Spermidine Is a Morphogenetic Determinant for Cell Fate Specification in the Male Gametophyte of the Water FernMarsilea vestita   

Abstract

Here, we show that the polyamine spermidine plays a key role as a morphogenetic determinant during spermatid development in the water fern Marsilea vestita. Spermidine levels rise first in sterile jacket cells and then increase dramatically in spermatogenous cells as the spermatids mature. RNA interference and drug treatments were employed to deplete spermidine in the gametophyte at different stages of gametogenesis. Development in spermidine-depleted gametophytes was arrested before the completion of the last round of cell divisions. In spermidine-depleted spermatogenous cells, chromatin failed to condense properly, basal body positioning was altered, and the microtubule ribbon was in disarray. When cyclohexylamine, a spermidine synthase (SPDS) inhibitor, was added at the start of spermatid differentiation, the spermatid nuclei remained round, centrin failed to localize into basal bodies, thus blocking basal body formation, and the microtubule ribbon was completely abolished. In untreated gametophytes, spermidine made in the jacket cells moves into the spermatids, where it is involved in the unmasking of stored SPDS mRNAs, leading to substantial spermidine synthesis in the spermatids. We found that treating spores directly with spermidine or other polyamines was sufficient to unmask a variety of stored mRNAs in gametophytes and arrest development. Differences in patterns of transcript distribution after these treatments suggest that specific transcripts reside in different locations in the dry spore; these differences may be linked to the timing of unmasking and translation for that mRNA during development.

Masked mRNA is stored with aggregated nuclear speckles and its asymmetric redistribution requires a homolog of mago nashi

“…Since additions of SPD cause mitotic arrest and the precocious unmasking of transcripts [15], it is reasonable to assume that if these transcripts are associated with nuclear speckles, then SPD should perturb speckle aggregation within the microspore nucleus. We tested this hypothesis by adding 10 mM SPD to microspores, which were then allowed to develop for 4 hours.…”

Transcriptome analysis reveals a diverse family of kinesins essential for spermatogenesis in the fern Marsilea

“…Introduction W e are interested in the processes that regulate rapid development of the male gametophyte in Marsilea vestita. The male gametophyte of Marsilea exhibits exquisite spatial and temporal precision during development [Wolniak et al, 2015] and allows the study of mechanisms that regulate changes in cell fate determination [Tsai et al, 2004;van der Weele et al, 2007;Deeb et al, 2010], cellular morphogenesis [Sharp, 1914;Myles andHepler, 1977, 1982], the de novo formation of basal bodies [Mizukami and Gall, 1966;Hepler, 1976;Hart and Wolniak, 1998;Klink and Wolniak, 2001], and ciliogenesis [Myles and Hepler, 1977]. Marsilea is a semi-aquatic water fern that produces megaspores, which develop into female gametophytes, and microspores, which develop into male gametophytes.…”

Phloem-Specific Methionine Recycling Fuels Polyamine Biosynthesis in a Sulfur-Dependent Manner and Promotes Flower and Seed Development

“…Spermine synthase (SPMS) has been shown to protect plants during salt stress. Additionally, thermospermine, which is synthesized by thermospermine synthase (ACL5), functions in vascular development by repressing xylem differentiation (Vera-Sirera et al, 2010;Takano et al, 2012), and spermidine has been proven important for plant reproduction (Imai et al, 2004;Deeb et al, 2010). The acl5/spms double mutant was shown to be hypersensitive to salt stress but could be rescued by the exogenous application of spermine (Yamaguchi et al, 2006).…”