Cellulose synthase interactive protein 1 (CSI1) mediates the intimate relationship between cellulose microfibrils and cortical microtubules

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.

Download Full-text

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.

Download Full-text

Auxin and Cell Wall Crosstalk as Revealed by the Arabidopsis thaliana Cellulose Synthase Mutant Radially Swollen 1

Plant and Cell Physiology ◽

10.1093/pcp/pcz055 ◽

2019 ◽

Vol 60 (7) ◽

pp. 1487-1503 ◽

Cited By ~ 3

Author(s):

Thiel A. Lehman ◽

Karen A Sanguinet

Keyword(s):

Arabidopsis Thaliana ◽

Cell Wall ◽

Cellulose Synthase ◽

Cellulose Microfibrils ◽

Single Amino Acid ◽

Cell Wall Biosynthesis ◽

Restrictive Temperature ◽

Permissive Temperature ◽

Anisotropic Expansion ◽

Single Amino Acid Change

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 30ï¿½C. 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 19ï¿½C. 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.

Download Full-text

Cellulose synthase complexes act in a concerted fashion to synthesize highly aggregated cellulose in secondary cell walls of plants

Proceedings of the National Academy of Sciences ◽

10.1073/pnas.1613273113 ◽

2016 ◽

Vol 113 (40) ◽

pp. 11348-11353 ◽

Cited By ~ 50

Author(s):

Shundai Li ◽

Logan Bashline ◽

Yunzhen Zheng ◽

Xiaoran Xin ◽

Shixin Huang ◽

...

Keyword(s):

Cell Wall ◽

Cell Walls ◽

Plant Cell Wall ◽

Cellulose Synthase ◽

Cellulose Microfibrils ◽

Critical Component ◽

Distinct Structure ◽

Secondary Cell Walls ◽

Composition Structure ◽

Membrane Spanning

Cellulose, often touted as the most abundant biopolymer on Earth, is a critical component of the plant cell wall and is synthesized by plasma membrane-spanning cellulose synthase (CESA) enzymes, which in plants are organized into rosette-like CESA complexes (CSCs). Plants construct two types of cell walls, primary cell walls (PCWs) and secondary cell walls (SCWs), which differ in composition, structure, and purpose. Cellulose in PCWs and SCWs is chemically identical but has different physical characteristics. During PCW synthesis, multiple dispersed CSCs move along a shared linear track in opposing directions while synthesizing cellulose microfibrils with low aggregation. In contrast, during SCW synthesis, we observed swaths of densely arranged CSCs that moved in the same direction along tracks while synthesizing cellulose microfibrils that became highly aggregated. Our data support a model in which distinct spatiotemporal features of active CSCs during PCW and SCW synthesis contribute to the formation of cellulose with distinct structure and organization in PCWs and SCWs of Arabidopsis thaliana. This study provides a foundation for understanding differences in the formation, structure, and organization of cellulose in PCWs and SCWs.

Download Full-text

Mechanical properties of the stigmatic cell wall mediate pollen tube path in Arabidopsis

10.1101/384321 ◽

2018 ◽

Author(s):

Lucie Riglet ◽

Frédérique Rozier ◽

Chie Kodera ◽

Isabelle Fobis-Loisy ◽

Thierry Gaude

Keyword(s):

Cell Wall ◽

Pollen Tube ◽

Cell Shape ◽

Cell Imaging ◽

Pollen Tubes ◽

Mechanical Anisotropy ◽

Cellulose Microfibrils ◽

Mechanical Forces ◽

Cortical Microtubules ◽

Isotropic Reorientation

ABSTRACTSuccessful fertilization in angiosperms depends on the proper trajectory of pollen tubes through the pistil tissues to reach the ovules. Pollen tubes first grow within the cell wall of the papilla cells, applying pressure to the cell. Mechanical forces are known to play a major role in plant cell shape by controlling the orientation of cortical microtubules (CMTs), which in turn mediate deposition of cellulose microfibrils (CMFs). Here, by combining cell imaging and genetic approaches, we show that isotropic reorientation of CMTs and CMFs in aged and katanin1-5 (ktn1-5) papilla cells is accompanied by a tendency of pollen tubes to coil around the papillae. Furthermore, we uncover that aged and ktn1-5 papilla cells have a softer cell wall and provide less resistance to pollen tube growth. Our results reveal an unexpected role for KTN1 in pollen tube guidance by ensuring mechanical anisotropy of the papilla cell wall.

Download Full-text

Synthesis and Self-Assembly of Cellulose Microfibrils from Reconstituted Cellulose Synthase

PLANT PHYSIOLOGY ◽

10.1104/pp.17.00619 ◽

2017 ◽

Vol 175 (1) ◽

pp. 146-156 ◽

Cited By ~ 18

Author(s):

Sung Hyun Cho ◽

Pallinti Purushotham ◽

Chao Fang ◽

Cassandra Maranas ◽

Sara M. Díaz-Moreno ◽

...

Keyword(s):

Self Assembly ◽

Cellulose Synthase ◽

Cellulose Microfibrils

Download Full-text

Chemical Genetic Screening Identifies a Novel Inhibitor of Parallel Alignment of Cortical Microtubules and Cellulose Microfibrils

Plant and Cell Physiology ◽

10.1093/pcp/pcm120 ◽

2007 ◽

Vol 48 (10) ◽

pp. 1393-1403 ◽

Cited By ~ 50

Author(s):

Arata Yoneda ◽

Takumi Higaki ◽

Natsumaro Kutsuna ◽

Yoichi Kondo ◽

Hiroyuki Osada ◽

...

Keyword(s):

Genetic Screening ◽

Cellulose Microfibrils ◽

Cortical Microtubules ◽

Chemical Genetic

Download Full-text

Regulation by Gibberellins of the Orientation of Cortical Microtubules in Plant Cells

Functional Plant Biology ◽

10.1071/pp9930461 ◽

1993 ◽

Vol 20 (5) ◽

pp. 461 ◽

Cited By ~ 20

Author(s):

H Shibaoka

Keyword(s):

Plasma Membrane ◽

Cell Expansion ◽

Plant Cells ◽

Cellulose Microfibrils ◽

Molecular Architecture ◽

Cortical Microtubules ◽

Microtubule Stability ◽

The Stability ◽

The Way

Gibberellins control the direction of expansion of plant cells. They change the orientation of cellulose microfibrils by changing the orientation of cortical microtubules and, hence, the direction of cell expansion. When gibberellins change the orientation of cortical microtubules, they also change their stability. If the way in which gibberellins change the orientation of microtubules is identical to the way in which they change microtubule stability, then studies on the mechanism that regulates this stability should give us some clues to the mechanism that regulates the orientation of microtubules. With this possibility in mind, we undertook a series of studies on the stability of cortical microtubules. These revealed that the association of cortical microtubules with the plasma membrane is an important part of the mechanism for their stabilisation. Gibberellins seem to change the stability of microtubules by affecting their association with the plasma membrane. To study the way in which the gibberellins affect this association, it is necessary to clarify the molecular architecture of the structure that links cortical microtubules with the plasma membrane.

Download Full-text