pp 1–17 | Cite as

New trends in Passiflora L. pollen grains: morphological/aperture aspects and wall layer considerations

  • Jaiana Richardo
  • Adriano SilvérioEmail author
Original Article


Passifloraceae shows a huge variability of pollen wall characteristics, most still little described. Passiflora is the largest genus with about 580 species with tropical distribution. Few studies in palynological approaches have described the intine layer which can fill existent gaps. Passiflora L. present four subgenera, from which Passiflora, Astrophea, and Decaloba were described in this study. The pollen wall variations were poorly studied, with the objective of describing the morphological and histochemical structure of Passiflora sporoderm that occurs in South America, aims to supply more pollen wall characters in some contexts. Besides the inference of evolutive trends, we described the number of apertures, type, reticule, and variations of the morphology and sporoderm and we related them with possible evolutive trends for the group. As a result, the pollen grains were not far from the patterns found by the literature, with exceptions. The species of the subgenus Passiflora have fused colpi, varying from 6 to 12 colpi, with type 2-reticulate exine. The species of the subgenus Astrophea have colporus and the species of Decaloba varied as the type of aperture, in which a new type of exine to be considered was found: the type 3. The subgenus Passiflora showed the thickest intine, slim endexine, and absent foot layer. While the species that belong to the other subgenera present a slim intine, the endexine is thick and the foot layer is continuous, among other variable characteristics. The size of the pollen grain seems to be related to the thickness of the intine, and consequently, related to possible pollinators. Through the cluster analysis, we reinforce the affinity of the species to its respective subgenus. To conclude, the analysis of the ultrastructure of the sporoderm and external morphology would be useful for an almost complete interpretation of the variations occurring in the genus, giving more information that the subgenus Passiflora is apomorphic when compared to the other two. The pollen wall characters should be considered on the interpretation of natural history, as well as the phylogenetic relationships of the family, mainly in the Passiflora genus, that has a large number of species distributed across the Neotropical regions.


Intine Sporoderm Palynology Pollination Pollen wall structure 



The authors would like to thank Adriana Carolina Aguirre Morales and Miguel Bonilla Morales for their help in collecting fields in Colombia and the Laboratório de Genética e Evolução, Laboratório de Bioenergia and Centro de Ciências Moleculares e Nanotecnologia da UNICENTRO for support during the image collection. The article is part of the dissertation of the first author that was sponsored by a CAPES master’s degree scholarship.

Compliance with ethical standards

Conflict of interest

The authors declare that they have no conflict of interest.


