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Protoplasma

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Calycinal secretory structures in Calolisianthus pedunculatus (Cham. & Schltdl) Gilg (Gentianaceae): anatomy, histochemistry, and functional aspects

  • Valdnéa Casagrande DalviEmail author
  • Giselle Santos de Faria
  • Aristéa Alves Azevedo
Original Article
  • 11 Downloads

Abstract

Secretory structures were little studied in Gentianaceae. Glandular areas on the calyx dorsal region are commonly reported for Helieae species, the main tribe of Gentianaceae. So, the elucidation of nature of glandular areas is particularly relevant. Trichomes secreting mucilage, interpreted as colleters, are reported only for the sepals of Gentianinae species. We aimed to anatomically characterize and identify the nature of the calycinal secretory structures in Calolisianthus pedunculatus. Samples from floral buds, flowers, and fruits were collected, fixed, and processed following usual procedures for light and scanning electron microscopies. Histochemical tests were performed to determine the nature of the secretion. Glucose, fructose, and sucrose were measured with an ELISA reader. Colleters occur on the sepal ventral region and are composed of a multicellular secretory head and a stalk. These structures secrete polysaccharides and proteins, and the secretion is probably released through cuticle microchannels. Nectaries, on the other hand, occur on the sepal dorsal region. They are formed by 3–5 cells arranged in rosettes circling a central cell or pore. These structures also secrete polysaccharides (mainly fructose), lipids, and proteins. The identification of the secretory structures in the sepals of Calolisianthus pedunculatus highlights the importance of anatomical studies in this family. The interpretation of the glandular areas on the calyx of the Helieae species as nectaries has been proven, as well as the confirmation of colleters as common structures in the sepals of Gentianaceae. Besides the taxonomic and phylogenetic importance of nectars and colleters, we highlight the importance of the secretion for the protection of floral buds against dehydration.

Keywords

Calyx Colleters Mucilage Nectaries Secretion 

Notes

Acknowledgments

We thank the LABMIC (Laboratório Multiusuário de Microscopia de Alta Resolução) at Universidade Federal de Goiânia (UFG, campus Samambaia) for the technical support provided, the Laboratory of Plant Anatomy at Instituto Federal Goiano (IF Goiano, campus Rio Verde) for the anatomical analyses, and the Laboratory of Nutrition and Metabolism of Plants at Universidade Federal de Viçosa (UFV, campus Viçosa) for the nectar analyses. Finally, we thank Analú Zanotti for the chemical analyses of the nectar.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.

