Skip to main content

Advertisement

Log in

Pollen wall ontogeny in Polemonium caeruleum (Polemoniaceae) and suggested underlying mechanisms of development

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

Abstract

By a detailed ontogenetic study of Polemonium caeruleum pollen, tracing each stage of development at high TEM resolution, we aim to understand the establishment of the pollen wall and to unravel the mechanisms underlying sporoderm development. The main steps of exine ontogeny in Polemonium caeruleum, observed in the microspore periplasmic space, are spherical units, gradually transforming into columns, then to rod-like units (procolumellae), the appearance of the initial tectum, growth of columellae in height and tectum in thickness and initial sporopollenin accumulation on them, the appearance of the endexine lamellae and of dark-contrasted particles on the tectum, the appearance of a sponge-like layer and of the intine in aperture sites, the appearance of the foot layer on the base of the sponge-like layer and of spinules on the tectum, and massive sporopollenin accumulation. This sequence of developmental events fits well to the sequence of self-assembling micellar mesophases. This gives (together with earlier findings and experimental exine simulations) strong evidence that genome and self-assembly probably share control of exine formation. It is highly probable that self-assembly is an intrinsic instrument of evolution.

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

Access this article

Subscribe and save

Springer+ Basic
$34.99 /Month
  • Get 10 units per month
  • Download Article/Chapter or eBook
  • 1 Unit = 1 Article or 1 Chapter
  • Cancel anytime
Subscribe now

Buy Now

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

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5
Fig. 6
Fig. 7
Fig. 8
Fig. 9
Fig. 10
Fig. 11
Fig. 12
Fig. 13
Fig. 14

Similar content being viewed by others

Abbreviations

ER:

Endoplasmic reticulum

RER:

Rough endoplasmic reticulum

SAPs:

SP-acceptor particles

SEM:

Scanning electron microscope

TEM:

Transmission electron microscope

SP:

Sporopollenin

References

  • Achnine L, Blancaflor EB, Rasmussen S, Dixon RA (2004) Colocalization of l-phenylalanine ammonia-lyase and cinnamate 4-hydroxylase for metabolic channelling in phenylpropanoid biosynthesis. Plant Cell 16:3098–3109

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ariizumi T, Toriyama K (2011) Genetic regulation of sporopollenin synthesis and pollen exine development. Ann Rev Plant Biol 62:437–460

    Article  CAS  Google Scholar 

  • Ariizumi T, Hatakeyama K, Hinata K, Inatsugi R, Nishida I, Sato S, Kato T, Tabata S, Toriyama K (2004) Disruption of the novel plant protein NEF1 affects lipid accumulation in the plastids of the tapetum and exine formation of pollen, resulting in male sterility in Arabidopsis thaliana. Plant J 39:170–181. doi:10.1111/j.1365-313X.2004.02118.x

    Article  CAS  PubMed  Google Scholar 

  • Audran J-C (1981) Pollen and tapetum development in Ceratozamia mexicana (Cycadaceae): sporal origin of the exinic sporopollenin in cycads. Rev Palaeobot Palynol 33:315–346

    Article  Google Scholar 

  • Ball P (1994) Designing the molecular world. Princeton University Press, Princeton

    Google Scholar 

  • Benítez M (2013) An interdisciplinary view on dynamic models for plant genetics and morphogenesis: scope, examples and emerging research avenues. Front Plant Sci 4:7. doi:10.3389/fpls.2013.00007

    Article  PubMed  PubMed Central  Google Scholar 

  • Blackmore S, Barnes SH (1987) Pollen wall morphogenesis in Tragopogon porrifolius L. (Compositae: Lactuceae) and its taxonomic significance. Rev Palaeobot Palynol 52:233–246

    Article  Google Scholar 

  • Blackmore S, Claugher D (1987) Observations on the substructural organization of the exine in Fagus sylvatica L. (Fagaceae) and Scorzonera hispanica L. (Compositae: Lactuceae). Rev Palaeobot Palynol 5:175–184

    Article  Google Scholar 

  • Blackmore S, Wortley AH, Skvarla JJ, Rowley JR (2007) Pollen wall development in flowering plants. New Phytol 174:483–498

    Article  CAS  PubMed  Google Scholar 

  • Burbulis IE, Winkel-Shirley B (1999) Interactions among enzymes of the Arabidopsis flavonoid biosynthetic pathway. Proc Nat Acad Sci USA 96:12929–12934