  1. Abrahamczyk S, Souto-Vilarós D, Renner SS (2014) Escape from extreme specialization: passionflowers, bats and the sword-billed hummingbird. Proc R Soc B 281:20140888. CrossRefGoogle Scholar
  2. Amela Garcia MT, Galati BG, Anton AM (2002) Microsporogenesis microgametogenesis and pollen morphology of Passiflora spp. (Passifloraceae). Bot J Linn Soc 139:383–394. CrossRefGoogle Scholar
  3. Amorim JS, Souza MM, Viana AJC et al (2014) Cytogenetic, molecular and morphological characterization of Passiflora capsularis L. and Passiflora rubra L. Plant Syst Evol 300:1147–1162. CrossRefGoogle Scholar
  4. APG IV (2016) An update of the angiosperm phylogeny group classification for the orders and families of flowering plants: APG IV. Bot J Linn Soc 300:1147–1162. Google Scholar
  5. Araújo RCM, Santos FA (2004) Palinologia de espécies do gênero Passiflora L. (Passifloraceae) da Chapada Diamantina, Bahia, Brasil. Sitientibus Ser Cienc Biol 4:37–42Google Scholar
  6. Barrios L, Caetano CM, Cardoso CI, Eeckenbrugge GC, Arroyave, JÁ, Olaya CA (2005) Caracterización del polen de especies de los gêneros Passiflora y Dilkea. Acta Agron 54(3):19–23Google Scholar
  7. Corbet SA, Beament L, Eisikowitch D (1982) Are electrostatic forces involved in pollen transfer? Plant Cell Environ 5:125–129Google Scholar
  8. Costa M, Pereira A, Rudall P, Coimbra JS (2013) Immunolocalization of arabinogalactan proteins (AGPs) in reproductive structures of an early-divergent angiosperm, Trithuria (Hydatellaceae). Ann Bot 111:183–190. CrossRefGoogle Scholar
  9. Deginani NB (2001) Las especies argentinas del género Passiflora (Passifloraceae). Darwiniana 39:43–129Google Scholar
  10. Dettke GA, Santos RP (2009) Tipos de aberturas dos grãos de pólen de espécies de Passiflora L. (Passifloraceae). Acta Bot Bras 23:1119–1129CrossRefGoogle Scholar
  11. Dettke GA, Santos RP (2011) Morfologia externa, anatomia e histoquímica da antera e grãos de pólen de Passifloraceae do Rio Grande do Sul, Brasil. Rev Bras Biol 9(S1)Google Scholar
  12. Edlund AF, Swanson R, Preuss D (2004) Pollen and stigma structure and function: the role of diversity in pollination. Plant Cell 16(S1):S84–S97. CrossRefGoogle Scholar
  13. El-Tantawy AA, Solis M-T, Risueno MC, Testillano PS (2014) Changes in DNA methylation levels and nuclear distribution patterns after microspore reprogramming to embryogenesis in barley. Cytogenet Genome Res 143:200–208. CrossRefGoogle Scholar
  14. Erdtman G (1952) Pollen morphology and plant taxonomy – angiosperms. Almqvist & Wiksell, StockholmGoogle Scholar
  15. Erdtman G (1960) The acetolysis method. A revised description. Svensk Bot Tidskr 39:561–564Google Scholar
  16. Erdtman G (1969) Handbook of palynology. Munksgaard, CopenhagenGoogle Scholar
  17. Evaldt ACP, Bauermann SG, Cancelli RR, Acioli M, Neves PCP (2011) Morfologia polínica de Passifloraceae Juss. ex Kunth. no Rio Grande do Sul, Brasil. Rev Bras Biol 9:75–87Google Scholar
  18. Faegri K, Iversen J (1964) Textbook of pollen analysis. Blackwell Scientific Publications, OxfordGoogle Scholar
  19. Fazal H, Ahmad N, Abbasi BH (2013) Identification, characterization, and palynology of high-valued medicinal plants. Sci World J 2013:1–9CrossRefGoogle Scholar
  20. Feuillet C, MacDougal JM (2003) A new infrageneric classification of Passiflora L. (Passifloraceae). Passiflora 13:34–35 37–38Google Scholar
  21. Feuillet C, MacDougal JM (2007) The families and genera of vascular plants. In: Kubitzki K (ed) Passifloraceae. Springer, BerlinCrossRefGoogle Scholar
