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Sperm cell architecture, insemination, and fertilization in the model fern, Ceratopteris richardii

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Abstract

Motile sperm cells of land plants are released directly into the environment and encounter numerous constraints on their way to the egg. Sperm cell organization, shape, size, and plasticity are crucial to the processes associated with fertilization. We conducted an ultrastructural investigation to detail insemination (sperm release, swimming and movement within the archegonium) and fertilization in the model fern Ceratopteris richardii. Gametophytes were grown from spores using sterile culture techniques and flooded in water when sexually mature. Materials were examined at different stages post-flooding. During insemination in C. richardii, the sperm cytoskeleton and flagella rearrange, and the coils of the cell extend while entering the neck canal. In this nearly linear configuration, the dense ridge, a densely compacted band of filaments presumed to be actin, expands to surround the leading edge of the sperm cell. This ridge fuses with the receptive site on the female gamete and is the sperm component that initiates contact with the egg nuclear envelope. All cellular components, except plastids, enter the egg cytoplasm. Sperm mitochondria are distinguishable from those of the egg because they are encased by two or three additional membranes and are sequestered from the zygote cytoplasm. During karyogamy, the sperm components, including the microtubule cytoskeleton (spline) and flagella, maintain their spatial integrity. Microtubules play key roles not only in sperm cell structure but also in facilitating karyogamy in this fern. After karyogamy is completed, microtubule arrays of the sperm cell and the components of the locomotory apparatus are disassembled. We provide the first demonstration of the likely involvement of sperm actin in egg penetration in land plants and new insights into the fate of paternal organelles. This study points to the roles sperm cell structure and dynamics play in the intricate processes of insemination and fertilization in land plants.

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Acknowledgments

The authors wish to thank Leslie Hickok for graciously providing C. richardii spores, and Jeffrey Duckett and an anonymous reviewer for comments on the manuscript. We thank the staff at IMAGE for their technical support, the members of the Renzaglia lab for their constant encouragement, and Lawrence Mainwaring for images of pre-released sperm cells. Special thanks to Gabriel Johnson for all his assistance and expertise. This research was supported by research grants (DEB-0322664, DEB-0423625, DEB-0521177, and DEB-0228679) from the National Science Foundation as part of the Research Experience for Undergraduates and Assembling the Tree of Life Programs.

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  1. Department of Plant Biology, Southern Illinois University, Carbondale, IL, 62901-6509, USA

    Renee Lopez-Smith & Karen Renzaglia

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Correspondence to Renee Lopez-Smith.

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Communicated by Scott Russell.

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Lopez-Smith, R., Renzaglia, K. Sperm cell architecture, insemination, and fertilization in the model fern, Ceratopteris richardii . Sex Plant Reprod 21, 153–167 (2008). https://doi.org/10.1007/s00497-008-0068-x

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