Green love talks; cell-cell communication during double fertilization in flowering plants

Abstract

Background: Flowering plant seeds originate from a unique double-fertilization event, which involves two sperm cells and two female gametes, the egg cell and the central cell. For many years our knowledge of mechanisms involved in angiosperm fertilization remained minimal. It was obvious that several signals were required to explain how the male gametes are delivered inside the maternal reproductive tissues to the two female gametes but their molecular nature remained unknown. The difficulties in imaging the double-fertilization process prevented the identification of the mode of sperm cell delivery. It was believed that the two sperm cells were not functionally equivalent.

Scope: We review recent studies that have significantly improved our understanding of the early steps of double fertilization. The attractants of the pollen tube have been identified as small proteins produced by the synergid cells that surround the egg cell. Genetic studies have identified the signalling pathways required for the release of male gametes from the pollen tube. High-resolution imaging of the trajectory of the two male gametes showed that their transport does not involve the synergid cells directly and that isomorphic male gametes are functionally equivalent. We also outline major outstanding issues in the field concerned with the barrier against polyspermy, gamete recognition and mechanisms that prevent interspecies crosses.

Fig. 1

Schematic representation of sexual reproduction in A. thaliana. The pollen grain, once hydrated on the stigma, elongates the pollen tube into the style. After emerging onto the surface of the placenta, the pollen tube keeps elongating to reach the funiculus, which connects the placenta and the ovule. When the ovule is not fertilized, the pollen tube is guided to grow onto the surface of the funiculus to the ovule by unknown mechanisms (funicular guidance). The chemoattractants secreted from the synergid cells then guide the pollen tube to the micropyle of the ovule (micropylar guidance). The pollen tube stops its growth (pollen tube perception), and discharges sperm cells. The two sperm cells are released and one fertilizes with the egg and the other with the central cell, giving rise to the embryo and the endosperm, respectively (double fertilization).

Fig. 2

Schematic representation of the role of genes involved in the early steps of double fertilization in A. thaliana. (A) The pollen tube on the funiculus is guided to the micropyle of the unfertilized ovule. Chemo-attractants such as LUREs in Arabidopsis and ZmEA1 in maize are secreted from the synergid cells through the filiform apparatus, generating a concentration gradient to conduct the directional growth of the pollen tube into the micropylar end of the embryo sac. (B) Through communication between the synergid cell and the pollen tube, the pollen tube arrests its elongation at the proper position and prepares for pollen tube discharge. (C) Pollen tube discharge generates cytoplasmic flow of the pollen tube content, which is likely to be sufficient for sperm cells to migrate directly into the intercellular region between the egg cell and the central cell. The ejected two sperm cells then start plasmogamy with the egg cell and the central cell. An, antipodal cells; Cc, central cell; Ec, egg cell; Dsy, degenerated synergid cell; Fa, filiform apparatus; Fn, funiculus; Mp, micropyle; Pt, pollen tube; Sc, sperm cell; Sy, synergid cell; Vn, pollen vegetative nucleus.