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Ultrastructure and diversity of recent and fossil zona-aperturate pollen grains

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Abstract

A survey of recent and fossil zona-aperturate pollen grains within the angiosperms was undertaken. Zona-aperturate pollen (with complete ring-like apertures) has been evolved independently in several genera of basal angiosperm families (Nymphaeaceae, Eupomatiaceae, Annonaceae, Monimiaceae, Atherospermataceae) and monocots (Araceae, Iridaceae, Laxmanniaceae, Arecaceae, and Rapateaceae). The special case of the eudicot Limnanthes (Limnanthaceae) is discussed. New examples of recent and fossil fully zonate pollen are presented; a noteworthy new example are Scrophulariaceae, with Pedicularis; our fossil examples show affinities either to Nymphaeaceae, or Araceae, or Iridaceae, or cannot be related to an extant taxon. The zona-aperturate pollen grains differ in ornamentation and stratification mostly in the respect of the aperture areas, but sometimes also outside the aperture. The question of polarity is settled only for some taxa because of the frequent lack of tetrad observations. A ring-like aperture may divide the pollen grains in symmetric halves, or if running asymmetrically, divides the pollen grain in two more or less unequal halves; the presence of clearly unequal halves gives a strong argument to assume an equatorial ring in such cases where tetrad configurations were not available. The zona-aperturate condition may be a functional benefit in wet environments: while in dry pollen the apertural ring is completely closed, in wet or very moist realm it expands greatly, and the pollen tube can be formed quickly and everywhere in this area.

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References

  • M. T Amela García B. G Galati A. M Anton (2002) ArticleTitleMicrosporogenesis, microgametogenesis and pollen morphology of Passiflora spp. (Passifloraceae) Bot. J. Linn. Soc 139 383–394 Occurrence Handle10.1046/j.1095-8339.2002.00072.x

    Article  Google Scholar 

  • E Anger (2001) Morphologie und Ontogenie der Pollenwand von Arum alpinum. Diploma Thesis. Formal- und Naturwiss Fakultät der Universität Wien Wien

    Google Scholar 

  • APG (1998) An ordinal classification for the families of flowering plants. Ann. Missouri Bot. Gard. 85: 531–553.

    Google Scholar 

  • APG (2003) An update of the Angiosperm Phylogeny Group classification for the orders and families of flowering plants: APG II. Bot. J. Linn. Soc. 141: 399–436.

    Google Scholar 

  • Beug H.-J. (2004) Leitfaden der Pollenbestimmung für Mitteleuropa und angrenzende Gebiete. Verlag Dr. Friedrich Pfeil, München, 542 pp.

  • R Buchner H Halbritter G Pfundner M Hesse (1990) ArticleTitlePollen of Limnanthes douglasii: A reinvestigation Grana 29 207–211

    Google Scholar 

  • S Carlquist (1961) ArticleTitlePollen morphology of Rapateaceae Aliso 5 39–66

    Google Scholar 

  • S Chanda K Ghosh (1976) Pollen morphology and its evolutionary significance in Xanthorroeaceae I. K Ferguson J Muller (Eds) The evolutionary significance of the exine. Linn. Soc. Symp. Ser. I Academic Press London 527–559

    Google Scholar 

  • S Chanda K Ghosh S Nilsson (1979) ArticleTitleOn the polarity and tetrad arrangements in some mono- and diaperturate angiosperm pollen grains Grana 18 21–31

    Google Scholar 

  • M. E Collinson M. C Boulter P. L Holmes (1993) Magnoliophyta (`Angiospermae') M. J Benton (Eds) The Fossil Record 2 Chapman and Hall London 809–841

    Google Scholar 

  • A. O Dahl J. R Rowley (1965) ArticleTitlePollen of Degeneria vitiensis J. Arnold Arbor 46 308–323

    Google Scholar 

  • J. A Doyle (2000) ArticleTitlePalaeobotany, relationships, and geographic history of the Winteraceae Ann. Missouri Bot. Gard 87 303–316

    Google Scholar 

  • J. A Doyle S Jardiné A Doerenkamp (1982) ArticleTitleAfropollis, a new genus of early angiosperm pollen, with notes on the Cretaceous palynostratigraphy and palaeoenvironmments of Northern Gondwana Bull. Centres Rech. Exprol-Prod. Elf-Aquitaine 6 39–117

