Skip to main content
SpringerLink
Log in

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

  • Original Article
  • Published:
Protoplasma Aims and scope Submit manuscript

Abstract

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.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig 1
Fig 2
Fig 3
Fig 4
Fig 5
Fig 6

Similar content being viewed by others

References

  • 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. https://doi.org/10.1098/rspb.2014.0888

    Article  PubMed  PubMed Central  Google Scholar 

  • Amela Garcia MT, Galati BG, Anton AM (2002) Microsporogenesis microgametogenesis and pollen morphology of Passiflora spp. (Passifloraceae). Bot J Linn Soc 139:383–394. https://doi.org/10.1046/j.1095-8339.2002.00072.x

    Article  Google Scholar 

  • 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. https://doi.org/10.1007/s00606-013-0952-1

    Article  CAS  Google Scholar 

  • 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. https://doi.org/10.1111/boj.12385

    Article  Google Scholar 

  • Araújo RCM, Santos FA (2004) Palinologia de espécies do gênero Passiflora L. (Passifloraceae) da Chapada Diamantina, Bahia, Brasil. Sitientibus Ser Cienc Biol 4:37–42

    Google Scholar 

  • 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):19–23

  • Corbet SA, Beament L, Eisikowitch D (1982) Are electrostatic forces involved in pollen transfer? Plant Cell Environ 5:125–129

  • 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. https://doi.org/10.1093/aob/mcs256

    Article  CAS  PubMed  Google Scholar 

  • Deginani NB (2001) Las especies argentinas del género Passiflora (Passifloraceae). Darwiniana 39:43–129

    Google Scholar 

  • Dettke GA, Santos RP (2009) Tipos de aberturas dos grãos de pólen de espécies de Passiflora L. (Passifloraceae). Acta Bot Bras 23:1119–1129

    Article  Google Scholar 

  • 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)

  • 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. https://doi.org/10.1105/tpc.015800

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • 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. https://doi.org/10.1159/000365232

    Article  CAS  PubMed  Google Scholar 

  • Erdtman G (1952) Pollen morphology and plant taxonomy – angiosperms. Almqvist & Wiksell, Stockholm

    Google Scholar 

  • Erdtman G (1960) The acetolysis method. A revised description. Svensk Bot Tidskr 39:561–564

    Google Scholar 

  • Erdtman G (1969) Handbook of palynology. Munksgaard, Copenhagen

    Google Scholar 

  • 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 9:75–87

    Google Scholar 

  • Faegri K, Iversen J (1964) Textbook of pollen analysis. Blackwell Scientific Publications, Oxford

    Google Scholar 

  • Fazal H, Ahmad N, Abbasi BH (2013) Identification, characterization, and palynology of high-valued medicinal plants. Sci World J 2013:1–9

    Article  Google Scholar 

  • Feuillet C, MacDougal JM (2003) A new infrageneric classification of Passiflora L. (Passifloraceae). Passiflora 13:34–35 37–38

    Google Scholar 

  • Feuillet C, MacDougal JM (2007) The families and genera of vascular plants. In: Kubitzki K (ed) Passifloraceae. Springer, Berlin

    Chapter  Google Scholar 

  • Galen C (1999) Why do flowers vary? The functional ecology of variation in flower size and form within natural plant populations. BioScience 49:631–640

    Article  Google Scholar 

  • 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 132:81–85

    Article  CAS  PubMed  Google Scholar 

  • 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. https://doi.org/10.1590/S1516-89132007000700012

    Article  Google Scholar 

  • Hansen AK, Gilbert LE, Simpson BB, Downie S-R, Cervi AC, Jansen RK (2006) Phylogenetic relationships and chromosome number evolution in Passiflora. Syst Bot 31:138–150

    Article  Google Scholar 

  • Herrera CM (1988) Variation in mutualisms: the spatiotemporal mosaic of a pollinator assemblage. Bio J Linn Soc 35:95–125

    Article  Google Scholar 

  • Heslop-Harrison Y (1977) The pollen–stigma interaction: pollen-tube penetration in Crocus. Ann Bot 41:913–922

    Article  Google Scholar 

  • 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, Oxford

    Google Scholar 

  • Hesse M (2000) Pollen wall stratification and pollination. Plant Syst Evol 222:1–17. https://doi.org/10.1007/978-3-7091-6306-1_1

    Article  Google Scholar 

  • Janzen DH (1968) Reproductive behaviour in the Passifloraceae and some of its pollinators in the Central America. Behavior 32:33–48

    Article  Google Scholar 

  • Johansen DA (1940) Plant microtechnique. McGraw-Hill Book, New York

    Google Scholar 

  • Johnson SD, Steiner KE (2000) Generalization versus specialization in plant pollination systems. Trends Ecol Evol 15:140–143

    Article  CAS  PubMed  Google Scholar 

  • Judd WS, Campbell CS, Kellogg EA, Stevens PF, Donoghue MJ (2015) A phylogenetic approach. Sinauer Associates, Inc, Sunderland