References

  1. Appezzato-da-Glória B, Estelita MEM (2000) Development, structure and distribution of colleters in Mandevilla illustris and M. velutina (Apocynaceae). Rev Bras Bot 23:113–120.  https://doi.org/10.1590/S0100-84042000000200001 Google Scholar
  2. Ballego-Campos I, Paiva EAS (2018) Mucilage secretion in the inflorescences of Aechmea blanchetiana: evidence of new functions of scales in Bromeliaceae. Flora 246-247:246–247.  https://doi.org/10.1016/j.flora.2018.06.003 CrossRefGoogle Scholar
  3. Bozzola JJ, Russel LD (1992) Electron microscopy. Jones and Bartlett Publishers, BostonGoogle Scholar
  4. Calió MFA (2009) Sistemática de Helieae Gilg (Gentianaceae). Ph.D. Dissertation, University of São PauloGoogle Scholar
  5. Calió MF, Lepis KB, Pirani JR, Struwe L (2017) Phylogeny of Helieae (Gentianaceae): resolving taxonomic chaos in a Neotropical clade. Mol Phylogenet Evol 106:192–208.  https://doi.org/10.1016/j.ympev.2016.09.013 CrossRefGoogle Scholar
  6. Canaveze Y, Machado SR (2015) Leaf colleters in Tabernaemontana catharinensis (Apocynaceae, Rauvolfioideae): structure, ontogenesis, and cellular secretion. Botany 93:287–296.  https://doi.org/10.1139/cjb-2014-0229 CrossRefGoogle Scholar
  7. Carlquist S (1969) Toward acceptable evolutionary interpretations of floral anatomy. Phytomorphol 19:332–362Google Scholar
  8. Conceição AS, Queiroz LP, Lewis GP et al (2009) Phylogeny of Chamaecrista Moench (Leguminosae-Caesalpinioideae) based on nuclear and chloroplast DNA regions. Taxon 58:1168–1180.  https://doi.org/10.1002/tax.584010 CrossRefGoogle Scholar
  9. Coutinho IAC, 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.  https://doi.org/10.1016/j.flora.2012.03.007 CrossRefGoogle Scholar
  10. Coutinho IAC, Francino DMT, Meira RMSA (2015) New records of colleters in Chamaecrista (Leguminosae, Caesalpinioideae S.L.): structural diversity, secretion, functional role, and taxonomic importance. Int J Plant Sci 176:72–85.  https://doi.org/10.1086/679016 CrossRefGoogle Scholar
  11. Crespo SEM (2003) Revisão taxonômica do gênero Curtia Cham. & Schltdl. (Gentianaceae Juss.). Doctor Science Thesis, Universidade Estadual de Campinas, São PauloGoogle Scholar
  12. 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 CrossRefGoogle Scholar
  13. Dalvi VC, Meira RMSA, 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 CrossRefGoogle Scholar
  14. Dalvi VC, Cardinelli RMSA, Meira AAA (2014b) Foliar colleters in Macrocarpaea obtusifolia (Gentianaceae): anatomy, ontogeny, and secretion. Botany 92:59–67.  https://doi.org/10.1139/cjb-2013-0203 CrossRefGoogle Scholar
  15. Dejean A, Corbara B, Leroy C, Delabie JHC, Rossi V, Céréghino R (2011) Inherited biotic protection in a neotropical pioneer plant. PLoS One 6:18071.  https://doi.org/10.1371/journal.pone.0018071 CrossRefGoogle Scholar
  16. Delgado MN, Azevedo AA, Valente GE, Kasuya MCM (2011a) Comparative anatomy of Calolisianthus species (Gentianaceae - Helieae) from Brazil: taxonomic aspects. Edinb J Bot 68:139–155.  https://doi.org/10.1017/S0960428610000284 CrossRefGoogle Scholar
  17. Delgado MN, Silva LC, Silva SN, Báo HC, Morais HC, Azevedo AA (2011b) 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 CrossRefGoogle Scholar
  18. Demarco D (2017) Floral glands in Asclepiads: structure, diversity and evolution. Acta Bot Bras 31:477–502.  https://doi.org/10.1590/0102-33062016abb0432 CrossRefGoogle Scholar
  19. Elias TS (1983) Extrafloral nectaries: their structure and distribution. In: Bentley BL, Elias TS (eds) The biology of Nectaries. Columbia University Press, New YorkGoogle Scholar
  20. Elias TS, Gelband H (1976) Morphology and anatomy of floral and extrafloral nectaries of Campsis (Bignoniaceae). Am J Bot 63:1349–1353.  https://doi.org/10.2307/2441843 CrossRefGoogle Scholar
