Cortical microtubule patterning in roots ofArabidopsis thalianaprimary cell wall mutants reveals the bidirectional interplay with cell expansion

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.

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Cortical microtubule patterning in roots of Arabidopsis thaliana primary cell wall mutants reveals the bidirectional interplay with cell expansion

Plant Signaling & Behavior ◽

10.1080/15592324.2015.1028701 ◽

2015 ◽

Vol 10 (6) ◽

pp. e1028701 ◽

Cited By ~ 2

Author(s):

Emmanuel Panteris ◽

Ioannis-Dimosthenis S Adamakis ◽

Gerasimos Daras ◽

Stamatis Rigas

Keyword(s):

Arabidopsis Thaliana ◽

Cell Wall ◽

Cell Expansion ◽

Cortical Microtubule ◽

Primary Cell ◽

Primary Cell Wall

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Faculty Opinions recommendation of AUXIN BINDING PROTEIN1 links cell wall remodeling, auxin signaling, and cell expansion in arabidopsis.

Faculty Opinions – Post-Publication Peer Review of the Biomedical Literature ◽

10.3410/f.718238665.793490595 ◽

2014 ◽

Author(s):

Jürgen Kleine-Vehn ◽

Elke Barbez

Keyword(s):

Cell Wall ◽

Cell Expansion ◽

Auxin Signaling ◽

Cell Wall Remodeling ◽

Auxin Binding

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Directional cell expansion requires NIMA-related kinase 6 (NEK6)-mediated cortical microtubule destabilization

Scientific Reports ◽

10.1038/s41598-017-08453-5 ◽

2017 ◽

Vol 7 (1) ◽

Cited By ~ 5

Author(s):

Shogo Takatani ◽

Shinichiro Ozawa ◽

Noriyoshi Yagi ◽

Takashi Hotta ◽

Takashi Hashimoto ◽

...

Keyword(s):

Cell Expansion ◽

Cortical Microtubule

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Golgi-localized exo-β1,3-galactosidases involved in AGP modification and root cell expansion in Arabidopsis

10.1101/2020.02.13.947820 ◽

2020 ◽

Author(s):

Pieter Nibbering ◽

Bent L. Petersen ◽

Mohammed Saddik Motawia ◽

Bodil Jørgensen ◽

Peter Ulvskov ◽

...

Keyword(s):

Cell Wall ◽

Cell Expansion ◽

Glycosyl Hydrolase ◽

Functional Characterization ◽

Gum Arabic ◽

Root Cell ◽

Growth Media ◽

Galactosidase Activity ◽

Loss Of Function ◽

Yariv Phenylglycoside

AbstractPlant arabinogalactan proteins (AGPs) are a diverse group of cell surface- and wall-associated glycoproteins. Functionally important AGP glycans are synthesized in the Golgi apparatus, but the relationships between their glycosylation, processing, and functionality are poorly understood. Here we report the identification and functional characterization of two Golgi-localized exo-β-1,3-galactosidases from the glycosyl hydrolase 43 (GH43) family in Arabidopsis thaliana. GH43 loss of function mutants exhibit root cell expansion defects in sugar-containing growth media. This root phenotype is associated with an increase in the extent of AGP cell wall association, as demonstrated by Yariv phenylglycoside dye quantification and comprehensive microarray polymer profiling of sequentially extracted cell walls. Recombinant GH43 characterization showed that the exo-β-1,3-galactosidase activity of GH43s is hindered by β-1,6 branches on β-1,3-galactans. In line with this steric hindrance, the recombinant GH43s did not release galactose from cell wall extracted glycoproteins or AGP rich gum arabic. These results show that Arabidopsis GH43s are involved in AGP glycan biosynthesis in the Golgi, and suggest their exo-β-1,3-galactosidase activity influences AGP and cell wall matrix interactions, thereby adjusting cell wall extensibility.

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FRA1 modulates cortical microtubule localization of CMU proteins

10.1101/760389 ◽

2019 ◽

Author(s):

Anindya Ganguly ◽

Chuanmei Zhu ◽

Weizu Chen ◽

Ram Dixit

Keyword(s):

Arabidopsis Thaliana ◽

Cell Wall ◽

Molecular Mechanisms ◽

Cortical Microtubule ◽

Cellulose Synthase ◽

Lateral Stability ◽

Cortical Microtubules ◽

Tail Region ◽

Opposing Effect ◽

Growth And Reproduction

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.

