Myrtaceae). Australian Journal of Botany 68, 403
Seasonal variation in colleter exudates in Myrcia splendens (Myrtaceae).Crossref | GoogleScholarGoogle Scholar |

Coutinho ÍAC, Francino DMT, Azevedo AA, Meira RMSA (2012) Anatomy of the extrafloral nectaries in species of Chamaecrista section Absus subsection Baseophyllum (Leguminosae, Caesalpinioideae). Flora 207, 427–435.
Anatomy of the extrafloral nectaries in species of Chamaecrista section Absus subsection Baseophyllum (Leguminosae, Caesalpinioideae).Crossref | GoogleScholarGoogle Scholar |

Coutinho ÍAC, Meira RMSA (2015) Structural diversity of extrafloral nectaries in Chamaecrista sect. Apoucouita. Botany 93, 379–388.
Structural diversity of extrafloral nectaries in Chamaecrista sect. Apoucouita.Crossref | GoogleScholarGoogle Scholar |

Curry KJ, McDowell LM, Judd WS, Stern WL (1991) Osmophores, floral features, and systematics of Stanhopea (Orchidaceae). American Journal of Botany 78, 610–623.
Osmophores, floral features, and systematics of Stanhopea (Orchidaceae).Crossref | GoogleScholarGoogle Scholar |

Curtis JD, Lersten NR (1978) Heterophylly in Populus grandidentata (Salicaceae) with emphasis on resin glands and extrafloral nectaries. American Journal of Botany 65, 1003–1010.
Heterophylly in Populus grandidentata (Salicaceae) with emphasis on resin glands and extrafloral nectaries.Crossref | GoogleScholarGoogle Scholar |

Curtis JD, Lersten NR (1980) Morphology and anatomy of resin glands in Salix lucida (Salicaceae). American Journal of Botany 67, 1289–1296.
Morphology and anatomy of resin glands in Salix lucida (Salicaceae).Crossref | GoogleScholarGoogle Scholar |

David R, Carde JP (1964) Coloration differentielle des inclusions lipidique et terpeniques des pseudophylles du Pin maritime au moyen du reactif Nadi. Comptes Rendus de I’Academie des Sciences Paris 258, 1338–1340.

Dell B, McComb AJ (1979) Plant resins—their formation, secretion and possible functions. Advances in Botanical Research 6, 277–316.
Plant resins—their formation, secretion and possible functions.Crossref | GoogleScholarGoogle Scholar |

Dufaÿ M, Hossaert-McKey M, Anstett MC (2003) When leaves act like flowers: how dwarf palms attract their pollinators. Ecology Letters 6, 28–34.
When leaves act like flowers: how dwarf palms attract their pollinators.Crossref | GoogleScholarGoogle Scholar |

Durkee LT, Baird CW, Cohen PF (1984) Light and electron microscopy of the resin glands of Passiflora foetida (Passifloraceae). American Journal of Botany 71, 596–602.
Light and electron microscopy of the resin glands of Passiflora foetida (Passifloraceae).Crossref | GoogleScholarGoogle Scholar |

Fahn A (1979) ‘Secretory tissues in plants.’ (Academic Press: London, UK)

Fahn A (1988) Secretory tissues in vascular plants. New Phytologist 108, 229–257.
Secretory tissues in vascular plants.Crossref | GoogleScholarGoogle Scholar |

Falcão PF, Melo-de-Pinna GFA, Leal IR, Almeida-Cortez JS (2003) Morphology and anatomy of extrafloral nectaries in Solanum stramonifolium (Solanaceae). Canadian Journal of Botany 81, 859–864.
Morphology and anatomy of extrafloral nectaries in Solanum stramonifolium (Solanaceae).Crossref | GoogleScholarGoogle Scholar |

Francino DMT, Sant’Anna-Santos BF, Silva KLF, Thadeo M, Meira RMSA, Azevedo AA (2006) Anatomia foliar e caulinar de Chamaecrista trichopoda (Caesalpinioideae) e histoquímica do nectário extrafloral. Planta Daninha 24, 695–705.
Anatomia foliar e caulinar de Chamaecrista trichopoda (Caesalpinioideae) e histoquímica do nectário extrafloral.Crossref | GoogleScholarGoogle Scholar |

Freitas L, Bernardello G, Galetto L, Paoli AAS (2001) Nectaries and reproductive biology of Croton sarcopetalus (Euphorbiaceae). Botanical Journal of the Linnean Society 136, 267–277.
Nectaries and reproductive biology of Croton sarcopetalus (Euphorbiaceae).Crossref | GoogleScholarGoogle Scholar |

Frodin DG (2004) History and concepts of big plant genera. TAXON 53, 753–776.
History and concepts of big plant genera.Crossref | GoogleScholarGoogle Scholar |

