Kinesin-13 and Kinesin-8 Function during Cell Growth and Division in the Moss <i>Physcomitrella patens</i>

Leong, Shu Yao; Edzuka, Tomoya; Goshima, Gohta; Yamada, M.

doi:10.1105/tpc.19.00521

Cited by 26 publications

(15 citation statements)

References 76 publications

(129 reference statements)

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“…While the physiological significance of these movements is unclear, studies in P. patens have identified microtubule motor proteins that mediate these nuclear migration events. Specifically, kinesin-14 drives basal movements (Yamada and Goshima, 2018), while kinesin-13 drives apical nuclear movement during prophase (Leong et al, 2020). Mutations in these motor proteins resulted in exaggerated movements in the opposite direction rather than a stationary nucleus, indicating that nuclear movement results from a balance of forces.…”

Section: Discussionmentioning

confidence: 99%

“…The average instantaneous velocity of the nucleus in ∆sabre was expectedly smaller, since the cells were not always actively growing ( Figure 6F). Given that SABRE influences the ER and that the nuclear envelope is contiguous with the ER, defects in nuclear migration likely result from altered ER function and suggest that SABRE may provide a link between the nuclear envelope and motors responsible for nuclear migration (Leong et al, 2020;Yamada and Goshima, 2018).…”

Section: Loss Of Sabre Impacts Er Morphology In the Cytoplasm During mentioning

confidence: 99%

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SABRE populates ER domains essential for cell plate maturation and cell expansion influencing cell and tissue patterning

Cheng

Bezanilla

2020

Preprint

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The SABRE protein, originally identified in plants, is found throughout eukaryotes. In plants, SABRE has been implicated in cell expansion, division plane orientation and planar polarity. However, how SABRE mediates these processes remains an open question. Here, we have taken advantage of the fact that the bryophyte Physcomitrium patens has a single copy of SABRE, is an excellent model for cell biology and is readily amenable to precise genetic alterations to investigate SABRE’s mechanism of action. We discovered that SABRE null mutants were stunted in both polarized growing and diffusely growing tissues, similar to reported phenotypes in seed plants. However, in polarized growing cells, we observed significant delays in cell plate formation and sometimes catastrophic failures in cell division. We generated a functional SABRE fluorescent fusion protein and determined that it forms dynamic puncta on regions of the endoplasmic reticulum (ER) both in the cytoplasm during interphase and at the new cell plate during division. In the absence of SABRE, ER morphology was severely compromised with large aggregates accumulating in the cytoplasm and abnormal buckling along the developing cell plate late in cytokinesis. In fact, SABRE and the ER maximally accumulated on the developing plate specifically during cell plate maturation, coincident with the timing of the onset of failures in cell plate formation in cells lacking SABRE. Further we discovered that callose deposition is delayed in Δsabre cells, and in cells that failed to divide, abnormal callose accumulations formed at the cell plate. Our findings demonstrated that SABRE functions by influencing the ER and callose deposition, revealing a surprising and essential role for the ER in cell plate maturation. Given that SABRE is conserved, understanding how SABRE influences cell and tissue patterning has profound significance across eukaryotes.

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Section: Discussionmentioning

confidence: 99%

Section: Loss Of Sabre Impacts Er Morphology In the Cytoplasm During mentioning

confidence: 99%

SABRE populates ER domains essential for cell plate maturation and cell expansion influencing cell and tissue patterning

Cheng

Bezanilla

2020

Preprint

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“…Select motors are labelled. Values were obtained from: kinesin-1, 35,38,51,77,79,85,[109][110][111][112][113][114] kinesin-3, 32,35,38,79,110,112,113,[115][116][117][118][119][120][121] kinesin-5, 40,67,68,111,[122][123][124][125][126][127][128][129][130][131] kinesin-8, 51,53,69,85,93,94,97,[132][133][134][135]…”

Section: Conflict Of Interest Statementmentioning

confidence: 99%

These motors were made for walking

Hunter

Allingham

2020

Protein Science

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Kinesins are a diverse group of ATP-dependent motor proteins that transport cargos along microtubules (MTs) and change the organization of MT networks. Shared among all kinesins is a ~ 40 kDa motor domain that has evolved an impressive assortment of motility and MT remodeling mechanisms as a result of subtle tweaks and edits within its sequence.Several elegant studies of different kinesin isoforms have exposed the purpose of structural changes in the motor domain as it engages and leaves the MT. However, few studies have compared the sequences and MT contacts of these kinesins systematically. Along with clever strategies to trap kinesin-tubulin complexes for X-ray crystallography, new advancements in cryo-electron microscopy have produced a burst of high-resolution structures that show kinesin-MT interfaces more precisely than ever. This review considers the MT interactions of kinesin subfamilies that exhibit significant differences in speed, processivity, and MT remodeling activity. We show how their sequence variations relate to their tubulin footprint and, in turn, how this explains the molecular activities of previously characterized mutants. As more high-resolution structures become available, this type of assessment will quicken the pace toward establishing each kinesin's designfunction relationship.

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“…Microtubule motor proteins that mediate these nuclear movements during cell division have been identified in P. patens . Kinesin-14 drives basal movements ( Yamada and Goshima, 2018 ), and kinesin-13 drives apical nuclear movement during prophase ( Leong et al, 2020 ). Mutations in these motor proteins resulted in exaggerated movements in the opposite direction rather than a stationary nucleus, indicating that nuclear movement results from a balance of forces.…”

Section: Discussionmentioning

confidence: 99%

SABRE populates ER domains essential for cell plate maturation and cell expansion influencing cell and tissue patterning

Cheng

Bezanilla

2021

eLife

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SABRE, which is found throughout eukaryotes and was originally identified in plants, mediates cell expansion, division plane orientation and planar polarity in plants. How and where SABRE mediates these processes remain open questions. We deleted SABRE in Physcomitrium patens, an excellent model for cell biology. SABRE null mutants were stunted, similar to phenotypes in seed plants. Additionally, polarized growing cells were delayed in cytokinesis, sometimes resulting in catastrophic failures. A functional SABRE fluorescent fusion protein localized to dynamic puncta on regions of the ER during interphase and at the cell plate during cell division. Without SABRE, cells accumulated ER aggregates and the ER abnormally buckled along the developing cell plate. Notably, callose deposition was delayed in Δsabre, and in cells that failed to divide, abnormal callose accumulations formed at the cell plate. Our findings revealed a surprising and fundamental role for the ER in cell plate maturation.

show abstract

Kinesin-13 and Kinesin-8 Function during Cell Growth and Division in the Moss Physcomitrella patens

Cited by 26 publications

References 76 publications

SABRE populates ER domains essential for cell plate maturation and cell expansion influencing cell and tissue patterning

SABRE populates ER domains essential for cell plate maturation and cell expansion influencing cell and tissue patterning

These motors were made for walking

SABRE populates ER domains essential for cell plate maturation and cell expansion influencing cell and tissue patterning

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