Abstract
In animals, microtubules and centrosomes direct the migration of gamete pronuclei for fertilization. By contrast, flowering plants have lost essential components of the centrosome, raising the question of how flowering plants control gamete nuclei migration during fertilization. Here, we use Arabidopsis thaliana to document a novel mechanism that regulates F-actin dynamics in the female gametes and is essential for fertilization. Live imaging shows that F-actin structures assist the male nucleus during its migration towards the female nucleus. We identify a female gamete-specific Rho-GTPase that regulates F-actin dynamics and further show that actin-myosin interactions are also involved in male gamete nucleus migration. Genetic analyses and imaging indicate that microtubules are dispensable for migration and fusion of male and female gamete nuclei. The innovation of a novel actin-based mechanism of fertilization during plant evolution might account for the complete loss of the centrosome in flowering plants.
Highlights
Flowering plants have evolved a double fertilization process that requires the fusion of two sperm cells with the two female gametes, the egg cell and the central cell
F-actin movement was extremely reduced in central cells expressing dominantnegative ROP8 (DN-ROP8) (Figure 6C–E; Videos 3; Video 4; Video 5; 45% and 30% defects in DN-ROP8 Line 1 [n = 11] and Line 2 [n = 10], respectively, compared to 0% defect in WT [n = 7] and constitutively-active ROP8 (CA-ROP8) Line 1 [n = 5] and Line 2 [n = 6]). These results show that ROP8 controls novel constant inward dynamics of F-actin movement in the central cell and that this ROP8-dependent inward F-actin movement is required for the proper transport of the sperm cell nucleus to the central cell nucleus
Pronuclear migration in the fertilized egg is microtubule dependent, but both actin filament and microtubules are indispensable for nuclear positioning in many somatic cells (Reinsch and Gonczy, 1998; Gundersen and Worman, 2013)
Summary
Flowering plants have evolved a double fertilization process that requires the fusion of two sperm cells with the two female gametes, the egg cell and the central cell. This is achieved in a series of complex processes (Kawashima and Berger, 2011). Several factors and molecular mechanisms controlling these early events such as pollen tube guidance and reception have been recently characterized (Higashiyama et al, 2001; Palanivelu et al, 2003; Kasahara et al, 2005; Escobar-Restrepo et al, 2007; Okuda et al, 2009; Kessler et al, 2010; Tsukamoto et al, 2010; Takeuchi and Higashiyama, 2012; Leydon et al, 2013; Liang et al, 2013; Ngo et al, 2014), and mechanisms governing plasmogamy have been identified (Mori et al, 2006; Von Besser et al, 2006; Mori et al, 2014; Sprunck et al, 2012). How gamete nuclei migrate and fuse in flowering plants still remain largely elusive
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