    Google Scholar 

  • J. A Doyle C. L Hotton J. V Ward (1990) ArticleTitleEarly Cretaceous tetrads, zonasulculate pollen, and Winteraceae. I. Taxonomy, morphology, and ultrastructure Amer. J. Bot 77 1544–1557

    Google Scholar 

  • F Ehrendorfer (1998) Evolution und Systematik P Sitte H Ziegler F Ehrendorfer A Bresinsky (Eds) Strasburger Lehrbuch der Botanik für Hochschulen. 34. Auflage Gustav Fischer Verlag Stuttgart Jena 459–819

    Google Scholar 

  • P. K Endress (2003) ArticleTitleEarly floral development and nature of the calyptra in Eupomatiaceae (Magnoliales) Int. J. Pl. Sci 164 489–503 Occurrence Handle10.1086/375319

    Article  Google Scholar 

  • G Erdtman (1943) An introduction pollen analysis Chronica Botanica Group Waltham, Mass

    Google Scholar 

  • G Erdtman Vishnu-Mittre (1956) ArticleTitleOn terminology in pollen and spore morphology Grana Palynol 1 IssueID3 6–9

    Google Scholar 

  • E. M Friis K. R Pedersen P. R Crane (1999) ArticleTitleEarly angiosperm diversification: the diversity of pollen associated with angiosperm reproductive structures in Early Cretaceous floras from Portugal Ann. Missouri Bot. Gard 86 259–296

    Google Scholar 

  • E. M Friis K. R Pedersen P. R Crane (2004) ArticleTitleAraceae from the Early Cretaceous of Portugal: Evidence on the emergence of monocotyledons Proc. Natl. Acad. Sci 101 16565–16570 Occurrence Handle10.1073/pnas.0407174101 Occurrence Handle15546982

    Article  PubMed  Google Scholar 

  • C. A Furness P. J Rudall (1999) ArticleTitleMicrosporogenesis in monocotyledons Ann. Bot 84 475–499 Occurrence Handle10.1006/anbo.1999.0942

    Article  Google Scholar 

  • C. A Furness P. J Rudall (2003) ArticleTitleApertures with lids:distribution and significance of operculate pollen in monocotyledons Int. J. Pl. Sci 164 835–854 Occurrence Handle10.1086/378656

    Article  Google Scholar 

  • C. A Furness P. J Rudall F. B Sampson (2002) ArticleTitleEvolution of microsporogenesis in angiosperms Int. J. Pl. Sci 163 235–260 Occurrence Handle10.1086/338322

    Article  Google Scholar 

  • N. I Gabarayeva G El-Ghazaly (1997) ArticleTitleSporoderm development in Nymphaea mexicana (Nymphaeaceae) Pl. Syst. Evol 204 1–19 Occurrence Handle10.1007/BF00982528

    Article  Google Scholar 

  • N. I Gabarayeva J. R Rowley (1994) ArticleTitleExine development in Nymphaea colorata (Nymphaeaceae) Nordic J. Bot 14 671–691

    Google Scholar 

  • N. I Gabarayeva B Walles G El-Ghazaly J. R Rowley (2001) ArticleTitleExine and tapetum development in Nymphaea capensis (Nymphaeaceae):a comparative study Nordic J. Bot 21 529–548

    Google Scholar 

  • P Goldblatt Thomas A Le (1992) ArticleTitlePollen morphology of Madagascan Aristea and Geosiris (Iridaceae-Nivenioideae) in relation to systematics and phylogeny Bull. Mus. Natl. Hist. Nat 2 223–233

    Google Scholar 

  • P Goldblatt Thomas A Le (1997) ArticleTitlePalynology, phylogenetic reconstruction, and classification of the Afro-Madagascan genus Aristea (Iridaceae) Ann. Missouri Bot. Gard 84 263–284

    Google Scholar 

  • P Goldblatt J. C Manning A Bari (1991) ArticleTitleSulcus and operculum structure in the pollen grains of Iridaceae subfamily Ixioideae Ann. Missouri Bot. Gard 78 950–961

    Google Scholar 

  • P Goldblatt Thomas A Le M Suárez-Cervera (2004) ArticleTitlePhylogeny of the Afro-Madagascan Aristea (Iridaceae) revisited in the light of new data on pollen morphology Bot. J. Linn. Soc 144 41–68 Occurrence Handle10.1111/j.0024-4074.2004.00246.x

