Mathematical model of polar auxin transport

Polar auxin transport can be simulated by a model which achieves polarity through the preferential secretion of more auxin from the lower end than from the upper end of each cell. Solution of the model using a computer provides a possible explanation of the differences between the polarity expressed by different tissues and the differences between pieces of different lengths, on the basis of small differences in the polarity of auxin secretion from individual cells. A method of estimating the polarity of individual cells is described.     

The Electrical Control of Growth in Plant Tissue 7

Goldsworthy, A. and Rathore, K. S. 1985. The electrical controlof growth in plant tissue cultures: The polar transport of auxin.—J.exp. Bot. 36: 1134–1141. The reasons for a many-fold stimulation of shoot formation anda 60–70% stimulation of growth in tobacco callus causedby passing a very weak electric current (1 or 2 µA) betweenthe callus and the culture medium have been investigated. Thestimulation of callus growth occurred only when the callus wasmade negative to the medium and then only when IAA was added.It was abolished, even in the presence of IAA, by the additionof TIBA which is an inhibitor of polar auxin transport, andalso when the IAA was substituted by either IAN or the syntheticauxin 2,4-D, neither of which show significant polar transport.This suggests that the electrical treatment may have alignedthe physiological polarities of the callus cells so as to promotethe polar transport of IAA into the tissue when the callus wasnegative to the medium. If so, the enhanced shoot formationmay have been due to the parallel orientation of the growthaxes of individual cells so as to make the production of organformingmeristems more likely. The mechanism of the effect and its relationshipto the natural forces controlling differentiation is discussed. Key words: —Auxin, electrophysiology, polarity, tissue-culture, tobacco, transport     

Long-range coordination of planar polarity in Drosophila

The mechanisms by which cells become polarised in the plane of an epithelium have been studied in Drosophila for many years. Work has focussed on two key questions: firstly, how individual cells adopt a defined polarity, and secondly how the polarity of each cell within a tissue is aligned with its neighbours. It has been established that asymmetric subcellular localisation of a number of polarity proteins is an essential mechanism underlying polarisation of single cells. The process by which this polarity is coordinated between cells however is less well understood, but is thought to involve gradients of activity of the atypical cadherins Dachsous and Fat. Subsequently, this long-range polarity signal is refined by local cell-cell interactions involving the transmembrane molecules Frizzled, Strabismus and Flamingo. The role of these factors in coordinating polarity will be discussed.     

Rac1 orientates epithelial apical polarity through effects on basolateral laminin assembly

Cellular polarization involves the generation of asymmetry along an intracellular axis. In a multicellular tissue, the asymmetry of individual cells must conform to the overlying architecture of the tissue. However, the mechanisms that couple cellular polarization to tissue morphogenesis are poorly understood. Here, we report that orientation of apical polarity in developing Madin-Darby canine kidney (MDCK) epithelial cysts requires the small GTPase Rac1 and the basement membrane component laminin. Dominant-negative Rac1 alters the supramolecular assembly of endogenous MDCK laminin and causes a striking inversion of apical polarity. Exogenous laminin is recruited to the surface of these cysts and rescues apical polarity. These findings implicate Rac1-mediated laminin assembly in apical pole orientation. By linking apical orientation to generation of the basement membrane, epithelial cells ensure the coordination of polarity with tissue architecture.     

Ups and downs of tissue and planar polarity in plants

The polar orientation of cells within a tissue is an intensively studied research area in animal cells. The term planar polarity refers to the common polar arrangement of cells within the plane of an epithelium. In plants, the subcellular analysis of tissue polarity has been limited by the lack of appropriate markers. Recently, research on plant tissue polarity has come of age. Advances are based on studies of Arabidopsis patterning, cell polarity and auxin transport mutants employing the coordinated, polar localization of auxin transporters and the planar polarity of root epidermal hairs as markers. These approaches have revealed auxin transport and response, vesicular trafficking, membrane sterol and cytoskeletal requirements of tissue polarity. This review summarizes recent progress in research on vascular tissue and planar epidermal polarity in the Arabidopsis root and compares it to findings on planar polarity in animals and cell polarity in yeast.     