Gagliardi KB, Cordeiro I, Demarco D (2017) Flower development in species of Croton (Euphorbiaceae) and its implications for floral morphological diversity in the genus. Australian Journal of Botany 65, 538–549.
Flower development in species of Croton (Euphorbiaceae) and its implications for floral morphological diversity in the genus.Crossref | GoogleScholarGoogle Scholar |

Gastauer M, Campos LAO, Wittmann D (2011) Handling sticky resin by stingless bees (Hymenoptera, Apidae). Revista Brasileira de Entomologia 55, 234–240.
Handling sticky resin by stingless bees (Hymenoptera, Apidae).Crossref | GoogleScholarGoogle Scholar |

Heil M (2011) Nectar: generation, regulation and ecological functions. Trends in Plant Science 16, 191–200.
Nectar: generation, regulation and ecological functions.Crossref | GoogleScholarGoogle Scholar | 21345715PubMed |

Heil M, Rattke J, Boland W (2005) Postsecretory hydrolysis of nectar sucrose and specialization in ant/plant mutualism. Science 308, 560–563.
Postsecretory hydrolysis of nectar sucrose and specialization in ant/plant mutualism.Crossref | GoogleScholarGoogle Scholar | 15845855PubMed |

Hetherington-Rauth MC, Ramírez SR (2016) Evolution and diversity of floral scent chemistry in the euglossine bee-pollinated orchid genus Gongora. Annals of Botany 118, 135–148.
Evolution and diversity of floral scent chemistry in the euglossine bee-pollinated orchid genus Gongora.Crossref | GoogleScholarGoogle Scholar | 27240855PubMed |

Hunziker AT (2001) ‘Genera Solanacearum: the genera of Solanaceae illustrated, arranged according to a new system.’ (A.R.G. Gantner Verlag: Ruggell, Liechtenstein)

Johansen DA (1940) ‘Plant microtechnique.’ (McGraw-Hill Book: New York, NY, USA)

Judd WS, Campbell CS, Kellogg EA, Stevens PF, Donoghue MJ (2008) ‘Plant systematics: a phylogenetic approach.’ (Sinauer Associates: Sunderland, MA, USA)

Karnovsky MJJ (1965) A formaldehyde-glutaraldehyde fixative of high osmolality for use in electron microscopy. The Journal of Cell Biology 27, 137–138.

Keeler KH (1979) Species with extrafloral nectaries in a temperate flora (Nebraska). Prairie Naturalist 11, 33–38.

King MJ, Buchmann SL (2003) Floral sonication by bees: mesosomal vibration by Bombus and Xylocopa, but not Apis (Hymenoptera: Apidae), ejects pollen from poricidal anthers. Journal of the Kansas Entomological Society 76, 295–305.

Knapp S (2008) A revision of the Solanum havanense species group and new taxonomic additions to the geminata clade (Solanum, Solanaceae). Annals of the Missouri Botanical Garden 95, 405–458.
A revision of the Solanum havanense species group and new taxonomic additions to the geminata clade (Solanum, Solanaceae).Crossref | GoogleScholarGoogle Scholar |

Knapp S, Barboza GE, Bohs L, Särkinen T (2019) A revision of the Morelloid Clade of Solanum L. (Solanaceae) in North and Central America and the Caribbean. PhytoKeys 123, 1–144.
A revision of the Morelloid Clade of Solanum L. (Solanaceae) in North and Central America and the Caribbean.Crossref | GoogleScholarGoogle Scholar | 31198402PubMed |

Krömer T, Kessler M, Lohaus G, Schmidt-Lebuhn AN (2008) Nectar sugar composition and concentration in relation to pollination syndromes in Bromeliaceae. Plant Biology 10, 502–511.
Nectar sugar composition and concentration in relation to pollination syndromes in Bromeliaceae.Crossref | GoogleScholarGoogle Scholar | 18557910PubMed |

Lemos RCC, Silva DC, Melo-de-Pinna GFA (2017) A structural review of foliar glands in Passiflora L. (Passifloraceae). PLoS One 12, e0187905
A structural review of foliar glands in Passiflora L. (Passifloraceae).Crossref | GoogleScholarGoogle Scholar | 29136029PubMed |

Lortzing T, Calf OW, Böhlke M, Schwachtje J, Kopka J, Geuß D, Kosanke S, Van Dam NM, Steppuhn A (2016) Extrafloral nectar secretion from wounds of Solanum dulcamara. Nature Plants 2, 16056
Extrafloral nectar secretion from wounds of Solanum dulcamara.Crossref | GoogleScholarGoogle Scholar | 27243650PubMed |