    Article  Google Scholar 

  • M. H Grayum (1992) ArticleTitleComparative external pollen ultrastructure of the Araceae and putatively related taxa Monographs Syst. Bot. Missouri Bot. Gard 43 1–167

    Google Scholar 

  • H Halbritter (1998) ArticleTitlePreparing living pollen material for Scanning Electron Microscopy using 2,2-Dimethoxypropane (DMP) and Critical-Point Drying Biotech. Histochem 73 137–143 Occurrence Handle9674883

    PubMed  Google Scholar 

  • Halbritter H. (2000 onwards) Passiflora racemosa. In:Buchner R., Weber M., PalDat – a palynological database:Descriptions, illustrations, identification, and information retrieval. http://www.paldat.org/.

  • H Halbritter M Hesse (1993) ArticleTitleSulcus morphology in some monocot families Grana 32 87–99

    Google Scholar 

  • H Halbritter M Hesse (2004) ArticleTitlePrincipal modes of infoldings in tricolp(or)ate Angiosperm pollen Grana 34 1–14 Occurrence Handle10.1080/00173130310017625

    Article  Google Scholar 

  • Harley M. M. (1999a) Tetrad variations: its influence on pollen form and systematics in the Palmae. In: Kurmann M. H., Hemsley A. R. (eds.) The evolution of plant architecture. Royal Botanic Gardens, Kew, pp. 289–304.

  • Harley M. M. (1999b) Palm pollen: overview and examples of taxonomic value at species level. In: Henderson A., Borchsenius F. (eds.) Evolution, variation, classification of palms. Mem. New york Bot. Garden 83: 95–120.

  • M. M Harley (2004) ArticleTitleTriaperturate pollen in the monocotyledons:configurations and conjectures Pl. Syst. Evol 247 75–122 Occurrence Handle10.1007/s00606-003-0107-x

    Article  Google Scholar 

  • M. M Harley W. J Baker (2001) ArticleTitlePollen aperture morphology in recaceae:application within phylogenetic analyses, and a summary of the fossil record of palm-like pollen Grana 40 45–77 Occurrence Handle10.1080/00173130152591877

    Article  Google Scholar 

  • M. M Harley J Dransfield (2003) ArticleTitleTriporate pollen in the Arecaceae Grana 42 3–19 Occurrence Handle10.1080/00173130310008535

    Article  Google Scholar 

  • M. M Harley M. H Kurmann I. K Ferguson (1991) Systematic implications of comparative morphology and in selected Tertiary and extant pollen from the Palmae and the Sapotaceae S Blackmore S. H Barnes (Eds) Pollen and spores. Pattern of diversification. The Systematics Association Special Volume 44 Clarendon Press Oxford 225–238

    Google Scholar 

  • M. M Harley M. S Zavada (2000) Pollen of the monocotyledons:selecting characters for cladistic analysis K Wilson D Morrison (Eds) Monocots:Systematics and evolution CSIRO Melbourne 191–210

    Google Scholar 

  • A. R Hemsley (2000) Self-assembly of colloidal units in exine development M. M Harley C. M Morton S Blackmore (Eds) Pollen and spores:Morphology and biology Royal Botanic Gardens Kew 31–44

    Google Scholar 

  • Hesse M. (2003) Toward a deeper understanding of sporoderm structure and function. In: Stuessy T. F., Mayer V., Hörandl E. (eds.) Deep morphology. Toward a renaissance of morphology in plant systematics. Regnum Vegetabile Volume 141: 207–220. IAPT (Institute of Botany, University of Vienna). A.R.G. Gantner Verlag, Ruggell, Liechtenstein.

  • M Hesse J Bogner H Halbritter M Weber (2001) ArticleTitlePalynology of the perigoniate Aroideae:Zamioculcas, Gonatopus and Stylochaeton (Araceae) Grana 40 26–34 Occurrence Handle10.1080/00173130152591859

    Article  Google Scholar 

  • Hoen P (1999) Glossary of pollen and spore terminology. Second and revised edition. http://www.bio.uu.nl/~palaeo/glossary/glos-int.htm.

  • M. I. A Ibrahim (2002) ArticleTitleNew angiosperm pollen from the Upper Barremian-Aptian of the Western Desert, Egypt Palynology 26 107–133 Occurrence Handle10.2113/0260107

    Article  Google Scholar 

  • Jarzen D. M., Nichols D. J. (1996) Pollen. In: Jansonius J., McGregor D. C. (eds.) Palynology, principles and applications. AASP Vol 1: pp. 261–291. AASP Foundation, Texas University, Station College.

