Double Fertilization in Gnetum gnemon: The Relationship between the Cell Cycle and Sexual Reproduction.

Abstract

Gnetum gnemon, a nonflowering seed plant and member of the Gnetales, expresses a rudimentary pattern of double fertilization that results in the formation of two zygotes per pollen tube. The process of double fertilization in G. gnemon was examined with light and fluorescence micmscopy, and the DNA content of various nuclei involved in sexual reproduction was quantified with 4',6-diamidino9-phenylindole microspectrofluommetry. Male and female gamete nuclei pass through the synthesis phase of the cell cycle and increase their DNA content from 1C to 2C before fertilization. Each of the two zygotes found in association with a pollen tube is diploid and contains the 4C quantity of DNA at inception. Based on these results as well as previous studies of nuclear DNA content in plant sperm, eggs, and zygotes, three fundamental and distinct patterns of gamete karyogamy among seed plants can be circumscribed: (1) G1 karyogamy, in which male and female gametes contain the 1C quantity of DNA throughout karyogamy and the zygote undergoes DNA replication; (2) S-phase karyogamy, in which gamete nuclei initiate fusion at 1C but pass through the S phase of the cell cycle before completely fusing; and (3) G2 karyogamy, in which male and female gamete nuclei pass through the S phase of the cell cycle before the onset of fertilization. Our results show definitively a pattern of G2 karyogamy in G. gnemon.

Nuclear Endosperm Development in Cereals and Arabidopsis thaliana

“…Until recently, several lines of evidence suggested that the Gnetales represent the extant seed plants most closely related to angiosperms. Based on this assumption, and the observation that double fertilization results in a diploid supernumerary embryo in Ephedra and Gnetum species, Friedman and co-workers supported the twinembryo hypothesis (Carmichael and Friedman, 1995). However, recent discoveries in angiosperm phylogeny do not support Gnetales as an angiosperm predecessor (for details, see Mathews and Donoghue, 1999;Qiu et al, 1999;Soltis et al, 1999;reviewed by Friedman and Williams, 2003), lending little support to the twin-embryo hypothesis.…”

Arabidopsis GLAUCEpromotes fertilization-independent endosperm development and expression of paternally inherited alleles

“…The second fusion event between a sperm cell nucleus and a ventral canal nucleus has also been observed in the non-flowering seed plant genera Ephedra (Friedman, 1990;Friedman, 1992) and Gnetum (Carmichael and Friedman, 1995), which, together with Welwitchia, are collectively referred to as the Gnetales (Bowe et al, 2000;Chaw et al, 2000). To date, three angiosperm mutants of known molecular identity, DUO1 (Rotman et al, 2005), GCS1 (Mori et al, 2006;von Besser et al, 2006) and NFD1 (Portereiko et al, 2006a), have been reported to disturb both fertilization events, where neither gamete fusion nor embryo and endosperm development are observed.…”

Developmental Evolution of the Sexual Process in Ancient Flowering Plant Lineages

“…Double fertilization processes, defined as two fertilization events in a single female gametophyte by two sperm from a single pollen tube, also occur in nonflowering seed plants, particularly among members of the Gnetales and possibly some conifers (Friedman, 1990(Friedman, , 1992a(Friedman, , 1992bCarmichael and Friedman, 1995). However, the second fertilization event in nonflowering seed plants yields a supernumerary diploid zygote, not an endosperm.…”

“…A diploid ancestral condition is congruent with an embryo homology for endosperm, because (obviously) embryos are diploid. Although double fertilization events in Gnetales may not be evolutionarily related to those of flowering plants, it is certainly notable that the second fertilization product in Ephedra and Gnetum is a diploid embryo (Friedman, 1992a;Carmichael and Friedman, 1995), as appears to be the case in conifers that are reported to have a second fertilization process (Friedman, 1992b). Inclusive fitness theory shows that the loss of individual fitness by an embryo could have been compensated for by overall gains in the inclusive fitness of a sibling embryo that is the beneficiary of the embryo-nourishing behavior of its altruist partner (Friedman, 1995).…”