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

BMC Cell Biology

Research Article

Stephen M. Wolniak¹  Erika J. Tomei¹ 

[1] Department of Cell Biology and Molecular Genetics, University of Maryland at College Park, 20742, College Park, MD, USA;

关键词: Kinesin-2;    Kinesin-9;    Ciliogenesis;    Cytokinesis;    Intraflagellar transport;    Basal bodies;   

DOI  :  10.1186/s12860-016-0107-7

 received in 2016-03-02, accepted in 2016-07-07,  发布年份 2016

来源: Springer

【 摘 要 】

BackgroundSpermatogenesis 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.ResultsAnalysis 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.ConclusionsOur 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.

【 授权许可】

CC BY   
© The Author(s). 2016