Evidence for polar positional information independent of cell division and nucleoid occlusion

In multicellular organisms, a stringent control of the transition between cell division and differentiation is crucial for correct tissue and organ development. In the Arabidopsis root, the boundary between dividing and differentiating cells is positioned by the antagonistic interaction of the hormones auxin and cytokinin. Cytokinin affects polar auxin transport, but how this impacts the positional information required to establish this tissue boundary, is still unknown. By combining computational modeling with molecular genetics, we show that boundary formation is dependent on cytokinin’s control on auxin polar transport and degradation. The regulation of both processes shapes the auxin profile in a well-defined auxin minimum. This auxin minimum positions the boundary between dividing and differentiating cells, acting as a trigger for this developmental transition, thus controlling meristem size.

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H3K9me2 orchestrates inheritance of spatial positioning of peripheral heterochromatin through mitosis

eLife ◽

10.7554/elife.49278 ◽

2019 ◽

Vol 8 ◽

Cited By ~ 10

Author(s):

Andrey Poleshko ◽

Cheryl L Smith ◽

Son C Nguyen ◽

Priya Sivaramakrishnan ◽

Karen G Wong ◽

...

Keyword(s):

Cell Division ◽

Spatial Organization ◽

Nuclear Periphery ◽

Nuclear Lamina ◽

Positional Information ◽

Specific Gene ◽

Cell Type ◽

Histone 3 ◽

Spatial Positioning ◽

Peripheral Heterochromatin

Cell-type-specific 3D organization of the genome is unrecognizable during mitosis. It remains unclear how essential positional information is transmitted through cell division such that a daughter cell recapitulates the spatial genome organization of the parent. Lamina-associated domains (LADs) are regions of repressive heterochromatin positioned at the nuclear periphery that vary by cell type and contribute to cell-specific gene expression and identity. Here we show that histone 3 lysine 9 dimethylation (H3K9me2) is an evolutionarily conserved, specific mark of nuclear peripheral heterochromatin and that it is retained through mitosis. During mitosis, phosphorylation of histone 3 serine 10 temporarily shields the H3K9me2 mark allowing for dissociation of chromatin from the nuclear lamina. Using high-resolution 3D immuno-oligoFISH, we demonstrate that H3K9me2-enriched genomic regions, which are positioned at the nuclear lamina in interphase cells prior to mitosis, re-associate with the forming nuclear lamina before mitotic exit. The H3K9me2 modification of peripheral heterochromatin ensures that positional information is safeguarded through cell division such that individual LADs are re-established at the nuclear periphery in daughter nuclei. Thus, H3K9me2 acts as a 3D architectural mitotic guidepost. Our data establish a mechanism for epigenetic memory and inheritance of spatial organization of the genome.

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Cell cycle progression, growth and patterning in imaginal discs despite inhibition of cell division after inactivation of Drosophila Cdc2 kinase

Development ◽

10.1242/dev.124.18.3555 ◽

1997 ◽

Vol 124 (18) ◽

pp. 3555-3563 ◽

Cited By ~ 20

Author(s):

K. Weigmann ◽

S.M. Cohen ◽

C.F. Lehner

Keyword(s):

Cell Division ◽

Cell Cycle Progression ◽

Positional Information ◽

Imaginal Discs ◽

Physical Distance ◽

Cdc2 Kinase ◽

Cycle Progression ◽

Mitotic Kinase ◽

Control Growth ◽

Local Cell

During larval development, Drosophila imaginal discs increase in size about 1000-fold and cells are instructed to acquire distinct fates as a function of their position. The secreted signaling molecules Wingless and Decapentaplegic have been implicated as sources of positional information that globally control growth and patterning. Evidence has also been presented that local cell interactions play an important role in controlling cell proliferation in imaginal discs. As a first step to understanding how patterning cues influence growth we investigated the effects of blocking cell division at different times and in spatially controlled manner by inactivation of the mitotic kinase Cdc2 in developing imaginal discs. We find that cell growth continues after inactivation of Cdc2, with little effect on overall patterning. The mechanisms that regulate size of the disc therefore do not function by regulating cell division, but appear to act primarily by regulating size in terms of physical distance or tissue volume.

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H3K9me2 orchestrates inheritance of spatial positioning of peripheral heterochromatin through mitosis

10.1101/678987 ◽

2019 ◽

Author(s):

Andrey Poleshko ◽

Cheryl L. Smith ◽

Son C. Nguyen ◽

Priya Sivaramakrishnan ◽

John Isaac Murray ◽

...

