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Comparative structure of the pollen in species of Passiflora: insights from the pollen wall and cytoplasm contents

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Abstract

Pollen grains of three Brazilian species of Passiflora (P. elegans, P. suberosa and P. haematostigma) belonging to different subgenera were studied with respect to the wall and cytoplasm. New data were obtained on pollen wall histochemistry, cytoplasm contents and organelle inheritance. The structure of the pollen wall layers differed in all the species; P. elegans shares characters with those found in other species from the same subgenus. The exine foot layer is structured and evident only in P. haematostigma and is not structured in P. elegans. The pollen grains have pollenkitt with lipid components. The cytoplasm of the vegetative cell contains dissolved and non-dissolved polysaccharides. The generative cell contains plastids and mitochondria in all the species analyzed, and consequently has the potential for paternal or biparental extranuclear inheritance. Aspects of the evolution of the characters of the species are discussed in the light of a recent phylogeny of the group, with a focus on the three subgenera.

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References

  • Acioli MF (1999) Estudo Preliminar da Biologia Floral de Passiflora suberosa Linnaeus (Passifloraceae). Monografia (Trabalho de conclusão do curso de Bacharelado). Instituto de Biociências. Universidade Federal do Rio Grande do Sul, Porto Alegre

    Google Scholar 

  • Acioli MF (2003) Ecologia da Polinização de Passiflora suberosa Linnaeus (Passifloraceae). Dissertação de Mestrado. Instituto de Biociências. Universidade Federal do Rio Grande do Sul, Porto Alegre

    Google Scholar 

  • Amela Garcia MT, Hoc PS (1998) Biologia Floral de Passiflora foetida (Passifloraceae). Rev Biol Trop 46(2):191–202

    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

    Article  Google Scholar 

  • Angiosperm Phylogeny Group (2009) An update of the Angiosperm Phylogeny Group classification for the orders and families of flowering plants: APG III. Bot J Linn Soc 161:105–121

    Article  Google Scholar 

  • Baker HG, Baker I (1979) Starch in angiosperm pollen grains and its evolutionary significance. Am J Bot 66(5):591–600

    Article  Google Scholar 

  • Bozzola JJ, Russel LD (1998) Electron microscopy: principles and techniques for biologists. Jones and Bartlett, Boston

    Google Scholar 

  • Braum AF (2008) Morfologia, anatomia e imunocitoquímica da interação entre pólen e estigma em duas espécies de Passiflora (Passifloraceae). Dissertação de Mestrado. Universidade Federal do Rio Grande do Sul, Porto Alegre

    Google Scholar 

  • Bray DF, Wagenaar EB (1978) A double staining technique for improved contrast of thin sections from Spurr-embedded tissue. Can J Botany 56:129–132

    Article  Google Scholar 

  • Carreira LMM (1977) Aspectos da ultra-estrutura do pólen de Passiflora coccinea Aubl. (Passifloraceae). Acta Amazonica 7(3):329–332

    Google Scholar 

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

    Google Scholar 

  • Corriveau JL, Coleman AW (1988) Rapid screening method to detect potential biparental inheritance of plastid DNA and results for over 200 angiosperm species. Am J Bot 75(10):1443–1458

    Article  Google Scholar 

  • Cronquist A (1988) The evolution and classification of flowering plants, 2nd edn. Bronx, New York

    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 Bioc 9(s1):48–74

    Google Scholar 

  • Erdtman G (1952) Pollen morphology and plant taxonomy: angiosperms. The Chronica Botanica Co, Waltham

    Google Scholar 

  • Erdtman G (1960) The acetolysis method. A revised description. Sven Bot Tidsskr 54:561–564

    Google Scholar 

  • Feder N, O′Brien TP (1968) Plant microtechnique, some principles and new methods. Am J Bot 55:123–142

    Article  Google Scholar 

  • Gerrits PO, Smid L (1983) A new, less toxic polymerisation system for the embedding of soft tissue in glycol methacrylate and subsequent preparing of serial sections. J Microsc-Oxford 132:81–85