Martine CT, Jordon-Thaden IE Martine CT, Jordon-Thaden IE (2019) Phylogeny of the Australian Solanum dioicum group using seven nuclear genes, with consideration of Symon’s fruit and seed dispersal hypotheses. PLoS ONE 14, e0207564
Phylogeny of the Australian Solanum dioicum group using seven nuclear genes, with consideration of Symon’s fruit and seed dispersal hypotheses.Crossref | GoogleScholarGoogle Scholar | 30998778PubMed |

Matias LJ, Mercadante-Simões MO, Royo VA, Ribeiro LM, Santos AC, Fonseca JMS (2016) Structure and histochemistry of medicinal species of Solanum. Revista Brasileira de Farmacognosia 26, 147–160.
Structure and histochemistry of medicinal species of Solanum.Crossref | GoogleScholarGoogle Scholar |

Mayer JLS, Cardoso-Gustavson P, Appezzato-da-Glória B (2011) Colleters in monocots: new record for Orchidaceae. Flora - Morphology, Distribution, Functional Ecology of Plants 206, 185–190.
Colleters in monocots: new record for Orchidaceae.Crossref | GoogleScholarGoogle Scholar |

Meira RMSA, Francino DMT, Ascensão L (2014) Oleoresin trichomes of Chamaecrista dentata (Leguminosae): structure, function, and secretory products. International Journal of Plant Sciences 175, 336–345.
Oleoresin trichomes of Chamaecrista dentata (Leguminosae): structure, function, and secretory products.Crossref | GoogleScholarGoogle Scholar |

Meira RMSA, Miranda JDB, Coutinho ÍAC (2020) Anatomical reevaluation and novelties on the leaf marginal tooth glands in Sapium glandulosum (L.) Morong. (Euphorbiaceae): the importance of distinguishing colleters from nectaries. In ‘Plant ontogeny: studies, analyses and evolutionary implications’. (Ed. D Demarco) pp. 63–82. (Nova Science Publishers, Inc.: New York, NY, USA)

Moro MF, Macedo MB, Moura-Fé MM, Castro ASF, Costa RC (2015) Vegetação, unidades fitoecológicas e diversidade paisagística do estado do Ceará. Rodriguésia 66, 717–743.
Vegetação, unidades fitoecológicas e diversidade paisagística do estado do Ceará.Crossref | GoogleScholarGoogle Scholar |

Nepi M, Guarnieri M, Mugnaini S, Cresti L, Pacini E, Piotto B (2005) A modified FCR test to evaluate pollen viability in Juniperus communis L. Grana 44, 148–151.
A modified FCR test to evaluate pollen viability in Juniperus communis L.Crossref | GoogleScholarGoogle Scholar |

Nicolson SW, Nepi M, Pacini E (2007) ‘Nectaries and nectar.’ (Springer: Dordrecht, Netherlands)

Nobel PS, Cavelier J, Andrade JL (1992) Mucilage in cacti: its apoplastic capacitance, associated solutes, and influence on tissue water relations. Journal of Environmental Quality 43, 641–648.

O’Brien TP, McCully ME (1981) ‘The study of plant structure: principles and selected methods.’ (Termarcarphi Pty Ltd: Melbourne, Vic., Australia)

Pearse AGE (1980) ‘Histochemistry theoretical and applied.’ (Churchill Livingston: Edinburgh, UK)

Rocha DI, Silva LC, Valente VMM, Francino DMT, Meira RMSA (2009) Morphoanatomy and development of leaf secretory structures in Passiflora amethystina Mikan (Passifloraceae). Australian Journal of Botany 57, 619
Morphoanatomy and development of leaf secretory structures in Passiflora amethystina Mikan (Passifloraceae).Crossref | GoogleScholarGoogle Scholar |

Roe KE (1972) A revision of Solanum section Brevantherum (Solanaceae). Brittonia 24, 239
A revision of Solanum section Brevantherum (Solanaceae).Crossref | GoogleScholarGoogle Scholar |

Roshchina VV, Roshchina VD (1993) ‘The excretory function of higher plants.’ (Springer-Verlag: Berlin, Germany)
| Crossref |

Roubik DW (2006) Stingless bee nesting biology. Apidologie 37, 124–143.
Stingless bee nesting biology.Crossref | GoogleScholarGoogle Scholar |

Roy R, Schmitt AJ, Thomas JB, Carter CJ (2017) Review: nectar biology: from molecules to ecosystems. Plant Science 262, 148–164.
Review: nectar biology: from molecules to ecosystems.Crossref | GoogleScholarGoogle Scholar | 28716410PubMed |

Sadala-Castilho R, Machado SR, Sá-Haiad B, Lima HA (2016) Oil-resin glands in Velloziaceae flowers: structure, ontogenesis and secretion. Plant Systematics and Evolution 302, 585–599.
Oil-resin glands in Velloziaceae flowers: structure, ontogenesis and secretion.Crossref | GoogleScholarGoogle Scholar |

