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Dynamic F-actin movement is essential for fertilization in Arabidopsis thaliana.

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.

SUBMITTER: Kawashima T

PROVIDER: S-EPMC4221737 | biostudies-literature | 2014 Oct

REPOSITORIES: biostudies-literature

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Dynamic F-actin movement is essential for fertilization in Arabidopsis thaliana.

Kawashima Tomokazu T Maruyama Daisuke D Shagirov Murat M Li Jing J Hamamura Yuki Y Yelagandula Ramesh R Toyama Yusuke Y Berger Frédéric F

eLife 20141010

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 ...[more]

PMID: 25303363

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Project description:BACKGROUND: To understand transcriptional regulatory networks (TRNs), especially the coordinated dynamic regulation between transcription factors (TFs) and their corresponding target genes during development, computational approaches would represent significant advances in the genome-wide expression analysis. The major challenges for the experiments include monitoring the time-specific TFs' activities and identifying the dynamic regulatory relationships between TFs and their target genes, both of which are currently not yet available at the large scale. However, various methods have been proposed to computationally estimate those activities and regulations. During the past decade, significant progresses have been made towards understanding pollen development at each development stage under the molecular level, yet the regulatory mechanisms that control the dynamic pollen development processes remain largely unknown. Here, we adopt Networks Component Analysis (NCA) to identify TF activities over time course, and infer their regulatory relationships based on the coexpression of TFs and their target genes during pollen development. RESULTS: We carried out meta-analysis by integrating several sets of gene expression data related to Arabidopsis thaliana pollen development (stages range from UNM, BCP, TCP, HP to 0.5 hr pollen tube and 4 hr pollen tube). We constructed a regulatory network, including 19 TFs, 101 target genes and 319 regulatory interactions. The computationally estimated TF activities were well correlated to their coordinated genes' expressions during the development process. We clustered the expression of their target genes in the context of regulatory influences, and inferred new regulatory relationships between those TFs and their target genes, such as transcription factor WRKY34, which was identified that specifically expressed in pollen, and regulated several new target genes. Our finding facilitates the interpretation of the expression patterns with more biological relevancy, since the clusters corresponding to the activity of specific TF or the combination of TFs suggest the coordinated regulation of TFs to their target genes. CONCLUSIONS: Through integrating different resources, we constructed a dynamic regulatory network of Arabidopsis thaliana during pollen development with gene coexpression and NCA. The network illustrated the relationships between the TFs' activities and their target genes' expression, as well as the interactions between TFs, which provide new insight into the molecular mechanisms that control the pollen development.

Project description:During double fertilization in angiosperms, two male gametes (sperm cells), are released from a pollen tube into the receptive region between two female gametes; the egg cell and the central cell of the ovule. The sperm cells fertilize the egg cell and the central cell in a one-to-one manner to yield a zygote and an endosperm, respectively. The one-to-one distribution of the sperm cells to the two female gametes is strictly regulated, possibly via communication among the four gametes. Polyspermy block is the mechanism by which fertilized female gametes prevent fertilization by a secondary sperm cell, and has been suggested to operate in the egg cell rather than the central cell. However, whether the central cell also has the ability to avoid polyspermy during double fertilization remains unclear. Here, we assessed the one-to-one fertilization mechanism of the central cell by laser irradiation of the female gametes and live cell imaging of the fertilization process in Arabidopsis thaliana. We successfully disrupted an egg cell within the ovules by irradiation using a femtosecond pulse laser. In the egg-disrupted ovules, the central cell predominantly showed single fertilization by one sperm cell, suggesting that neither the egg cell nor its fusion with one sperm cell is necessary for one-to-one fertilization (i.e., monospermy) of the central cell. In addition, using tetraspore mutants possessing multiple sperm cell pairs in one pollen, we demonstrated that normal double fertilization was observed even when excess sperm cells were released into the receptive region between the female gametes. In ovules accepting four sperm cells, the egg cell never fused with more than one sperm cell, whereas half of the central cells fused with more than one sperm cell (i.e., polyspermy) even 1 h later. Our results suggest that the central cell can block polyspermy during double fertilization, although the central cell is more permissive to polyspermy than the egg cell. The potential contribution of polyspermy block by the central cell is discussed in terms of how it is involved in the one-to-one distribution of the sperm cells to two distinct female gametes.

Dataset Information

Dynamic F-actin movement is essential for fertilization in Arabidopsis thaliana.

Publications

Dynamic F-actin movement is essential for fertilization in Arabidopsis thaliana.

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