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chen W et al (2011) Male Sterile2 encodes a plastid-localized fatty acyl carrier protein reductase required for pollen exine development in Arabidopsis. Plant Physiol 157:842–853

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Collinson ME, Hemsley AR, Taylor WA (1993) Sporopollenin exhibiting colloidal organization in spore walls. Grana Suppl 1:31–39

    Article  Google Scholar 

  • de Leeuw JW, Versteegh GJM, van Bergen PF (2006) Biomacromolecules of algae and plants and their fossil analogues. Plant Ecol 182:209–233

    Article  Google Scholar 

  • Dickinson HG (1970) Ultrastructural aspects of primexine formation in the microspore tetrad of Lilium longiflorum. Cytobiologie 1:437–449

    Google Scholar 

  • Dickinson HG (1976) Common factors in exine deposition. In: Ferguson IK, Muller J (eds) The evolutionary significance of the exine. Academic Press, London, pp 67–89

    Google Scholar 

  • Dickinson HG, Potter U (1976) The development of patterning in the alveolar sexine of Cosmos bipinnatus. New Phytol 76:543–550

    Article  Google Scholar 

  • Dickinson HG, Sheldon JM (1986) The generation of patterning at the plasma membrane of the young microspore of Lilium. In: Blackmore S, Ferguson IK (eds) Pollen and spores: form and function. Linn Soc Symp Ser, no. 12. Academic Press, London, pp 1–18

    Google Scholar 

  • Dobritsa AA et al (2009) CYP704B1 is a long-chain fatty acid omega-hydroxylase essential for sporopollenin synthesis in pollen of Arabidopsis. Plant Physiol 151:574–589

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Dobritsa AA, Geanconteri A, Shrestha J et al (2011) A large-scale genetic screen in Arabidopsis to identify genes involved in pollen Exine production. Pl Physiol (Lancaster) 157:947–970. doi:10.1104/pp.111.179523

    Article  CAS  Google Scholar 

  • Echlin P (1971) The role of the tapetum during microsporogenesis of angiosperms. In: Heslop-Harrison J (ed) Pollen development and physiology. Butterworths, London, pp 41–61

    Chapter  Google Scholar 

  • Fridrichsberg DA (1995) Colloidal chemistry. Chemistry, St.-Petersburg

    Google Scholar 

  • Gabarayeva NI (1990) Hypothetical ways of exine structure determination. Botanicheski Zhurnal 75:1353–1362 (in Russian, with English abstract)

    Google Scholar 

  • Gabarayeva NI (1991) Patterns of development in primitive angiosperm pollen. In: Blackmore S, Barnes SH (eds) Pollen and spores. Clarendon Press, Oxford, pp 257–268

    Google Scholar 

  • Gabarayeva NI (1993) Hypothetical ways of exine pattern determination. Grana 33(Suppl 2):54–59

    Article  Google Scholar 

  • Gabarayeva NI (1995) Pollen wall and tapetum development in Anaxagorea brevipes (Annonaceae): sporoderm substructure, cytoskeleton, sporopollenin precursor particles, and the endexine problem. Rev Palaeobot Palynol 85:123–152

    Article  Google Scholar 

  • Gabarayeva NI (1996) Sporoderm development in Liriodendron chinense (Magnoliaceae): a probable role of the endoplasmic reticulum. Nordic J Bot 16:1–17

    Article  Google Scholar 

  • Gabarayeva NI (2000) Principles and recurrent themes in sporoderm development. In: Harley MM, Morton CM, Blackmore S (eds) Pollen and spores: morphology and biology. Royal Botanic Gardens, Kew, pp 1–17

    Google Scholar 

  • Gabarayeva NI (2014) Role of genetic control and self-assembly in gametophyte sporoderm ontogeny: hypotheses and experiment. Russian J Develop Biol 45:177–195

    Article  Google Scholar 

  • Gabarayeva NI, Grigorjeva VV (2002) Exine development in Stangeria eriopus (Stangeriaceae): ultrastructure and substructure, SP accumulation, the equivocal character of the aperture, and stereology of microspore organelles. Rev Palaeob Palynol 122:185–218

    Article  Google Scholar 

  • Gabarayeva NI, Grigorjeva VV (2004) Exine development in Encephalartos altensteinii (Cycadaceae): ultrastructure, substructure and the modes of SP accumulation. Rev Palaeobot Palynol 132:175–193