Sampaio VS, Moura RL, Loiola MIB (2016) Solanum fernandesii (Solanaceae): a new species of ‘spiny solanum’ of the gardneri clade from northeastern Brazil. Phytotaxa 270, 33–40.
Solanum fernandesii (Solanaceae): a new species of ‘spiny solanum’ of the gardneri clade from northeastern Brazil.Crossref | GoogleScholarGoogle Scholar |

Särkinen T, Bohs L, Olmstead RG, Knapp S (2013) A phylogenetic framework for evolutionary study of the nightshades (Solanaceae): a dated 1000-tip tree. BMC Evolutionary Biology 13, 214
A phylogenetic framework for evolutionary study of the nightshades (Solanaceae): a dated 1000-tip tree.Crossref | GoogleScholarGoogle Scholar | 24283922PubMed |

Särkinen T, Poczai P, Barboza GE, van der Weerden GM, Baden M, Knapp S (2018) A revision of the Old World black nightshades (morelloid clade of Solanum L., Solanaceae. PhytoKeys 106, 1–223.
A revision of the Old World black nightshades (morelloid clade of Solanum L., Solanaceae.Crossref | GoogleScholarGoogle Scholar |

Silva EO, Feio AC, Cardoso-Gustavson P, Milward-De-Azevedo MA, Santos JUM, Aguiar Dias ACA (2017) Extrafloral nectaries and plant–insect interactions in Passiflora L. (Passifloraceae). Brazilian Journal of Botany 40, 331–340.
Extrafloral nectaries and plant–insect interactions in Passiflora L. (Passifloraceae).Crossref | GoogleScholarGoogle Scholar |

Simpson MG (2006) ‘Plant systematics.’ (Elsevier Academic Press: Amsterdan, Netherlands)

Singh K, Naidoo Y, Bharuth V, Baijnath H (2019) Micromorphology and histochemistry of the secretory apparatus of Plumbago auriculata Lam. South African Journal of Botany 121, 230–238.
Micromorphology and histochemistry of the secretory apparatus of Plumbago auriculata Lam.Crossref | GoogleScholarGoogle Scholar |

Spiteller D (2008) Plant defense strategies. In ‘Encyclopedia of ecology’. (Eds SE Jørgensen, BD Fath) pp. 2798–2811. (Elsevier: Amsterdam, Netherlands)
| Crossref |

Stern S, Fátima Agra M, Bohs L (2011) Molecular delimitation of clades within new world species of the ‘spiny solanums’ (Solanum subg. Leptostemonum. TAXON 60, 1429–1441.
Molecular delimitation of clades within new world species of the ‘spiny solanums’ (Solanum subg. Leptostemonum.Crossref | GoogleScholarGoogle Scholar | 32327851PubMed |

Tsoar H, Levin N, Porat N, Maia LP, Herrmann HJ, Tatumi SH, Claudino-Sales V (2009) The effect of climate change on the mobility and stability of coastal sand dunes in Ceará State (NE Brazil). Quaternary Research 71, 217–226.
The effect of climate change on the mobility and stability of coastal sand dunes in Ceará State (NE Brazil).Crossref | GoogleScholarGoogle Scholar |

Villamil N, Márquez-Guzmán J, Boege K (2013) Understanding ontogenetic trajectories of indirect defence: ecological and anatomical constraints in the production of extrafloral nectaries. Annals of Botany 112, 701–709.
Understanding ontogenetic trajectories of indirect defence: ecological and anatomical constraints in the production of extrafloral nectaries.Crossref | GoogleScholarGoogle Scholar | 23380241PubMed |

Vogel S (1990) ‘Role scent glands in pollination: on the structure and function of osmophores.’ (Smithsonian Institution Libraries, Washington, DC, USA)

Wagner GJ, Wang E, Shepherd RW (2004) New approaches for studying and exploiting an old protuberance, the plant trichome. Annals of Botany 93, 3–11.
New approaches for studying and exploiting an old protuberance, the plant trichome.Crossref | GoogleScholarGoogle Scholar | 14678941PubMed |

Werker E (2000) Trichome diversity and development. Advances in Botanical Research 31, 1–35.
Trichome diversity and development.Crossref | GoogleScholarGoogle Scholar |

Western TL (2012) The sticky tale of seed coat mucilages: production, genetics, and role in seed germination and dispersal. Seed Science Research 22, 1–25.
The sticky tale of seed coat mucilages: production, genetics, and role in seed germination and dispersal.Crossref | GoogleScholarGoogle Scholar |

Williams NH, Whitten WM (1983) Orchid floral fragrances and male euglossine bees: methods and ad- vances in the last sesquidecade.