  22. Galen C (1999) Why do flowers vary? The functional ecology of variation in flower size and form within natural plant populations. BioScience 49:631–640CrossRefGoogle Scholar
  23. Gerrits PO, Smith L (1983) A new, less toxic polimerization system for the embedding of soft tissue in glycol methacrylate and subsequent preparing of serial section. J Microsc 132:81–85CrossRefGoogle Scholar
  24. Gottsberger G, Camargo JMF, Silberbauer-Gottsberger I (1988) A bee-pollinated tropical community: the beach dune vegetation of Ilha de São Luiz, Maranhão, Brazil. Bot Jahrb Syst 109(4):469–500. Google Scholar
  25. Hansen AK, Gilbert LE, Simpson BB, Downie S-R, Cervi AC, Jansen RK (2006) Phylogenetic relationships and chromosome number evolution in Passiflora. Syst Bot 31:138–150CrossRefGoogle Scholar
  26. Herrera CM (1988) Variation in mutualisms: the spatiotemporal mosaic of a pollinator assemblage. Bio J Linn Soc 35:95–125CrossRefGoogle Scholar
  27. Heslop-Harrison Y (1977) The pollen–stigma interaction: pollen-tube penetration in Crocus. Ann Bot 41:913–922CrossRefGoogle Scholar
  28. Heslop-Harrison J, Heslop-Harrison Y (1991) Structural and functional variation in pollen intines. In: Blackmore S, Barnes S-H (eds) Pollen and spores: patterns of diversification. Clarendon Press, OxfordGoogle Scholar
  29. Hesse M (2000) Pollen wall stratification and pollination. Plant Syst Evol 222:1–17. CrossRefGoogle Scholar
  30. Janzen DH (1968) Reproductive behaviour in the Passifloraceae and some of its pollinators in the Central America. Behavior 32:33–48CrossRefGoogle Scholar
  31. Johansen DA (1940) Plant microtechnique. McGraw-Hill Book, New YorkGoogle Scholar
  32. Johnson SD, Steiner KE (2000) Generalization versus specialization in plant pollination systems. Trends Ecol Evol 15:140–143CrossRefGoogle Scholar
  33. Judd WS, Campbell CS, Kellogg EA, Stevens PF, Donoghue MJ (2015) A phylogenetic approach. Sinauer Associates, Inc, SunderlandGoogle Scholar
  34. Knox RB (1984) The pollen grain. In: Johri BM (ed) Embryology of angiosperms. Springer-Verlag, Berlin, pp 197–271CrossRefGoogle Scholar
  35. Kohler E (1976) Pollen dimorphism and heterostyly in the genus Waltheria L. (Sterculiaceae). In: Ferguson IK, Muller J (eds) The evolutionary significance of the exine, pp 147–161Google Scholar
  36. Koschnitzke C, Sazima M (1997) Biologia floral de cinco espécies de Passiflora L. (Passifloraceae) em mata semidecídua. Rev Bra Bot 20:119–126CrossRefGoogle Scholar
  37. Kraus JE, Sousa HC, Rezende MH, Castro NM, Vecchi C, Luque R (1998) Astra blue and basic fuchsin double staining for plant material. Biotech Histochem 73:235–243CrossRefGoogle Scholar
  38. Larson DA (1966) On the significance of the detailed structure of Passiflora caerulea exine. Bot Gaz 127:40–48CrossRefGoogle Scholar
  39. May PG, Spears JEE (1988) Andromonoecy and variation in phenotypic gender of Passiflora incarnata (Passifloraceae). Am J Bot 75:1830–1841CrossRefGoogle Scholar
  40. Mezzonato-Pires AC, Mendonça CBF, Gonçalves-Esteves V (2015) Pollen morphology of selected species of Passiflora L. (Passifloraceae) from the Atlantic Forest. Acta Bot Bras 29(3):391–399. CrossRefGoogle Scholar
  41. Milward-de-Azevedo MA, Freitas LB, Kinoshita LS (2014) Taxonomy and evolutionary relationships of Passiflora subg. Decaloba supersect. Decaloba sect. Xerogona (Passifloraceae): contributions of palynological, morphological and molecular studies. Acta Bot Bras 28:301–30Google Scholar
