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Evolution of endoapertures in early-divergent eudicots, with particular reference to pollen morphology in Sabiaceae

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Abstract

Endoapertures, the inner openings of compound apertures in pollen grains, are common in eudicots, but occur infrequently in early-divergent eudicot lineages, in which they are restricted to three families: Menispermaceae, Sabiaceae and Buxaceae. Pollen of Sabiaceae was examined using light, scanning and transmission electron microscopy. The endoapertures are large and lalongate, and intine onci are associated with their development. Optimisation of endoapertures onto an existing angiosperm phylogeny indicates that endoapertures have evolved at least three times independently: in Menispermaceae, in Sabiaceae plus Buxaceae (or possibly separately in these two families), and in the core eudicot clade. Sabiaceae are unusual among early-divergent eudicots in that they possess some characters that are more common in core eudicots, including pollen with endoapertures and pentamerous flowers. This indicates either that they are more closely related to core eudicots than is indicated by current molecular evidence, or that these characters are homoplastic. The latter would suggest a high degree of experimentation prior to evolutionary canalisation of some key morphological features in eudicots. The evolution of endoapertures in early-divergent eudicots is probably associated with possession of endexine sculpture (endosculpture) such as endocracks; endoapertures may have been retained in eudicots as a harmomegathic mechanism.

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References

  • C. L. Anderson K. Bremer E. M. Friis (2005) ArticleTitleDating phylogenetically basal eudicots using rbcL sequences and multiple fossil reference points Amer. J. Bot. 92 1737–1748 Occurrence Handle1:CAS:528:DC%2BD2MXhtFOgsL7O

    CAS  Google Scholar 

  • Angiosperm Phylogeny Group [APG] (1998) An ordinal classification for the families of flowering plants. Ann. Missouri Bot. Gard. 85: 531–533.

    Google Scholar 

  • Angiosperm Phylogeny Group [APG II] (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 

  • S. Blackmore S. H. Barnes (1986) Harmomegathic mechanisms in pollen grains S. Blackmore I. K. Ferguson (Eds) Pollen and spores: form and function Academic Press London 137–149

    Google Scholar 

  • S. Blackmore P. R. Crane (1998) The evolution of apertures in the spores and pollen grains of embryophytes S. J. Owens P. J. Rudall (Eds) Reproductive biology Royal Botanic Gardens Kew 159–182

    Google Scholar 

  • Blackmore S., Stafford P., Persson V. (1995) Palynology and systematics of the Ranunculiflorae. Pl. Syst. Evol. [Suppl.] 9: 71–82.

    Google Scholar 

  • T. Borsch V. Wilde (2000) Pollen variability within species, populations, and individuals, with particular reference to Nelumbo M. M. Harley C. M. Morton S. Blackmore (Eds) Pollen and spores: morphology and biology Royal Botanic Gardens Kew 285–299

    Google Scholar 

  • P. Brückner (1993) ArticleTitlePollen morphology and taxonomy of Eurasiatic species of the genus Buxus (Buxaceae) Grana 32 65–78

    Google Scholar 

  • G. C. S. Clarke W. Punt P. P. Hoen (1991) ArticleTitleRanunculaceae The Northwest European Pollen Flora, 51. Rev. Palaeobot. Palynol. 69 117–271

    Google Scholar 

  • M. J. Donoghue J. A. Doyle (1989) Phylogenetic analysis of angiosperms and the relationships of Hamamelidae P. R. Crane S. Blackmore (Eds) Evolution, systematics, and fossil history of the Hamamelidae, vol. 1 Clarendon Press Oxford 17–45

    Google Scholar 

  • J. A. Doyle C. L. Hotton (1991) Diversification of early angiosperm pollen in a cladistic context S. Blackmore S. H. Barnes (Eds) Pollen and spores: patterns of diversification Clarendon Press Oxford 169–195

    Google Scholar 

  • F. Eide (1981) ArticleTitleKey for Northwest European Rosaceae pollen Grana 20 101–118

    Google Scholar 

  • G. E. B. El Ghazali (1990) ArticleTitleAn illustrated key to endoaperture morphology Rev. Palaeobot. Palynol. 63 227–231 Occurrence Handle10.1016/0034-6667(90)90101-N

    Article  Google Scholar 

  • P. K. Endress (1986) ArticleTitleFloral structure, systematics, and phylogeny in Trochodendrales Ann. Missouri Bot. Gard. 73 297–324 Occurrence Handle10.2307/2399115

    Article  Google Scholar 

  • G. Erdtman (1952) Pollen morphology and plant taxonomy. Angiosperms Almqvist and Wiksell Stockholm

    Google Scholar 

  • Erdtman G. (1960a) Pollen walls and angiosperm phylogeny. Bot. Not. 113: 41–45.

