scholarly journals Establishment of Polarity during Organization of the Acentrosomal Plant Cortical Microtubule Array

2006 ◽  
Vol 17 (3) ◽  
pp. 1298-1305 ◽  
Author(s):  
Ram Dixit ◽  
Eric Chang ◽  
Richard Cyr

The plant cortical microtubule array is a unique acentrosomal array that is essential for plant morphogenesis. To understand how this array is organized, we exploited the microtubule (+)-end tracking activity of two Arabidopsis EB1 proteins in combination with FRAP (fluorescence recovery after photobleaching) experiments of GFP-tubulin to examine the relationship between cortical microtubule array organization and polarity. Significantly, our observations show that the majority of cortical microtubules in ordered arrays, within a particular cell, face the same direction in both Arabidopsis plants and cultured tobacco cells. We determined that this polar microtubule coalignment is at least partially due to a selective stabilization of microtubules, and not due to a change in microtubule polymerization rates. Finally, we show that polar microtubule coalignment occurs in conjunction with parallel grouping of cortical microtubules and that cortical array polarity is progressively enhanced during array organization. These observations reveal a novel aspect of plant cortical microtubule array organization and suggest that selective stabilization of dynamic cortical microtubules plays a predominant role in the self-organization of cortical arrays.

2020 ◽  
Author(s):  
Marco Saltini ◽  
Bela M. Mulder

The light-induced reorientation of the cortical microtubule array in dark-grown A. thaliana hypocotyl cells is a striking example of the dynamical plasticity of the microtubule cytoskeleton. A consensus model, based on katanin-mediated severing at microtubule crossovers, has been developed that successfully describes the onset of the observed switch between a transverse and longitudinal array orientation. However, we currently lack an understanding of of why the newly populated longitudinal array direction remains stable for longer times, when the initial trigger for the reorientation has died out, and re-equilibration effects would tend to drive the system back to a mixed orientation state. Using both simulations and analytical calculations, we show that the assumption of a small orientation-dependent shift in microtubule dynamics is sufficient to explain the long term lock-in of the longitudinal array orientation. Furthermore, we show that the natural alternative hypothesis that there is a selective advantage in severing longitudinal microtubules, is neither necessary nor sufficient to achieve cortical array reorientation, but is able to accelerate this process significantly.


2021 ◽  
Vol 2 ◽  
Author(s):  
Marco Saltini ◽  
Bela M. Mulder

Abstract The light-induced reorientation of the cortical microtubule array in dark-grown Arabidopsis thaliana hypocotyl cells is a striking example of the dynamical plasticity of the microtubule cytoskeleton. A consensus model, based on katanin-mediated severing at microtubule crossovers, has been developed that successfully describes the onset of the observed switch between a transverse and longitudinal array orientation. However, we currently lack an understanding of why the newly populated longitudinal array direction remains stable for longer times and re-equilibration effects would tend to drive the system back to a mixed orientation state. Using both simulations and analytical calculations, we show that the assumption of a small orientation-dependent shift in microtubule dynamics is sufficient to explain the long-term lock-in of the longitudinal array orientation. Furthermore, we show that the natural alternative hypothesis that there is a selective advantage in severing longitudinal microtubules, is neither necessary nor sufficient to achieve cortical array reorientation, but is able to accelerate this process significantly.


Development ◽  
1991 ◽  
Vol 112 (1) ◽  
pp. 107-117 ◽  
Author(s):  
E. Houliston ◽  
R.P. Elinson

Following fertilization, the Xenopus egg cortex rotates relative to the cytoplasm by 30 degrees about a horizontal axis. The direction of rotation, and as a result the orientation of the embryonic body axes, is normally specified by the position of sperm entry. The mechanism of rotation appears to involve an array of aligned microtubules in the vegetal cortex (Elinson and Rowning, 1988, Devl Biol. 128, 185–197). We performed anti-tubulin immunofluorescence on sections to follow the formation of this array. Microtubules disappear rapidly from the egg following fertilization, and reappear first in the sperm aster. Surprisingly, astral microtubules then extend radially through both the animal and vegetal cytoplasm. The cortical array arises as they reach the vegetal cell surface. The eccentric position of the sperm aster gives asymmetry to the formation of the array and may explain its alignment since microtubules reaching the cortex tend to bend away from the sperm entry side. The radial polymerization of cytoplasmic microtubules is not dependent on the sperm aster or on the female pronucleus: similar but more symmetric patterns arise in artificially activated and enucleate eggs, slightly later than in fertilized eggs. These observations suggest that the cortical microtubule array forms as a result of asymmetric microtubule growth outward from cytoplasm to cortex and, since cortical and cytoplasmic microtubules remain connected throughout the period of the rotation, that the microtubules of the array rotate with the cytoplasm.