Keyword(s):

Cell Division ◽

Spatial Organization ◽

Nuclear Periphery ◽

Nuclear Lamina ◽

Positional Information ◽

Specific Gene ◽

Cell Type ◽

Histone 3 ◽

Spatial Positioning ◽

Peripheral Heterochromatin

AbstractCell-type-specific 3D organization of the genome is unrecognizable during mitosis. It remains unclear how essential positional information is transmitted through cell division such that a daughter cell recapitulates the spatial genome organization of the parent. Lamina-associated domains (LADs) are regions of repressive heterochromatin positioned at the nuclear periphery that vary by cell type and contribute to cell-specific gene expression and identity. Here we show that histone 3 lysine 9 dimethylation (H3K9me2) is an evolutionarily conserved, specific mark of nuclear peripheral heterochromatin and that it is retained through mitosis. During mitosis, phosphorylation of histone 3 serine 10 temporarily shields the H3K9me2 mark allowing for dissociation of chromatin from the nuclear lamina. Using high-resolution 3D immuno-oligoFISH, we demonstrate that H3K9me2-enriched genomic regions, which are positioned at the nuclear lamina in interphase cells prior to mitosis, re-associate with the forming nuclear lamina before mitotic exit. The H3K9me2 modification of peripheral heterochromatin ensures that positional information is safeguarded through cell division such that individual LADs are re-established at the nuclear periphery in daughter nuclei. Thus, H3K9me2 acts as a 3D architectural mitotic guidepost. Our data establish a mechanism for epigenetic memory and inheritance of spatial organization of the genome.

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Positional information and pattern regulation in hydra: the effect of γ-radiation

Development ◽

10.1242/dev.30.3.741 ◽

1973 ◽

Vol 30 (3) ◽

pp. 741-752

Author(s):

J. Hicklin ◽

L. Wolpert

Keyword(s):

Cell Division ◽

Positional Information ◽

Γ Irradiation ◽

Γ Radiation ◽

Head Formation ◽

High Doses ◽

Mitotic Figures ◽

Pattern Regulation

Hydra exposed to high doses of γ-irradiation (25000 rad) are still capable of regeneration although no normal mitotic figures could be seen for up to 48 h after irradiation. Irradiated heads could still inhibit head formation in other regions in graft combinations. The time for head end determination in irradiated animals appeared to be increased. It is concluded that head end regeneration need not involve cell division.

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The evolutionary origin of development: cycles, patterning, privilege and continuity

Development ◽

10.1242/dev.1994.supplement.79 ◽

1994 ◽

Vol 1994 (Supplement) ◽

pp. 79-84

Author(s):

L. Wolpert

Keyword(s):

Cell Division ◽

Asymmetric Cell Division ◽

Positional Information ◽

Cell Types ◽

Eukaryotic Cell ◽

Cytoplasmic Localization ◽

Baldwin Effect ◽

Continuity Principle ◽

Primitive Condition ◽

The Baldwin Effect

A scenario for the evolution of a simple spherical multicellular organism from a single eukaryotic cell is proposed. Its evolution is based on environmentally induced alterations in the cell cycle, which then, by the Baldwin effect, become autonomous. Further patterning of this primitive organism - a Blastaea, could again involve environmentally induced signals like contact with the substratum, which could then become autonomous, by, perhaps, cytoplasmic localization and asymmetric cell division. Generating differences between cells based on positional information is probably very primitive, and is well conserved; its relation to asymmetric cell division is still unclear. Differentiation of new cell types can arise from non equivalence and gene duplication. Periodicity also evolved very early on. The origin of gastrulation may be related to mechanisms of feeding. The embryo may be evolutionarily privileged and this may facilitate the evolution of novel forms. Larvae are secondarily derived and direct development is the primitive condition as required by the continuity principle.

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The role of targeted secretion in the establishment of cell polarity and the orientation of the division plane in Fucus zygotes

Development ◽

10.1242/dev.122.9.2623 ◽

1996 ◽

Vol 122 (9) ◽

pp. 2623-2630 ◽

Cited By ~ 4

Author(s):

S.L. Shaw ◽

R.S. Quatrano

Keyword(s):

Cell Wall ◽

Cell Division ◽

Cell Polarity ◽

Polar Axis ◽

Positional Information ◽

Target Site ◽

Polar Growth ◽

Division Plane ◽

Axis Fixation

In this study, we investigate the role of polar secretion and the resulting asymmetry in the cell wall in establishing polarity in Fucus zygotes. We have utilized brefeldin-A to selectively interrupt secretion of Golgi-derived material into the cell wall as assayed by toluidine blue O staining of sulfated fucoidin. We show that the polar secretion of Golgi-derived material is targeted to a cortical site of the zygote identified by the localization of actin filaments and dihydropyridine receptors. The deposition of Golgi-derived material into the cell wall at this target site is temporally coincident with and required for polar axis fixation. We propose that local secretion of Golgi-derived material into the cell wall transforms the target site into the fixed site of polar growth. We also found that polar secretion of Golgi-derived material at the fixed site is essential for growth and differentiation of the rhizoid, as well as for the proper positioning of the first plane of cell division. We propose that the resulting asymmetry in the cell wall serves as positional information for the underlying cortex to initiate these polar events. Our data supports the hypothesis that cell wall factors in embryos, previously shown to be responsible for induction of rhizoid cell differentiation, are deposited simultaneously with and are responsible for polar axis fixation. Furthermore, the pattern of polar growth is attributable to a positional signal at the fixed site and appears to be independent of the orientation of the first cell division plane. Thus, the establishment of zygotic cell polarity and not the position of the first division plane, is critical for the formation of the initial embryonic pattern in Fucus.