  • S. S Kreunen J. M Osborn (1999) ArticleTitlePollen and anther development in Nelumbo (Nelumbonaceae) Amer. J. Bot 86 1662–1676

    Google Scholar 

  • A Thomas ParticleLe W Morawetz M Waha (1986) Pollen of palaeo- and neotropical Annonaceae:definition of the aperture by morphological and functional characters S Blackmore I. K Ferguson (Eds) Pollen and spores:form and function Academic Press London 375–388

    Google Scholar 

  • A Thomas ParticleLe M Suarez-Cervera P Goldblatt (1996) ArticleTitleDeux types polliniques originaux dans le genre Aristea(Iridaceae-Nivenoideae):implications phylogénetiques Grana 35 87–96

    Google Scholar 

  • A Thomas ParticleLe M Suarez-Cervera P Goldblatt (2001) ArticleTitlePollen of Nivenoideae and its phylogenetic implications Annali di Botanica 1 (n. 2) 67–72

    Google Scholar 

  • S. C Maheshwari P. P Khanna (1956) ArticleTitleThe embryology of Arisaema wallichianum Hook f. and the systematic position of the Araceae Phytomorphology 6 379–388

    Google Scholar 

  • McGowran B., Archer M., Bock P., Darragh T. A.,Godthelp H., Hageman S., Hand S. J., Hill R., Li Q., Maxwell P. A., McNamara K. J., MacPhail M., Mildenhall D., Partridge A. D., Richardson J., Shafik S., Truswell E. M., Warne M. (2000) Australasian palaeobiogeography: the Paleogene and Neogene record. In: Wright A. J., Young G. C., Talent J. A., Laurie J. R. (eds.) Palaeobiogeography of Australasian faunas and floras. Memoir 23 of the association of the Australasian Palaeontologists. Canberra, pp. 405–470.

  • Moore P. D., Webb J. A., Collinson M. E. (1991) Pollen analysis. 2. edition. Blackwell Scientific Publications, Oxford London Edinburgh Boston Melbourne Paris Berlin Vienna, 216 pp.

  • W Morawetz M Waha (1985) ArticleTitleA new pollen type, C-banded and fluorochrome counterstained chromosomes, and evolution in Guatteria and related genera (Annonaceae) Pl. Syst. Evol 150 119–141 Occurrence Handle10.1007/BF00984191

    Article  Google Scholar 

  • J Muller (1981) ArticleTitleFossil pollen records of extant angiosperms Bot. Review 47 1–142

    Google Scholar 

  • J Muller (1984) ArticleTitleSignificance of fossil pollen for angiosperm history Ann. Missouri Bot. Gard 71 419–443

    Google Scholar 

  • E Pacini B. E Juniper (1983) ArticleTitleThe ultrastructure of the formation and development of the amoeboid tapetum in Arum italicum Miller Protoplasma 117 116–129 Occurrence Handle10.1007/BF01288350

    Article  Google Scholar 

  • K. B Pigg R. A Stockey (1996) ArticleTitleThe siginificance of the Princeton chert permineralized flora to the middle Eocene upland biota of the Okanogan Highlands Washington Geology 24 32–36

    Google Scholar 

  • S. A. J Pocock G Vasanthy B. S Venkatachala (1990) ArticleTitlePollen of Circumpolles – an enigma or morphotrends showing evolutionary adaptation Rev. Palaeobot. Palynol 65 179–193 Occurrence Handle10.1016/0034-6667(90)90069-U

    Article  Google Scholar 

  • A. E Pozhidaev (2000) Pollen variety and aperture patterning M. M Harley C. M Morton S Blackmore (Eds) Pollen and spores:morphology and biology Royal Botanic Gardens Kew 205–225

    Google Scholar 

  • Punt W., Blackmore S., Nilsson S., Le Thomas A. (1994) Glossary of pollen and spore terminology. LPP Contributions Series No. 1. LPP Foundation, Laboratory of Palaeobotany and Palynology, University of Utrecht, Utrecht, 71 pp. (http://www.bio.uu.nl/~palaeo/glossary/glos-int. htm)

  • M Reille (1998) Pollen et Spores d'Europeet d'Afrique du Nord Suppl. 2 – Laboratoire de Botanique Historique et Palynologie Marseille France 523