    Article  Google Scholar 

  • Gabarayeva NI, Grigorjeva VV (2010) Sporoderm ontogeny in Chamaedorea microspadix (Arecaceae). Self-assembly as the underlying cause of development. Grana 49:91–114

    Article  Google Scholar 

  • Gabarayeva NI, Grigorjeva VV (2011) Sporoderm development in Swida alba (Cornaceae), interpreted as a self-assembling colloidal system. Grana 50:81–101

    Article  Google Scholar 

  • Gabarayeva NI, Grigorjeva VV (2012) Sporoderm development and substructure in Magnolia sieboldii and other Magnoliaceae: an interpretation. Grana 51:119–147

    Article  Google Scholar 

  • Gabarayeva NI, Grigorjeva VV (2013) Experimental modelling of exine-like structures. Grana 52:241–257. doi:10.1080/00173134.2013.818165

    Article  Google Scholar 

  • Gabarayeva NI, Grigorjeva VV (2014) Sporoderm and tapetum development in Eupomatia laurina (Eupomatiaceae). An interpretation Protoplasma 251:1321–1345

    PubMed  Google Scholar 

  • Gabarayeva N, Grigorjeva V (2016) Simulation of exine patterns by self-assembly. Pl Syst Evol 302:1135–1156. doi:10.1007/s00606-016-1322-6

    Article  Google Scholar 

  • Gabarayeva NI, Hemsley AR (2006) Merging concepts: the role of self-assembly in the development of pollen wall structure. Rev Palaeobot Palynol 138:121–139

    Article  Google Scholar 

  • Gabarayeva NI, Rowley JR (1994) Exine development in Nymphaea Colorata (Nymphaeaceae). Nord J Bot 14:671–691

    Article  Google Scholar 

  • Gabarayeva NI, Rowley JR, Skvarla JJ (1998) Exine development in Borago (Boraginaceae). 1. Microspore tetrad period. Taiwania 43:203–214

    Google Scholar 

  • Gabarayeva NI, Blackmore S, Rowley JR (2003a) Observations on the experimental destruction and on substructural organization of the pollen wall of some selected gymnosperms and angiosperms. Rev Palaeobot Palynol 124:203–226

    Article  Google Scholar 

  • Gabarayeva NI, Grigorjeva VV, Rowley JR (2003b) Sporoderm ontogeny in Cabomba aquatica (Cabombaceae). Rev Palaeobot Palynol 127:147–173

    Article  Google Scholar 

  • Gabarayeva N, Grigorjeva V, Rowley JR, Hemsley AR (2009a) Sporoderm development in Trevesia burckii (Araliaceae). I. Tetrad period: further evidence for the participation of self-assembly processes. Rev Palaeobot Palynol 156:211–232

    Article  Google Scholar 

  • Gabarayeva N, Grigorjeva V, Rowley JR, Hemsley AR (2009b) Sporoderm development in Trevesia burckii (Araliaceae). II. Post-tetrad period: further evidence for participating of self-assembly processes. Rev Palaeob Palynol 156:233–247

    Article  Google Scholar 

  • Gabarayeva NI, Grigorjeva VV, Rowley JR (2010a) A new look at sporoderm ontogeny in Persea americana. Micelles and the hidden side of development. Ann Bot 105:939–955

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gabarayeva NI, Grigorjeva VV, Rowley JR (2010b) Sporoderm development in Acer tataricum (Aceraceae). An interpretation. Protoplasma 247:65–81

    Article  PubMed  Google Scholar 

  • Gabarayeva NI, Grigorjeva VV, Polevova SV (2011a) Exine and tapetum development in Symphytum officinale (Boraginaceae). Exine substructure and its interpretation. Plant Syst Evol 296:101–120

    Article  Google Scholar 

  • Gabarayeva NI, Grigorjeva VV, Marquez G (2011b) Ultrastructure and development during meiosis and the tetrad period of sporogenesis in the leptosporangiate fern Alsophila setosa (Cyatheaceae) compared with corresponding stages in Psilotum nudum (Psilotaceae). Grana 50:235–262

    Article  Google Scholar 

  • Gabarayeva NI, Grigorjeva V, Kosenko Y (2013a) I. Primexine development in Passiflora racemosa Brot. Overlooked aspects of development. Plant Syst Evol 299:1013–1035

