Maintenance and regulation of cellular handedness in Tetrahymena

Development ◽  
1989 ◽  
Vol 105 (3) ◽  
pp. 457-471
Author(s):  
E.M. Nelsen ◽  
J. Frankel
Keyword(s):  
Positional Information ◽  
Mirror Image ◽  
Local Geometry ◽  
Preferred Direction ◽  
Left Handed ◽  
Polar Coordinate ◽  
Nuclear Events ◽  
Coordinate Model ◽  
Lh Cells ◽  
Lh Rh

The left-handed phenotype of Tetrahymena thermophila (LH) is a global mirror image of its right-handed counterpart (RH). LH cells are ‘wound’ in the opposite direction from that of RH cells with respect to the placement of all structures that are asymmetrically disposed on the cell circumference. However, the local geometry of ciliary rows, including the asymmetrically placed microtubule bands and other accessory structures, is identical in RH and LH cells. Populations of LH cells grow more slowly than those of RH cells, probably because of nutritional problems due to faulty construction of the cell mouth. LH cells, like RH cells, conjugate in a homopolar configuration, while LH cells mate with RH cells in a heteropolar union which suffices to initiate the conjugal nuclear events but is insufficient to allow survival of progeny. Subclonal analyses indicate that reversion of the LH to the RH form is relatively rare. However, the frequency of reversion is greatly increased by conditions that promote the formation of doublets by fission arrest. An analysis of intermediate doublet forms in such cultures strongly suggests that reversion takes place through a specific pathway, with LH-LH doublets regulating to LH-RH forms that then may give rise to RH singlets. The origin and fate of the LH-RH intermediate forms can be explained by applying a modified polar coordinate model of positional information with the proviso that there is a preferred direction for the intercalation of new positional values.

Regeneration in the medial-lateral axis of the insect thoracic segment

Development ◽  
1988 ◽  
Vol 102 (1) ◽  
pp. 175-192
Author(s):  
V. French ◽  
T.F. Rowlands
Keyword(s):  
Mirror Image ◽  
The Body ◽  
Dorsal Midline ◽  
Unequally Spaced ◽  
Polar Coordinate ◽  
Coordinate Model ◽  
Boundary Model ◽  
Almost All ◽  
Pattern Regulation ◽  
Lateral Axis

We have studied pattern regulation in the medial-lateral axis of the insect segment by grafting legs of beetle larvae (Tenebrio molitor) in different orientations into different positions medial and lateral to the leg site. The Boundary Model and Polar Coordinate Model of the insect appendage predict various patterns of supernumerary leg regeneration, and these grafts were designed to test the predictions. When a larval leg is grafted with normal anterior-posterior orientation medial to the normal leg, larvae and subsequent adults bear the graft plus a supernumerary leg. This is located where the lateral edge of the grafted leg confronted medial thorax (from the leg base across to the midline) and is orientated as a mirror image of the graft. The tarsal structure of supernumeraries resulting from grafts of the mesothoracic leg onto the metathorax shows that the supernumeraries may be derived from the graft, the host site or from both sources. Similarly, when a leg is grafted lateral to the leg site, a supernumerary forms at the confrontation between the medial edge of the graft and lateral thorax (from leg base across to the dorsal tergite). These results agree with the predictions of both models and would indicate that the compartments or the positional values extend out from the leg to the midline and the edge of the tergite. The two models differ in their predictions for the number, position and orientation of supernumeraries following 180 degree rotation of the grafted leg. When the rotated graft is placed lateral to the leg, larvae and adults form a single supernumerary which, in accordance with the Polar Coordinate Model, is lateral to the graft and orientated as a mirror image of it. However, the results of the corresponding medial graft cannot be readily explained by either model. Larvae form a single supernumerary either posterior or medial to the graft, suggesting a modified model with unequally spaced positional values, but the subsequent adult supernumeraries are almost all located medially. Experiments involving a graft placed medial to the leg site frequently show duplication of the adult midline suture, an extra branch forming between the thorax and the graft or supernumerary leg. In this case, as in the regeneration of the dorsal midline, the extreme medial structure is formed between two more lateral regions, which need not come from opposite sides of the body, but must have opposite mediolateral polarities. At present, no model can adequately explain all the results of grafting and extirpation on the insect ventral thorax.

