Structural and developmental variability in the female gametophyte of Griffithella hookeriana, Polypleurum stylosum, and Zeylanidium lichenoides and its bearing on the occurrence of single fertilization in Podostemaceae

Abstract

Angiosperms are characterized by the phenomenon of double fertilization with Podostemaceae as an exception that appears to extend to the entire family. Our earlier work demonstrated the cause of failure of double fertilization and ascertained the occurrence of single fertilization in Dalzellia zeylanica (Tristichoideae, Podostemaceae). In continuation with this work, three more members, i.e., Griffithella hookeriana (Tul.) Warming, Polypleurum stylosum (Wight) Hall, and Zeylanidium lichenoides (Kurz) Engl. (Podostemoideae), have been investigated in the present work. We studied the ontogenetic development of female gametophyte and tracked the path of the two sperm cells from the time of their formation in the pollen tube through their entry into the synergid and gamete fusion. We report the occurrence of a remarkably reduced 3-nucleate, 3-celled mature female gametophyte consisting of an egg cell and two synergids in all the three genera. Interestingly, the central cell is formed during female gametophyte development, but exhibits a species-specific, limited life span, and eventually degenerates prior to the entry of the pollen tube into the synergid, resulting in a failure of double fertilization. Sperm dimorphism on the basis of fluorochrome stainability has been recorded in Z. lichenoides. Further, morphogenetic constraints on the part of male (sperm selection, functional reductionism) and female gametophyte (structural reductionism, inaccessibility of central cell) presumably ensure the failure of double fertilization in these species. Thus, loss of double fertilization in this family is likely a derived condition.

Fertilization Mechanisms in Flowering Plants

“…Cell fusion (plasmogamy) then occurs, but only after successful sperm cell positioning, adhesion, and activation. With the exception of the Podostemaceae (Riverweed) family and some orchids where single fertilization occurs between the egg and a sperm (the second sperm cell is either not formed or disintegrates [15, 16]), in all other investigated angiosperm families one sperm cell fuses with the haploid egg cell generating the diploid embryo, while the second sperm cell fuses with the homo-diploid central cell forming the triploid endosperm [9]. Tremendous progress has been made during the past five years to understand the molecular mechanisms of fertilization in plants including the fusion of gamete nuclei (karyogamy) and the prevention of polyspermy (fusion of multiple sperm cells with female gametes) by avoiding the attraction of multiple pollen tubes (polytubey).…”

The reproductive biology of Marathrum rubrum Novelo & C. T. Philbrick: morphological and anatomical changes during flower development

“…Therefore, they have been considered an evolutionary enigma (Jäger-Zürn 1997, Rutishauser 1997, Chaudhary et al 2014, Leleeka et al 2017. Regarding embryology, they are characterized by the formation of a tetracellular and tetranucleate female gametophyte, with the absence of antipodes (Battaglia 1971, Mukkada & Chopra 1973, Arekal & Nagendran 1975, 1977, Jäger-Zürn 1997, Murguía-Sánchez et al 2002, Sikolia & Ochora 2008, Chaudhary et al 2014, Sehgal et al 2014, Sikolia 2015. The absence of double fertilization (Chopra & Mukkada 1966, Battaglia 1971, Mohan Ram & Sehgal 1992, Sikolia & Onyango 2009, Sehgal et al 2011, Chaudhary et al 2014, Sikolia 2015, Khanduri et al 2016, Jiménez-Durán et al 2021 has been documented within the family.…”

Reproduction Multitasking: The Male Gametophyte

“…During double fertilization, two dimorphic female reproductive cells (the egg cell and central cell) within the embryo sac are fertilized by the two sperm cells to produce a diploid zygote and a triploid nutritive endosperm (recently reviewed in 71). Exceptionally, in a few orchid species and Podostemaceae (Malpighiales), only single fertilization occurs between a sperm cell and an egg Plasmogamy: the fusion of the cytoplasm of two gametes bringing together two compatible haploid nuclei Polytubey: the attraction of more than one pollen tube by a single ovule Heterofertilization: the fertilization of two female gametes within an ovule by genetically different sperm cells delivered by two pollen tubes cell to generate a diploid embryo; the second sperm cell is either not formed or it disintegrates (176).…”