scholarly journals Inhibition of cell expansion enhances cortical microtubule stability in the root apex of Arabidopsis thaliana

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.

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.


PLoS ONE ◽  
2013 ◽  
Vol 8 (12) ◽  
pp. e82442 ◽  
Author(s):  
Emmanuel Panteris ◽  
Ioannis-Dimosthenis S. Adamakis ◽  
Gerasimos Daras ◽  
Polydefkis Hatzopoulos ◽  
Stamatis Rigas

2020 ◽  
Vol 126 (5) ◽  
pp. 807-824
Author(s):  
Liu Wang ◽  
Bret E Hart ◽  
Ghazanfar Abbas Khan ◽  
Edward R Cruz ◽  
Staffan Persson ◽  
...  

Abstract Background Phytohormones are small molecules that regulate virtually every aspect of plant growth and development, from basic cellular processes, such as cell expansion and division, to whole plant environmental responses. While the phytohormone levels and distribution thus tell the plant how to adjust itself, the corresponding growth alterations are actuated by cell wall modification/synthesis and internal turgor. Plant cell walls are complex polysaccharide-rich extracellular matrixes that surround all plant cells. Among the cell wall components, cellulose is typically the major polysaccharide, and is the load-bearing structure of the walls. Hence, the cell wall distribution of cellulose, which is synthesized by large Cellulose Synthase protein complexes at the cell surface, directs plant growth. Scope Here, we review the relationships between key phytohormone classes and cellulose deposition in plant systems. We present the core signalling pathways associated with each phytohormone and discuss the current understanding of how these signalling pathways impact cellulose biosynthesis with a particular focus on transcriptional and post-translational regulation. Because cortical microtubules underlying the plasma membrane significantly impact the trajectories of Cellulose Synthase Complexes, we also discuss the current understanding of how phytohormone signalling impacts the cortical microtubule array. Conclusion Given the importance of cellulose deposition and phytohormone signalling in plant growth and development, one would expect that there is substantial cross-talk between these processes; however, mechanisms for many of these relationships remain unclear and should be considered as the target of future studies.


2019 ◽  
Vol 60 (7) ◽  
pp. 1487-1503 ◽  
Author(s):  
Thiel A. Lehman ◽  
Karen A Sanguinet

AbstractPlant cells sheath themselves in a complex lattice of polysaccharides, proteins and enzymes forming an integral matrix known as the cell wall. Cellulose microfibrils, the primary component of cell walls, are synthesized at the plasma membrane by CELLULOSE SYNTHASE A (CESA) proteins throughout cellular growth and are responsible for turgor-driven anisotropic expansion. Associations between hormone signaling and cell wall biosynthesis have long been suggested, but recently direct links have been found revealing hormones play key regulatory roles in cellulose biosynthesis. The radially swollen 1 (rsw1) allele of Arabidopsis thaliana CESA1 harbors a single amino acid change that renders the protein unstable at high temperatures. We used the conditional nature of rsw1 to investigate how auxin contributes to isotropic growth. We found that exogenous auxin treatment reduces isotropic swelling in rsw1 roots at the restrictive temperature of 30�C. We also discovered decreases in auxin influx between rsw1 and wild-type roots via confocal imaging of AUX1-YFP, even at the permissive temperature of 19�C. Moreover, rsw1 displayed mis-expression of auxin-responsive and CESA genes. Additionally, we found altered auxin maxima in rsw1 mutant roots at the onset of swelling using DII-VENUS and DR5:vYFP auxin reporters. Overall, we conclude disrupted cell wall biosynthesis perturbs auxin transport leading to altered auxin homeostasis impacting both anisotropic and isotropic growth that affects overall root morphology.