    Google Scholar 

  • S. S Renner D. B Foreman D Murray (2000) ArticleTitleTiming transantarctic disjunctions in the Atherospermataceae (Laurales):evidence from coding and noncoding chloroplast sequences Syst. Biol 49 579–591 Occurrence Handle10.1080/10635159950127402 Occurrence Handle12116428

    Article  PubMed  Google Scholar 

  • F Roland (1965) ArticleTitlePrécisions sur la structure et l'ultrastructure d'une tétrade calymmée Pollen et Spores 7 5–8

    Google Scholar 

  • F. B Sampson (1975) ArticleTitleAperture orientation in Laurelia pollen (Atherospermataceae syn. Subfamily Atherospermoideae of Monimiaceae) Grana 15 153–167

    Google Scholar 

  • F. B Sampson (1996) ArticleTitlePollen morphology and ultrastructure of Laurelia, Laureliopsis, and Dryadodaphne (Atherospermataceae [Monimiaceae]) Grana 35 257–265

    Google Scholar 

  • F. B Sampson (2000) ArticleTitlePollen diversity in some modern Magnoliids Int. J. Pl. Sci 161 (Suppl. 6) S193–S210 Occurrence Handle10.1086/317573

    Article  Google Scholar 

  • F. B Sampson D. B Foreman (1988) ArticleTitlePollen morphology of Atherosperma, Daphnandra and Doryphora (Atherospermataceae [Monimiaceae]) Grana 27 17–25

    Google Scholar 

  • A.-M Schmid R Eberwein M Hesse (1996) ArticleTitlePattern morphogenesis in cell walls of diatoms and pollen grains:a comparison Protoplasma 193 144–173 Occurrence Handle10.1007/BF01276642

    Article  Google Scholar 

  • Schulze W. (1971a) Beitraäge zur Pollenmorphologie der Gattungen um Iris L. Feddes Repert. 81: 507–517.

  • Schulze W. (1971b) Beiträge zur Pollenmorphologie der Iridaceae und ihre Bedeutung fü r die Taxonomie. Feddes Repert. 82: 101–124.

  • R. A Stockey (2001) The Princeton Chert D. E. G Briggs P. R Crowther (Eds) Palaeobiology II Blackwell Scientific Publications Oxford 359–362

    Google Scholar 

  • G Thanikaimoni (1969) ArticleTitleEsquisse palynologique des Aracées Institut Français de Pondichéry, Traveaux de la Section Scientifique et Technique 5 IssueID5 1–31

    Google Scholar 

  • G Thanikaimoni (1970) ArticleTitleLes palmiers:palynologie et systématique Institut Français de Pondichéry, Traveaux de la Section Scientifique et Technique 11 1–286

    Google Scholar 

  • Tiemann A. (1985) Untersuchungen zur Embryologie, Blütenmorphologie und Systematik der Rapateaceen und der Xyridaceen-Gattung Abolboda (Monocotyledoneae). Dissertationes Botanicae 82: 1–201. J. Cramer, Vaduz, Liechtenstein. michael.

  • B Valdés M. J Díez I Fernández (1987) Atlas polinico de Andalucia occidental. Instituto de Desarrollo Regional No. 43 Universidad de Sevilla Sevilla 451

    Google Scholar 

  • J. E Walker (1974) ArticleTitleAperture evolution in the pollen of primitive angiosperms Amer. J. Bot 61 1112–1136

    Google Scholar 

  • M Weber H Halbritter M Hesse (1999) ArticleTitleThe basic pollen wall types in Araceae Int. J. Plant Sci 160 415–423 Occurrence Handle10.1086/314122

    Article  Google Scholar 

  • P. S Woodland P. R Garlick (1982) ArticleTitleThe fine structure of the pollen of Eupomatiaceae Austral. J. Bot 30 297–301

    Google Scholar 

  • R Zetter M Hesse A Frosch-Radivo (2001) ArticleTitleEarly Eocene zona-aperturate pollen grains of the Proxapertites type with affinity to Araceae Rev. Palaeobot. Palynol 117 267–279 Occurrence Handle10.1016/S0034-6667(01)00096-3

    Article  Google Scholar 

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Hesse, M., Zetter, R. Ultrastructure and diversity of recent and fossil zona-aperturate pollen grains. Plant Syst. Evol. 255, 145–176 (2005). https://doi.org/10.1007/s00606-005-0358-9

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