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Central Cell Degeneration Leads to Three-Celled Female Gametophyte in Zeylanidium Lichenoides Engl

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Central Cell Degeneration Leads to Three-Celled Female Gametophyte in Zeylanidium Lichenoides Engl South African Journal of Botany 91 (2014) 99–106 Contents lists available at ScienceDirect South African Journal of Botany journal homepage: www.elsevier.com/locate/sajb Central cell degeneration leads to three-celled female gametophyte in Zeylanidium lichenoides Engl. (Podostemaceae) A. Chaudhary a, P. Khanduri a,R.Tandona,⁎, P.L. Uniyal a, H.Y. Mohan Ram b a Department of Botany, University of Delhi, Delhi 110007, India b Shriram Institute for Industrial Research, 19 University Road, Delhi 110007, India article info abstract Article history: The absence of double fertilization and lack of endosperm formation are key embryological features of Received 13 June 2013 Podostemaceae, which is unique among the angiosperms. Double fertilization fails in spite of the fact that Received in revised form 8 January 2014 two male gametes are carried in the pollen tube and the incipient embryo sac is equipped with an egg Accepted 8 January 2014 cellandacentralcell.Littleisknownabouttheproximatecausesofthefailureofdoublefertilization.The Available online 27 January 2014 female gametophyte of Zeylanidium lichenoides, (subfamily — Podostemoideae) has a monosporic mode Edited by GV Goodman-Cron of development resulting in an initial four-celled/four-nucleate condition. However, the central cell degen- erates before the arrival of the pollen tube in the vicinity of micropyle, thus the mature and functional Keywords: female gametophyte of Z. lichenoides is ontogenically a three-celled/three-nucleate structure. It is inferred Female gametophyte that the formation of a highly reduced female gametophyte, presumably is a result of degeneration of the Podostemaceae central cell. Podostemads © 2014 SAAB. Published by Elsevier B.V. All rights reserved. Single fertilization Three-celled/three-nucleate embryo sac 1. Introduction rocks or boulders. The plant body of podostemads is thalloid. The conventional demarcation into root, shoot and leaf, is lacking, leading Double fertilization leading to endosperm formation is believed to to a ‘fuzzy morphology’ (Cook and Rutishauser, 2007; Mohan Ram be a universal feature and a key developmental innovation in the diver- and Sehgal, 2007). The occurrence of high developmental plasticity sification of angiosperms (Williams and Friedman, 2004). Molecular and perplexing polymorphism has made taxonomic delimitation of cross-talk between the endosperm and the embryo at various stages Podostemaceae a daunting task. Position of the family in the phylogeny of development is considered crucial in forming a successful sporophyt- of angiosperms was also unresolved, till recently it was placed at differ- ic phase in the sexually reproducing flowering plants (Ungru et al., ent positions in the phylogeny of angiosperms. Ruhfel et al. (2011) 2008; Nowack et al., 2010). Yet some plants successfully defy the defin- provide evidences that Podostemaceae belong to Clusioid clade of the ing second fusion of double fertilization. Among these, all the species order Malpighiales with Bonnetiaceae, Calophyllaceae, Clusiaceae and of Podostemaceae invariably lack double fertilization despite the forma- Hypericaceae as its sister families. tion of two male gametes and differentiation of an egg cell and a central Podostemaceae has been cited as an embryological family (Kapil, cell in the female gametophyte (Sehgal et al., 2011). 1970). Besides the absence of double fertilization, occurrence of a With 50 genera and 280 species, Podostemaceae represent the larg- four-celled/four-nucleate embryo sac, absence of antipodals, presence est natural assemblage of fresh water flowering plants with several of a pseudo-embryo sac (Nucellar plasmodium) and lack of plumule unusual vegetative and reproductive features (Cook and Rutishauser, and radicle in the mature embryo are believed to be among the other 2007; Mohan Ram and Sehgal, 2007). The family is pan-tropical in defining embryological features of the family (Kapil, 1970; Mohan occurrence, found in Africa, Asia, Australia and the Americas. Africa Ram and Sehgal, 2007). (including Madagascar) has 16 genera and ca. 77 species (Engler, Absence of double fertilization in an angiospermic family is an in- 1930; Cusset, 1987), 21 genera (ca. 135 species) are documented triguing feature, since the presence of double fertilization has historical- from the Americas (Tippery et al., 2011) and 18 genera (ca. 84 spp.) ly defined reproduction in the angiosperms. The absence of double occur in Asia and Australia (Cusset and Cusset, 1988; Cusset, 1992). fertilization in Podostemaceae was attributed to the inability of the sec- All taxa of this family begin their life in flowing