    Google Scholar 

  • Erdtman G. (1960b) The acetolysis method, a revised description. Svensk Bot. Tidskr. 54: 561–564.

  • S. Feuer (1986) ArticleTitlePollen morphology and evolution in the Persoonioideae, Sphalmioideae and Carnarvonioideae (Proteaceae) Pollen Spores 28 123–156

    Google Scholar 

  • S. Feuer (1990) ArticleTitlePollen aperture evolution among the subfamilies Persoonioideae, Sphalmioideae, and Carnvonioideae (Proteaceae) Amer. J. Bot. 77 783–794 Occurrence Handle10.2307/2444370

    Article  Google Scholar 

  • C. A. Furness (1985) ArticleTitleA review of spiraperturate pollen Pollen Spores 27 307–320

    Google Scholar 

  • C. A. Furness P. J. Rudall (2001) ArticleTitleThe tapetum in basal angiosperms: early diversity Int. J. Pl. Sci. 162 375–392 Occurrence Handle10.1086/319580

    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 (2004) ArticleTitlePollen aperture evolution – a crucial factor for eudicot success? Trends Pl. Sci. 9 1360–1385

    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 

  • Guinet P. (1962) Pollens d'Asie Tropicale. Fasc. I. Inst. Fr. Pondichéry, Trav. Sect. Sci. Tech. 5: 1–8 (+52 plates).

  • M. M. Harley I. K. Ferguson (1982) ArticleTitlePollen morphology and taxonomy of the tribe Menispermeae (Menispermaceae) Kew Bull. 37 353–366

    Google Scholar 

  • J. Heslop-Harrison (1979) ArticleTitleAn interpretation of the hydrodynamics of pollen Amer. J. Bot. 66 737–743 Occurrence Handle10.2307/2442418

    Article  Google Scholar 

  • S. Huysmans S. Dessein E. Smets E. Robbrecht (2003) ArticleTitlePollen morphology of NW European representatives confirms monophyly of Rubieae (Rubiaceae) Rev. Palaeobot. Palynol. 127 219–240 Occurrence Handle10.1016/S0034-6667(03)00121-0

    Article  Google Scholar 

  • S. Huysmans E. Robbrecht P. Delprete E. Smets (1999) ArticleTitlePollen morphological support for the Catesbaeeae-Chiococceae-Exostema-complex (Rubiaceae) Grana 38 325–338 Occurrence Handle10.1080/00173130050136118

    Article  Google Scholar 

  • S. Huysmans E. Robbrecht E. Smets (1998) ArticleTitleA collapsed tribe revisited: pollen morphology of the Isertieae (Cinchonoideae-Rubiaceae) Rev. Palaeobot. Palynol. 104 85–113 Occurrence Handle10.1016/S0034-6667(98)00054-2

    Article  Google Scholar 

  • R. C. Jackson J. J. Skvarla W. F. Chissoe (2000) ArticleTitleA unique pollen wall mutation in the family Compositae: ultrastructure and genetics Amer. J. Bot. 87 1571–1577 Occurrence Handle10.2307/2656732

    Article  Google Scholar 

  • Kalis A. J. (1979) Papaveraceae. The Northwest European Pollen Flora, 20. Rev. Palaeobot. Palynol. 28: 209–260.