    Article  CAS  Google Scholar 

  • Gabarayeva N, Grigorjeva V, Kosenko Y (2013b) II. Exine development in Passiflora racemosa Brot.: post-tetrad period. Overlooked aspects of development. Plant Syst Evol 299:1037–1055

    Article  Google Scholar 

  • Gabarayeva N, Grigorjeva V, Polevova S (2014) Sporoderm and tapetum ontogeny in Juniperus communis (Cupressaceae). Connective structures between tapetum and microspores. Rev Palaeobot Palynol 206:23–44

    Article  Google Scholar 

  • Gabarayeva NI, Grigorjeva VV, Blackmore S (2016) Pollen wall substructure and development in Tanacetum vulgare (Compositae: Anthemideae): revisiting hypotheses on pattern formation in complex cell walls. Int J Plant Sci 177:347–370. doi:10.1086/684946

    Article  Google Scholar 

  • Gabarayeva N, Grigorjeva V, Polevova S, Hemsley AR (2017) Pollen wall and tapetum development in Plantago major (Plantaginaceae): assisting self-assembly. Grana 56:81–111. doi:10.1080/ 00173134.2016.1159729

    Article  Google Scholar 

  • Gerasimova-Navashina EN (1973) Physico-chemical nature of primexine formation of angiosperm pollen grains. In: Kovarski A (ed) Embryology of angiosperms. Ştiinţǎ, Kishinev, pp 57–70

    Google Scholar 

  • Geyer G (1973) Ultrahistochemie. Veb Gustav Fischer Verlag, Jena

    Google Scholar 

  • Goodwin TW, Mercer EI (1983) Introduction to plant biochemistry. Pergamon, Oxford

  • Grienenberger E, Kim SS, Lallemand B, Geoffroy P, Heintz D, Souza CA, Heitz T, Douglas CJ, Legrand M (2010) Analysis of tetraketide α-pyrone reductase function in Arabidopsis thaliana reveals a previously unknown, but conserved, biochemical pathway in sporopollenin monomer biosynthesis. Pl Cell 22:4067–4083. doi:10.1105/tpc.110.080036

    Article  CAS  Google Scholar 

  • Griffiths PC, Hemsley AR (2001) Rasberries and muffins—mimicking biological pattern formation. Colloids and Surfaces B Biointerfaces 25:163–170

    Article  Google Scholar 

  • Grigorjeva V, Gabarayeva N (2015) The development of sporoderm, tapetum and Ubisch bodies in Dianthus deltoides (Caryophyllaceae): self-assembly in action. Rev Palaeobot Palynol 219:1–27

    Article  Google Scholar 

  • Gubatz S, Wiermann R (1992) Studies on sporopollenin biosynthesis in Tulipa anthers. 3. Incorporation of specifically labeled C-14 phenylalanine in comparison to other precursors. Bot Acta 105:407–413

    Article  CAS  Google Scholar 

  • Gubatz S, Wiermann R (1993) Studies on sporopollenin biosynthesis in Cucurbita maxima. 1. The substantial labeling of sporopollenin from Cucurbita maxima after application of [C-14] phenylalanine. J Biosci 48:10–15

    CAS  Google Scholar 

  • Gubatz S, Herminghaus S, Meurer B, Strack D, Wiermann R (1986) The location of hydroxycinnamic acid amides in the exine of Corylus pollen. Pollen Spores 28:347–354

    Google Scholar 

  • Gubatz S, Rittscher M, Meuter A, Nagler A, Wiermann R (1993) Tracer experiments on sporopollenin biosynthesis. Grana Suppl 1:12–17

    Article  Google Scholar 

  • Halbritter H, Svojtka M (2005) Polemonium caeruleum. In: PalDat (2005–06-01)—a palynological database

  • Hemsley AR (1998) Nonlinear variation in simulated complex pattern development. J Theor Biol 192:73–79

    Article  CAS  PubMed  Google Scholar 

  • Hemsley AR, Gabarayeva NI (2007) Exine development: the importance of looking through a colloid chemistry “window”. Plant Syst Evol 263:25–49

    Article  Google Scholar 

  • Hemsley AR, Griffiths PC (2000) Architecture in the microcosm: biocolloids, self-assembly and pattern formation. Phil Trans R Soc Lond A 358:547–564

