Abstract
A review of our own and literature data on the mechanisms of sporoderm (the wall of pollen grains and spores) development is presented in terms of colloidal interactions—the so-called micellar hypothesis (Gabarayeva and Hemsley, 2006; Hemsley and Gabarayeva, 2007), which suggests the participation of self-assembly processes in development. The development of exine (sporopollenin-containing part of the sporoderm) in five plant species from remote taxa has been traced in detail and interpreted as a micellar sequence. An experimental modeling of exine-like structures carried out in vitro, in which physicochemical patterns of colloidal systems (hydrophobic interactions) were the driving force, is strong evidence for the relevance of the micellar hypothesis and the promising nature of these studies. The correlation between the role of genomic control and self-assembly in the development of complex biological walls is discussed.
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Abbreviations
- SAS:
-
surface active substance
- SAPs:
-
sporopollenin-acceptor particles
- SP:
-
sporopollenin
- HPMC:
-
hydroxypropyl methylcellulose
- TEM:
-
transmission electron microscope
References
D’Arcy Thompson, W., On Growth and Form, Cambridge: Cambridge University Press, 1917.
D’Arcy Thompson, W., On Growth and Form, Cambridge: Cambridge University Press, 1959.
Ariizumi, T. and Toriyama, K., Genetic regulation of sporopollenin synthesis and pollen exine development, Ann. Rev. Plant Biol., 2011, vol. 62, no. 1, pp. 1–1.24.
Ariizumi, T., Hatakeyama, K., Hinata, K., et al., 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., 2004, vol. 39, pp. 170–181.
Ariizumi, T., Hatakeyama, K., Hinata, K., et al., The HKM gene, which is identical to the MS1 gene of Arabidopsis thaliana, is essential for primexine formation and exine pattern formation, Sex. Plant Reprod., 2005, vol. 18, pp. 1–7.
Blackmore, S., Sporoderm homologies and morphogenesis in land plants, with a discussion on Echinops sphaerocephala (Compositae), Plant Syst. Evol., 1990, vol. 5, pp. 1–12.
Blackmore, S. and Barnes, S.H., Pollen wall morphogenesis in Tragopogon porrifolius L. (Compositae: Lactuceae) and its taxonomic significance, Rev. Palaeob. Palynol., 1987, vol. 52, pp. 233–246.
Blackmore, S. and Barnes, S.H., Comparative studies of mature and developing pollen grains, in Scanning Electron Microscopy in Taxonomy and Functional Morphology. Systematics Association, Claugher, D., Ed., Oxford: Clarendon Press, 1990, spec. vol. no. 41, pp. 1–21.
Blackmore, S. and Claugher, D., Observations at the substructural organization of the exine in Fagus sylvatica L. (Fagaceae) and Scorzonera hispanica L. (Compositae: Lactuceae), Rev. Palaeob. Palynol., 1987, vol. 5, pp. 175–184.
Blackmore, S., Wortley, A.H., Skvarla, J.J., and Rowley, J.R., Pollen wall development in flowering plants, New Phytol., 2007, vol. 174, pp. 483–498.
Clark, A.H., Richardson, R.K., Ross-Murphy, S.B., and Stubbs, J.M., Structural and mechanical properties of agar/gelatin co-gels, Marcomolecules, 1983, vol. 16, pp. 1367–1374.
Collinson, M.E., Hemsley, A.R., and Taylor, W.A., Sporopollenin exhibiting colloidal organization in spore walls, Grana, 1993, Suppl. 1, pp. 31–39.
Dahl, A.O., Rowley, J.R., Stein, O.L., and Wegstedt, L., The intracellular distribution of mass during ontogeny of pollen in Tradescantia L., Exp. Cell Res., 1957, vol. 13, pp. 31–46.
Dong, X.Y., Hong, Z.L., Sivaramakrichnan, M., et al., Callose synthase (CalS5) is required for exine formation during microgametogenesis and for pollen viability in Arabidopsis, Plant J., 2005, vol. 42, pp. 315–328.
Fridrikhsberg, D.A., Kolloidnaya khimiya (Colloidal Chemistry), St. Petersburg: Khimiya, 1995.
Gabarayeva, N.I., The development of exine in Michelia fuscata (Magnoliaceae) in connection with changes of cytoplasmic organelles and tapetum, Bot. Zh., 1986a, vol. 71, no. 3, pp. 311–322.
Gabarayeva, N.I., Ultrastructural study on the development of intine in Michelia fuscata (Magnoliaceae) in connection with changes of cytoplasmic organelles and tapetum, Bot. Zh., 1986b, vol. 71, no. 4, pp. 416–428.