1992 ◽  
Vol 19 (4) ◽  
pp. 427 ◽  
Author(s):  
TI Baskin ◽  
AS Betzner ◽  
R Hoggart ◽  
A Cork ◽  
RE Williamson

We have begun a mutational analysis of root morphogenesis in Arabidopsis thaliana. We report here the initial genetic and physiological characterisation of six mutations that affect root growth and development. Three of them (rsw1, rsw2, rsw3) cause extensive radial swelling of the root apex. These mutations are recessive at different loci and show temperature-sensitive expression, such that the roots appear wild type when grown at 18�C but express the mutant phenotype when transferred to 31�C. Following transfer to the restrictive temperature, these three mutations have different kinetic and morphological patterns of radial swelling, and grow at different rates with continued time at high temperature. We believe that these mutations represent three different loci active in the wild type in regulating the shape of the root. We have also characterised two mutations that affect only the root epidermis, causing many epidermal cells to bulge (reb1-1, reb1-2). The two mutations are recessive and are alleles. However, rebl-1 is constitutive whereas reb1-2 is temperature sensitive, only expressing at 33�C. Reb1-2 also causes a deviation from the normal straight growth of the root such that the affected roots grow with sharp bends or meanders. The final mutant reported here is a stunted plant (stp1), in which the root growth rate is approximately 25% of the wild type rate. Moreover, root growth steadily accelerates over 5 days following germination in the wild type but remains constant in stp1, which grows at a constant rate over the same interval.


PLoS Genetics ◽  
2014 ◽  
Vol 10 (9) ◽  
pp. e1004627 ◽  
Author(s):  
Ushio Fujikura ◽  
Lore Elsaesser ◽  
Holger Breuninger ◽  
Clara Sánchez-Rodríguez ◽  
Alexander Ivakov ◽  
...  

2014 ◽  
Vol 9 (6) ◽  
pp. e28737 ◽  
Author(s):  
Emmanuel Panteris ◽  
Ioannis-Dimosthenis S Adamakis ◽  
Gerasimos Daras ◽  
Stamatis Rigas

Author(s):  
Emmanuel Panteris ◽  
Anna Kouskouveli ◽  
Dimitris Pappas ◽  
Ioannis-Dimosthenis S. Adamakis

Cytokinesis is accomplished in higher plants by the phragmoplast, creating and conducting the cell plate, to separate daughter nuclei by a new cell wall. The microtubule-severing enzyme p60-katanin plays an important role in the centrifugal expansion and timely disappearance of phragmoplast microtubules. Consequently, aberrant structure and delayed expansion rate of the phragmoplast occur in p60-katanin mutants. Here, the consequences of p60-katanin malfunction in cell plate/daughter wall formation were investigated by transmission electron microscopy (TEM), while deviations in the chemical composition of cell plate/new cell wall were identified by immunolabeling and confocal microscopy, in root cells of the fra2 Arabidopsis thaliana mutant. It was found that, apart from defective phragmoplast microtubule organization, cell plates/new cell walls appeared also faulty in structure, being unevenly thick and perforated by large gaps. In addition, demethylesterified homogalacturonans were prematurely present in fra2 cell plates, while callose content was significantly lower than in the wild-type. Furthermore, KNOLLE syntaxin disappeared from newly formed cell walls in fra2 earlier than in the wild-type. Taken together, these observations indicate that delayed cytokinesis, due to faulty phragmoplast organization and expansion, results in a loss of synchronization between cell plate growth and its chemical maturation.


Author(s):  
A.R. Hardham ◽  
B.E.S. Gunning

Microtubules in the plant cell cortex are usually aligned parallel to microfibrils of cellulose that are being deposited in the cell wall, and are considered to function in guiding or orienting cellulose synthetase complexes that lie in or on the plasma membrane. The cellulose component is largely responsible for the mechanical reaction of the wall to turgor forces, thereby determining cell size and shape, and therefore the role of the cortical microtubules is a fundamental part of the overall morphogenetic process in plants. It is important to determine the structure of cortical arrays of microtubules and to learn how the cell regulates their development, neither of these aspects having been investigated adequately since the original description likened the microtubules to “hundreds of hoops around the cell”.


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