    Article  CAS  Google Scholar 

  • Hemsley AR, Chaloner WG, Scott AC, Groombridge CJ (1992a) Carbon-13 solid-state nuclear magnetic resonance of sporopollenins from modern and fossil plants. Ann Bot (Oxford) 69:545–549

    Article  CAS  Google Scholar 

  • Hemsley AR, Collinson ME, Brain APR (1992b) Colloidal crystal-like structure of sporopollenin in the megaspore walls of recent Selaginella and similar fossil spores. Bot J Linn Soc 108:307–320

    Article  Google Scholar 

  • Hemsley AR, Barrie PJ, Chaloner WG, Scott AC (1993) The composition of sporopollenin: its contribution to living and fossil spore systematics. Grana Suppl 1:2–11

    Article  Google Scholar 

  • Hemsley AR, Jenkins PD, Collinson ME, Vincent B (1996a) Experimental modelling of exine self-assembly. Bot J Linn Soc 121:177–187

    Article  Google Scholar 

  • Hemsley AR, Scott AC, Barrie PJ, Chaloner WG (1996b) Studies of fossil and modern spore wall biomacromolecules using 13C solid state NMR. Ann Bot (Oxford) 78:83–94

    Article  Google Scholar 

  • Hemsley AR, Vincent B, Collinson ME, Griffiths PC (1998) Simulated self-assembly of spore exines. Ann Bot (Oxford) 82:105–109

    Article  Google Scholar 

  • Hemsley AR, Collinson ME, Vicent B, Griffiths PC, Jenkins PD (2000) Self-assembly of colloidal units in exine development. In: Harley MM, Morton CM, Blackmore S (eds) Pollenand spores: morphology and biology. Whitstable Printers Ltd, Whitstable, pp 31–44

    Google Scholar 

  • Hemsley AR, Griffiths PC, Mathias R, Moore SEM (2003) A model for the role of surfactants in the assembly of exine sculpture. Grana 42:38–42

    Article  Google Scholar 

  • Herminghaus S, Gubatz S, Arendt S, Wiermann R (1988) The occurrence of phenols as degradation products of natural sporopollenin—a comparison with “synthetic sporopollenin”. Z Naturf 43c:491–500

    Google Scholar 

  • Heslop-Harrison J (1972) Pattern in plant cell wall: morphogenesis in miniature. Proc Royal Inst Great Brit 45:335–351

    Google Scholar 

  • Heslop-Harrison J (1976) The adaptive significance of the exine. In: Ferguson IK, Muller J (eds) The evolutionary significance of the exine. Academic Press, London, pp 27–37

    Google Scholar 

  • Heslop-Harrison J, Dickinson HG (1969) Time relationships of sporopollenin synthesis associated with tapetum and microspores in Lilium. Planta 84:199–214

    Article  CAS  PubMed  Google Scholar 

  • Hu J, Wang Z, Zhang L, Sun MX (2014) The Arabidopsis Exine formation defect (EFD) gene is required for primexine patterning and is critical for pollen fertility. New Phytol 203:140–154

    Article  CAS  PubMed  Google Scholar 

  • Ingber DE (2003) Tensegrity II. How structural networks influence cellular information processing networks. J Cell Sci 116:1397–1408

    Article  CAS  PubMed  Google Scholar 

  • Kauffman SA (1993) The origins of order. Univ. Press, Oxford

    Google Scholar 

  • Kurakin A (2005) Self-organization versus watchmaker: stochastic dynamics of cellular organization. Biol Chem 386:247–254

    Article  CAS  PubMed  Google Scholar 

  • Lallemand B, Erhardt M, Heitz T, Legrand M (2013) Sporopollenin biosynthetic enzymes interact and constitute a metabolon localized to the endoplasmic reticulum of tapetum cells. Plant Physiol 162:616–625

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Legrand M (2010) Analysis of of tetraketide α-pyrone reductase function in Arabidopsis thaliana reveals a previously unknown, but conserved, biochemical pathway in sporopollenin monomer biosynthesis. Pl Cell 22:4067–4083

    Article  CAS  Google Scholar 

  • Li H, Zhang D (2010) Biosynthesis of anther cuticle and pollen exine in rice. Plant Signal Behav 5:1121–1123