Gabarayeva, N.I., Ultrastructure and development of sporoderm in Manglietia tenuipes (Magnoliaceae) in the course of the tetrad period: the formation of primexine in connection with cytoplasmic organelles activity, Bot. Zh., 1987a, vol. 72, no. 3, pp. 281–290.
Gabarayeva, N.I., Ultrastructure and development of endexine lamellae in Manglietia tenuipes (Magnoliaceae) in connection with the question about the presence of the endexine in primitive angiosperms, Bot. Zh., 1987b, vol. 72, no. 10, pp. 1310–1317.
Gabarayeva, N.I., Ultrastructure and development of the pollen wall in Manglietia tenuipes (Magnoliaceae) the intine formation in connection with cytoplasmic organelles activity, Bot. Zh., 1987c, vol. 72, no. 11, pp. 1470–1477.
Gabarayeva, N.I., On the site of synthesis of sporopollenin precursors in the developing pollen grains of Magnoliaceae representatives, Bot. Zh., 1990a, vol. 75, no. 6, pp. 783–791.
Gabarayeva, N.I., Hypothetical ways of exine structure determination, Bot. Zh., 1990b, vol. 75, no. 10, pp. 1353–1362.
Gabarayeva, N.I., Patterns of development in primitive angiosperm pollen, in Pollen Spores: Patterns of Diversification, Blackmore, S. and Barnes, S.H., Eds., Oxford: Clarendon Press, 1991a, pp. 257–268.
Gabarayeva, N.I., Ultrastructure and development of exine and orbicules in Magnolia delavayi (Magnoliaceae) in the tetrad and at the beginning of post-tetrad period, Bot. Zh., 1991b, vol. 76, no. 1, pp. 10–19.
Gabarayeva, N.I., Hypothetical ways of exine pattern determination, Grana, 1993, vol. 33, suppl. 2, pp. 54–59.
Gabarayeva, N.I., Ultrastructural foundations of sporoderm development in representatives of Dicotyledons of subclass Magnoliidae, Extended Abstract of Doctoral (Biol.) Dissertation, St. Petersburg: Botan. Inst., 1997.
Gabarayeva, N.I., Principles and recurrent themes in sporoderm development, in Pollen and Spores: Morphology and Biology, Harley, M.M., Morton, C.M., and Blackmore, S., Eds., Kent, Whitstable: Whitstable Printers Ltd., 2000, pp. 1–17.
Gabarayeva, N.I., The theoretical prerequisites of declinations in pollen wall development, in Pyl’tsa kak indikator sostoyaniya okruzhayushchei sredy i paleoekologicheskie rekonstruktsii. Trudy mezhdunarodnogo seminara (Pollen as Indicator of the Condition of the Environment and Palaeoecological Reconstructions. Proceedings of the International Seminar), Dzyuba, O., Ed., St. Petersburg, 2001, pp. 49–61.
Gabarayeva, N.I. and El-Ghazaly, G., Sporoderm development in Nymphaea mexicana (Nymphaeaceae), Plant Syst. Evol., 1997, vol. 20, pp. 1–19.
Gabarayeva, N.I. and Grigorjeva, V.V., Exine development in Stangeria eriopus (Stangeriaceae): ultrastructure and substructure, sporopollenin accumulation, the equivocal character of the aperture, and stereology of microspore organelles, Rev. Palaeobot. Palynol., 2002, vol. 122, pp. 185–218.
Gabarayeva, N.I. and Grigorjeva, V.V., Comparative study of the pollen wall development in Illicium floridanum (Illiciaceae) and Schisandra chinensis (Schisandraceae), Taiwania, 2003, vol. 48, pp. 147–167.
Gabarayeva, N.I. and Grigorjeva, V.V., Exine development in Encephalartos altensteinii (Cycadaceae): ultrastructure, substructure and the modes of sporopollenin accumulation, Rev. Palaeobot. Palynol., 2004, vol. 132, pp. 175–193.
Gabarayeva, N.I. and Grigorjeva, V.V., Sporoderm ontogeny in Chamaedorea microspadix (Arecaceae): self-assembly as the underlying cause of development, Grana, 2010, vol. 49, pp. 91–114.
Gabarayeva, N. and Grigorjeva, V., Sporoderm development and substructure in Magnolia sieboldii and other Magnoliaceae: an interpretation, Grana, 2012, vol. 51, pp. 119–147.
Gabarayeva, N. and Grigorjeva, V., Experimental modelling of exine-like structures, Grana, 2013, vol. 52, pp. 241–257. doi: 10.1080/00173134.2013.818165.