  21. Evert RF (2006) Esau’s plant anatomy: meristems, cells and tissues of the plant body: their structure function and development. John Wiley and Sons, New JerseyCrossRefGoogle Scholar
  22. Fahn A (1979) Secretory tissues in plants. Academic Press, LondonGoogle Scholar
  23. Feio AC, Riina R, Meira RMSA (2016) Secretory structures in leaves and flowers of two dragon’s blood Croton (Euphorbiaceae): new evidence and interpretations. Int J Plant Sci 177.  https://doi.org/10.1086/685705
  24. Fernandes VF, Thadeo M, Dalvi VC, Marquete R, Meira RMSA (2016) Colleters in Casearia (Salicaceae): a new interpretation for the theoid teeth. Bot J Linn Soc 181:682–691.  https://doi.org/10.1111/boj.12432 CrossRefGoogle Scholar
  25. Figueiredo ACS, Pais MS (1992) Ultrastructural aspects of the nectary spur of Limodorum abortivum (L.) Sw. (Orchidaceae). Ann Bot 70:325–331 http://www.jstor.org/stable/42764496 CrossRefGoogle Scholar
  26. Furr M, Mahlberg PG (1981) Histochemical analyses of laticifers and glandular trichomes in Cannabis sativa. J Nat Prod 44:153–159.  https://doi.org/10.1021/np50014a002 CrossRefGoogle Scholar
  27. Gabe M (1968) Techniques histologiques. Masson and Cie, ParisGoogle Scholar
  28. Gagliardi KB, Cordeiro I, Demarco D (2016) Protection and attraction: bracts and secretory structures in reduced inflorescences of Malpighiales. Flora 220:52–62.  https://doi.org/10.1016/j.flora.2016.02.003 CrossRefGoogle Scholar
  29. Gilg EF (1895) Gentianaceae. In Engler A, Prantl K (Eds) Die Natürlichen flanzenfamilien, 4. Verlag von Wilhelm Engelmann: LeipzigGoogle Scholar
  30. Gutterman A, Evenri M (1967) Seed dispersal and germination in Blepharis persica (Burm.) Y., Whitztum, Kunze. Isr J Bot 16:213–234Google Scholar
  31. Johansen DA (1940) Plant microtechnique. McGraw-Hill Book Company, New YorkGoogle Scholar
  32. Judd WS, Campbell CS, Kellog EA, Stevens PF (2009) Plant systematics: a phylogenetic approach. Sinauer Associates, SunderlandGoogle Scholar
  33. Klein DE, Gomes VM, Da Silva-Neto SJ, Da 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 CrossRefGoogle Scholar
  34. Lacchia APS, Tölke EEAD, Carmello-Guerreiro SM. et al (2016) Foliar colleters in Anacardiaceae: first report for the family. Botany 337–346.  https://doi.org/10.1139/cjb-2015-0236
  35. Leitão CAE, Cortelazzo AL (2008) Structural and histochemical characterization of the colleters of Rodriguesia venusta (Orchidaceae). Aust J Bot 5:161–165.  https://doi.org/10.1071/BT07114 CrossRefGoogle Scholar
  36. Lillie RD (1965) Histopathologic technic and pratical histochemistry. McGraw Hill, New YorkGoogle Scholar
  37. Macêdo TP, Cortez PA, Costa LCB (2016) First record of colleters in Zanthoxylum Linn. species (Rutaceae Juss., Sapindales): structural, functional and taxonomic considerations. Flora 224:66–74.  https://doi.org/10.1016/j.flora.2016.07.007 CrossRefGoogle Scholar
  38. Mangalan S, Kurien KP, John P, Nair GM (1990) Development, structure and cytochemistry of resin secreting colleters of Gardenia gummifera (Rubiaceae). Ann Bot 66:123–132.  https://doi.org/10.1093/oxfordjournals.aob.a088006 CrossRefGoogle Scholar
  39. Marazzi B, Endress PK, Queiroz LP, Conti E (2006) Phylogenetic relationships within Senna (Leguminosae, Cassinae) based on three chloroplast DNA regions: patterns in the evolution of floral symmetry and extrafloral nectaries. Am J Bot 93:288–303.  https://doi.org/10.3732/ajb.93.2.288 CrossRefGoogle Scholar
  40. Martins FM, Cunha-Neto L, Pereira TM (2016) Floral morphology and anatomy of Dalechampia alata Klotzsch ex Baill. (Euphorbiaceae), with emphasis on secretory structures. Braz J Biol 76:233–244  https://doi.org/10.1590/1519-6984.19514 CrossRefGoogle Scholar