1986 ◽  
Vol 64 (7) ◽  
pp. 1373-1381 ◽  
Author(s):  
Robert W. Seagull

Cotton fibers provide an excellent system to study how cortical microtubule arrays are established and the relationship between microtubule organization and wall microfibril deposition. Throughout development, cotton fibers maintain highly organized arrays of microtubules. For the first 15–18 days postanthesis microtubules are oriented transverse to the cell long axis. Older fibers contain microtubule arrays that are organized in a spiral pattern. The switch from transverse to spiral appears to be coordinated along the entire cell length since cells do not simultaneously contain both arrays. Older fibers also exhibit abrupt reversals in microtubule orientation. Reversals occur in two different forms that may represent a developmental sequence in the establishment of reversal regions. Throughout development, the cotton fiber walls exhibit increasing amounts of birefringence. In all cases, the most recently deposited wall microfibrils parallel the cortical microtubules.


2021 ◽  
Vol 28 (1) ◽  
Author(s):  
Veronica Giourieva ◽  
Emmanuel Panteris

Abstract Background Cortical microtubules regulate cell expansion by determining cellulose microfibril orientation in the root apex of Arabidopsis thaliana. While the regulation of cell wall properties by cortical microtubules is well studied, the data on the influence of cell wall to cortical microtubule organization and stability remain scarce. Studies on cellulose biosynthesis mutants revealed that cortical microtubules depend on Cellulose Synthase A (CESA) function and/or cell expansion. Furthermore, it has been reported that cortical microtubules in cellulose-deficient mutants are hypersensitive to oryzalin. In this work, the persistence of cortical microtubules against anti-microtubule treatment was thoroughly studied in the roots of several cesa mutants, namely thanatos, mre1, any1, prc1-1 and rsw1, and the Cellulose Synthase Interacting 1 protein (csi1) mutant pom2-4. In addition, various treatments with drugs affecting cell expansion were performed on wild-type roots. Whole mount tubulin immunolabeling was applied in the above roots and observations were performed by confocal microscopy. Results Cortical microtubules in all mutants showed statistically significant increased persistence against anti-microtubule drugs, compared to those of the wild-type. Furthermore, to examine if the enhanced stability of cortical microtubules was due to reduced cellulose biosynthesis or to suppression of cell expansion, treatments of wild-type roots with 2,6-dichlorobenzonitrile (DCB) and Congo red were performed. After these treatments, cortical microtubules appeared more resistant to oryzalin, than in the control. Conclusions According to these findings, it may be concluded that inhibition of cell expansion, irrespective of the cause, results in increased microtubule stability in A. thaliana root. In addition, cell expansion does not only rely on cortical microtubule orientation but also plays a regulatory role in microtubule dynamics, as well. Various hypotheses may explain the increased cortical microtubule stability under decreased cell expansion such as the role of cell wall sensors and the presence of less dynamic cortical microtubules.


Development ◽  
1992 ◽  
Vol 114 (3) ◽  
pp. 699-709 ◽  
Author(s):  
M.M. Schroeder ◽  
D.L. Gard

