Dividing without centrioles: innovative plant microtubule organizing centres organize mitotic spindles in bryophytes, the earliest extant lineages of land plants

Brown, Roy C.; Lemmon, Betty E.

doi:10.1093/aobpla/plr028

Cited by 21 publications

(24 citation statements)

References 29 publications

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“…Notably, in liverworts, two aster-like structures, called polar organizers, emerge on opposite sides of the nucleus before the PPB appearance (i.e., independent of the PPB function) (44)(45)(46)(47). Although not experimentally addressed, it is tempting to speculate that polar organizers also function as the main determinants of spindle orientation in liverworts.…”

Section: Discussionmentioning

confidence: 99%

Cytoplasmic MTOCs control spindle orientation for asymmetric cell division in plants

Kosetsu

Murata

Yamada

et al. 2017

Proc. Natl. Acad. Sci. U.S.A.

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Proper orientation of the cell division axis is critical for asymmetric cell divisions that underpin cell differentiation. In animals, centrosomes are the dominant microtubule organizing centers (MTOC) and play a pivotal role in axis determination by orienting the mitotic spindle. In land plants that lack centrosomes, a critical role of a microtubular ring structure, the preprophase band (PPB), has been observed in this process; the PPB is required for orienting (before prophase) and guiding (in telophase) the mitotic apparatus. However, plants must possess additional mechanisms to control the division axis, as certain cell types or mutants do not form PPBs. Here, using live imaging of the gametophore of the moss Physcomitrella patens, we identified acentrosomal MTOCs, which we termed "gametosomes," appearing de novo and transiently in the prophase cytoplasm independent of PPB formation. We show that gametosomes are dispensable for spindle formation but required for metaphase spindle orientation. In some cells, gametosomes appeared reminiscent of the bipolar MT "polar cap" structure that forms transiently around the prophase nucleus in angiosperms. Specific disruption of the polar caps in tobacco cells misoriented the metaphase spindles and frequently altered the final division plane, indicating that they are functionally analogous to the gametosomes. These results suggest a broad use of transient MTOC structures as the spindle orientation machinery in plants, compensating for the evolutionary loss of centrosomes, to secure the initial orientation of the spindle in a spatial window that allows subsequent fine-tuning of the division plane axis by the guidance machinery.H ow do plants set their spindle division axis without centrosomes? In many angiosperm cell types, the cortical microtubules (MTs) are reorganized in G2 phase into a MT-based ring structure, the preprophase band (PPB), which encircles the nucleus at the cell cortex and represents a unique and key structure for oriented divisions in plants (1, 2). The PPB gradually degenerates during prophase. However, it defines the future division zone by recruiting a specific set of proteins to the cortex (3-8). During telophase, the phragmoplast, the postanaphase mitotic apparatus that recruits membrane and cell plate material for cytokinesis, centrifugally expands toward the cell cortex and strikingly precisely reaches the zone that the PPB formerly occupied. In addition to this "phragmoplast guidance" function, the PPB also sets initial spindle orientation. During degeneration of the PPB, nuclear envelope (NE)-associated MT structures, called polar caps, are formed on the opposite sides of the nucleus, perpendicular to the plane of the PPB (this structure is also called prospindle or prophase spindle) (9-12). Arabidopsis cell lines that do not assemble PPBs fail to establish these caps, indicating a critical role of the PPB in initial spindle orientation (9). However, whether initial spindle orientation by the PPB is critical for division plane determination i...

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Section: Discussionmentioning

confidence: 99%

Cytoplasmic MTOCs control spindle orientation for asymmetric cell division in plants

Kosetsu

Murata

Yamada

et al. 2017

Proc. Natl. Acad. Sci. U.S.A.

