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

ABSTRACT: Spermatogenesis in the semi-aquatic fern, Marsilea vestita, is a rapid, synchronous process that is initiated when dry microspores are placed in water. Development is post-transcriptionally driven and can be divided into two phases. The first phase consists of nine mitotic division cycles that produce 7 sterile cells and 32 spermatids. During the second phase, each spermatid differentiates into a corkscrew-shaped motile spermatozoid with ~140 cilia.Analysis of the transcriptome from the male gametophyte of Marsilea revealed that one kinesin-2 (MvKinesin-2) and two kinesin-9 s (MvKinesin-9A and MvKinesin-9B) are present during spermatid differentiation and ciliogenesis. RNAi knockdowns show that MvKinesin-2 is required for mitosis and cytokinesis in spermatogenous cells. Without MvKinesin-2, most spermatozoids contain two or more coiled microtubule ribbons with attached cilia and very large cell bodies. MvKinesin-9A is required for the correct placement of basal bodies along the organelle coil. Knockdowns of MvKinesin-9A have basal bodies and cilia that are irregularly positioned. Spermatozoid swimming behavior in MvKinesin-2 and -9A knockdowns is altered because of defects in axonemal placement or ciliogenesis. MvKinesin-2 knockdowns only quiver in place while MvKinesin-9A knockdowns swim erratically compared to controls. In contrast, spermatozoids produced after the silencing of MvKinesin-9B exhibit normal morphology and swimming behavior, though development is slower than normal for these gametes.Our results show that MvKinesin-2 and MvKinesin-9A are required for ciliogenesis and motility in the Marsilea male gametophyte; however, these kinesins display atypical roles during these processes. MvKinesin-2 is required for cytokinesis, a role not typically associated with this protein, as well as for ciliogenesis during rapid development and MvKinesin-9A is needed for the correct orientation of basal bodies. Our results are the first to investigate the kinesin-linked mechanisms that regulate ciliogenesis in a land plant.

SUBMITTER: Tomei EJ

PROVIDER: S-EPMC4947347 | biostudies-literature | 2016 Jul

REPOSITORIES: biostudies-literature

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

Tomei Erika J EJ Wolniak Stephen M SM

BMC cell biology 20160716 1

<h4>Background</h4>Spermatogenesis in the semi-aquatic fern, Marsilea vestita, is a rapid, synchronous process that is initiated when dry microspores are placed in water. Development is post-transcriptionally driven and can be divided into two phases. The first phase consists of nine mitotic division cycles that produce 7 sterile cells and 32 spermatids. During the second phase, each spermatid differentiates into a corkscrew-shaped motile spermatozoid with ~140 cilia.<h4>Results</h4>Analysis of ...[more]

PMID: 27421907

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Project description:Pollen, an extremely reduced bicellular or tricellular male reproductive structure of flowering plants, serves as a model for numerous studies covering wide range of developmental and physiological processes. The pollen development represents a fragile and vital phase of plant ontogenesis and pollen was among the first singular plant tissues thoroughly characterized at the transcriptomic level (Honys and Twell [5]). Arabidopsis pollen developmental transcriptome has been published over a decade ago (Honys and Twell, 2004) and transcriptomes of developing pollen of other species have followed (Rice, Deveshwar et al. [2]; Triticeae, Tran et al. [11]; upland cotton, Ma et al. [8]). However, the transcriptomic data describing the development of tobacco pollen, a bicellular model for cell biology studies, have been missing. Here we provide the transcriptomic data covering three stages (Tupý et al., 1983) of wild type tobacco (Nicotiana tabacum, cv. Samsun) pollen development: uninucleate microspores (UNM, stage 1), early bicellular pollen (eBCP, stage 3) and late bicellular pollen (lBCP, stage 5) as a supplement to the mature pollen (MP), 4 h-pollen tube (PT4), 24 h-pollen tubes (PT24), leaf (LF) and root (RT) transcriptomic data presented in our previous studies (Hafidh et al., 2012a; Hafidh et al., 2012b). We characterized these transcriptomes to refine the knowledge base of male gametophyte-enriched genes as well as genes expressed preferentially at the individual stages of pollen development. Alongside updating the list of tissue-specific genes, we have investigated differentially expressed genes with respect to early expressed genes. Pollen tube growth and competition of pollen tubes in female pistil can be viewed as a race of the fittest. Accordingly, there is an apparent evolutionary trend among higher plants to store significant material reserves and nutrients during pollen maturation. This supply ensures that after pollen germination, the pollen tube utilizes its resource predominantly for its rapid elongation in the female pistil. Previous transcriptomic data from Arabidopsis showed massive expression of genes encoding proteins forming both ribosomal subunits that were accumulated in developing pollen, whereas their expression was not detectable in growing pollen tubes (Honys and Twell, 2004). We observed a similar phenomenon in less advanced bicellular tobacco pollen. Here, we describe in detail how we obtained and analyzed validated microarray dataset deposited in Gene Expression Omnibus (GSE62349).

Dataset Information

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

Publications

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

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