A boundary model for pattern formation in vertebrate limbs

Development ◽  
1983 ◽  
Vol 76 (1) ◽  
pp. 115-137
Author(s):  
Hans Meinhardt
Keyword(s):  
Pattern Formation ◽  
Positional Information ◽  
Cell Types ◽  
Cooperative Interaction ◽  
Main Body ◽  
Polar Coordinate ◽  
Coordinate Model ◽  
Supernumerary Limbs ◽  
Boundary Model

We postulate that positional information for secondary embryonic fields is generated by a cooperative interaction between two pairs of differently determined cell types. Positional information is thus generated at the boundaries between cells of different determination. The latter are assumed to result from the primary pattern formation in the embryo. The application of this model to vertebrate limbs accounts for the pairwise determination of limbs at a particular location, with a particular handedness and alignment to the main body axes of the embryo. It accounts further for the gross difference in the regeneration of double anterior and double posterior amphibian limbs as well as for the formation of supernumerary limbs after certain graft experiments including supernumeraries in which the dorsoventral polarity changes or which consist of two anterior or two posterior halves. Our model provides a feasible molecular basis for the polar coordinate model and successfully handles recently found violations, for instance formation of supernumerary limbs after ipsilateral grafting with 90° rotation. The most frequent types of developmental malformations become explicable. The models allow specific predictions which are fully supported by recent experiments (see the accompanying paper of M. Maden).

Microsurgically generated discontinuities provoke heritable changes in cellular handedness of a ciliate, Stylonychia mytilus

Development ◽  
1991 ◽  
Vol 111 (2) ◽  
pp. 337-356
Author(s):  
X.B. Shi ◽  
Z.I. Qiu ◽  
W. He ◽  
J. Frankel
Keyword(s):  
Large Scale ◽  
Mirror Image ◽  
The Other ◽  
Left Edge ◽  
Left Handed ◽  
Specific Manner ◽  
The Right ◽  
Anteroposterior Polarity ◽  
Posterior Anterior ◽  
Stylonychia Mytilus

Stylonychia mytilus is a dorsoventrally flattened ciliate with compound ciliary structures arranged in a specific manner on the cell surface. In mirror-image (MI) doublets of this ciliate, two nearly complete sets of ciliary structures are arrayed side-by-side, one in a normal or ‘right-handed’ (RH) arrangement, the other in a reversed or ‘left-handed’ (LH) arrangement. MI-doublets exist in two forms, one with the RH component on the right, the LH component on the left, and feeding structures near the center (‘buccal-adjoining MI-doublet’); the other with the RH component on the left, the LH component on the right, and feeding structures on the lateral edges (‘buccal-opposing MI-doublet’). We describe an operation that can generate either type of MI-doublet. This operation interchanges large anterior and posterior regions of the cell, transposing the original posterior region anteriorly (P—A) and the original anterior region posteriorly (A—P), while retaining the original anteroposterior polarity of each region. Two sets of new ciliary structures then are formed in mirror-image arrangement, with the set in the P—A region oriented normally and the set in the A—P region undergoing a reversal of polarity along its anteroposterior axis. This sometimes creates end-to-end MI forms, but more commonly produces side-by-side MI-doublets through a folding together of the P—A and A—P regions. This folding occurs because one lateral edge of the cell had been removed during the operation; if the left edge was removed, the complex folds to the left and forms a buccal-adjoining MI-doublet, whereas if the right edge was removed, the complex folds to the right and forms a buccal-opposing MI-doublet. Both types can reorganize and later divide true-to-type, although the ‘buccal-opposing’ type is by far the more stable of the two. The generation of mirror-image forms is dependent on the prior abnormal juxtaposition of regions from opposite ends of the cell, and involves a coordinated respecification of large-scale organization. We interpret this response to be a consequence of intercalation of missing intervening positional values in the zone of posterior-anterior abutment.

Regeneration from duplicating fragments of the Drosophila wing disc

Development ◽  
1981 ◽  
Vol 66 (1) ◽  
pp. 117-126
Author(s):  
Jane Karlsson ◽  
R. J. Smith
Keyword(s):  
Imaginal Disc ◽  
General Rule ◽  
Wing Disc ◽  
The Other ◽  
Posterior Compartment ◽  
Drosophila Wing ◽  
Polar Coordinate ◽  
New Type ◽  
Coordinate Model

It is a general rule that of two complementary Drosophila imaginal disc fragments, one regenerates and the other duplicates. This paper reports an investigation of an exception to this rule. Duplicating fragments from the periphery of the wing disc which lacked presumptive notum were found to regenerate notum structures during and after duplication. The propensity for this was greatest in fragments lying close to the presumptive notum, with the exception of a fragment confined to the posterior compartment, which did not regenerate notum. Structures were added sequentially, and regeneration stopped once most of the notum was present. These results are not easily explained by the polar coordinate model, which states that regeneration cannot occur from duplicating fragments. Since compartments appear to be involved in this type of regeneration as in others, it is suggested that a new type of model is required, one which permits simultaneous regeneration and duplication, and assigns a major role to compartments.

