The Development of Sporoderm, Tapetum and Ubisch Bodies in Dianthus Deltoides (Caryophyllaceae): Self-Assembly in Action

See discussions, stats, and author profiles for this publication at: https://www.researchgate.net/publication/274838849 The development of sporoderm, tapetum and Ubisch bodies in Dianthus deltoides (Caryophyllaceae): Self-assembly in action Article in Review of Palaeobotany and Palynology · August 2015 DOI: 10.1016/j.revpalbo.2015.03.005 CITATIONS READS 10 66 2 authors: Valentina Grigorjeva Nina Gabarayeva Russian Academy of Sciences 33 PUBLICATIONS 533 CITATIONS 67 PUBLICATIONS 1,520 CITATIONS SEE PROFILE SEE PROFILE Some of the authors of this publication are also working on these related projects: Pollen wall development View project Sporoderm development View project All content following this page was uploaded by Nina Gabarayeva on 21 January 2019. The user has requested enhancement of the downloaded file. Review of Palaeobotany and Palynology 219 (2015) 1–27 Contents lists available at ScienceDirect Review of Palaeobotany and Palynology journal homepage: www.elsevier.com/locate/revpalbo The development of sporoderm, tapetum and Ubisch bodies in Dianthus deltoides (Caryophyllaceae): Self-assembly in action Valentina Grigorjeva, Nina Gabarayeva ⁎ Komarov Botanical Institute, Popov st., 2, 197376 St. Petersburg, Russia article info abstract Article history: The purpose of this work was to study in detail with TEM the successive stages of pollen wall and tapetum devel- Received 11 October 2014 opment in Dianthus deltoides and to clarify the mechanisms underlying the developmental processes. At the Received in revised form 6 March 2015 young tetrad stage a thin glycocalyx layer is poorly structured, being a mixture of glycoproteins, secreted by Accepted 20 March 2015 Golgi vesicles through the process of exocytosis. At the middle tetrad stage the plasma membrane acquires a Available online 28 March 2015 deeply invaginated profile as a result of self-assembly cellular tensegrity, and its pinnacles determine the sites Keywords: of the future spines. Then, lipoid sporopollenin (SP) precursors and monomers are added into the periplasmic Sporoderm and Ubisch body development space. The concentrations of all substances in the periplasmic space are under genome control. As a consequence Pattern formation of self-assembly hydrophilic–hydrophobic interactions, “islets” of osmiophilic lipoid substances occur in the gly- Biocolloids cocalyx mixture, first as spherical units, then as plates, with further lateral growth and the appearance of the hex- Self-assembly agonal reticulate pattern of the future tectum. At maturity, the reticulate pattern is not evident. At the late tetrad Micelles stage spines are initiated as outgrowths of the glycocalyx in the form of cone-like liquid-crystal “skeletons”,the latter accumulate SP. Columellae are initiated very late in ontogeny, at the stage when the tetrads separate into monads, on the base of the glycocalyx rod-like units — the cylindrical micelles. The first endexine lamella with a central white line appears at the young free microspore stage on the base of laminate micelles. The second endexine layer is granulate and appears on the base of spherical micelles. Pollen grains are polyporate with aperturate membranes, consisting of lamellate endexine-1 and an underlying dilation – oncus – comprising granulate endexine-2. The pore membranes bear large cupola-like tectal spines. The tapetum secretes a peri-tapetal membrane with Ubisch bodies, first with clusters of globules, then exine-like spines on the top of clusters. These Ubisch bodies mimic the pattern of the exine. The entire sequence of developmental events can be ex- plained as the development of a self-assembling system under initial genomic regulation. © 2015 Elsevier B.V. All rights reserved. 1. Introduction self-assembly processes pick up the initiatives and drive the exine development to completion (Heslop-Harrison, 1972; Gerasimova-Navashina, It was shown by many ontogenetic palynologists that the tetrad pe- 1973; van Uffelen, 1991). To develop this idea, we consider that the gly- riod is a key one in determination of the ectexine pattern (Rowley and cocalyx, a framework of the exine, is a colloidal solution (Gabarayeva, co-authors — see the full list of references in Blackmore and Skvarla, 1990, 1993) and consists of glycoproteins and lipopolysaccharides 2012; Heslop-Harrison, 1968a,b, 1972; Heslop-Harrison and Dickinson, (Pettitt and Jermy, 1974; Pettitt, 1979). In the course of development, 1968; Dickinson, 1976a,b, 1982; Sheldon and Dickinson, 1983; Dickin- this colloidal mixture is replenished with lipoid SP precursors and son and Sheldon, 1984; Hesse, 1985; Blackmore and Barnes, 1987, monomers (phenylpropanoids, especially p-coumaric acid, and fatty 1990; Blackmore and Claugher, 