    Google Scholar 

  • Knox RB (1984) The pollen grain. In: Johri BM (ed) Embryology of angiosperms. Springer-Verlag, Berlin, pp 197–271

    Chapter  Google Scholar 

  • 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 147–161

    Google Scholar 

  • Koschnitzke C, Sazima M (1997) Biologia floral de cinco espécies de Passiflora L. (Passifloraceae) em mata semidecídua. Rev Bra Bot 20:119–126

    Article  Google Scholar 

  • 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 73:235–243

    Article  CAS  PubMed  Google Scholar 

  • Larson DA (1966) On the significance of the detailed structure of Passiflora caerulea exine. Bot Gaz 127:40–48

    Article  Google Scholar 

  • May PG, Spears JEE (1988) Andromonoecy and variation in phenotypic gender of Passiflora incarnata (Passifloraceae). Am J Bot 75:1830–1841

    Article  Google Scholar 

  • 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. https://doi.org/10.1590/0102-33062015abb0014

    Article  Google Scholar 

  • 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 28:301–30

  • Milward-de-Azevedo MA, Baumgratz JF (2004) Passiflora L. subgênero Decaloba (DC.) Rchb. (Passifloraceae) na região Sudeste do Brasil. Rodriguésia 55:17–54

    Article  Google Scholar 

  • 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):655–665

    Article  Google Scholar 

  • 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. https://doi.org/10.3732/ajb.90.8.1229

    Article  CAS  PubMed  Google Scholar 

  • Muschner VC, Lorenz-Lemke AP, Vecchia M, Bonatto SL, Salzano FM, Freitas LB (2006) Differential organellar inheritance in Passiflora’s (Passifloraceae) subgenera. Genetica 128:449–453

    Article  PubMed  Google Scholar 

  • Pacini E, Hesse M (2007) Pollenkitt – its composition, forms and functions. Flora 200:399–415. https://doi.org/10.1016/j.flora.2005.02.006

    Article  Google Scholar 

  • 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. https://doi.org/10.3897/phytokeys.43.7804

  • Presting D (1965) Zur morphologie der Pollenkörner der Passifloraceen. Pollen Spores 7:193–247

    Google Scholar 

  • Punt W, Hoen PP, Blackmore S, Nilsson† S, le Thomas A (2007) Glossary of pollen and spore terminology. Rev Paleobot Palynol 143:1–81

    Article  Google Scholar 

  • Reis NR, Peracchi AL, Pedro WA, Lima IP (eds) (2007) Morcegos do Brasil. Universidade Estadual de Londrina, Londrina

    Google Scholar 

  • Richards AJ (1986) Plant breeding systems. George Allen & Unwin, London

    Google Scholar 

  • Sazima M, Sazima I (1978) Bat pollination of the passion flower, Passiflora mucronata, in southeastern Brazil. Biotropica 10:100–109

    Article  Google Scholar 

  • 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. https://doi.org/10.1007/s00606-013-0887-6

    Article  Google Scholar 

  • Snow AA (1982) Pollination intensity and potencial seed set in Passiflora vitifolia. Oecologia 55:231–237

    Article  PubMed  Google Scholar 

  • Soares L, Jesus ON, Souza EH et al (2017) Comparative pollen morphological analysis in the subgenera Passiflora and Decaloba. An Acad Bras Cienc 92:2381–2396

    Article  Google Scholar 

  • Spirlet ML (1965) Utilisation taxonomique dês grains de pollen de Passifloracées. Pollen Spores 7:249–301

    Google Scholar 

  • Stroo A (2000). Pollen morphological evolution in bat pollinated plants. Plant Syst Evol 25–242

  • 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. 14:291–298

  • 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 136:139–152

    Article  Google Scholar 

  • 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. https://doi.org/10.3417/2015035

    Article  Google Scholar 

Download references

Acknowledgements

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.

Author information

Authors and Affiliations

  1. Laboratório de Botânica Estrutural, Departamento de Ciências Biológicas, Universidade Estadual do Centro-Oeste—UNICENTRO—Campus CEDETEG, Guarapuava, Brazil

    Jaiana Richardo & Adriano Silvério

  2. Programa de Pós-graduação em Biologia Evolutiva, Universidade Estadual do Centro-Oeste—UNICENTRO—Campus CEDETEG, Guarapuava, Brazil

    Jaiana Richardo & Adriano Silvério

Authors
  1. Jaiana Richardo
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Adriano Silvério
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Adriano Silvério.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interest.

Additional information

Handling Editor: Peter Nick

Publisher’s note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Richardo, J., Silvério, A. New trends in Passiflora L. pollen grains: morphological/aperture aspects and wall layer considerations. Protoplasma 256, 923–939 (2019). https://doi.org/10.1007/s00709-019-01350-w

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00709-019-01350-w

Keywords

Search

Navigation