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li-Beisson Y, Shorrosh B, Beisson F, Andersson MX, Arondel V, Bates PD, Baud S, Bird D, DeBono A, Durrett TP, Franke RB, Graham IA, Katayama K, Kelly AA, Larson T, Markham JE, Miquel M, Molina I, Nishida I, Rowland O, Samuels L, Schmid KM, Wada H, Welti R, Xu C, Zallot R, Ohlrogge J (2010) Acyl-Lipid Metabolism. The Arabidopsis Book 8:e0133. doi:10.1199/tab.0133

    Article  PubMed  PubMed Central  Google Scholar 

  • Lintilhac PM (2014) The problem of morphogenesis: unscripted biophysical control systems in plants. Protoplasma 251:25–36. doi:10.1007/s00709-013-0522-y

    Article  CAS  PubMed  Google Scholar 

  • Liu L, Fan X-D (2013) Tapetum: regulation and role in SP biosynthesis in Arabidopsis. Plant Mol Biol 83:165–175

    Article  CAS  PubMed  Google Scholar 

  • Lou Y, Xu XF, Zhu J, Gu JN, Blackmore S, Yang ZN (2014) The tapetal AHL family protein TEK determines nexine formation in the pollen wall. Nature Plants. doi:10.1038/ncomms4855

  • Mandelbrot BB (1982) The fractal geometry of nature. W. H. Freeman and co., San Francisco

    Google Scholar 

  • Markham KR, Gould KS, Winefield CS, Mitchell KA, Bloor SJ, Boase MR (2000a) Anthocyanic vacuolar inclusions–their nature and significance in flower colouration. Phytochemistry 55:327–336

    Article  CAS  PubMed  Google Scholar 

  • Markham KR, Ryan KG, Gould KS, Rickards GK (2000b) Cell wall sited flavonoids in Lisianthus flower petals. Phytochemistry 54:681–687

    Article  CAS  PubMed  Google Scholar 

  • Moore SEM, Gabarayeva N, Hemsley AR (2009) Morphological, developmental and ultrastructural comparison of Osmunda regalis L. spores with spore mimics. Rev Paleobot Palynol 156:177–184

    Article  Google Scholar 

  • Mousdale DM, Coggins JR (1985) Subcellular localization of the common shikimate-pathway enzymes in Pisum sativum L. Planta 163:231–249

    Article  Google Scholar 

  • Muravnik LE, Shavarda AL (2011) Pericarp peltate trichomes in Pterocarya rhoifolia: histochemistry, ultrastructure, and chemical composition. Int J Plant Sci 172(2):159–172

    Article  CAS  Google Scholar 

  • Murphy DJ, Vance J (1999) Mechanisms of lipid-bodies formation. TIBS 24:109–115

    CAS  PubMed  Google Scholar 

  • Niester-Nyveld C, Haubrich A, Kampendonk H et al. (1997) Immunocytochemical localization of phenolic compounds in pollen walls using antibodies against p-coumaric acid coupled to bovine serum albumin. Protoplasma 197: 148-159

  • Pettitt JM (1979) Ultrastructure and cytochemistry of spore wall morphogenesis. In: Dyer AF (ed) The experimental biology of ferns. Academic Press, London – New York – San Francisco, pp 211–252

    Google Scholar 

  • Pettitt JM, Jermy AC (1974) The surface coats on spores. Biol J Linn Soc 6:245–257

    Article  Google Scholar 

  • Piffanelli P, Ross JHE, Murphy DJ (1998) Biogenesis and function of the lipidic structures of pollen grains. Sex Plant Reprod 11:65–80

    Article  CAS  Google Scholar 

  • Quilichini TD, Douglas CJ, Samuels AL (2014) New views of tapetum ultrastructure and pollen exine development in Arabidopsis thaliana. Ann Bot, mcu042. doi:10.1093/aob/mcu042

  • Quilichini TD, Grienenberger E, Douglas CJ (2015) The biosynthesis, composition and assembly of the outer pollen wall: a tough case to crack. Phytochemistry 113:170–182

    Article  CAS  PubMed  Google Scholar 

  • Regier JC, Hatzopoulos AK (1988) Evolution in steps: the role of regulatory alterations in the diversification of the moth chorion morphogenetic pathway. In: Varner JE (ed) Self-assembling architecture. Alan R. Liss, New York, pp 179–202

    Google Scholar 

  • Roughan PG, Slack CR (1982) Cellular organization of glycerolipid metabolism. Ann Rev Plant Physiol 33:97–132