Cell polarity, auxin transport, and cytoskeleton-mediated division planes: who comes first?

In plants, cell polarity is an issue more recurring than in other systems, because plants, due to their adaptive and flexible development, often change cell polarity postembryonically according to intrinsic cues and demands of the environment. Recent findings on the directional movement of the plant signalling molecule auxin provide a unique connection between individual cell polarity and the establishment of polarity at the tissue, organ, and whole-plant levels. Decisions about the subcellular polar targeting of PIN auxin transport components determine the direction of auxin flow between cells and consequently mediate multiple developmental events. In addition, mutations or chemical interference with PIN-based auxin transport result in abnormal cell divisions. Thus, the complicated links between cell polarity establishment, auxin transport, cytoskeleton, and oriented cell divisions now begin to emerge. Here we review the available literature on the issues of cell polarity in both plants and animals to extend our understanding on the generation, maintenance, and transmission of cell polarity in plants.     

Insect epidermis: disturbance of supracellular tissue polarity does not prevent the expression of cell polarity

Summary The insect integument displays planar tissue polarity in the uniform orientation of polarized cuticular structures. In a body segment, for example, the denticles and bristles produced by the constituent epidermal cells point posteriorly. Colchicine can abolish this uniform orientation while still allowing individual cells to form orientated cuticular structures and thereby to express cell polarity. This suggests that an individual cell in a sheet can establish planar polarity without reference to some kind of covert supracellular cue (such as a morphogen gradient) in the epidermis as a whole. The results also indicate that colchicine interferes — directly or indirectly — with the mechanisms involved in aligning the polarity axes of individual cells into a common orientation, thereby generating supracellular or tissue polarity.     

Overgrowth of Douglas fir (Pseudotsuga menziesii Franco) stumps with regenerative tissue as an example of cell ordering and tissue reorganization

Main conclusion

Stump overgrowth may serve as a unique model for studying cellular reorganization and mechanisms responsible for cell polarity changes during the process of vascular tissue differentiation from initially unorganized parenchymatous cells. Cellular ordering and tissue reorganization during the overgrowth process of the transverse surfaces of Douglas fir stumps in forest stand was studied. At the beginning of stump overgrowth, the produced parenchymatous cells form an unorganized tissue. Particular parenchyma cells start arranging into more ordered structures which resemble rays. Application of digital image analysis software based on structure tensor was used. The analysis showed that at this stage of tissue development, cellular elements display a wide range of angular orientation values and attain very low coherency coefficients. The progress of the tissue differentiation process is associated with the formation of local regions with tracheids oriented circularly around the rays. This coincides with an increase in the range of angular orientations and greater values of coherency coefficients. At the most advanced stage of tissue development, with tracheids arranged parallelly in longitudinal strands, the degree of cell ordering is the highest what is manifested by the greatest values attained by coherency coefficients, and the narrow range of angular orientations. It is suggested that the ray-like structures could act as organizing centers in the morphogenetic field responsible for differentiation of the overgrowth tissue. The circular pattern of tracheids around rays in the initial phase of tissue development can be interpreted in terms of local rotation of the morphogenetic field which afterward is transformed into irrotational field. This transformation is noted by the presence of tracheids arranged parallelly in longitudinal strands. The possible involvement of a mechanism controlling cell polarity with respect to auxin transport is discussed.     