  41. Mayer JLS, Cardoso-Gustavson P, Appezzato-da-Glória B (2011) Colleters in monocots: new record for Orchidaceae. Flora 206:185–190.  https://doi.org/10.1016/jflora.2010.09.0003 CrossRefGoogle Scholar
  42. Mayer JLS, Carmello-Guerreiro SM, Mazzafera P (2013) A functional role for the colleters of coffee flowers. Ann Bot 5:1–13.  https://doi.org/10.1093/aobpla/plt029 Google Scholar
  43. McManus JFA (1948) Histological and histochemical uses of periodic acid. Stain Technol 23:99–108CrossRefGoogle Scholar
  44. Mercadante-Simões MO, Paiva EAS (2013) Leaf colleters in Tontelea micrantha (Celastraceae, Salacioideae): ecological, morphological and structural aspects. C R Biol 336:400–406.  https://doi.org/10.1016/j.crvi.2013.06.007 CrossRefGoogle Scholar
  45. Mészaros S, Laet J, Goethals V, Smets E, Nilsson S (2002) Cladistics of Gentianaceae: A morphological approach. In Struwe L and Albert VA (Eds) Gentianaceae: Systematics and Natural History (pp. 310–376). Cambridge University Press, Cambridge, New York,Google Scholar
  46. Miguel EC, Gomes VM, Oliveira MA, Cunha M (2006) Colleters in Bathysa nicholsonii K. Schum. (Rubiaceae): ultrastructure, secretion protein composition, and antifungal activity. Plant Biol 8:715–722.  https://doi.org/10.1055/s-2006-924174 CrossRefGoogle Scholar
  47. MOBOT (2019) Angiosperm phylogeny website. http://www.mobot.org/MOBOT/research/APweb/. Acessado 03 dez 2018
  48. Morellato LPC, Oliveira PS (1994) Extrafloral nectaries in the tropical tree Guarea macrophylla (Meliaceae). Can J Bot 72(157):160–160.  https://doi.org/10.1139/b94-021 Google Scholar
  49. Nicolson SW, Thornburg RW (2007) Nectar chemistry. In: Nicolson SW, Nepi M, Pacini E (eds) Nectaries and nectar. Springer, Dordrecht, pp 215–264CrossRefGoogle Scholar
  50. O’Brien TP, Mccully ME (1981) The study of plant structure principles and selected methods. Termarcarphi Ptey. Ltd., MelbourneGoogle Scholar
  51. O’Brien TP, Feder N, McCully ME (1964) Polychromatic staining of plant cell walls by toluidine blue O. Protoplasma 59:368–373CrossRefGoogle Scholar
  52. Oliveira CS, Salino A, Paiva EAS (2017) Colleters in Thelypteridaceae: unveiling mucilage secretion and its probable role in ferns. Flora 228:65–70.  https://doi.org/10.1016/j.flora.2017.01.009 CrossRefGoogle Scholar
  53. Paiva EAS (2009) Ultrastructure and post-floral secretion of the pericarpial nectaries of Erythrina speciosa (Fabaceae). Ann Bot 104:937–944.  https://doi.org/10.1093/aob/mcp175 CrossRefGoogle Scholar
  54. Paiva EAS (2012) Colleters in Cariniana estrellensis (Lecythidaceae): structure, secretion and evidences for young leaf protection. J Torrey Bot Soc 139:1–8.  https://doi.org/10.3159/TORREY-D-11-00046.1 CrossRefGoogle Scholar
  55. Paiva EAS, Machado SR (2006) Ontogênese, anatomia e ultra-estrutura dos nectários extraflorais de Hymenaea stigonocarpa Mart. ex Hayne (Fabaceae- Caesalpinioideae). Acta Bot Bras 20:471–482.  https://doi.org/10.1590/S0102-33062006000200022 CrossRefGoogle Scholar
  56. 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 CrossRefGoogle Scholar
  57. Pearse AGE (1985) Histochemistry theoretical and applied: preparative and optical technology. Churchill Livingston, EdinburghGoogle Scholar
  58. Praxedes SC, DaMatta FM, Loureiro ME, Maria MA, Cordeiro AT (2006) Effects of long-term soil drought on photosynthesis and carbohydrate metabolism in mature robusta coffee (Coffea canephora Pierre var. kouillou) leaves. Environ Exp Bot 56:263–273.  https://doi.org/10.1016/j.envexpbot.2005.02.008 CrossRefGoogle Scholar
  59. Rasmussen H (1981) Terminology and classification of stomata and stornatal development-a critical survey. Bot J Linn Soc 83:199–212.  https://doi.org/10.1111/j.1095-8339.1981.tb00345.x CrossRefGoogle Scholar