    Article  CAS  Google Scholar 

  • Rowley JR (1971) Implications on the nature of sporopollenin based upon pollen development. In: Brooks J, Grant PR, Muir M, van Gijzel P, Shaw G (eds) Sporopollenin. Academic Press, London, pp 174–219

    Chapter  Google Scholar 

  • Rowley JR (1973) Formation of pollen exine bacules and microchannels on a glycocalyx. Grana 13:129–138

    Article  Google Scholar 

  • Rowley JR (1975) Lipopolysaccharide embedded within the exine of pollen grains. In: Bailey GW (ed), 33rd Ann Proc Electron Microscopy Soc Amer Las Vegas, Nevada, pp 572–573

  • Rowley JR (1990) The fundamental structure of the pollen exine. Plant Syst Evol Suppl 5:13–29

    Article  Google Scholar 

  • Rowley JR, Dahl AO (1977) Pollen development in Artemisia vulgaris with special reference to glycocalyx material. Pollen Spores 19:169–284

    Google Scholar 

  • Rowley JR, Claugher D (1991) Receptor-independent sporopollenin. Botanica Acta 104:316–323

    Article  Google Scholar 

  • Rowley JR, Rowley JS (1998) Stain reversal in pollen exines. In: Narendra MD (ed) Current concepts in pollen-spore and biopollination research. Research Periodicals and Book Publishing House, India – USA – UK, pp 223–232

    Google Scholar 

  • Rowley JR, Prijianto B (1977) Selective destruction of the exine of pollen grains. Geophytology 7:1–23

    Google Scholar 

  • Rowley JR, Flynn JJ, Takahashi M (1995) Atomic force microscope information on pollen exine substructure in Nuphar. Bot Acta 108:300–308

    Article  Google Scholar 

  • Rowley JR, Skvarla JJ, Gabarayeva NI (1999) Exine development in Borago (Boraginaceae). 2. Free microspore stages. Taiwania 44:212–229

    Google Scholar 

  • Rowley JR, Gabarayeva NI, Skvarla JJ, El-Ghazaly G (2001) The effect of 4-methylmorpholine N-oxide monohydrate (MMNO.H2O) on pollen and spore exines. Taiwania 46:246–273

    Google Scholar 

  • Sampson FB (1977) Pollen tetrads of Hedycarya arborea J. R. Et G. Forst. (Monimiaceae). Grana 16:61–73

    Article  Google Scholar 

  • Sampson FB (2000) Pollen diversity in some modern magnoliids. Int J Plant Sci 161:193–210

    Article  Google Scholar 

  • Scott RJ (1994) Pollen exine—the sporopollenin enigma and the physics of pattern. In: Scott RJ, Stead MA (eds) Society for Experimental Biology seminar Ser 55: molecular and cellular aspects of plant reproduction. Cambridge Univ Press, Cambridge, pp 49–81

    Chapter  Google Scholar 

  • Sheldon JM, Dickinson HG (1983) Determination of patterning in the pollen wall of Lilium henryi. J Cell Sci 63:191–208

    CAS  PubMed  Google Scholar 

  • Shi J, Cui M, Yang L, Kim Y-J, Zhang D (2015) Genetic and biochemical mechanisms of pollen wall development. Trends Pl Sci 20:741–753

    Article  CAS  Google Scholar 

  • Skvarla JJ, Rowley JR (1987) Ontogeny of pollen in Poinciana (Leguminosae). I. Development of exine template. Rev Palaeobot Palynol 50:239–311

    Article  Google Scholar 

  • Southworth D (1974) Solubility of pollen exines. Am J Bot 61:36–44

    Article  Google Scholar 

  • Southworth D (1986) Substructural organization of pollen exines. In: Blackmore S, Ferguson IK (eds) Pollen spores: form and function. Acad. Press, London, pp 61–69

    Google Scholar 

  • Southworth D, Jernstedt JA (1995) Pollen exine development precedes microtubule rearrangement in Vigna unguiculata (Fabaceae): a model for pollen wall patterning. Protoplasma 187:79–87

    Article  Google Scholar 

  • Taylor ML, Osborn JM (2006) Pollen ontogeny in Brasenia (Cabombaceae, Nymphaeales). Amer J Bot 93:344–356

    Article  Google Scholar 

  • Taylor ML, Hudson PJ, Rigg JM, Strandquist JN, Green JS, Thiemann TC, Osborn JM (2013) Pollen ontogeny in Victoria (Nymphaeales). Int J Plant Sci 174:1259–1276

