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Description of a Novel Organ in the Gametophyte of the Fern Schizaea Pusilla and Its Contribution to Overall Plant Architecture

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Description of a Novel Organ in the Gametophyte of the Fern Schizaea Pusilla and Its Contribution to Overall Plant Architecture 1217 NOTE / NOTE Description of a novel organ in the gametophyte of the fern Schizaea pusilla and its contribution to overall plant architecture Carla Davidson, Przemyslaw Prusinkiewicz, and Patrick von Aderkas Abstract: Plant architecture is determined by cell division and growth, thus simulation models describing these processes are ideal for determining how local development produces the overall plant form. Because fern gametophytes are structur- ally simple, they are ideal for investigating the effects of cellular growth and division on plant form. In this work we ex- amine the gametophytic development of Schizaea pusilla Pursh., a small, bog-adapted fern whose gametophyte forms as a mass of single-celled filaments. Using light and scanning electron microscopy we made detailed observations of gameto- phyte development to generate data for a simulation mechanical model of S. pusilla gametophyte development. To exam- ine how plant architecture is an emergent property of cell division, we constructed a simulation model expressed using the formalism of L-systems. While developing a model of growth in this fern we discovered a previously undescribed structure that contributes to the architecture of this plant, which we term knots. We document the development of knots and demon- strate how they contribute to the overall plant architecture. Key words: Schizaea pusilla, fern, gametophyte, simulation model, L-system. Re´sume´ : La division cellulaire et la croissance de´terminent l’architecture des plantes, de sorte que les mode`les de simula- tion de´crivant ces processus sont tre`s utiles pour de´terminer comment le de´veloppement local ge´ne`re la forme ge´ne´rale de la plante. Compte tenu de leur structure simple, les game´tophytes des fouge`res permettent d’e´tudier facilement les effets de la croissance cellulaire et de la division sur la forme de la plante. Les auteurs ont examine´ le de´veloppement du game´- tophyte du Schizaea pusilla Purs., une petite fouge`re adapte´e aux tourbie`res dont le game´tophyte est constitue´ d’une masse de filaments unicellulaires. A` l’aide de la microscopie photonique et e´lectronique par balayage, les auteurs ont conduit des observations de´taille´es sur le de´veloppement des game´tophytes pour obtenir les donne´es ne´cessaires a` la construction d’un mode`le de simulation me´canique du de´veloppement du game´tophyte du S. pusilla. Afin d’examiner comment l’architecture de la plante provient de la division cellulaire, les auteurs ont construit un mode`le de simulation exprime´ a` l’aide du forma- lisme de syste`mes L. Tout en de´veloppant un mode`le de croissance pour cette fouge`re, les auteurs ont de´couvert une struc- ture jamais de´crite qui contribue a` l’architecture de cette plante et qu’ils nomment nœuds. Ils de´crivent le de´veloppement des nœuds et montrent comment ils contribuent a` l’architecture ge´ne´rale de la plante. Mots-cle´s : Schizaea pusilla, fouge`re, game´tophyte, mode`le de simulation, syste`me L. Introduction Plant architecture is a result of cell division and growth, Received 1 May 2008. Published on the NRC Research Press thus one can use cellular-level models of plant development Web site at botany.nrc.ca on 3 October 2008. to explore the effects of local development on global form 1,2 (de Boer 1990; de Boer and de Does 1990; Prusinkiewicz et C. Davidson. Department of Biochemistry and Molecular al. 1994; Holloway and Lantin 2002; Ruiz-Ramos and Biology, University of Calgary, 3330 Hospital Drive NW, Calgary, AB T2N 4N1, Canada. Minguez 2006) In theory, a model could reproduce the P. Prusinkiewicz. Department of Computer Science, University growth of an entire plant if the rules governing cell division of Calgary, 2500 University Drive NW, Calgary, AB T2N 1N4, at the local scale were understood. However, although suc- Canada. cessful developmental models of meristematic organization P. von Aderkas. Department of Biology, University of Victoria, and phyllotaxis have been proposed (Jo¨nsson et al. 2006; P.O. Box 3020, Station CSC, Victoria, BC V8W 3N5, Canada. Smith et al. 2006), the modeling of even the simplest mature 1Corresponding author (e-mail: [email protected]). angiosperms is at present computationally intractable owing 2Present address: Department of Microbiology and Molecular to prohibitively large numbers of cells. Genetics, Michigan State University, 2209 Biomedical and Fern cells express similar biochemical and regulatory mo- Physical Sciences, East Lansing, MI 48824-4320, USA. tifs as angiosperms (Banks 1999; Holloway and Lantin Botany 86: 1217–1223 (2008) doi:10.1139/B08-085 # 2008 NRC Canada 1218 Botany Vol. 86, 2008 2002), but gametophyte development is much simpler. Fur- a starting point for modeling, spores collected in New Jersey thermore, cellular structures that are difficult to observe in in 1994 and 1995 (donated by Dr. J. Kiss, Miami