  60. 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 CrossRefGoogle Scholar
  61. 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 CrossRefGoogle Scholar
  62. Schmid R, (1988) Reproductive versus extra-reproductive nectaries—historical perspective and terminological recommendations. The Botanical Review 54(2):179–227Google Scholar
  63. Silva CJA, Barbosa LCA, Marques AE, Baracat-Pereira MC, Pinheiro AL, Meira RMSA (2012) Anatomical characterization of the foliar colleters in Myrtoideae (Myrtaceae). Aust J Bot 60:707–717.  https://doi.org/10.1071/BT12149 CrossRefGoogle Scholar
  64. Silva MS, Coutinho IAC, Araújo MN, Meira RMSA (2017) Colleters in Chamaecrista (L.) Moench sect. Chamaecrista and sect. Caliciopsis (Leguminosae-Caesalpinioideae): anatomy and taxonomic implications. Acta Bot Bras 31:381–392.  https://doi.org/10.1590/0102-33062016abb0339 Google Scholar
  65. Simões AO, Castro M, 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 CrossRefGoogle Scholar
  66. Stpiczynska M, Davies KL, Gregg A (2005) Comparative account of nectary structure in Hexisea imbricata (Lindl.) Rchb. f. (Orchidaceae). Ann Bot 95:749–756.  https://doi.org/10.1093/aob/mci081 CrossRefGoogle Scholar
  67. Struwe L, Kadereit JW, Klackenberg J, Nilsson S, Thiv M, Von-Hagen KB, Albert VA (2002) Systematics, character evolution, and biogeography of Gentianaceae, incluinding a new tribal and subtribal classification. In: Struwe L, Albert VA (eds) Gentianaceae: Systematics and Natural History. Cambridge University Press, CambridgeGoogle Scholar
  68. Thomas V (1991) Review article. Structural, functional and phylogenetic aspects of the colleter. Ann Bot 68:287–305.  https://doi.org/10.1093/oxfordjournals.aob.a088256 CrossRefGoogle Scholar
  69. Thomas V, Dave Y (1989a) Structure, origin, development and senescence of colleters in Nerium indicum Mill. (N. odorum Soland., Apocynaceae). Kor J Bot 32:163–172Google Scholar
  70. Thomas V, Dave Y (1989b) Histochemistry and senescence of colleters of Allamanda cathartica (Apocynaceae). Ann Bot 64:201–203.  https://doi.org/10.1093/oxfordjournals.aob.a087826 CrossRefGoogle Scholar
  71. Vitarelli NC, Santos M (2009) Anatomia de estípulas e coléteres de Psychotria carthagenensis Jacq. (Rubiaceae). Act Bot Bras 23:923–928.  https://doi.org/10.1590/S0102-33062009000400002 CrossRefGoogle Scholar
  72. Vitarelli NC, Riina R, Caruzo MBR, Cordeiro I, Fuertes-Aguilar J, Meira RMSA (2015) Foliar secretory structures in Crotoneae (Euphorbiaceae): diversity, anatomy, and evolutionary significance. Am J Bot 12:1–15.  https://doi.org/10.3732/ajb.1500017 Google Scholar
  73. 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 CrossRefGoogle Scholar
  74. Wagenitz G (1999) Botanical terminology and homology in their historical context. Syst Geogr P1 68:33–37 https://www.jstor.org/stable/3668587 CrossRefGoogle Scholar
  75. Wandersee JH (1988) The terminology problem in biology education: a reconnaissance. Am Biol Teach 50:97–100 https://www.jstor.org/stable/4448654 CrossRefGoogle Scholar
  76. Weber MG, Keeler KH (2013) The phylogenetic distribution of extrafloral nectaries in plants. Ann Bot 11:1251–1261.  https://doi.org/10.1093/aob/mcs225 CrossRefGoogle Scholar

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Authors and Affiliations

  1. 1.Programa de Pós-Graduação em Biodiversidade e Conservação, Instituto Federal de EducaçãoCiência e Tecnologia Goiano (IF Goiano, Campus Rio Verde)Rio VerdeBrazil
  2. 2.Programa de Pós-Graduação em Ciências Agrárias, Instituto Federal de EducaçãoCiência e Tecnologia Goiano (IF Goiano, Campus Rio Verde)Rio VerdeBrazil
  3. 3.Programa de Pós-Graduação em Botânica, Departamento de Biologia VegetalUniversidade Federal de Viçosa (UFV)ViçosaBrazil

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