Transcriptome analysis reveals a diverse family of kinesins essential for spermatogenesis in the fern <scp><i>M</i></scp><i>arsilea</i>

Tomei, Erika; Wolniak, Stephen M.

doi:10.1002/cm.21285

Cited by 15 publications

(15 citation statements)

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“…We used these kinesins as the base of our search because the entire kinesin family in Physcomitrella has recently been identified [ 37 ] and because Physcomitrella and Chlamydomonas are two of the more closely related ciliated species to Marsilea with an annotated kinesin family. We then verified our results by comparing them to the 56 kinesin-like transcripts that were previously identified in our transcriptome [ 38 ]. Our search identified one candidate kinesin-2 (MvKinesin-2) transcript and two candidate kinesin-9 (MvKinesin-9A and MvKinesin-9B) transcripts (Additional file 1 ).…”

Section: Resultssupporting

confidence: 55%

“…For example, comparative analyses of the kinesin family has shown that kinesin-2, kinesin-9, and the more recently identified, kinesin-‘orphan’ III (also referred to as kinesin-16) and kinesin-17, are only found in organisms that are ciliated at some point during the life cycle [ 28 , 36 ]. Members of these kinesin families can be found in ciliated plants such as Chlamydomonas , the moss Physcomitrella , and the water fern Marsilea , except kinesin-17, which is only present in Chlamydomona s [ 28 , 36 – 38 ]. The genome of Arabidopsis , a flowering plant that is never makes ciliated cells, contains none of these kinesins [ 39 ].…”

Section: Introductionmentioning

confidence: 99%

“…Transcripts that encode members of the kinesin-2 and kinesin-9 families were selected as targets for our studies on the regulation of ciliogenesis in spermatids of Marsilea . mRNAs that encode kinesin-2 and kinesin-9 increase in abundance during the stage of development associated with spermatid shaping and ciliogenesis [ 38 ]. These late rises in transcript abundance led us to suspect that kinesin-2 and kinesin-9 may play critical roles for spermatid differentiation and ciliogenesis.…”

Section: Introductionmentioning

confidence: 99%

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

Tomei

Wolniak

2016

BMC Cell Biol

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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.Electronic supplementary materialThe online version of this article (doi:10.1186/s12860-016-0107-7) contains supplementary material, which is available to authorized users.

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Section: Resultssupporting

confidence: 55%

Section: Introductionmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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

Tomei

Wolniak

2016

BMC Cell Biol

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“…After spores are rehydrated, pre-mRNAs are unmasked, processed, and translated according to a precise spatiotemporal pattern. Stored transcripts include those encoding tubulins and centrins (Tsai et al, 2004), as well as proteins important for mitosis and flagella formation, such as kinesins (Tomei & Wolniak, 2016). More detailed information is available for the transcriptome of developing antheridia of M. polymorpha (Higo et al, 2016).…”

Section: Gene Expression In Male Germ Cellsmentioning

confidence: 99%

The evolution and patterning of male gametophyte development

Hackenberg

Twell

2019

Current Topics in Developmental Biology

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1. The evolutionary history of the male gametophyte 1.1. The origins of spermatogenesis in green plants 1.2. The sporophyte was key for terrestrial plant evolution 1.3. Heterospory and the origin of microgametophytes 1.4. Adaptations of seed plant microgametophytes 2. Male germline development in angiosperms 2.1. Asymmetric division and cell fate determination 2.2. Cell cycle control and male gametophyte patterning 2.3. Transcriptional control of male gametophyte patterning 2.4. Chromatin remodelling in male gametophyte development 2.5. Communication between non-germ and germ cells 3. Molecular evolution of the male germline 3.1. Motile plant and animal sperm share common features 3.2. Gene expression in male germ cells 3.3. The evolution of transcription factors regulating male gametogenesis 4. Perspective 5. Acknowledgements 2 6. References Abstract: The reproductive adaptations of land plants have played a key role in their terrestrial colonization and radiation. These encompass mechanisms used for the production, dispersal and union of gametes to support sexual reproduction. The production of small motile male gametes and larger immotile female gametes (oogamy) in specialized multicellular gametangia evolved in the charophyte algae, the closest extant relatives of land plants.Reliance on water and motile male gametes for sexual reproduction was retained by bryophytes and basal vascular plants, but was overcome in seed plants by the dispersal of pollen and the guided delivery of non-motile sperm to the female gametes. Here we discuss the evolutionary history of male gametogenesis in streptophytes (green plants) and the underlying developmental biology, including recent advances in bryophyte and angiosperm models. We conclude with a perspective on research trends that promise to deliver a deeper understanding of the evolutionary and developmental mechanisms of male gametogenesis in plants.

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“…Investigations into representatives of other major plant lineages could address this question. The recent identification of a kinesin-4 with mitotic function in the fern Marsilea vestita certainly proposes to be a good starting point (Tomei & Wolniak 2016).…”

Section: Making Ends Meet: Overlaps In Flowering Plantsmentioning

confidence: 99%

Shaping plant microtubule networks via overlap formation

Keijzer¹

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Microtubules are dynamic polymers that are vital for a vast range of cellular functions. For virtually all of these functions microtubules are organized into specifically tailored networks. Plant cells present us with a remarkably diverse range of microtubule networks, one of which supports the unique manner in which these cells divide. The physical separation of two daughter cells at the end of cell division in plants is achieved by formation of an interior, disc-shaped membrane compartment called the cell plate that ultimately gives rise to a dividing cell wall segment. Cell plate construction starts in the centre of the cell and continues radially outwards until the cell plate fuses with the existing plasma membrane. Cell plate assembly is fuelled by fusion of vesicles that are targeted to the division plane by the microtubules of the phragmoplast apparatus. Phragmoplast microtubules are organized in a bipolar configuration that is propagated during radial expansion of the cell plate. In contrast to most animal cells, plants do not use centrosomes as foci of microtubule growth initiation. Instead, plant microtubule networks are striking examples of self-organizing systems that emerge from physically constrained interactions of dispersed microtubules. How microtubule-based activities including growth, shrinkage, severing, sliding, nucleation and bundling interrelate to jointly generate a required ordered structure is a fascinating but underexplored question. Evidence mounts that adapter proteins sense the local geometry of microtubules to locally modulate the activity of proteins involved in microtubule growth regulation and severing. One particular geometry that is a prime candidate for serving as an integrative hub in a bipolar configuration such as the phragmoplast, is the antiparallel overlap formed between opposing microtubules. The finding that proteins fostering this interaction are also important in interphase plant cells hints that overlaps may have roles in constructing microtubule networks beyond bipolar arrays. Insight into control of overlap formation gained from plants has broader relevance since many other microtubule assemblies encountered in eukaryotes rely on these structures as well. pp.2909-2923. Hotta, T. et al., 2012. Characterization of the Arabidopsis augmin complex uncovers its critical function in the assembly of the acentrosomal spindle and phragmoplast microtubule arrays.

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

Cited by 15 publications

References 61 publications

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

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

The evolution and patterning of male gametophyte development

Shaping plant microtubule networks via overlap formation

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