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Successive microsporogenesis in eudicots, with particular reference to Berberidaceae (Ranunculales)

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Abstract

The eudicot clade of angiosperms is characterised by simultaneous microsporogenesis and tricolpate pollen apertures. Successive microsporogenesis, where a distinct dyad stage occurs after the first meiotic division, is relatively rare in eudicots although it occurs in many early branching angiosperms including monocots. An extensive literature survey shows that successive microsporogenesis has arisen independently at least six times in eudicots, in five different orders, including Berberidaceae (Ranunculales). Microsporogenesis and pollen apertures were examined here using light and transmission electron microscopy in eleven species representing six genera of Berberidaceae. Successive microsporogenesis is a synapomorphy for the sister taxa Berberis and Mahonia (and possibly also Ranzania), the remaining genera are simultaneous. Callose wall formation in Berberis and Mahonia is achieved by centripetal furrowing, though centrifugal cell plates are more usual for this microsporogenesis type. This discrepancy could reflect the fact that the successive type in Berberidaceae is derived from the simultaneous type, and centripetal furrowing has been retained. Eudicots with successive microsporogenesis usually produce tetragonal or decussate tetrads, though occasional tetrahedral or irregular tetrads in Berberis and Mahonia indicate that the switch from simultaneous to successive division is incomplete or “leaky”. In contrast, linear tetrads produced by successive microsporogenesis in Asclepiadoideae (Apocynaceae s.l.) are the result of a highly specialised developmental pathway leading to the production of pollinia. Pollen in successive eudicots is dispersed as monads, dyads, tetrads, and as single grains in pollinia. Apertures are diverse, and patterns include spiraperturate, clypeate, irregular, monocolpate, diporate and inaperturate. It is possible that successive microsporogenesis, although rare, potentially occurs in other eudicots, for example, in species where pollen is inaperturate.

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References

  • Adachi J, Kosuge K, Denda T, Watanabe K (1995) Phylogenetic relationships in the Berberidaceae based on partial sequences of the gapA gene. Pl Syst Evol [Suppl] 9:351–353

    Google Scholar 

  • Airy Shaw HK (1973) J. C. Willis’ a dictionary of the flowering plants and ferns. 8th edn. Cambridge University Press, Cambridge

    Google Scholar 

  • Angiosperm Phylogeny Group (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

    Article  Google Scholar 

  • Banks H, Stafford P, Crane PR (2007) Another look at the pollen of Nelumbo (Nelumbonaceae). Grana 46:157–163

    Article  Google Scholar 

  • Barkman TJ, Lim S-H, Salleh KM, Nais J (2004) Mitochondrial DNA sequences reveal the photosynthetic relatives of Rafflesia, the world’s largest flower. Proc Nat Acad Sci USA 101:787–792

    Article  PubMed  CAS  Google Scholar 

  • Blackmore S, Barnes SH (1995) Garside’s rule and the microspore tetrads of Grevillea rosmarinifolia A. Cunningham and Dryandra polycephala Bentham (Proteaceae). Rev Palaeobot Palynol 85:111–121

    Article  Google Scholar 

  • Blackmore S, Crane PR (1998) The evolution of apertures in the spores and pollen grains of embryophytes. In: Owens S, Rudall PJ (eds) Reproductive biology. Royal Botanic Gardens, Kew, pp 159–182

    Google Scholar 

  • Blackmore S, Thiele K (1988) Successive cytokinesis during microsporogenesis in the Proteaceae. In: Knox RB, Singh MB, Troiani LF (eds) Pollination ’88. Univ. Melbourne, pp 47–49

  • Blarer A, Nickrent DL, Endress PK (2004) Comparative floral structure and systematics in Apodanthaceae (Rafflesiales). Pl Syst Evol 245:119–142

    Article  Google Scholar 

  • Carafa AM, Pizzolongo P (1990) Callose in cell walls during reproductive processes in Cytinus hypocistis L. Caryologia 43:57–63

    Google Scholar 

  • Dan Dicko-Zafimahova L (1980) Etude ontogénique de la pollinie de Calotropis procera (Ascelpiadaceae). Apport de la microscopie photonique. Grana 19:85–98

    Google Scholar 

  • Dan Dicko-Zafimahova L, Audran J-C (1981) Etude ontogénique de la pollinie de Calotropis procera (Ascelpiadaceae). Apports préliminaires de la microscopie électronique. Grana 20:81–99

    Google Scholar 

  • Dannenbaum C, Schill R (1991) Die Entwicklung der Pollentetraden und Pollinien bei den Asclepiadaceae. Biblio Bot 141:1–138

    Google Scholar 

  • Davis CC, Wurdack KJ (2004) Host-to-parasite gene transfer in flowering plants: phylogenetic evidence from Malpighiales. Science 305:676–678