Gabarayeva, N.I. and Hemsley, A.R., Merging concepts: the role of self-assembly in the development of pollen wall structure, Rev. Palaeobot. Palynol., 2006, vol. 138, pp. 121–139.
Gabarayeva, N.I. and Hemsley, A.R., The formation of pattern in microcosm: role of self-assembly in development of complex walls of biological subjects, Zh. Obshch. Biol., 2010, vol. 71, no. 4, pp. 310–336.
Gabarayeva, N.I. and Rowley, J.R., Exine development in Nymphaea colorata (Nymphaeaceae), Nordic. J. Bot., 1994, vol. 14, pp. 671–691.
Gabarayeva, N.I., Rowley, J.R., and Skvarla, J.J., Exine development in Borago (Boraginaceae). 1. Microspore tetrad period, Taiwania, 1998, vol. 43, no. 3, pp. 203–214.
Gabarayeva, N.I., Blackmore, S., and Rowley, J.R., Observations on the experimental destruction and substructural organisation of the pollen wall of some selected gymnosperms and angiosperms, Rev. Palaeobot. Palynol., 2003a, vol. 124, pp. 203–226.
Gabarayeva, N.I., Grigorjeva, V.V., and Rowley, J.R., Sporoderm ontogeny in Cabomba aquatica (Cabombaceae), Rev. Palaeobot. Palynol., 2003b, vol. 127, pp. 147–173.
Gabarayeva, N., Grigorjeva, V., Rowley, J.R., and Hemsley, A.R., Sporoderm development in Trevesia burckii (Araliaceae). I. Tetrad period: further evidence for participating of self-assembly processes, Rev. Palaeobot. Palynol., 2009a, vol. 156, pp. 211–232.
Gabarayeva, N.I., Grigorjeva, V.V., Rowley, J.R., and Hemsley, A.R., Sporoderm development in Trevesia burckii (Araliaceae). II. Post-tetrad period: further evidence for the participation of self-assembly processes, Rev. Paleobot. Palynol., 2009b, vol. 156, nos. 1–2, pp. 233–247.
Gabarayeva, N.I., Grigorjeva, V.V., and Rowley, J.R., Sporoderm ontogeny and tapetum input in Persea americana. The micellar seamy side of the development, Ann. Bot., 2010, vol. 105, pp. 939–955.
Gabarayeva, N.I., Grigorjeva, V.V., and Marquez, G., 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, 2011a, vol. 50, no. 4, pp. 235–262.
Gabarayeva, N.I., Grigorjeva, V.V., and Polevova, S.V., Exine and tapetum development in Symphytum officinale (Boraginaceae): exine substructure and its interpretation, Plant Syst. Evol., 2011b, vol. 296, pp. 101–120.
Gabarayeva, N., Grigorjeva, V., and Kosenko, Y., I. Primexine development in Passiflora racemosa Brot. Overlooked aspects of development, Plant Syst. Evol., 2013a, vol. 299, pp. 1013–1035.
Gabarayeva, N., Grigorjeva, V., and Kosenko, Y., II. Exine development in Passiflora racemosa Brot.: post-tetrad period. Overlooked aspects of development, Plant Syst. Evol., 2013b, vol. 299, pp. 1037–1055.
Gabarayeva, N.I., Grigorjeva, V.V., and Polevova, S.V., Sporoderm and tapetum ontogeny in Juniperus communis (Cupressaceae). Connective structures between tapetum and microspores, Rev. Palaeobot. Palynol. (in press).
Gerasimova-Navashina, E.N., Physicochemical nature of the primexine formation in pollen grains of Angiosperms, in Embriologiya pokrytosemennykh (Embryology of Angiosperms), Chisinau: Shtiintsa, 1973, pp. 57–70.
Griffiths, P.C. and Hemsley, A.R., Raspberries and muffins-mimicking biological pattern formation, Colloids Surf., B, 2001, vol. 25, pp. 163–170.
Grigorjeva, V.V. and Gabarayeva, N.I., Dynamics of cell components of the developing microspores in the course of exine formation in Stangeria eriopus (Stangeriaceae): stereological study, Bot. Zh., 1998, vol. 83, no. 12, pp. 1–11.
Hemsley, A.R., Non-linear variation in simulated complex pattern development, J. Theor. Biol., 1998, vol. 192, pp. 73–79.
Hemsley, A.R. and Gabarayeva, N.I., Exine development: the importance of looking through a colloid chemistry “window”, Plant Syst. Evol., 2007, vol. 263, pp. 25–49.
Hemsley, A.R. and Griffiths, P.C., Architecture in the microcosm: biocolloids, self-assembly and pattern formation, Phil. Trans. R. Soc. Lond. A, 2000, vol. 358, pp. 547–564.