Non-genic inheritance of cellular handedness

Development ◽  
1989 ◽  
Vol 105 (3) ◽  
pp. 447-456 ◽  
Author(s):  
E.M. Nelsen ◽  
J. Frankel ◽  
L.M. Jenkins
Keyword(s):  
Positional Information ◽  
Regulatory Elements ◽  
Genetic Change ◽  
Surface Structures ◽  
Phenotypic Alteration ◽  
Left Handed ◽  
A Cell ◽  
Usual Order ◽  
Genic Control ◽  
Rule Out

Ciliates exhibit an asymmetry in arrangement of surface structures around the cell which could be termed handedness. If the usual order of placement of structures defines a ‘right-handed’ (RH) cell, then a cell with this order reversed would be ‘left-handed’ (LH). Such LH forms appear to be produced in Tetrahymena thermophila through aberrant reorganization of homopolar doublets back to the singlet condition. Four clones of LH forms were selected and subjected to genetic analysis to test whether this drastic phenotypic alteration resulted from a nuclear genetic change. The results of this analysis indicate that the change in handedness is not due to a genetic change in either the micronucleus or macronucleus. The LH form can, under certain circumstances, revert to the RH form, but typically it propagates itself across both vegetative and sexual generations with similar fidelity. While this analysis does not formally rule out certain possibilities of nuclear genic control involving regulatory elements transmitted through the cytoplasm, when the circumstances of origin and propagation of the LH condition are taken into account direct cortical perpetuation seems far more likely. Here we outline a conceptual framework centred on the idea of longitudinally propagated positional information; the positive evidence supporting this idea as well as further application of the idea itself are presented in the accompanying paper.

Regeneration in the anterior—posterior axis of the insect thoracic segment

Development ◽  
1986 ◽  
Vol 98 (1) ◽  
pp. 137-165
Author(s):  
Vernon French ◽  
Tamara F. Rowlands
Keyword(s):  
Abdominal Segment ◽  
Adjacent Tissue ◽  
Local Pattern ◽  
Shortest Route ◽  
Polar Coordinate ◽  
Coordinate Model ◽  
Deletion Pattern ◽  
Boundary Model ◽  
Third Line ◽  
Anterior Posterior

After removal of a transverse strip of ventral thorax from the beetle, Tenebrio molitor, interaction occurred between epidermis posterior to the mesothoracic leg and that anterior to the metathoracic leg. Depending on the size and position of the excision, this interaction resulted in either the regeneration of the extirpated tissue or its replacement by an A/P reversed pattern of sclerites and supernumerary leg. By either route, local pattern continuity was restored between the normal meso- and metathoracic legs. Similarly, when a leg plus adjacent tissue was extirpated, continuity was restored by leg regeneration or by formation of an A/P reversed duplication of sclerites. The results of these strip excisions can be understood in terms of two current models of the ventral thorax (the Boundary Model and the Polar Coordinate Model), each of which postulates a distinct compartment or region intervening between the epidermis surrounding the bases of successive legs. However, the models do not explain the large differences in the frequency of formation of the duplication/deletion pattern after excisions of different widths. The results are also compatible with a different model, involving an A–P sequence of positional values similar to that proposed for the abdominal segment. Regeneration would restore continuity within the sequence by the shortest route, forming either the midsegment (including the leg) or the intersegmental region. The meso- and metathorax differ in the structure of the ventral sclerites and in the segmentation of the tarsus of the leg. The structures regenerated after the various excisions show that the segment border is not crossed during regeneration and indicate that an A/P compartment border running through the leg is usually also respected. There is no sign, however, of a third line of lineage restriction that would indicate a subdivision of the segment into three compartments (as proposed in the Boundary Model).

Morphology and Development of Left-Handed Singlets Derived from Mirror-Image Doublets ofStylonychia mytilus

1990 ◽  
Vol 37 (1) ◽  
pp. 14-19 ◽  
Author(s):  
XINBAI SHI ◽  
ZIJIAN QIU ◽  
LI LU ◽  
JOSEPH FRANKEL
Keyword(s):  
Mirror Image ◽  
Left Handed

Pattern formation and growth in the regenerating limbs of urodelean amphibians

Development ◽  
1981 ◽  
Vol 65 (Supplement) ◽  
pp. 19-36
Author(s):  
Nigel Holder
Keyword(s):  
Quantitative Analysis ◽  
Pattern Formation ◽  
Limb Regeneration ◽  
Polar Coordinate ◽  
Coordinate Model ◽  
Pattern Regulation

The results of numerous types of grafting experiments involving the amputation of symmetrical limbs are described. These experiments were designed to test the tenets of the polar coordinate model. The analysis of the results of these grafts coupled with a quantitative analysis of blastemal shape strongly indicates that pattern regulation during amphibian limb regeneration can be understood in terms of the model.

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