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

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.

Removal of Retained Introns Regulates Translation in the Rapidly Developing Gametophyte of Marsilea vestita

“…These spores are meiotic products that form and then desiccate as part of their natural developmental cycle. The desiccated microspore of M. vestita contains a single cell, that when rehydrated, will rapidly develop into a gametophyte comprising seven sterile cells and 32 motile, male gametes (reviewed in Wolniak et al, 2011). From the time that the spores are hydrated, it takes only 11 hr for spermatogenesis to reach completion.…”

Organelle Genome Inheritance in Deparia Ferns (Athyriaceae, Aspleniineae, Polypodiales)

“…Moreover, it is almost impossible to infer organelle genome transmission in ferns by examining the organelle identity of germ line cells (e.g., eggs or sperms). Generally, mitochondria and plastids are present in both their sperms (or spermatocytes) and eggs ( Duckett, 1973 ; Raghavan, 1989 and references therein; Kotenko, 1990 ; Gori et al, 1997 ; Muccifora et al, 2000 ; Renzaglia et al, 2001 ; Lopez-Smith and Renzaglia, 2002 , 2008 ; Sakaushi et al, 2003 ; Cao et al, 2009 , 2010 ; Wolniak et al, 2011 ; Cao, 2014 and references therein), thus any manner of organelle inheritance—maternal, paternal, and even biparental—is possible.…”

“…Cytologically, maternal inheritance of the organelle genomes in some ferns is implicated by the anatomical ontology during fertilization. Both plastids and mitochondria exist in fern egg cells and functional sperms ( Duckett, 1973 ; Raghavan, 1989 and references listed therein; Kotenko, 1990 ; Gori et al, 1997 ; Muccifora et al, 2000 ; Renzaglia et al, 2001 ; Lopez-Smith and Renzaglia, 2002 , 2008 ; Sakaushi et al, 2003 ; Cao et al, 2009 , 2010 ; Wolniak et al, 2011 ; Cao, 2014 ), but plastids from sperm are known to be excluded before immersion into an egg ( Bell and Duckett, 1976 ; Lopez-Smith and Renzaglia, 2002 , 2008 ; Cao et al, 2010 , 2016 ). In Osmunda, Pteridium , and Ceratopteris , mitochondria from sperms are digested soon after fertilization ( Bell and Duckett, 1976 ; Lopez-Smith and Renzaglia, 2008 ; Cao et al, 2010 , 2016 ).…”

Kinesin-2 and kinesin-9 have atypical functions during ciliogenesis in the male gametophyte of Marsilea vestita

“…All divisions are complete approximately 5 h after microspore hydration. During the second phase, only the spermatids undergo drastic morphological changes and differentiate into motile, corkscrew-shaped spermatozoids [ 4 , 12 ].…”