University) angiosperms, such as plasmodesmata, and mechanisms of in- were sterilized and germinated on Knudson’s medium, as tracellular communication, such as the establishment of api- described by von Aderkas and Raghavan (von Aderkas and cal dominance, may be more readily observed in fern Raghavan 1985). Stock cultures of gametophytes were main- gametophytes than angiosperms (Holloway and Lantin tained on Knudson’s medium at 23 8Cat35mmolÁm–2Ás–1 2002). For example, a physiological model of intercellular PAR with a 16 h (light) – 8 h (dark) photoperiod. signaling via plasmodesmata in Onoclea sensibilis proved sufficient to explain maintenance of apical dominance and Microscopy response to removal of the apical region in this fern (Hol- All observations of cell division and organ development loway and Lantin 2002). These results indicate that cellular were made with a Zeiss Axioplan compound light photomi- processes in fern gametophytes can easily be modeled and croscope. Cell division events were classified as either sub- are informative for both fern and angiosperm development. apical, diagonal leading to a branch, or longitudinal. Light Within the largely tropical primitive family of ferns Schi- photographs, as well as DAPI stained fluorescent photo- zaeaceae, Schizaea pusilla Pursh. is the only member with a graphs, of various stages of gametophyte development and distribution from central America to northeastern Canada of organs such as rhizoidophores, antheridia and knots, (Bartoo 1930; Atkinson 1965; Stolze 1987; Cody and were taken with Fuji 64T film. Gametophytes were micro- Britton 1989; Goltz and Hinds 1993). It grows in bogs, an waved for 20 s at medium power with acetocarmine and di- environment that is nutrient stressed. Within the genus, ga- lute chloral hydrate to partially clear cell contents and stain metophyte morphology, which varies from filamentous to nuclei. They were then incubated for 30 min with phos- tuberous, is used to define different subgroups; conse- phate-buffered saline and 10 mgÁmL–1 DAPI (4’,6-diami- quently, pattern development in gametophytes has taxo- dino-2-phenylindole). Gametophyte filaments were also nomic significance (Bower 1926; Bierhorst 1967, 1971a, processed for scanning electron microscopy. Samples were 1975; Wikstrom et al. 2002). The gametophyte of the fern fixed overnight in 2.5% glutaraldehyde with 0.05 molÁL–1 S. pusilla grows as a clump of single-celled filaments, which phosphate buffer, then post-fixed for 1 h in 1% osmium tetr- may give rise to small multicellular organs. These include oxide in 0.05 molÁL–1 phosphate buffer. The samples were the male and female reproductive organs, antheridia and ar- rinsed three times in phosphate buffer for 15 min, then de- chegonia, and a large structure that houses a fungal sym- hydrated with a graded ethanol series (30%–100%). Half of biont, called a rhizoidophore (Britton and Taylor 1901). The these samples were critical-point dried (Bomar SPC 1500, rhizoidophores serve as the point of entry of mycorrhizal Bomar Co., Tacoma Wash.) and the other half were dried fungi, which improve the fern’s ability to take up nutrients in hexamethyldisilazane before being mounted on stubs (Crotty 1967; Swatzell et al. 1996). While investigating the with double-sided tape and gold coated (Edwards Sputter growth of the gametophyte, we discovered clusters of cells Coater S150B, Edwards, Mississauga, Ont.). Scanning elec- from which growth would radiate in many directions. These tron microscopy was carried out at 15 MHz (Hitachi S- structures arise periodically and were found to be integral to 3500N, Hitachi, Pleasanton, Calif.). the growth of the plant; we have chosen to call them knots. Observations of light treated gametophytes were taken These structures are not recorded in the literature on this with a Leitz dissecting photomicroscope and Fuji 64T film. fern in any publications known to the authors. A useful framework for modeling plant development in Observation of knots space and time is the formalism L-systems (Lindenmayer Filaments from 10 stock gametophytes established on 1968, 1975; Prusinkiewicz and Lindenmayer 1990), which Knudson’s medium were randomly selected for analysis. describes the growth of branching structures as a function of Measurements included branching angles, frequency of dif- processes taking place in individual modules, for example, ferent types of cell division, and organ frequency and posi- cells or organs. Thus spatial relationships are not described tion. From these measurements we estimated the distribution by reference to a global coordinate system, but instead (mean and standard deviation) of branching angles and fre- emerge from interactions between cells at a local scale quency of knot formation. To investigate the role of stress (Coen et al. 2004). L-system models are inherently dynamic: on knot formation, 50 apical cells were isolated by crushing with the correct productions one can start from a single cell proximal cells with Dumont No. 5 forceps, and observed un- and simulate the development of an entire branching organ- til approximately the 10-cell stage, when survival and fre- ism.
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