Kif3a regulates planar polarization of auditory hair cells through both ciliary and non-ciliary mechanisms

Auditory hair cells represent one of the most prominent examples of epithelial planar polarity. In the auditory sensory epithelium, planar polarity of individual hair cells is defined by their V-shaped hair bundle, the mechanotransduction organelle located on the apical surface. At the tissue level, all hair cells display uniform planar polarity across the epithelium. Although it is known that tissue planar polarity is controlled by non-canonical Wnt/planar cell polarity (PCP) signaling, the hair cell-intrinsic polarity machinery that establishes the V-shape of the hair bundle is poorly understood. Here, we show that the microtubule motor subunit Kif3a regulates hair cell polarization through both ciliary and non-ciliary mechanisms. Disruption of Kif3a in the inner ear led to absence of the kinocilium, a shortened cochlear duct and flattened hair bundle morphology. Moreover, basal bodies are mispositioned along both the apicobasal and planar polarity axes of mutant hair cells, and hair bundle orientation was uncoupled from the basal body position. We show that a non-ciliary function of Kif3a regulates localized cortical activity of p21-activated kinases (PAK), which in turn controls basal body positioning in hair cells. Our results demonstrate that Kif3a-PAK signaling coordinates planar polarization of the hair bundle and the basal body in hair cells, and establish Kif3a as a key component of the hair cell-intrinsic polarity machinery, which acts in concert with the tissue polarity pathway.     

Quantification of nematic cell polarity in three-dimensional tissues

How epithelial cells coordinate their polarity to form functional tissues is an open question in cell biology. Here, we characterize a unique type of polarity found in liver tissue, nematic cell polarity, which is different from vectorial cell polarity in simple, sheet-like epithelia. We propose a conceptual and algorithmic framework to characterize complex patterns of polarity proteins on the surface of a cell in terms of a multipole expansion. To rigorously quantify previously observed tissue-level patterns of nematic cell polarity (Morales-Navarrete et al., eLife 2019), we introduce the concept of co-orientational order parameters, which generalize the known biaxial order parameters of the theory of liquid crystals. Applying these concepts to three-dimensional reconstructions of single cells from high-resolution imaging data of mouse liver tissue, we show that the axes of nematic cell polarity of hepatocytes exhibit local coordination and are aligned with the biaxially anisotropic sinusoidal network for blood transport. Our study characterizes liver tissue as a biological example of a biaxial liquid crystal. The general methodology developed here could be applied to other tissues and in-vitro organoids.     

Misshapen decreases integrin levels to promote epithelial motility and planar polarity in Drosophila

Complex organ shapes arise from the coordinate actions of individual cells. The Drosophila egg chamber is an organ-like structure that lengthens along its anterior–posterior axis as it grows. This morphogenesis depends on an unusual form of planar polarity in the organ’s outer epithelial layer, the follicle cells. Interestingly, this epithelium also undergoes a directed migration that causes the egg chamber to rotate around its anterior–posterior axis. However, the functional relationship between planar polarity and migration in this tissue is unknown. We have previously reported that mutations in the Misshapen kinase disrupt follicle cell planar polarity. Here we show that Misshapen’s primary role in this system is to promote individual cell motility. Misshapen decreases integrin levels at the basal surface, which may facilitate detachment of each cell’s trailing edge. These data provide mechanistic insight into Misshapen’s conserved role in cell migration and suggest that follicle cell planar polarity may be an emergent property of individual cell migratory behaviors within the epithelium.     

Polarity proteins are required for left-right axis orientation and twin-twin instruction

Two main classes of models address the earliest steps of left-right patterning: those postulating that asymmetry is initiated via cilia-driven fluid flow in a multicellular tissue at gastrulation, and those postulating that asymmetry is amplified from intrinsic chirality of individual cells at very early embryonic stages. A recent study revealed that cultured human cells have consistent left-right (LR) biases that are dependent on apical-basal polarity machinery. The ability of single cells to set up asymmetry suggests that cellular chirality could be converted to embryonic laterality by cilia-independent polarity mechanisms in cell fields. To examine the link between cellular polarity and LR patterning in a vertebrate model organism, we probed the roles of apical-basal and planar polarity proteins in the orientation of the LR axis in Xenopus. Molecular loss-of-function targeting these polarity pathways specifically randomizes organ situs independently of contribution to the ciliated organ. Alterations in cell polarity also disrupt tight junction integrity, localization of the LR signaling molecule serotonin, the normally left-sided expression of Xnr-1, and the LR instruction occurring between native and ectopic organizers. We propose that well-conserved polarity complexes are required for LR asymmetry and that cell polarity signals establish the flow of laterality information across the early blastoderm independently of later ciliary functions. genesis 50:219-234, 2012. ? 2011 Wiley Periodicals, Inc.     