  42. Milward-de-Azevedo MA, Baumgratz JF (2004) Passiflora L. subgênero Decaloba (DC.) Rchb. (Passifloraceae) na região Sudeste do Brasil. Rodriguésia 55:17–54CrossRefGoogle Scholar
  43. Milward-de-Azevedo MA, Gonçalves-Esteves V, Baumgratz JF (2010) Palinotaxonomia das espécies de Passiflora L. subg. Decaloba (DC.) Rchb. (Passifloraceae) no sudeste do Brasil. Rev Bra Bot 27(4):655–665CrossRefGoogle Scholar
  44. Muschner VC, Lorenz AP, Cervi AC, Bonatto SL, Souza-Chies TT, Salzano FM, Freitas LB (2003) A first molecular phylogenetic analysis of Passiflora (Passifloraceae). Am J Bot 90(8):1229–1238. CrossRefGoogle Scholar
  45. Muschner VC, Lorenz-Lemke AP, Vecchia M, Bonatto SL, Salzano FM, Freitas LB (2006) Differential organellar inheritance in Passiflora’s (Passifloraceae) subgenera. Genetica 128:449–453CrossRefGoogle Scholar
  46. Pacini E, Hesse M (2007) Pollenkitt – its composition, forms and functions. Flora 200:399–415. CrossRefGoogle Scholar
  47. Porter-Utley K (2014) A review of Passiflora L. subgenus Decaloba (DC.) Rchb. super section Cieca (Medik.) MacDougal JM and Feuillet C (Passifloraceae). PhytoKeys 43.
  48. Presting D (1965) Zur morphologie der Pollenkörner der Passifloraceen. Pollen Spores 7:193–247Google Scholar
  49. Punt W, Hoen PP, Blackmore S, Nilsson† S, le Thomas A (2007) Glossary of pollen and spore terminology. Rev Paleobot Palynol 143:1–81CrossRefGoogle Scholar
  50. Reis NR, Peracchi AL, Pedro WA, Lima IP (eds) (2007) Morcegos do Brasil. Universidade Estadual de Londrina, LondrinaGoogle Scholar
  51. Richards AJ (1986) Plant breeding systems. George Allen & Unwin, LondonGoogle Scholar
  52. Sazima M, Sazima I (1978) Bat pollination of the passion flower, Passiflora mucronata, in southeastern Brazil. Biotropica 10:100–109CrossRefGoogle Scholar
  53. Silvério A, Mariath JEA (2013) Comparative structure of the pollen in species of Passiflora: insights from the pollen wall and cytoplasm contents. Plant Syst Evol 300:347–358. CrossRefGoogle Scholar
  54. Snow AA (1982) Pollination intensity and potencial seed set in Passiflora vitifolia. Oecologia 55:231–237CrossRefGoogle Scholar
  55. Soares L, Jesus ON, Souza EH et al (2017) Comparative pollen morphological analysis in the subgenera Passiflora and Decaloba. An Acad Bras Cienc 92:2381–2396CrossRefGoogle Scholar
  56. Spirlet ML (1965) Utilisation taxonomique dês grains de pollen de Passifloracées. Pollen Spores 7:249–301Google Scholar
  57. Stroo A (2000). Pollen morphological evolution in bat pollinated plants. Plant Syst Evol 25–242Google Scholar
  58. Suárez-Cervera M, Arcalís E, Le Thomas A, Seoane-Camba, JA (2002) Pectin distribution pattern in the apertural intine of Euphorbia peplus L. (Euphorbiaceae) pollen. Sex Plant Reprod. 14:291–298Google Scholar
  59. Varassin IG, Trigo JR, Sazima M (2001) The role of nectar production, flower pigments and odour in the pollination of four species of Passiflora (Passifloraceae) in South-Eastern Brazil. Bot J Linn Soc 136:139–152CrossRefGoogle Scholar
  60. Zhang MY, Lu LAHWH, Wang D, Li Z, Blackmore S (2017) Evolution of angiosperm pollen: 4. Basal eudicots. Ann Mo Bot Gard 102:141–182. CrossRefGoogle Scholar

Copyright information

© Springer-Verlag GmbH Austria, part of Springer Nature 2019

Authors and Affiliations

  1. 1.Laboratório de Botânica Estrutural, Departamento de Ciências BiológicasUniversidade Estadual do Centro-Oeste—UNICENTRO—Campus CEDETEGGuarapuavaBrazil
  2. 2.Programa de Pós-graduação em Biologia EvolutivaUniversidade Estadual do Centro-Oeste—UNICENTRO—Campus CEDETEGGuarapuavaBrazil

Personalised recommendations