Rho of Plants GTPases and Cytoskeletal Elements Control Nuclear Positioning and Asymmetric Cell Division during Physcomitrella patens Branching

Yi, Peishan; Goshima, Gohta

doi:10.1016/j.cub.2020.05.022

Cited by 47 publications

(62 citation statements)

References 50 publications

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“…In human cell cultures, the actin cytoskeleton collaborates with the dynein-based machinery that exerts cortical pulling forces on astral MTs, thereby positioning the nucleus at the center of the cell (Kiyomitsu, 2019). In the moss Physcomitrella patens , nuclear positioning is regulated by collaborative actions between MTs and F-actin (Yi and Goshima, 2020). Whether F-actin cables directly drive movement of nucleus/chromosomes in other systems is of great interest to explore.…”

Section: Resultsmentioning

confidence: 99%

Escape from mitotic catastrophe by actin-dependent nuclear displacement in fission yeast

Yukawa

Teratani

Toda

2020

Preprint

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SUMMARYProper nuclear positioning is essential for the execution of a wide variety of cellular processes in eukaryotic cells (Gundersen and Worman, 2013; Kopf et al., 2020; Lele et al., 2018). In proliferating mitotic cells, nuclear positioning is crucial for successful cell division. The bipolar spindle, which pulls sister chromatids towards two opposite poles, needs to assemble in the geometrical center of the cell. This ensures symmetrical positioning of the two nuclei that are reformed upon mitotic exit, by which two daughter cells inherit the identical set of the chromosomes upon cytokinesis. In fission yeast, the nucleus is positioned in the cell center during interphase; cytoplasmic microtubules interact with both the nucleus and the cell tips, thereby retaining the nucleus in the medial position of the cell (Daga et al., 2006; Tran et al., 2001). By contrast, how the nucleus is positioned during mitosis remains elusive. Here we show that several cell-cycle mutants that arrest in mitosis all displace the nucleus towards one end of the cell axis. Intriguingly, the actin cytoskeleton, not the microtubule counterpart, is responsible for the asymmetric movement of the nucleus. Time-lapse live imaging indicates that mitosis-specific F-actin cables interact with the nuclear membrane, thereby possibly generating an asymmetrical pushing force. In addition, constriction of the actomyosin ring further promotes nuclear displacement. This nuclear movement is beneficial, because if the nuclei were retained in the cell center, subsequent cell division would impose the lethal cut phenotype (Hirano et al., 1986; Yanagida, 1998), in which chromosomes are intersected by the contractile actin ring and the septum. Thus, fission yeast escapes from mitotic catastrophe by means of actin-dependent nuclear movement.

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Section: Resultsmentioning

confidence: 99%

Escape from mitotic catastrophe by actin-dependent nuclear displacement in fission yeast

Yukawa

Teratani

Toda

2020

Preprint

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“…The mechanisms underpinning the emergence of those tip growing cells in P. patens is remarkably well conserved throughout plants, as well as in fungi (Boyce et al, 2005): the emergence of root hairs from the root epidermis, the development of pollen tubes, and the formation of side branches in P. patens all require coordinated control of cell polarization, local cell wall loosening and cell expansion. These processes have been shown to be regulated by ROP GTPases, which localize to future bulge sites and mediate actin‐induced bulge formation (Chen et al, 2003; Jones et al, 2002; Molendijk et al, 2001; P. Yi & Goshima, 2020).…”

Section: Introductionmentioning

confidence: 99%

A fundamental developmental transition in Physcomitrium patens is regulated by evolutionarily conserved mechanisms

Jaeger

Moody

2021

Evolution and Development

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One of the most defining moments in history was the colonization of land by plants approximately 470 million years ago. The transition from water to land was accompanied by significant changes in the plant body plan, from those than resembled filamentous representatives of the charophytes, the sister group to land plants, to those that were morphologically complex and capable of colonizing harsher habitats. The moss Physcomitrium patens (also known as Physcomitrella patens) is an extant representative of the bryophytes, the earliest land plant lineage. The protonema of P. patens emerges from spores from a chloronemal initial cell, which can divide to self‐renew to produce filaments of chloronemal cells. A chloronemal initial cell can differentiate into a caulonemal initial cell, which can divide and self‐renew to produce filaments of caulonemal cells, which branch extensively and give rise to three‐dimensional shoots. The process by which a chloronemal initial cell differentiates into a caulonemal initial cell is tightly regulated by auxin‐induced remodeling of the actin cytoskeleton. Studies have revealed that the genetic mechanisms underpinning this transition also regulate tip growth and differentiation in diverse plant taxa. This review summarizes the known cellular and molecular mechanisms underpinning the chloronema to caulonema transition in P. patens.

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“…In other plant tissues, pre-ACD nuclear migrations enable the production of daughters of differing sizes and fates and also direct the relative placement of these cells [23,24]. Surprisingly, our time-lapse analyses of basl and MYR-BRX cotyledons revealed that unequally sized daughter cells could still be generated without appropriately oriented nuclear migrations ( Figures 2G and 2H).…”

Section: Nuclear Migrations Are Required For Proper Daughter Cell Plamentioning

confidence: 86%

“…Nuclear migrations preceding ACD are prevalent during plant development, and our work adds the Arabidopsis stomatal lineage to the compendium of cell types that utilize this mechanism. While several examples of polarity domains that guide pre-ACD nuclear migration have been described in other plant species [1,23,32], cortical BASL/BRXf's necessity and sufficiency for nuclear migrations and its role in coordinating the spatial positioning of successive ACDs are new. The use of time-lapse imaging to capture ACDs was critical, Please cite this article in press as: Muroyama et al, Opposing, Polarity-Driven Nuclear Migrations Underpin Asymmetric Divisions to Pattern Arabidopsis Stomata, Current Biology (2020), https://doi.org/10.1016/j.cub.2020.08.100…”

Section: Discussionmentioning

confidence: 99%

Opposing, Polarity-Driven Nuclear Migrations Underpin Asymmetric Divisions to Pattern Arabidopsis Stomata

2020

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Rho of Plants GTPases and Cytoskeletal Elements Control Nuclear Positioning and Asymmetric Cell Division during Physcomitrella patens Branching

Cited by 47 publications

References 50 publications

Escape from mitotic catastrophe by actin-dependent nuclear displacement in fission yeast

Escape from mitotic catastrophe by actin-dependent nuclear displacement in fission yeast

A fundamental developmental transition in Physcomitrium patens is regulated by evolutionarily conserved mechanisms

Opposing, Polarity-Driven Nuclear Migrations Underpin Asymmetric Divisions to Pattern Arabidopsis Stomata

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