Gamete Nuclear Migration in Animals and Plants

Abstract

The migration of male and female gamete nuclei to each other in the fertilized egg is a prerequisite for the blending of genetic materials and the initiation of the next generation. Interestingly, many differences have been found in the mechanism of gamete nuclear movement among animals and plants. Female to male gamete nuclear movement in animals and brown algae relies on microtubules. By contrast, in flowering plants, the male gamete nucleus is carried to the female gamete nucleus by the filamentous actin cytoskeleton. As techniques have developed from light, electron, fluorescence, immunofluorescence, and confocal microscopy to live-cell time-lapse imaging using fluorescently labeled proteins, details of these differences in gamete nuclear migration have emerged in a wide range of eukaryotes. Especially, gamete nuclear migration in flowering plants such as Arabidopsis thaliana, rice, maize, and tobacco has been further investigated, and showed high conservation of the mechanism, yet, with differences among these species. Here, with an emphasis on recent developments in flowering plants, we survey gamete nuclear migration in different eukaryotic groups and highlight the differences and similarities among species.

Keywords: F-actin; cytoskeleton; fertilization; gamete nuclear migration; microtubule; sexual reproduction.

FIGURE 1

Gamete nuclear migration and use of cytoskeleton for gamete nuclear migration in different kingdoms. In most animals, microtubules assist the migration of both male and female gamete nuclei toward their fusion site. Unlike animals, male gamete nucleus migrates to female gamete nucleus for fusion in algae and land plants. The direction of gamete nuclear migration in green algae is unclear. The use of cytoskeleton also varies among different groups within the same kingdom. In case of algal group, brown algae use microtubule for gamete nuclear migration, whereas red algae use F-actin. F-actin plays a role in green algae (Chlamydomonas) mating but its involvement in gamete nuclear migration is not clear. Among land plants, ferns use microtubule, whereas angiosperms use F-actin for sperm nuclear migration. The arrow shows the overall direction of the nuclear movement.

FIGURE 2

Migration and fusion of egg and sperm nuclei in the sea urchin egg cytoplasm. The sperm aster forms around the base of the sperm head after incorporation into the egg cell. Astral microtubule interacts with the female gamete nucleus (i). Astral microtubules increase in length, pushing the male gamete nucleus and pulling the female gamete nucleus for fusion (ii). The complex then moves to the center of the egg to complete the fertilization process (iii).

FIGURE 3

Factors linking cytoskeleton and gamete nuclear envelope for migration in animals (A) and its one possible model in flowering plants (B). (A) In animals, the LINC complex, containing KASH domain protein in the outer nuclear envelope and SUN in the inner nuclear envelope, links nucleus-kinesin/dynein-microtubules. (B) In flowering plants, the LINC complex links nucleus-myosin-actin in somatic cell nuclei and the pollen tube vegetative nucleus. Like animals, the SUN domain protein is present in the inner nuclear envelope in flowering plants that is connected with the outer nuclear envelope embedded proteins, WIT1/2 and WIP.

FIGURE 4

Brown algae sperm nuclear migration toward the egg nucleus. The egg nucleus stays at the center, which is maintained by microtubule and F-actin. Microtubules generate sperm aster around the sperm in the fertilized egg cell (i). Sperm nucleus then moves toward the egg nucleus positioned at the center for fusion (ii).

FIGURE 5

Fertilization in Red algae. Female gamete adheres to the male gamete (spermatia) through trichogyne (i). After adhesion, spermatial nucleus undergoes mitosis (ii) and generates two nuclei; one migrates toward the female nucleus through trichogyne using F-actin (iii and iv) and the other moves toward the tip of the trichogyne (v).

FIGURE 6

The fusion of male and female gamete in fern. (A) The sperm is coiled with an elongated nucleus, a ribbon of microtubules, and a dense layer of flagellar bands. The proximal part of the sperm is illustrated intact and the distal part is shown in cross section. (B) The sperm enters into the egg cytoplasm with nucleus, microtubule ribbon, and flagellar band by engulfing. The egg cytoplasm outflows into the region of sperm coil, forming a fertilization cone. (C) The sperm chromatin decondenses and moves toward the egg nucleus for fusion.

FIGURE 7

Double fertilization in Arabidopsis. (A) The pollen tube grows toward the female gametophyte, comprising the egg cell, two synergid cells, the central cell and three antipodal cells. The chemoattractant, secreted from the synergid cell filiform apparatus, guides the pollen tube through the micropylar end. (B) One synergid cell receives the pollen tube and the two sperm cells are released from the pollen tube. One sperm cell fertilizes the egg cell, giving rise to embryo and the other one fertilizes the central cell, developing the endosperm.

FIGURE 8

Factors controlling sperm nuclear migration in Arabidopsis. F-actin cytoskeleton is involved in sperm nuclear migration in Arabidopsis. Upon entry to the central cell, the sperm nucleus becomes surrounded by an aster-shaped F-actin structure. This aster-like structure moves toward the central cell nucleus together with the sperm nucleus for karyogamy. There is a constant “inward” movement of F-actin bundles, from the central cell membrane periphery to the cell nucleus. This inward movement is controlled by plasma membrane associated ROP8 and myosin.