    Article  PubMed  CAS  Google Scholar 

  • Donoghue MJ, Doyle JA (1989) Phylognetic analysis of angiosperms and the relationships of Hamamelidae. In: Crane PR, Blackmore S (eds) Evolution, systematics, and fossil history of the Hamamelidae, vol 1. Clarendon press, Oxford, pp 17–45

    Google Scholar 

  • Doyle JA, Hotton CL (1991) Diversification of early angiosperm pollen in a cladistic context. In: Blackmore S, Barnes SH (eds) Pollen and spores: patterns of diversification. Clarendon Press, Oxford, pp 169–195

    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

    Google Scholar 

  • Ernst A, Schmidt E (1913) Über Blüte und Frucht von Rafflesia. Ann Jard Bot Buitenzorg Ser 2(12):1–58

    Google Scholar 

  • Feng M, Pan K-Y, Lu A-M (1995) Embryology of Epimedium L. (Berberidaceae) and its systematic significance. Cathaya 7:125–132

    Google Scholar 

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

    Google Scholar 

  • Furness CA (2007) Why does pollen lack apertures? A review of inaperturate pollen in eudicots. Bot J Linn Soc 155:29–48

    Article  Google Scholar 

  • Furness CA, Rudall PJ (1999a) Microsporogenesis in monocotyledons. Ann Bot 84:475–499

    Article  Google Scholar 

  • Furness CA, Rudall PJ (1999b) Inaperturate pollen in monocotyledons. Int J Pl Sci 160:395–414

    Article  Google Scholar 

  • Furness CA, Rudall PJ (2000) The systematic significance of simultaneous cytokinesis during microsporogenesis in monocotyledons. In: Wilson KL, Morrison DA (eds) Monocots: systematics and evolution. CSIRO, Melbourne, pp 189–193

    Google Scholar 

  • Furness CA, Rudall PJ (2001) Pollen and anther characters in monocot systematics. Grana 40:17–25

    Article  Google Scholar 

  • Furness CA, Rudall PJ (2002) Evolution of microsporogenesis in angiosperms. Int J Pl Sci 163:235–260

    Article  Google Scholar 

  • Furness CA, Rudall PJ (2004) Pollen aperture evolution – a crucial factor for eudicot success? Trends Pl Sci 9:154–158

    Article  CAS  Google Scholar 

  • Garside S (1946) The developmental morphology of the pollen of Proteaceae. J S African Bot 12:27–34

    Google Scholar 

  • Hansen B, Straka H (1978) Palynologica Madagassica et Mascarenica. Families 61–64. Pollen Spores 20:157–166

    Google Scholar 

  • Hoot SB, Crane PR (1995) Inter-familial relationships in the Ranunculidae based on molecular systematics. Pl Syst Evol [Suppl] 9:119–131

    Google Scholar 

  • Hoot SB, Magallón S, Crane PR (1999) Phylogeny of basal eudicots based on three molecular datasets: atpB, rbcL and 18S nuclear ribosomal DNA sequences. Ann Missouri Bot Gard 86:1–32

    Article  Google Scholar 

  • Hutchinson J (1973) The familes of flowering plants. 3rd edn. Oxford University Press, Oxford

    Google Scholar 

  • Jäger-Zürn I, Novelo RA, Philbrick CT (2006) Microspore development in Podostemaceae-Podostemoideae, with implications on the characterization of the subfamilies. Pl Syst Evol 256:209–216

    Article  Google Scholar 

  • Johnson LAS, Briggs BG (1975) On the family Proteaceae––the evolution and classification of a southern family. Bot J Linn Soc 70:83–182

    Article  Google Scholar 

  • Khosla C, Shivanna KR, Mohan Ram HY (2001) Cleistogamy in Griffithella hookeriana (Podostemaceae). S African J Bot 67:320–324

    Google Scholar 

  • Kim Y-D, Jansen RK (1995) Phylogenetic implications of chloroplast DNA variation in the Berberidaceae. Pl Syst Evol [Suppl] 9:341–349

    Google Scholar 

  • Kim Y-D, Jansen RK (1996) Phylogenetic implications of rbcL and ITS sequence variation in the Berberidaceae. Syst Bot 21:381–396

    Article  Google Scholar 

  • Kim Y-D, Jansen RK (1998) Chloroplast DNA restriction site variation and phylogeny of the Berberidaceae. Amer J Bot 85:1766–1778

    Article  CAS  Google Scholar 

  • Kim Y-D, Kim S-H, Kim CH, Jansen RK (2004) Phylogeny of Berberidaceae based on sequences of the chloroplast gene ndhF. Biochem Syst Ecol 32:291–301

    Article  CAS  Google Scholar 

  • Kosenko VN (1980) Comparative palynomorphological study of the family Berberidaceae, 1. Morphology of pollen grains of the genera Diphylleia, Podophyllum, Nandina, Berberis, Mahonia, Ranzania. Bot Zhurn 65:198–205

    Google Scholar 

  • Loconte H, Estes JR (1989) Phylogenetic systematics of Berberidaceae and Ranunculales (Magnoliidae). Syst Bot 14:565–579