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Xcl1 causes delayed oblique periclinal cell divisions in developing maize leaves, leading to cellular differentiation by lineage instead of position

Development ◽

10.1242/dev.129.8.1859 ◽

2002 ◽

Vol 129 (8) ◽

pp. 1859-1869 ◽

Cited By ~ 1

Author(s):

Sharon Kessler ◽

Sumer Seiki ◽

Neelima Sinha

Keyword(s):

Cell Division ◽

Gene Product ◽

Cellular Differentiation ◽

Plant Cells ◽

Positional Information ◽

Mutant Phenotype ◽

Cell Divisions ◽

Maize Leaves ◽

Cell Layers ◽

Normal Gene

Differentiation of plant cells is regulated by position-dependent mechanisms rather than lineage. The maize Extra cell layers1 (Xcl1) mutation causes oblique, periclinal divisions to occur in the protoderm layer. These protodermal periclinal divisions occur at the expense of normal anticlinal divisions and cause the production of extra cell layers with epidermal characteristics, indicating that cells are differentiating according to lineage instead of position. Mutant kernels have several aleurone layers instead of one, indicating that Xcl1 alters cell division orientation in cells that divide predominantly in the anticlinal plane. Dosage analysis of Xcl1 reveals that the mutant phenotype is caused by overproduction of a normal gene product. This allows cells that have already received differentiation signals to continue to divide in aberrant planes and suggests that the timing of cell division determines differentiation. Cells that divide early and in the absence of differentiation signals use positional information, while cells that divide late after perceiving differentiation signals use lineage information instead of position.

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Ethylene provides positional information on cortical cell division but is not involved in Nod factor-induced root hair tip growth in Rhizobium-legume interaction

Development ◽

10.1242/dev.124.9.1781 ◽

1997 ◽

Vol 124 (9) ◽

pp. 1781-1787 ◽

Cited By ~ 1

Author(s):

R. Heidstra ◽

W.C. Yang ◽

Y. Yalcin ◽

S. Peck ◽

A.M. Emons ◽

...

Keyword(s):

Cell Division ◽

Root Hair ◽

Rhizobium Leguminosarum ◽

Tip Growth ◽

Cortical Cell ◽

Acc Oxidase ◽

Positional Information ◽

Nod Factors ◽

Nod Factor ◽

Root Hair Deformation

Nod factors secreted by Rhizobium leguminosarum bv. viciae induce root hair deformation, involving a reinitiation of tip growth, and the formation of nodule primordia in Vicia sativa (vetch). Ethylene is a potent inhibitor of cortical cell division, an effect that can be counteracted by applying silver ions (Ag+) or aminoethoxy-vinylglycine (AVG). In contrast to the inhibitory effect on cortical cell division, ethylene promotes the formation of root hairs (which involves tip growth) in the root epidermis of Arabidopsis. We investigate the possible paradox concerning the action of ethylene, putatively promoting Nod factor induced tip growth whilst, at the same time, inhibiting cortical cell division. We show, by using the ethylene inhibitors AVG and Ag+, that ethylene has no role in the reinitiation of root hair tip growth induced by Nod factors (root hair deformation) in vetch. However, root hair formation is controlled, at least in part, by ethylene. Furthermore, we show that ACC oxidase, which catalizes the last step in ethylene biosynthesis, is expressed in the cell layers opposite the phloem in that part of the root where nodule primordia are induced upon inoculation with Rhizobium. Therefore, we test whether endogenously produced ethylene provides positional information controlling the site where nodule primordia are formed by determining the position of nodules formed on pea roots grown in the presence of AVG or Ag+.

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Reconstitution of self-organizing protein gradients as spatial cues in cell-free systems

eLife ◽

10.7554/elife.03949 ◽

2014 ◽

Vol 3 ◽

Cited By ~ 86

Author(s):

Katja Zieske ◽

Petra Schwille

Keyword(s):

Cell Division ◽

Protein Concentration ◽

Spatial Organization ◽

Positional Information ◽

Intracellular Protein ◽

Spatial Cues ◽

Protein Patterns ◽

Division Site ◽

Soft Polymer ◽

Protein Gradients

Intracellular protein gradients are significant determinants of spatial organization. However, little is known about how protein patterns are established, and how their positional information directs downstream processes. We have accomplished the reconstitution of a protein concentration gradient that directs the assembly of the cell division machinery in E.coli from the bottom-up. Reconstituting self-organized oscillations of MinCDE proteins in membrane-clad soft-polymer compartments, we demonstrate that distinct time-averaged protein concentration gradients are established. Our minimal system allows to study complex organizational principles, such as spatial control of division site placement by intracellular protein gradients, under simplified conditions. In particular, we demonstrate that FtsZ, which marks the cell division site in many bacteria, can be targeted to the middle of a cell-like compartment. Moreover, we show that compartment geometry plays a major role in Min gradient establishment, and provide evidence for a geometry-mediated mechanism to partition Min proteins during bacterial development.

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