1987; Blackmore, 1990, 1994; acids — Gubatz et al., 1986, 1993; Herminghaus et al., 1988; Wehling Gabarayeva, 1991a, 2000; Hesse, 1995; Kreunen and Osborn, 1999; et al., 1989; Wiermann and Gubatz, 1992; Collinson et al., 1993; van Gabarayeva, 2000; Blackmore et al., 2007, 2010; Vinckier and Smets, Bergen et al., 1995; Wilmesmeier and Wiermann, 1995; Kawase and 2005; Taylor and Osborn, 2006; Taylor et al., 2013; Gabarayeva et al., Takahashi, 1995; Hemsley et al., 1996b; Niester-Nyveld et al., 1997; 2014). It was also suggested that, after initial genomic instructions, Meuter-Gerhards et al., 1999; Wiermann et al., 2001; Van Bergen et al., 2004), together with hydroxylated α-pyrone compounds (recently identified as SP precursors by Grienenberger et al., 2010). We suggested that this system, being a mixture of surface-active substances, enters ⁎ Corresponding author. Tel.: +7 812 346 36 43. into a self-assembling sequential process of micelle formation E-mail address: [email protected] (N. Gabarayeva). (Gabarayeva and Hemsley, 2006; Hemsley and Gabarayeva, 2007). http://dx.doi.org/10.1016/j.revpalbo.2015.03.005 0034-6667/© 2015 Elsevier B.V. All rights reserved. 2 V. Grigorjeva, N. Gabarayeva / Review of Palaeobotany and Palynology 219 (2015) 1–27 These successive main micellar structures (Scheme in the text) are columns of granules, columellae, alveolae, lamellae with central spherical, cylindrical and then layers of cylindrical (hexagonal white lines, etc. — are constructed on the base of the above- mesophase) and laminate micelles (so-called neat mesophase), mentioned micellar structures after SP accumulation on them with the addition of many transitional micelle forms and bicontinual (Gabarayeva and Hemsley, 2006; Gabarayeva, 2014), so that the suc- micellar structures. The main idea of our hypothesis was that all the cessive appearance of these structures in sporoderm ontogeny is a structural elements, observed during exine development — granules, natural continuation. (See Scheme 1.) Scheme 1. Schematic drawing, showing successive main (A–H) and transitive (I–M) micelle mesopases and bicontinual bilabyrinth structures (N–Q), self-assembling in a solution of a surface active substance (SAS) at increasing concentrations (Fig. 1 from: Gabarayeva, 2014, Russian J. Developmental Biology 45: 177–195). A — separate molecules of SAS with hydrophilic head and hydrophobic tail (true solution); B — spherical micelle, forming at a certain critical micelle concentration — CMC, individual for every SAS; C — cylindrical micelle (corresponding to tufts of Rowley); D — the middle (hexagonal) mesophase — layer of tightly packed cylindrical micelles; E — lamellar (neat) mesophase, where bilayers of the middle mesophases are separated from each other by water-filled gaps of several nanometers. If the dispersive medium is aquatic, micelles are called normal (A, B, C, D, E). If the supporting medium changes to lipophilic, normal micelles turn inside out and reverse micelles appear (A, F, G, H, E). Besides the main mesophases, many transitive and bicontinual mesophases exist, some of them are shown here, e.g., columns of spherical micelles (I) are transitive mesophase between spherical and cylindrical micelles; strings (J) are chains of spherical micelles, transitive to filaments; normal and reverse micelles in biological systems are often bent (“lazy” micelles — K); L — worm-like micelles consist of disk-like, compressed spherical micelles; M — columns of disk-like micelles form “columns of coins”; bicontinual disordered (N, at the top) and ordered (N, below) water–oil phase; O — periodical bicontinual surface of Schwarz with 2 equal subvolumes; P — perforated plate is formed by different ways, e.g. as a particular case of 1-layered structure of Schwarz; Q — sponge-like structure, a particular case of disordered surface of Schwarz. (adapted Fig. 3 from: Hemsley and Gabarayeva, 2007, Plant Syst. Evol. 263: 25–49). V. Grigorjeva, N. Gabarayeva / Review of Palaeobotany and Palynology 219 (2015) 1–27 3 No ontogenetic studies have been undertaken on the sporoderm of osmiophilic roundish units are observed on the glycocalyx surface, at Dianthus. Some palynological data were presented in the PalDat data- the border with callose (Plate IV,1,2,arrowheads). These units are base (Halbritter and Svojtka, 2000). To clarify the evolutionary relation- distributed more or less evenly alongside the glycocalyx surface. Some- shipsofthemembersoftheDianthus polylepis complex, molecular and what later these spherical units increase in number, forming a monolay- morphological data were used (Farsietal.,2013). er on all the glycocalyx surface (Plate IV,3,4,arrowheads)and,judging Although such work is laborious and care must be taken to observe from their higher osmiophility, accumulate SP

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