Hemsley, A.R., Collinson, M.E., and Brain, A.P.R., Colloidal crystal-like structure of sporopollenin in the megaspore walls of recent Selaginella and similar fossil spores, Bot. J. Linn. Soc., 1992, vol. 108, pp. 307–320.
Hemsley, A.R., Jenkins, P.D., Collinson, M.E., and Vincent, B., Experimental modelling of exine self-assembly, Bot. J. Linn. Soc., 1996, vol. 121, pp. 177–187.
Hemsley, A.R., Vincent, B., Collinson, M.E., and Griffiths, P.C., Simulated self-assembly of spore exines, Ann. Bot., 1998, vol. 82, pp. 105–109.
Hemsley, A.R., Collinson, M.E., Vincent, B., et al., Selfassembly of colloidal units in exine development, in Pollen and Spores: Morphology and Biology, Royal Bot. Kew Gardens: Kew Gardens Press, 2000, pp. 31–44.
Hemsley, A.R., Griffiths, P.C., Mathias, R., and Moore, S.E.M., A model for the role of surfactants in the assembly of exine sculpture, Grana, 2003, vol. 42, pp. 38–42.
Heslop-Harrison, J., An ultrastructural study of pollen wall ontogeny in Silene pendula, Grana Palynologica, 1963, vol. 4, pp. 7–24.
Heslop-Harrison, J., The emergence of pattern in the cell walls of higher plants, Devel. Biol., 1968a, suppl. 2, pp. 118–150.
Heslop-Harrison, J., Pollen wall development, Science, 1968b, vol. 161, pp. 230–237.
Heslop-Harrison, J. and Dickinson, H.G., A common mode of deposition for the sporopollenin of sexine and nexine, Nature, 1968, vol. 220, pp. 926–927.
Heslop-Harrison, J. and Dickinson, H.G., Time relationships of sporopollenin synthesis associated with tapetum and microspores in Lilium, Planta, 1969, vol. 84, pp. 199–214.
Heslop-Harrison, J., Pattern in plant cell walls: morphogenesis in miniature, Proc. Royal Inst. Great Britain, 1972, vol. 45, pp. 335–351.
Hesse, M., An exine architecture model for viscin threads, Grana, 1984, vol. 23, pp. 69–75.
Meyer, N.R. The development of pollen walls in angiosperms, in Morfologiya tsvetkovykh rastenii (Morphology of Flowering Plants), Moscow: Nauka, 1971.
Meyer, N.R., Comparative-morphological studies of the development and ultrastructure of sporoderm in Gymnosperms and Angiosperms, Extended Abstract of Doctoral (Biol.) Dissertation, Leningrad: Botan. Inst., 1977.
Meyer, N.R. and Bernard, V.V., On the development of the pine-tree pollen wall, Vestn. Mosk. Univ., 1970, no. 5, pp. 49–53.
Meyer, N.R. and Bernard, V.V., Electron microscopy investigation of the formation of pollen grains in Pinus sylvestris L., Juniperus communis L. and Larix sibirica Ledeb. formation, in Morfologiya pyl’tsy i spor sovremennykh rastenii (Pollen and Spore Morphology of Living Plants), Leningrad: Nauka, 1973, pp. 21–24.
Meyer, N.R. and Yaroshevskaja, A.S., The phylogenetic significance of the development of pollen grain walls in Liliaceae, Juncaceae and Cyperaceae, in The Evolutionary Significance of the Exine, Ferguson, I.K. and Muller, J., Eds., London: Academic Press, 1976, pp. 91–100.
Meyer-Melikyan, N.R., Gabarayeva, N.I., Polevova, S.V., Grigorjeva, V.V., Kosenko, Ya.V., and Tekleva, M.V., The development of pollen walls and sporopollenin accumulation, Russ. J. Plant Physiol., 2003, vol. 50, no. 3, pp. 373–381.
Moore, S.E.M., Gabarayeva, N., and Hemsley, A.R., Morphological, developmental and ultrastructural comparison of Osmunda regalis L. spores with spore mimics, Rev. Palaeobot. Palynol., 2009, vol. 156, pp. 177–184.
Nishikawa, S., Zinkl, G.M., Swanson, R.J., et al., Callose (β-1,3 glucan) is essential for Arabidopsis pollen wall patterning, but not tube growth BMC, Plant Biol., 2005, vol. 5, pp. 22–30.
Reznikova, S.A., Microsporogenesis in the culture of isolated anthers of Lilium candidum L., Dokl. Akad. Nauk SSSR, 1972, vol. 203, no. 3, pp. 717–720.