    Article  Google Scholar 

  • Magnus W, Werner E (1913) Die atypische Embryonalentwicklung der Podostemaceen. Flora 105:276–336

    Google Scholar 

  • Maheswari Devi H (1964) Embryological studies in Ascelpiadaceae. Proc Indiana Acad Sci 60B:52–65

    Google Scholar 

  • Mukkada AJ (1962) Some observations on the embryology of Dicraea stylosa Wight. In: Plant morphology: a symposium. Council of Science and Industrial Research, New Delhi, pp 139–145

  • Nadot S, Forchoni A, Penet L, Sannier J, Ressayre A (2006) Links between early pollen development and aperture patttern in monocots. Protoplasma 228:55–64

    Article  PubMed  CAS  Google Scholar 

  • Nickrent DL, Blarer A, Qiu Y-L, Vidal-Russel R, Anderson FE (2004) Phylogenetic inference in Rafflesiales: the influence of rate heterogeneity and horizontal gene transfer. BMC Evol Biol 4:40. http://www.biomedcentral.com/1471-2148/4/40

    Google Scholar 

  • Nickol MG (1995) Phylogeny and inflorescences of Berberidaceae––a morphological survey. Pl Syst Evol [Suppl] 9:327–340

    Google Scholar 

  • Nowicke JW, Skvarla JJ (1979) Pollen morphology: the potential influence in higher order systematics. Ann Missouri Bot Gard 66:633–700

    Article  Google Scholar 

  • Nowicke JW, Skvarla JJ (1981) Pollen morphology and systematic relationships of the Berberidaceae. Smithsonian Contrib Bot 50:1–83

    Google Scholar 

  • O’Neill SP, Osborn JM, Philbrick CT, Novelo AR (1997) Comparative pollen morphology of five New World genera of Podostemaceae. Aquat Bot 57:133–150

    Article  Google Scholar 

  • Osborn JM, O’Neill SP, El-Ghazaly G (2000) Pollen morphology and ultrastructure of Marathrum schiedeanum. Grana 39:221–225

    Article  Google Scholar 

  • Passarelli LM, Girade SB, Tur NM (2002) Palynology of South American Podostemaceae. I. Apinagia Tul. Grana 41:10–15

    Article  Google Scholar 

  • Razi BA (1949) Embryological studies of two members of the Podostemaceae. Bot Gaz 111:211–218

    Article  Google Scholar 

  • Ressayre A, Dreyer L, Triki-Teurtroy S, Forchoni A, Nadot S (2005) Post-meiotic cytokinesis and pollen aperture pattern ontogeny: comparison of development in four species differing in aperture pattern. Amer J Bot 92:576–583

    Article  Google Scholar 

  • Roland-Heydacker F (1979) Aspects ultrastructuraux de l’ontogénie du pollen et du tapis chez Mahonia aquifolium Nutt. Berberidaceae. Pollen Spores 21:259–278

    Google Scholar 

  • Rudall PJ, Furness CA, Chase MW, Fay MF (1997) Microsporogenesis and pollen sulcus type in Asparagales (Lilianae). Canad J Bot 75:408–430

    Google Scholar 

  • Rutishauser R (1997) Structural and developmental diversity in Podostemaceae (river-weeds). Aquat Bot 57:29–70

    Article  Google Scholar 

  • Sampson FB (1963) The floral morphology of Pseudowintera, the new Zealand member of the vesselless Winteraceae. Phytomorphology 13:403–423

    Google Scholar 

  • Sampson FB (1970) Unusual features of cytokinesis in meiosis of pollen mother cells of Pseudowintera traversii (Buchan.) Dandy (Winteraceae). Beitr Biol Pflanz 47:71–77

    Google Scholar 

  • Sastri RLN (1969) Floral morphology, embryology, and relationships of the Berberidaceae. Austral J Bot 17:69–79

    Article  Google Scholar 

  • Smith FG (1968) “Dyads” in the Proteaceae. Grana Palynol 8:86–87

    Article  Google Scholar 

  • Takhtajan AL, Meyer NR, Kosenko VN (1985) Pollen morphology and classification in Rafflesiaceae s.l. Bot Zhurn 70:153–168

    Google Scholar 

  • Venkata Rao C, Rama Rao S (1954) Embryology of Cryptostegia grandiflora R.Br. and Caralluma attenuata WT. J Indian Bot Soc 33:453–472

    Google Scholar 

  • Verhoeven RL, Venter HJ (2001) Pollen morphology of the Periplocoideae, Secamonioideae, and Asclepiadoideae (Apocynaceae). Ann Missouri Bot Gard 88:569–582

    Article  Google Scholar 

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Furness, C.A. Successive microsporogenesis in eudicots, with particular reference to Berberidaceae (Ranunculales). Plant Syst Evol 273, 211–223 (2008). https://doi.org/10.1007/s00606-008-0001-7

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