Development of cycad ovules and seeds. 2. Histological and ultrastructural aspects of ontogeny of the embryo in Encephalartos natalensis (Zamiaceae)

Abstract

Development of the embryo of Encephalartos natalensis from a rudimentary meristematic structure approximately 700 μm in length extends over 6 months after the seed is shed from the strobilus. Throughout its development, the embryo remains attached to a long suspensor. Differentiation of the shoot meristem flanked by two cotyledonary protuberances occurs over the first 2 months, during which peripheral tannin channels become apparent. Tannins, apparently elaborated by the endoplasmic reticulum, first accumulate in the large central vacuole and ultimately fill the channel. By the fourth month of development, the root meristem is apparent and procambial tissue forming discrete vascular bundles can be discerned in the elongating cotyledons. Between 4 and 6 months, mucilage ducts differentiate; after 6 months, when the seed becomes germinable, the embryo is characterised by cotyledons far longer than the axis. Shoot and root meristem cells remain ultrastructurally similar throughout embryo ontogeny, containing small vacuoles, many well-differentiated mitochondria and endoplasmic reticulum (ER) profiles, abundant polysomes, plastids containing small starch deposits and Golgi bodies. Unusually, however, Golgi bodies are infrequent in other cells including those elaborating mucilage which is accumulated in distended ER and apparently secreted into the duct lumen directly by ER-derived vesicles. The non-meristematic cells accumulate massive starch deposits to the exclusion of any protein bodies and only very sparse lipid, features which are considered in terms of the prolonged period of embryo development and the high atmospheric oxygen content of the Carboniferous Period, when cycads are suggested to have originated.

Cycads in vitro

“…Although a few studies have been conducted, cycad seeds also appear to be recalcitrant (Dehgan and Schutzman 1989, Forsyth and van Staden 1983, Woodenberg et al 2010, i.e. they are 'wet' and desiccation-sensitive, and may succumb to dehydration in the field during the protracted development of the embryo after seed-shed (Woodenberg et al 2014). While rapid germination (2-6 weeks) of Zamia floridana (sensu lato) seeds is possible when the sarcotesta is removed and seeds are soaked in H2SO4 for 1 hr, rinsed, then soaked in 1 g/l GA 3 for 48 hrs (Dehgan and Johnson 1948), C. revoluta seeds lose viability rapidly and have low morphogenic potential or recalcitrance in vitro (Benson 2000).…”

Cytological analysis of ginseng carpel development

“…(Yu and Kim 1992;Venugopal et al 2013;Qi et al 2015), Cytisus striatus and C. multiflorus (Rodríguez-Riaño et al 2006), Hydatellaceae (Rudall et al 2008), Silene latifolia (Koizumi et al 2009), Drosera x obovata (Rodondi et al 2009), Psychotria carthagenensis and Rudgea macrophylla (Figueiredo et al 2013), rice (Oryza sativa) (Kubo et al 2013;Wu et al 2016a, b), Taraxacum Wigg. (Musiał et al 2013), Gaussia attenuata (Castaño et al 2014), Coffea arabica (de Oliveira et al 2014), and Encephalartos natalensis (Woodenberg et al 2014). These studies clearly illustrate that as a vital sexual reproductive organ, the ovule is involved in many complex systematic interactions during flower development.…”

“…This distribution pattern of the vascular bundles differs from those reported in other higher plants. For instance, they appear in an heterocarpellary position in Seemannaralia gerrardii , form an external circle in E. natalensis (Woodenberg et al 2014), form an external and a central complex in Gaussia attetuata (Castaño et al 2014), and form an arc in Vochysiaceae (Litt and Stevenson 2003). Anatomical studies of floral vasculature support the idea that in receptacular epigynous flowers, the vascular bundles provide traces to the floral appendages that run upward through the length of the ovary wall and then descend to supply nutrition to the ovule (Douglas 1957;Kaplan 1967;Costello and Motley 2004).…”

Chicken or egg—Weismann revisited

“…However, cell differentiation in organisms with open morphogenesis, where the developmental fate of individual cells is not predetermined by cell lineage, might follow different strategies. Three contributions in the current issue follow spatial organisation before and during the earliest stages of embryogenesis-in the fly Calliphora (Anan'ina et al 2014), in the moscito Acricotopus (Staiber 2014) and in the primitive gymnosperm Encephalartos (Woodenberg et al 2014)-and it is interesting to read these contributions in a context:…”

“…This situation changed with the transition to the seed plants, and it is, therefore, interesting to investigate embryogenesis in primitive seed plants. The work by Woodenberg et al (2014) in the current issue deals with the development of the ovule in the living fossile Encephalartos natalensis, a primitive gymnosperm representing an evolutionary stage prevalent around 200 Mya. Here, the zygotic nucleus undergoes numerous free divisions (similar to the situation in Drosophila), and these accumulate in the basal region of the proembryo (the free nuclei near the apex degenerate).…”