Reznikova, S.A., Regularities of cell differentiation in microsporoand gametogenesis (on example of Lilium candidum L.), Extended Abstract of Doctoral (Biol.) Dissertation, Moscow: Gl. Bot. Sad AN SSSR, 1975.
Reznikova, S.A., Tsitologiya i fiziologiya razvivayushchegosya pyl’nika (Cytology and Physiology of the Developing Anther), Moscow: Nauka, 1984.
Reznikova, S.A. and Dickinson, H.G., Ultrastructural aspects of storage lipid mobilization in the tapetum of Lilium hybrida var. enchantment, Planta, 1982, vol. 155, pp. 400–408.
Reznikova, S.A. and Willemse, M.T.M., Formation of pollen in the anther of Lilium. 2. The function of surrounding tissues in the formation of pollen and pollen wall, Acta Bot. Neerl., 1980, vol. 29, pp. 141–156.
Rowley, J.R., Ubisch body development in Poa annua, Grana Palynologica, 1963, vol. 4, pp. 25–36.
Rowley, J.R., The fundamental structure of the pollen exine, Plant Syst. Evol., 1990, vol. 5(suppl.), pp. 13–29.
Rowley, J.R. and Claugher, D., Receptor-independent sporopollenin, Bot. Acta, 1991, vol. 104, pp. 316–323.
Rowley, J.R. and Flynn, J.J., Tubular fibrils and the ontogeny of the yellow water lily pollen grain, Cell Biol., 1968, vol. 39, p. 159.
Rowley, J.R. and Morbelli, M., Connective structures between tapetal cells and spores in Lycophyta and pollen grains in angiosperms-a review, Rev. Paleobot. Palynol., 2009, vol. 156, pp. 157–164.
Rowley, J.R. and Skvarla, J.J., Exine receptors, Grana, 1993, vol. 2, pp. 21–25.
Rowley, J.R., Flynn, J.J., and Takahashi, M., Atomic force microscope information on pollen substructure in Nyphar, Bot. Acta, 1995, vol. 108, pp. 300–308.
Rowley, J.R., Skvarla, J.J., and Gabarayeva, N.I., Exine development in Borago (Boraginaceae). 2. Free microspore stages, Taiwania, 1999, vol. 44, pp. 212–229.
Rowley, J.R., Gabarayeva, N.I., Skvarla, J.J., and El-Ghazaly, G., The effect of 4-methylmorpholine N-oxide monohydrate (MMNO.H2O) on pollen and spore exines, Taiwania, 2001, vol. 46, pp. 246–273.
Sheldon, J.M. and Dickinson, H.G., Determination of patterning in the pollen wall of Lilium henryi, J. Cell Sci., 1983, vol. 63, pp. 191–208.
Southworth, D. and Jernstedt, J.A., Pollen exine development precedes microtubule rearrangement in Vigna unguiculata (Fabaceae): a model for pollen wall patterning, Protoplasma, 1995, vol. 187, pp. 79–87.
Surova, T.D., The development of spores in fern Anemia phyllitidis (Schizaeaceae). Membrane contacts in the process of exine formation, Bot. Zh., 1981, vol. 66, no. 3, pp. 372–379.
Surova, T.D., Spore morphology and development of the representatives of the family Schizaeaceae Kaulf., Extended Abstract of Cand. Sci. (Biol.) Dissertation, Leningrad, 1985.
Suzuki, T., Masaoka, K., Nishi, M., Nakamura, K., and Ishiguro, S., Identification of Kaonashi mutants showing abnormal pollen exine structure in Arabidopsis thaliana, Plant Cell Physiol., 2008, vol. 49, pp. 1465–1477.
Van Uffelen, G.A., The control of spore wall formation, in Pollen and Spores: Patterns of Diversification, Oxford: Clarendon Press, 1991, pp. 89–102.
Wellman, C.H., Origin, function and development of the spore wall in early land plants, in The Evolution of Plant Physiology, Hemsley A.R. and Poole, I., Eds., Kew: Royal Botanic Gardens, 2004, pp. 43–63.
Willemse, M.T.M. and Reznikova, S.A., Formation of pollen in the anther of Lilium. Development of the pollen wall, Acta Bot. Neerl., 1980, vol. 29, nos. 2–3, pp. 127–140.
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Published in Russian in Ontogenez, 2014, Vol. 45, No. 4, pp. 219–239.
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Gabarayeva, N.I. Role of genetic control and self-assembly in gametophyte sporoderm ontogeny: Hypotheses and experiment. Russ J Dev Biol 45, 177–195 (2014). https://doi.org/10.1134/S1062360414040031
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DOI: https://doi.org/10.1134/S1062360414040031