Anti-tubulin antibodies and confocal immunofluorescence microscopy were used to examine the organization and regulation of cytoplasmic and cortical microtubules during the first cell cycle of fertilized Xenopus eggs. Appearance of microtubules in the egg cortex temporally coincided with the outgrowth of the sperm aster. Microtubules of the sperm aster first reached the animal cortex at 0.25, (times normalized to first cleavage), forming a radially organized array of cortical microtubules. A disordered network of microtubules was apparent in the vegetal cortex as early as 0.35. Cortical microtubule networks of both animal and vegetal hemispheres were reorganized at times corresponding to the cortical rotation responsible for specification of the dorsal-ventral (D-V) axis. Optical sections suggest that the cortical microtubules are continuous with the microtubules of the sperm aster in fertilized eggs, or an extensive activation aster in activated eggs. Neither assembly and organization, nor disassembly of the cortical microtubules coincided with MPF activation during mitosis. However, cycloheximide or 6-dimethylaminopurine, which arrest fertilized eggs at interphase, blocked cortical microtubule disassembly. Injection of p13, a protein that specifically inhibits MPF activation, delayed or inhibited cortical microtubule breakdown. In contrast, eggs injected with cyc delta 90, a truncated cyclin that arrest eggs in M-phase, showed normal microtubule disassembly. Finally, injection of partially purified MPF into cycloheximide-arrested eggs induced cortical microtubule breakdown. These results suggest that, despite a lack of temporal coincidence, breakdown of the cortical microtubules is dependent on the activation of MPF.


2020 ◽  
Vol 49 (34) ◽  
pp. 11859-11877 ◽  
Author(s):  
Ali Samie ◽  
Alireza Salimi ◽  
Jered C. Garrison

The coordination sphere can be influenced by many factors of inorganic and organic units. Despite the predominant role of inorganic unit in coordination sphere determination, organic unit can change it via one major or cooperativity of minor effects.


2019 ◽  
Author(s):  
Anindya Ganguly ◽  
Chuanmei Zhu ◽  
Weizu Chen ◽  
Ram Dixit

ABSTRACTConstruction of the cell wall demands harmonized deposition of cellulose and matrix polysaccharides. Cortical microtubules orient the deposition of cellulose by guiding the trajectory of plasma membrane-embedded cellulose synthase complexes. Vesicles containing matrix polysaccharides are thought to be transported by the FRA1 kinesin to facilitate their secretion along cortical microtubules. The cortical microtubule cytoskeleton thus provides a platform to coordinate the delivery of cellulose and matrix polysaccharides, but the underlying molecular mechanisms remain unknown. Here, we show that the tail region of the FRA1 kinesin physically interacts with CMU proteins which are important for the microtubule-dependent guidance of cellulose synthase complexes. Interaction with CMUs did not affect microtubule binding or motility of the FRA1 kinesin but had an opposing effect on the cortical microtubule localization of CMU1 and CMU2 proteins, thus regulating the lateral stability of cortical microtubules. Phosphorylation of the FRA1 tail region by CKL6 inhibited binding to CMUs and consequently reversed the extent of cortical microtubule decoration by CMU1 and CMU2. Genetic experiments demonstrated the significance of this interaction to the growth and reproduction of Arabidopsis thaliana plants. We propose that modulation of CMU’s microtubule localization by FRA1 provides a mechanism to control the coordinated deposition of cellulose and matrix polysaccharides.


2009 ◽  
Vol 187 (6) ◽  
pp. 831-845 ◽  
Author(s):  
George von Dassow ◽  
Koen J.C. Verbrugghe ◽  
Ann L. Miller ◽  
Jenny R. Sider ◽  
William M. Bement

Animal cells decide where to build the cytokinetic apparatus by sensing the position of the mitotic spindle. Reflecting a long-standing presumption that a furrow-inducing stimulus travels from spindle to cortex via microtubules, debate continues about which microtubules, and in what geometry, are essential for accurate cytokinesis. We used live imaging in urchin and frog embryos to evaluate the relationship between microtubule organization and cytokinetic furrow position. In normal cells, the cytokinetic apparatus forms in a region of lower cortical microtubule density. Remarkably, cells depleted of astral microtubules conduct accurate, complete cytokinesis. Conversely, in anucleate cells, asters alone can support furrow induction without a spindle, but only when sufficiently separated. Ablation of a single centrosome displaces furrows away from the remaining centrosome; ablation of both centrosomes causes broad, inefficient furrowing. We conclude that the asters confer accuracy and precision to a primary furrow-inducing signal that can reach the cell surface from the spindle without transport on microtubules.


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