A role of microtubules during the formation of cell processes in neuronal and non-neuronal cells

This review discusses the role of microtubules in the formation of processes from neuronal and non-neuronal cells. In elongating axons of the neuron, tubulin molecules are transported toward the end of pre-existing microtubules, which may be nucleated at the centrosome, via a mechanism called slow axonal flow. Two different hypotheses are presented to explain this mechanism; the transport of soluble monomers and/or oligomers versus the transport of polymerized microtubules. The majority of tubulin seems to be transported as small oligomers as shown by the data presented so far. Alternatively, an active transport of polymerized microtubules driven by microtubule-based motor proteins is postulated as being responsible for the non-uniform polarity of microtubule bundles in dendrites of the neuron. Microtubule-associated proteins (MAPs) play a crucial role in stabilizing the microtubular arrays, whereas the non-uniform polarity of microtubules may be established with the aid of microtubule-based motor proteins. The signals activating centrosomal proteins and MAPs, resulting in process formation, include phosphorylation and dephosphorylation of these proteins. Not only neuronal cells, but also renal glomerular podocytes develop prominent cell processes equipped with well-organized microtubular cytoskeletons, and intermediate and actin filaments. A novel cell culture system for podocytes, in which process formation can be induced, should provide further evidence that microtubules play a pivotal role in process formation of non-neuronal cells.     

Maintenance of Asymmetric Cellular Localization of an Auxin Transport Protein through Interaction with the Actin Cytoskeleton

In shoots, polar auxin transport is basipetal (that is, from the shoot apex toward the base) and is driven by the basal localization of the auxin efflux carrier complex. The focus of this article is to summarize the experiments that have examined how the asymmetric distribution of this protein complex is controlled and the significance of this polar distribution. Experimental evidence suggests that asymmetries in the auxin efflux carrier may be established through localized secretion of Golgi vesicles, whereas an attachment of a subunit of the efflux carrier to the actin cytoskeleton may maintain this localization. In addition, the idea that this localization of the efflux carrier may control both the polarity of auxin movement and more globally regulate developmental polarity is explored. Finally, evidence indicating that the gravity vector controls auxin transport polarity is summarized and possible mechanisms for the environmentally induced changes in auxin transport polarity are discussed.     

Transport of 125I-poly I : poly C incorporated in liposomes from the enteric cavity to the small intestine mucosa. An electron microscopic autoradiographic study

Transport of 125I-poly(I) : poly(C) incorporated into liposomes trough the small intestine mucose was investigated by electron microscopic autoradiography. With the migration of liposomes into the mucous layer on the luminal surface of the intestine up to the glycocalix level of microvilli these undergo degradation with the formation of monolayer liposomes from which polynucleotide is released. Later on the poly(I) : poly(C) or its fragments transported through the enterocytes to be accumulated in cells of the connective tissue stroma of the small intestine mucose. Part of polynucleotide was incorporated up to the arterial and lymphoid capillary level. Apparently, on the way of its transport the polynucleotide is affected by pancreatic and tissue nucleases. The accumulation of polynucleotide in macrophages, fibroblasts, lymphocytes, plasma cells and smooth muscle cells was traced. It is supposed that the polynucleotide accumulated in stroma of the small intestine mucose may preserve its interferon inducing activity.     