    Article  CAS  Google Scholar 

  • Hanaichi T, Sato T, Iwamoto T, Malavasiyamashiro J, Hoshiro M, Mizuno N (1986) A stable lead by modification of Sato method. J Electron Microsc 35(3):304–306

    CAS  Google Scholar 

  • Hansen AK, Gilbert LE, Simpson BB, Downie SR, Cervi AC, Jansen RK (2006) Phylogenetic Relationships and Chromosome Number Evolution in Passiflora. Syst Bot 31(1):138–150

    Google Scholar 

  • Hansen AK, Escobar LK, Gilbert LE, Jansen RK (2007) Paternal, maternal and biparental inheritance of the chloroplast genome in Passiflora (Passifloraceae): implications for phylogenetic studies. Am J Bot 94(1):42–46

    Article  CAS  PubMed  Google Scholar 

  • Heslop-Harrison J, Heslop-Harrison Y (1991) Structural and functional variation in pollen intines. In: Blackmore S, Barnes SH (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

    Google Scholar 

  • Huang CY, Ayliffe MA, Timmis JN (2003) Direct measurement of the transfer rate of chloroplast DNA into the nucleus. Nature 442:72–76

    Article  Google Scholar 

  • Ji X, Zhang Q, Liu Y, Sodmergen (2004) Presence of plastid and absence of mitochondrial DNA in male reproductive cells as evidence for cytoplasmic inheritance in Turnera and Zantedeschia aethiopica. Protoplasma 224:211–216

    Article  CAS  PubMed  Google Scholar 

  • Knox RB (1984) The pollen grain. In: Johri BM (ed) Embryology of angiosperms. Spring-Verlag, Berlin

    Google Scholar 

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

    Article  Google Scholar 

  • Knox RB, Heslop-Harrison J (1970) Pollen-wall proteins: localizations and enzymatic activity. J Cell Sci 6:1–27

    CAS  PubMed  Google Scholar 

  • Krosnick SE, Freudenstein JV (2005) Monophyly and floral character homology of old world Passiflora (Subgenus Decaloba: supersection Disemma). Syst Bot 30(1):139–152

    Article  Google Scholar 

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

    Article  Google Scholar 

  • Lillie RD (1965) Histopathologic technic and practical histochemistry. McGrawHill, New York

    Google Scholar 

  • MacDougal J, Feuillet C (2004) Systematics. In: Ulmer T, MacDougal JM (eds) Passiflora: passionflowers of the world. Timber Press, Portland, pp 27–31

    Google Scholar 

  • Martin FW (1959) Staining and observing pollen tubes in the style by means of fluorescence. Stain Technol 34:125–128

    CAS  PubMed  Google Scholar 

  • Mogensen HL (1996) The hows and whys of cytoplasmic inheritance in seed plants. Am J Bot 83:383–404

    Article  Google Scholar 

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

    Article  PubMed  Google Scholar 

  • Muschner VC (2005) Filogenia Molecular, taxas evolutivas, tempo de divergência e herança organelar em Passiflora L. (Passifloraceae). Tese de Doutorado. Universidade Federal do Rio Grande do Sul, Porto Alegre

    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

    Article  CAS  PubMed  Google Scholar 

  • Nepi M, Franchi GG (2000) Cytochemistry of mature angiosperm pollen. Plant Syst Evol 222(1–4):45–62

    Article  CAS  Google Scholar 

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

    Google Scholar 

  • Pacini E (2000) From anther and pollen ripening to pollen presentation. Plant Syst Evol 222:12–43

    Article  Google Scholar 

  • Pacini E, Franchi GG, Ripaccioli M (1999) Ripe structure and histochemistry of some gymnosperms. Plant Syst Evol 217:81–99

    Article  Google Scholar 

  • Pacini E, Hesse M (2005) Pollenkitt - its composition, forms and functions. Flora 200:399–415

    Google Scholar 

  • Presting D (1965) Zur Morphologie der Pollenkörner der Passifloraceen. Pollen Spores 7:193–245

    Google Scholar 

  • Punt W, Hoen PP, Blackmore S, Nilsson S, Le Thomas A (2007) Glossary of pollen and spore terminology. Rev Paleobot Palyno 143(1–2):1–81