water attached to ond male gamete to unite with the central cell (Mukkada and Chopra, 1973). However, a recent report in Dalzellia zeylanica Wight (subfamily ⁎ Corresponding author. Tel.: +91 9810760111. Tristichoideae), has shown that early degeneration of central cell just E-mail address: [email protected] (R. Tandon). before the release of the male gametes is the cause of this condition in 0254-6299/$ – see front matter © 2014 SAAB. Published by Elsevier B.V. All rights reserved. http://dx.doi.org/10.1016/j.sajb.2014.01.004 100 A. Chaudhary et al. / South African Journal of Botany 91 (2014) 99–106 D. zeylanica (Sehgal et al., 2011). Whether or not the degeneration of the Podostemoideae. Zeylanidium (Tul.) Engl., with its four species central cell is a prerequisite condition in the other taxa of this family has viz. Zeylanidium olivaceum (Gardn.) Engl., Zeylanidium johnsonii not been clearly established. (Wight) Engl., Z. lichenoides Engl., Zeylanidium maheshwarii Mathew The occurrence of a single fertilization has been documented in and Satheesh, is confined to peninsular India, the southern Indian sub- Spiranthes sinensis (Pers.) Ames. (Orchidaceae) and some natural hy- continent and Myanmar (Mathew and Satheesh, 1997). The earlier brids of maize (Terasaka et al., 1979; Kato, 1997, 1999). However, all embryological investigations in Z. olivaceum and Z. johnsonii have these three instances are distinct. S. sinensis represents an abnormality shown that the two species exhibit a four-celled/four-nucleate condi- of microgametogenesis as only one male gamete is formed due to the tion of embryo sac corresponding to the Apinagia (monosporic) and failure of the generative cell division (Terasaka et al., 1979). In maize Polypleurum (bisporic) type of embryo sac development, respectively hybrids single fertilization is a rare case (Kato, 1997, 1999). There is a (Arekal and Nagendran, 1977). We report that the female gametophyte rare example of Commiphora wightii (Arn.) Bhandari in which the egg development in Z. lichenoides is monosporic, Apinagia ‘b’ type and apparatus and the antipodal cells degenerate and the two polar nuclei its mature female gametophyte is similar to that described for fuse to form an autonomous diploid endosperm (Gupta et al., 1996). D. zeylanica. We also demonstrate that syngamy is the only fertiliza- The present work is the first report on the development of female tion event, as the central cell degenerates before the arrival of the gametophyte in Zeylanidium lichenoides Engl., of the subfamily pollen tube in the vicinity of the micropyle. Fig. 1. (A) Site of collection of plant material; (B) Habitat showing a patch of Zeylanidium lichenoides growing attached to partly submerged rocks; (C–H) Stages of flower bud (bd) to fruit development; (C) Flower bud (bd) (Stage I), (bract br; spathella, sp); (D) Flower at anthesis (Stage II); (E) Anthers (an) in contact with an interlocking bifid stigma (st) effecting self- pollination (Stage III) (ovary, ov); (F) The anthers (an) have shed all pollen and the andropodium (ap) has moved away from the interlocking stage (Stage IV); (G) The andropodium (ap) has elongated 2–3 times and the pedicel (pd) ~3–4 times andtheandropodium (ap) is far above the stigma (st) (Stage V); (H) A fully developed fruit (capsule) (Stage VI), bar = 0.5 mm. A. Chaudhary et al. / South African Journal of Botany 91 (2014) 99–106 101 2. Material and methods axile placenta. Ovules are anatropous, bitegmic and tenuinucellate (Fig. 2A). The two integuments of the ovule arise from the base of the The study material (Z. lichenoides) was collected in December nucellus; the outer integument arises first and contributes to the forma- 2009–2010 from a tributary of Periyar river near Campanywadi tion of the micropyle. The inner integument is shorter and is restricted (10°45′N and 77°9′S) in Idukki district, Kerala state in Southern India to the base of embryo sac. (Fig. 1A). In this season, the plant is available at various stages of repro- Although flowering is initiated under water, anthesis and pollination duction, spanning from initiation of floral primordia to completely invariably occurred above water. As the flowers are naked, the timing of mature but undehisced fruits (capsules). A patch of about 200 plants rupture of the spathella was considered as the time of anthesis (Fig. 1D, was selected to observe anther dehiscence, transfer of pollen grains Table 1). Pollination occurs soon after anthesis (Fig. 1F, Table 1); the and their deposition on the stigmas. stigmatic lobes become stretched and the anthers that lie entangled be- Flowers at several stages of development were fixed in Karnovsky's tween the stigmatic lobes, release the pollen grains thereby facilitating fixative (8% paraformaldehyde + 12% glutaraldehyde in 0.2 M sodium self-pollination (Fig. 1E) (Autopollination). After pollination, there is a cacodylate
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