Endocytosis optimizes the dynamic localization of membrane proteins that regulate cortical polarity

Diverse cell types require the ability to maintain dynamically polarized membrane-protein distributions through balancing transport and diffusion. However, design principles underlying dynamically maintained cortical polarity are not well understood. Here we constructed a mathematical model for characterizing the morphology of dynamically polarized protein distributions. We developed analytical approaches for measuring all model parameters from single-cell experiments. We applied our methods to a well-characterized system for studying polarized membrane proteins: budding yeast cells expressing activated Cdc42. We found that a balance of diffusion, directed transport, and endocytosis was sufficient for accurately describing polarization morphologies. Surprisingly, the model predicts that polarized regions are defined with a precision that is nearly optimal for measured endocytosis rates and that polarity can be dynamically stabilized through positive feedback with directed transport. Our approach provides a step toward understanding how biological systems shape spatially precise, unambiguous cortical polarity domains using dynamic processes.     

Buder revisited: cell and organ polarity during phototropism

The induction of a radial polarity by environmental stimuli was studied at the cellular and organ levels, with phototropism chosen as a model. The light gradient acting on the whole coleoptile was opposed to the light direction acting upon individual cells in the classical Buder experiment, irradiating from the inside out. Alternatively, the stimulus was administered to the coleoptile tip with a microbeam-irradiation device. Tropistic curvature was assayed as a marker for the response of the whole organ, whereas cell elongation and the orientation of cortical microtubules were taken as markers for the responses of individual cells. Upon tip irradiation, signals much faster than basipetal auxin transport migrate towards the base. The data are discussed in terms of an organ polarity that is the primary result of the asymmetric light signal and affects, in a second step, an endogenous radial polarity of epidermal cells.     

Cell polarity signaling in Arabidopsis involves a BFA-sensitive auxin influx pathway

Coordination of cell and tissue polarity commonly involves directional signaling. In the Arabidopsis root epidermis, cell polarity is revealed by basal, root tip-oriented, hair outgrowth from hair-forming cells (trichoblasts). The plant hormone auxin displays polar movements and accumulates at maximum concentration in the root tip. The application of polar auxin transport inhibitors evokes changes in trichoblast polarity only at high concentrations and after long-term application. Thus, it remains open whether components of the auxin transport machinery mediate establishment of trichoblast polarity. Here we report that the presumptive auxin influx carrier AUX1 contributes to apical-basal hair cell polarity. AUX1 function is required for polarity changes induced by exogenous application of the auxin 2,4-D, a preferential influx carrier substrate. Similar to aux1 mutants, the vesicle trafficking inhibitor brefeldin A (BFA) interferes with polar hair initiation, and AUX1 function is required for BFA-mediated polarity changes. Consistently, BFA inhibits membrane trafficking of AUX1, trichoblast hyperpolarization induced by 2,4-D, and alters the distal auxin maximum. Our results identify AUX1 as one component of a novel BFA-sensitive auxin transport pathway polarizing cells toward a hormone maximum.     

Polarity and the Induction of Organized Vascular Tissues

This work deals with those properties of plant tissues whichare responsible for the organization of vascular cells in orderedstrands. It is shown that auxin alone is sufficient to causethe differentiation of strands of xylem cells in the parenchymaof pea roots. An artificially induced strand, once it is formed,attracts towards itself newly induced vascular strands, andthis attraction results in the union of old and new strands.It is also shown that the application of auxin to natural vasculartissues prevents their being joined by newly induced vascularstrands. It is proved that this is dependent on a directionaleffect and not simply on a local accumulation of auxin. To understand these results, it must be assumed that the polarityin terms of auxin transport is increased during the processof vascular tissue induction. The same polarity, once established,is maintained by the presence of auxin, so that the differentiationof strands perpendicular to the axis of this polarity is prevented.These characteristics of plant tissues concerning auxin transportexplain the basic phenomena of the organization of vascularcells in defined and ordered strands.