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“…This suggests that the micronucleus in M154 is unable to form minispindles, resulting in their being incorporated into daughter nuclei or assimilated into the cytoplasm instead of forming microcytes. The microtubule-organising centre (MTOC) plays an important role in the microtubule nucleation and spindle organisation of plants (Brown and Lemmon 2011;Wasteneys 2002). Moreover, kinetochores seem to be necessary to generating a bipolar spindle (McKim and Hawley 1995;Yu et al 2000).…”

Section: Discussionmentioning

confidence: 99%

Pollen variation as a response to hybridisation in Populus L. section Aigeiros Duby

et al. 2015

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Interspecific hybrids often produce extensive gametic variation due to poor chromosome pairing and unbalanced chromosome segregation. To elucidate the influence of interspecific hybridisation on pollen variation in Populus L., we compared pollen size among three P. deltoides Marsh. clones, two P. nigra L. clones, and three P. deltoides 9 P. nigra hybrids and investigated the cytological mechanism of pollen variation by observing meiotic chromosome behaviour and microtubules. The frequency of shrunken and unstainable pollen grains was higher in the hybrids (15.54-57.28 %) than in the non-hybrid clones (0.98-4.82 %). The distribution of stained pollen size ranged more broadly in the hybrids than in the non-hybrids, suggesting that hybridisation increases pollen size variation. Precocious chromosome migration and lagging chromosomes were common in the hybrids, indicating poor chromosome pairing. Some micronuclei formed minispindles in metaphase II and emanated secondary nuclear-based radial microtubule systems in telophase II, undergoing cytokinesis to develop into microcytes in the meiotic products. Eliminated micronuclei might result in the formation of aneuploid pollen. The frequency of sporads with microcytes was higher in the hybrids (3.19-11.08 %) than in the non-hybrids (0-0.94 %). Disoriented spindles, including fused and tripolar spindles, led to the formation of dyads and triads, contributing to unreduced pollen production. These results provide new insights into the gametic variation of Populus interspecific hybrids and reveal several 2n pollen producers, which will be valuable in polyploid breeding of the section Aigeiros Duby.

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“…In moss, conversely, PO-like structures have not been observed; instead, MTs are enriched around the nuclear envelope in prophase. These MTs emanating from the nuclear envelope represent the major source of prometaphase spindles, similar to Haemanthus [15,17]. In the hornwort, MTOCs are associated with plastids [15,39].…”

Section: Microscopic Overview Of the Spindle Assemblymentioning

confidence: 99%

“…These MTs emanating from the nuclear envelope represent the major source of prometaphase spindles, similar to Haemanthus [15,17]. In the hornwort, MTOCs are associated with plastids [15,39]. Despite the apparent differences in the earliest phase of spindle assembly, the morphology of the metaphase spindle of bryophytes is similar to that of Haemanthus endosperm, suggesting that a similar molecular factor is involved in the spindle assembly process during the prometaphase [15].…”

Section: Microscopic Overview Of the Spindle Assemblymentioning

confidence: 99%

Mitotic Spindle Assembly in Land Plants: Molecules and Mechanisms

Yamada

Goshima

2017

Biology

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In textbooks, the mitotic spindles of plants are often described separately from those of animals. How do they differ at the molecular and mechanistic levels? In this chapter, we first outline the process of mitotic spindle assembly in animals and land plants. We next discuss the conservation of spindle assembly factors based on database searches. Searches of >100 animal spindle assembly factors showed that the genes involved in this process are well conserved in plants, with the exception of two major missing elements: centrosomal components and subunits/regulators of the cytoplasmic dynein complex. We then describe the spindle and phragmoplast assembly mechanisms based on the data obtained from robust gene loss-of-function analyses using RNA interference (RNAi) or mutant plants. Finally, we discuss future research prospects of plant spindles.

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Dividing without centrioles: innovative plant microtubule organizing centres organize mitotic spindles in bryophytes, the earliest extant lineages of land plants

Abstract: Triple staining of γ-tubulin, microtubules, and nuclei reveal that three types of MTOCs initiate spindles in bryophytes. Polar organizers in liverworts and plastid MTOCs in hornworts are unique and nuclear envelope MTOCs in mosses appear like those in seed plants.

Cited by 21 publications

References 29 publications

Cytoplasmic MTOCs control spindle orientation for asymmetric cell division in plants

Cytoplasmic MTOCs control spindle orientation for asymmetric cell division in plants

Pollen variation as a response to hybridisation in Populus L. section Aigeiros Duby

Mitotic Spindle Assembly in Land Plants: Molecules and Mechanisms

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