    Google Scholar 

  • E. Kohler (1980) ArticleTitleZur Pollenmorphologie und systematischen Stellung der Didymelaceae Leandri Feddes Repert. 91 581–591

    Google Scholar 

  • S. S. Kreunen J. M. Osborne (1999) ArticleTitlePollen and anther development in Nelumbo Amer. J. Bot. 86 1662–1676 Occurrence Handle10.2307/2656664

    Article  Google Scholar 

  • S. Layka (1975) ArticleTitleLes caractères de l'endexine chez les Papavéracées Bull. Soc. Bot. Fr., Colloque Morphologie Pollinique 122 103–107

    Google Scholar 

  • D. Lobreau-Callen V. Malecot M. Suárez-Cervera (2000) Comparative study of pollen from apetalous Crotonoideae and some other uniovulate Euphorbiaceae: exine ultrastructure at the aperture M. M. Harley C. M. Morton S. Blackmore (Eds) Pollen and spores: morphology and biology Royal Botanic Gardens Kew 301–324

    Google Scholar 

  • D. J. Mabberley (1987) The plant-book Cambridge University Press Cambridge

    Google Scholar 

  • M. S. Mondal (1990) Pollen morphology and systematic relationships of families Sabiaceae (s.l.) and Connaraceae. Advances in pollen spore research vol. 17 Today and Tomorrow's Publishers New Delhi

    Google Scholar 

  • M. S. Mondal K. Mitra (1982) ArticleTitlePollen morphology and systematic relationships of Sabiaceae Geophytology 12 166–180

    Google Scholar 

  • Nixon K. C. (2002) Winclada vers. 1.00.08. Ithaca, New York. Published by the author [Distributed through http://www.cladistics.com].

  • J. W. Nowicke J. J. Skvarla (1979) ArticleTitlePollen morphology: the potential influence in higher order systematics Ann. Missouri Bot. Gard. 66 633–700 Occurrence Handle10.2307/2398914

    Article  Google Scholar 

  • J. W. Nowicke J. J. Skvarla (1981) ArticleTitlePollen morphology and phylogenetic relationships of the Berberidaceae Smithsonian Contrib. Bot. 50 1–83

    Google Scholar 

  • J. W. Nowicke J. J. Skvarla (1982) ArticleTitlePollen morphology and the relationships of Circaeaster, of Kingdonia and Sargentodoxa to the Ranunculales Amer. J. Bot. 69 990–998 Occurrence Handle10.2307/2442896

    Article  Google Scholar 

  • J. W. Nowicke J. J. Skvarla (1984) ArticleTitlePollen morphology and relationships of Simmondsia chinensis to the order Euphorbiales Amer. J. Bot. 71 210–215 Occurrence Handle10.2307/2443747

    Article  Google Scholar 

  • Ochoterena H. (2000) Systematics of Hintonia Bullock and the Portlandia complex (Rubiaceae). PhD thesis, Cornell University.

  • D. M. Paxson-Sowders C. H. Dodrill H. Owen C. A. Makaroff (2001) ArticleTitleDEX1, a novel plant protein, is required for exine pattern formation during pollen development in Arabidopsis Pl. Physiol. 127 1739–1749 Occurrence Handle10.1104/pp.127.4.1739 Occurrence Handle1:CAS:528:DC%2BD38XjtVWlsA%3D%3D

    Article  CAS  Google Scholar 

  • J. Praglowski (1970) ArticleTitleThe pollen morphology of the Haloragaceae with reference to taxonomy Grana 10 159–239 Occurrence Handle10.1080/00173137009427397

    Article  Google Scholar 

  • J. Praglowski (1974) ArticleTitleThe pollen morphology of Trochodendraceae, Tetracentraceae, Cercidiphyllaceae and Eupteleaceae with reference to taxonomy Pollen Spores 26 449–467

    Google Scholar 

  • W. Punt (1986) ArticleTitleConvergence in some interesting pollen types of Phyllanthus (Euphorbiaceae) Canad. J. Bot. 64 3127–3129 Occurrence Handle10.1139/b86-411

    Article  Google Scholar 

  • W. Punt (1987) ArticleTitleA survey of pollen morphology in Euphorbiaceae with special reference to Phyllanthus Bot. J. Linn. Soc. 94 127–142

    Google Scholar 

  • W. Punt A. Marks (1991) ArticleTitleBuxaceae. The Northwest European Pollen Flora, 50. Rev Palaeobot. Palynol. 69 113–115 Occurrence Handle10.1016/0034-6667(91)90070-J

    Article  Google Scholar 

  • W. Punt W. Nienhuis (1976) ArticleTitleGentianaceae. The Northwest European pollen flora 6. Rev Palaeobot. Palynol. 21 89–123 Occurrence Handle10.1016/0034-6667(76)90018-X

    Article  Google Scholar 

  • Punt W., Blackmore S., Nilsson S., Le Thomas A. E. (1994) Glossary of pollen and spore terminology. LPP Contributions Series No. 1. Utrecht, LPP Foundation, Laboratory of Palaeobotany and Palynology, University of Utrecht.

