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Extremes in rapid cellular morphogenesis: post-transcriptional regulation of spermatogenesis in Marsilea vestita

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Abstract

The endosporic male gametophyte of the water fern, Marsilea vestita, provides a unique opportunity to study the mechanisms that control cell fate determination during a burst of rapid development. In this review, we show how the spatial and temporal control of development in this simple gametophyte involves several distinct modes of RNA processing that allow the translation of specific mRNAs at distinct stages during gametogenesis. During the early part of development, nine successive cell division cycles occur in precise planes within a closed volume to produce seven sterile cells and 32 spermatids. There is no cell movement in the gametophyte; so, cell position and size within the spore wall define cell fate. After the division cycles have been completed, the spermatids become sites for the de novo formation of basal bodies, for the assembly of a complex cytoskeleton, for nuclear and cell elongation, and for ciliogenesis. In contrast, the adjacent sterile cells exhibit none of these changes. The spermatids differentiate into multiciliated, corkscrew-shaped gametes that resemble no other cells in the entire plant. Development is controlled post-transcriptionally. The transcripts stored in the microspore are released (unmasked) in the gametophyte at different times during development. At the start of these studies, we identified several key mRNAs that undergo translation at specific stages of gametophyte development. We developed RNA silencing protocols that enabled us to block the translation of these proteins and thereby establish their necessity and sufficiency for the completion of specific stages of gametogenesis. In addition, RNAi enabled us to identify additional proteins that are essential for other phases of development. Since the distributions of mRNAs and the proteins they encode are not identical in the gametophyte, transcript processing is apparently important in allowing translation to occur under strict temporal and spatial control. Transcript polyadenylation occurs in the spermatogenous cells in ways that match the translation of specific mRNAs. We have found that the exon junction complex plays key roles in transcript regulation and modifications that underlie cell specification in the gametophyte. We have recently become interested in the mechanisms that control the unmasking of the stored transcripts and have linked the synthesis and redistribution of spermidine in the gametophyte to the control of mRNA release from storage during early development and later to basal body formation, cytoskeletal assembly, and nuclear and cell elongation in the differentiating spermatids.

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Acknowledgements

We gratefully acknowledge the support for this project in the form of grants from NSF (MCB 0720486 and DBI 0842525). We are also grateful for the support from Maryland Agriculture Experiment Station for this project. Faten Deeb was partially supported by a USDA Food and Agricultural Sciences National Needs Graduate and Postdoctoral Fellowship Grant (#20053842015761) while this work was being performed.

Conflicts of interest

The authors declare that they have no conflicts of interest.

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Author notes

  1. Faten Deeb

    Present address: Department of Molecular Microbiology and Immunology, School of Medicine, University of Missouri, Columbia, MO, 65211, USA

  2. Vincent P. Klink

    Present address: Department of Biological Sciences, Mississippi State University, 212 Harned Hall, Lee Blvd, Starkville, MS, 39762, USA

Authors and Affiliations

  1. Department of Cell Biology and Molecular Genetics, University of Maryland, College Park, MD, 20742, USA

    Stephen M. Wolniak, Corine M. van der Weele, Faten Deeb, Thomas Boothby & Vincent P. Klink

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  1. Stephen M. Wolniak
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  2. Corine M. van der Weele
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Correspondence to Stephen M. Wolniak.

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Wolniak, S.M., van der Weele, C.M., Deeb, F. et al. Extremes in rapid cellular morphogenesis: post-transcriptional regulation of spermatogenesis in Marsilea vestita . Protoplasma 248, 457–473 (2011). https://doi.org/10.1007/s00709-011-0276-3

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