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The Role of Brachypodium distachyon Wall-Associated Kinases (WAKs) in Cell Expansion and Stress Responses

Cells ◽

10.3390/cells9112478 ◽

2020 ◽

Vol 9 (11) ◽

pp. 2478

Author(s):

Xingwen Wu ◽

Antony Bacic ◽

Kim L. Johnson ◽

John Humphries

Keyword(s):

Cell Wall ◽

Stress Response ◽

Plant Cell ◽

Stress Responses ◽

Cell Expansion ◽

Plant Cell Wall ◽

Brachypodium Distachyon ◽

Critical Role ◽

Cell Integrity

The plant cell wall plays a critical role in signaling responses to environmental and developmental cues, acting as both the sensing interface and regulator of plant cell integrity. Wall-associated kinases (WAKs) are plant receptor-like kinases located at the wall—plasma membrane—cytoplasmic interface and implicated in cell wall integrity sensing. WAKs in Arabidopsis thaliana have been shown to bind pectins in different forms under various conditions, such as oligogalacturonides (OG)s in stress response, and native pectin during cell expansion. The mechanism(s) WAKs use for sensing in grasses, which contain relatively low amounts of pectin, remains unclear. WAK genes from the model monocot plant, Brachypodium distachyon were identified. Expression profiling during early seedling development and in response to sodium salicylate and salt treatment was undertaken to identify WAKs involved in cell expansion and response to external stimuli. The BdWAK2 gene displayed increased expression during cell expansion and stress response, in addition to playing a potential role in the hypersensitive response. In vitro binding assays with various forms of commercial polysaccharides (pectins, xylans, and mixed-linkage glucans) and wall-extracted fractions (pectic/hemicellulosic/cellulosic) from both Arabidopsis and Brachypodium leaf tissues provided new insights into the binding properties of BdWAK2 and other candidate BdWAKs in grasses. The BdWAKs displayed a specificity for the acidic pectins with similar binding characteristics to the AtWAKs.

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An extensin peroxidase is associated with white-light inhibition of lupin (Lupinus albus) hypocotyl growth

Functional Plant Biology ◽

10.1071/pp98126 ◽

1999 ◽

Vol 26 (1) ◽

pp. 29 ◽

Cited By ~ 6

Author(s):

P. Jackson ◽

S. Paulo ◽

C. P. P. Ricardo ◽

M. Brownleader ◽

P. O. Freire

Keyword(s):

Cell Wall ◽

White Light ◽

Cell Expansion ◽

Structural Changes ◽

Lupinus Albus ◽

Extension Rate ◽

Hypocotyl Growth ◽

Cross Links ◽

Quantitative Changes

The spatial distribution of the major basic (B2; pI 8.8) peroxidase of the intercellular fluid has an inverse relation with extension rate in etiolated hypocotyls of Lupinus albus L., suggesting its possible role in the control of cell expansion. White-light irradiation of etiolated hypocotyls resulted in growth inhibition and the induction of B2 and acidic (A2, pI 4.7–5.2) isoperoxidases (EC 1.1.11.7) to higher physiological activities. However, only the activities of the B2 isoperoxidases underwent quantitative changes in both space and time which suggested their role in growth-retardation. We have purified the B2 and A2 (pI 5.2) peroxidases to apparent electrophoretic homogeneity. To corroborate evidence obtained elsewhere that growth cessation coincides with cell wall structural changes and cell wall rigidification, we have shown that the B2 peroxidase, and not A2 peroxidase, cross-links tomato extensin in vitro. The B2 peroxidase may therefore catalyse the developmentally and light regulated formation of a covalently cross-linked cell wall extensin matrix in lupin hypocotyls. The cell wall would be more rigid or more recalcitrant to wall-loosening and subsequently contribute to the control of cell expansion.

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Why Measure Osmotic Adjustment?

Functional Plant Biology ◽

10.1071/pp9880717 ◽

1988 ◽

Vol 15 (6) ◽

pp. 717 ◽

Cited By ~ 112

Author(s):

R Munns

Keyword(s):

Cell Wall ◽

Stomatal Conductance ◽

Osmotic Adjustment ◽

Cell Expansion ◽

Control Cell ◽

Growth Yield ◽

Future Research ◽

Saline Soils ◽

Cell Wall Synthesis ◽

Adaptation To Drought

Osmotic adjustment (erroneously called 'osmoregulation') is generally regarded as an important adaptation to drought or salinity. Because it helps to maintain turgor and cell volume, it is often thought to promote growth, yield, or survival, of plants in dry or saline soils. However, a physiological rationale for such views is lacking. Osmotic adjustment itself cannot promote growth; the solutes which account for it must be diverted from essential processes such as protein and cell wall synthesis. Further, it now appears that turgor does not control cell expansion or stomatal conductance. Thus, osmotic adjustment cannot affect yields except via other processes, the controls of which are almost entirely unexplored. Future research in this area should test hypotheses, rather than merely measure osmotic adjustment.

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