  • H. Qin (1997) ArticleTitleA taxonomic revision of Lardizabalaceae Cathaya 8 1–214

    Google Scholar 

  • L. D. Rachele (1974) ArticleTitlePollen morphology of Papaveraceae of the northeastern United States and Canada Bull. Torrey Bot. Club 101 152–159 Occurrence Handle10.2307/2484181

    Article  Google Scholar 

  • R. J. Scott M. Spielman H. G. Dickinson (2004) ArticleTitleStamen structure and function Plant Cell 16 S46–S60 Occurrence Handle15131249 Occurrence Handle10.1105/tpc.017012 Occurrence Handle1:CAS:528:DC%2BD2cXlsFWltL8%3D

    Article  PubMed  CAS  Google Scholar 

  • D. E. Soltis A. E. Senters M. J. Zanis S. Kim J. D. Thompson P. S. Soltis L. P. Ronse de Craene P. K. Endress J. S. Farris (2003) ArticleTitleGunnerales are sister to other core eudicots: implications for the evolution of pentamery Amer. J. Bot. 90 461–470

    Google Scholar 

  • Thanikaimoni G. (1978) Palynological terms: proposed definitions – 1. Proc. 4th Internat. Palynol. Conf., Lucknow (1976–1977) 1: 228–239.

  • Thanikaimoni G. (1984) Ménispermacées: palynologie et systématique. Inst. Fr. Pondichéry, Trav. Sect. Sci. Tech. 18: 1–135 (+67 plates).

  • C. F. Beusekom Particlevan (1971) ArticleTitleRevision of Meliosma (Sabiaceae), section Lorenzanea excepted, living and fossil, geography and phylogeny Blumea 19 355–529

    Google Scholar 

  • M. Campo Particlevan (1958) ArticleTitlePalynologie Africaine II Bull. Inst. Fr. Afr. Noire, Ser. A 20 735–760

    Google Scholar 

  • M. Campo Particlevan (1967) ArticleTitlePollen et classification Rev. Palaeobot. Palynol. 3 65–71 Occurrence Handle10.1016/0034-6667(67)90040-1

    Article  Google Scholar 

  • M. Campo Particlevan (1976) Patterns of pollen morphological variation within taxa I. K. Ferguson J. Muller (Eds) The evolutionary significance of the exine Academic Press London 125–135

    Google Scholar 

  • van der Ham R. W. J. M. (1989) Palynology. In: Sabiaceae (by van Beusekom C. F., van de Water T. P. M.). Flora Malesiana, Series I, Vol. 10(4), p. 681.

  • T. P. M. Water Particlevan de (1980) ArticleTitleA taxonomic revision of the genus Sabia (Sabiaceae) Blumea 26 1–64

    Google Scholar 

  • J. W. Walker (1976) Comparative pollen morphology and phylogeny of the ranalean complex C. B. Beck (Eds) Origin and early evolution of angiosperms Columbia University Press New York

    Google Scholar 

  • L. Wanntorp J. Praglowski E. Grafström (2004) ArticleTitleNew insights into the pollen morphology of the genus Gunnera (Gunneraceae) Grana 43 15–21 Occurrence Handle10.1080/00173130310016473

    Article  Google Scholar 

  • M. S. Zavada D. L. Dilcher (1986) ArticleTitleComparative pollen morphology and its relationship to phylogeny of pollen in the Hamamelideae Ann. Missouri Bot. Gard. 73 348–381 Occurrence Handle10.2307/2399117

    Article  Google Scholar 

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Furness, C.A., Magallón, S. & Rudall, P.J. Evolution of endoapertures in early-divergent eudicots, with particular reference to pollen morphology in Sabiaceae. Plant Syst. Evol. 263, 77–92 (2007). https://doi.org/10.1007/s00606-006-0477-y

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