    Article  Google Scholar 

  • Rêgo MMR, Bruckner CH, Silva EAM, Finger FL, Siqueira DL, Fernandes AA (1999) Self-incompatibility in passion fruit: evidence of two locus genetic control. Theor Appl Genet 98(3–4):564–568

    Article  Google Scholar 

  • Rêgo MM, Rêgo ER, Bruckner CH, Da Silva EAM, Finger FL, Pereira KJC (2000) Pollen tube behavior in yellow passion fruit following compatible and incompatible crosses. Theor Appl Genet 101(5–6):685–689

    Google Scholar 

  • Roland JC, Vian B (1991) General preparation and staining of thin sections. In: Hall JL, Hawes C (eds) Electron microscopy of plant cells. Academic Press, London

    Google Scholar 

  • Russell SD (2003) Plant sexuality, cell expression and preferential fertilization. Bol Soc Argent Bot 38(3–4):349–356

    Google Scholar 

  • Sass JE (1951) Botanical microtechnique, 2a edn. The Iowa State College Press, Ames

    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 

  • Sears BB (1980) Elimination of plastids during spermatogenesis and fertilization in the plant kingdom. Plasmid 4:233–255

    Article  CAS  PubMed  Google Scholar 

  • Shore JS, McQueen KL, Little SH (1994) Inheritance of plastid DNA in the Turnera ulmifolia complex (Turneraceae). Am J Bot 81:1636–1639

    Article  Google Scholar 

  • Shore JS, Triassi M (1998) Paternally based cpDNA inheritance in Turnera ulmifolia (Turneraceae). Am J Bot 85:328–332

    Article  CAS  PubMed  Google Scholar 

  • Skvarla JJ, Larson DA (1966) Fine structure studies of Zea mays pollen. I. Cell membranes and exine ontogeny. Am J Bot 53(10):1112–1125

    Article  Google Scholar 

  • Southworth D (1973) Cytochemical reactivity of pollen walls. J Histochem Cytochem 21(1):73–80

    Article  CAS  PubMed  Google Scholar 

  • Suassuna TMF, Bruckner CH, Carvalho CR, Borém A (2003) Self-incompatibility in passionfruit: evidence of gametophytic–sporophytic control. Theor Appl Genet 106:298–302

    Google Scholar 

  • Spurr AR (1969) A low-viscosity epoxy resin embedding medium for electron microscopy. J Ultra Mol Struct R 26:31–34

    Article  CAS  Google Scholar 

  • Timmis JM, Ayliffe M, Huang CY, Martin W (2004) Endosymbiotic gene transfer organelle genomes forge eukaryotic chromosomes. Nat Rev Genet 5:123–135

    Article  CAS  PubMed  Google Scholar 

  • Ulmer T, MacDougal JM (2004) Passiflora. Passionflowers of the world. Timber Press, Portland

    Google Scholar 

  • 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 

  • Weber M (1992) The formation of pollenkitt in Apium nodiflorum (Apiaceae). Ann Bot 70:573–577

    Google Scholar 

  • Whatley JM (1982) Ultrastructure of plastid inheritance: green algae to angiosperms. Biol Rev 57(4):527–569

    Article  Google Scholar 

  • Zhang Q, Yang L, Sodmergen (2003) Examination of the cytoplasmic DNA in male reproductive cells to determine the potential for cytoplasmic inheritance in 295 Angiosperm species. Plant Cell Physiol 44(9):941–951

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

We thank Armando Carlos Cervi and Greta Aline Dettke for collecting P. haematostigma in the field, and the Centro de Microscopia Eletrônica (CME-UFRGS) for making the equipment available. This article is part of the PhD thesis of the first author, carried out with the support of a CAPES doctoral scholarship. The project was supported by CNPq-Proc. 305289/2008-0, 480622/2007-8, 474132/2003-4 and 300822/2005-7.

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Correspondence to Jorge Ernesto de Araujo Mariath.

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Silvério, A., de Araujo Mariath, J.E. Comparative structure of the pollen in species of Passiflora: insights from the pollen wall and cytoplasm contents. Plant Syst Evol 300, 347–358 (2014). https://doi.org/10.1007/s00606-013-0887-6

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