    Article  Google Scholar 

  • Taylor M, Cooper RL, Schneider EL, Osborn JM (2015) Pollen structure and development in Nymphaeales: insights into character evolution in an ancient angiosperm lineage. Am J Bot 102:1–18. doi:10.3732/ajb.1500249

    Article  Google Scholar 

  • Thompson DW (1961) On growth and form. Abridged edition. Cambridge university Press, Cambridge

    Google Scholar 

  • van Bergen PF, Blokker P, Collinson ME, Sinninghe Damsté JS, de Leeuw JW (2004) Structural biomacromolecules in plants: what can be learnt from the fossil record? In: Hemsley AR, Poole I (eds) The evolution of plant physiology. Academic Press, Amsterdam, pp 134–154

    Google Scholar 

  • van Uffelen GA (1991) The control of spore wall formation. In: Blackmore S, Barnes SH (eds) Pollen and spores: patterns of diversification. Clarendon Press, Oxford, pp 89–102

    Google Scholar 

  • Vinckier S, Smets E (2005) A histological study of microsporogenesis in Tarenna gracilipes (Rubiaceae). Grana 44:30–44

    Article  Google Scholar 

  • Waha M (1987) Sporodcrm development of pollen tetrads in Asimina triloba (Annonaceae). Pollen Spores 29:31–44

    Google Scholar 

  • Wallace S, Fleming A, Wellman CH, Beerling DJ (2011) Evolutionary development of the plant spore and pollen wall. AoB PLANTS 2011:plr027. doi:10.1093/aobpla/plr027

    Article  PubMed  PubMed Central  Google Scholar 

  • Wellman CH (2004) Origin, function and development of the spore wall in early land plants. In: Hemsley AR, Poole I (eds) The evolution of plant physiology. Royal Botanic Gardens, Kew, pp 43–63

    Chapter  Google Scholar 

  • Wiermann R, Gubatz S (1992) Pollen wall and sporopollenin. Int Rev Cytol 140:35–72

    Article  CAS  Google Scholar 

  • Wilmesmeier S, Wiermann R (1995) Influence of EPTC (S-ethyl-dipropyl-thiocarbamate) on the composition of surface waxes and sporopollenin structure in Zea mays. J Pl Physiol 146:22–28

    Article  CAS  Google Scholar 

  • Wilmesmeier S, Wiermann R (1997) Immunocytochemical localization of phenolic compounds in pollen walls using antibodies against p-coumaric acid coupled to bovine serum albumin. Protoplasma 197:148–159

    Article  Google Scholar 

  • Zaprometov MN (1993) Phenolic compounds: distribution, metabolism and functions in plants. Nauka, Moskow

    Google Scholar 

  • Zavada MS, Gabarayeva NI (1991) Comparative pollen wall development of Welwitschia mirabilis and selected primitive angiosperms. Bull Torrey Bot Club 118:292–302

    Article  Google Scholar 

  • Zhang D, Li H (2014) Exine export in pollen. In: Geisler M. et al., eds. Plant ABC Transporters. Springer, IPS, pp 49–62

Download references

Acknowledgements

This work was partly supported by grant no. 17-04-00517 of Russian Foundation for Basic Research for Nina Gabarayeva (chemicals) and partly provided in the framework of institutional research project of the Komarov Botanical Institute of the Russian Academy of Sciences (using equipment of The Core Facility Center “Cell and Molecular Technologies in Plant Science”). The authors wish to thank Dr. F. Bruce Sampson for some comments and suggested improvements to the English. Our special thanks to our anonymous reviewers.

Author information

Authors and Affiliations

Authors

Contributions

Conceptualization: N.G.; Methodology: N.G., V. G.; Investigation: N.G., V.G.; Righting original draft, review and editing: N.G.; Funding acquisition: N.G.; Resources: V.G.; Supervision: N.G.

Corresponding author

Correspondence to Nina Gabarayeva.

Ethics declarations

Conflict of interest

The authors declare that they have no conflict of interests.

Additional information

Handling Editor: Benedikt Kost

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Grigorjeva, V.V., Gabarayeva, N. Pollen wall ontogeny in Polemonium caeruleum (Polemoniaceae) and suggested underlying mechanisms of development. Protoplasma 255, 109–128 (2018). https://doi.org/10.1007/s00709-017-1121-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00709-017-1121-0

Keywords

Navigation