Atkinesin-13A Modulates Cell-Wall Synthesis and Cell Expansion in Arabidopsis thaliana via the THESEUS1 Pathway

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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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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Organization of cellulose synthase complexes involved in primary cell wall synthesis in Arabidopsis thaliana

Proceedings of the National Academy of Sciences ◽

10.1073/pnas.0706569104 ◽

2007 ◽

Vol 104 (39) ◽

pp. 15572-15577 ◽

Cited By ~ 285

Author(s):

T. Desprez ◽

M. Juraniec ◽

E. F. Crowell ◽

H. Jouy ◽

Z. Pochylova ◽

...

Keyword(s):

Arabidopsis Thaliana ◽

Cell Wall ◽

Cellulose Synthase ◽

Primary Cell ◽

Primary Cell Wall ◽

Cell Wall Synthesis

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Gibberellic acid promotes growth and cell wall synthesis in Avena internodes regardless of the orientation of cell expansion

Physiologia Plantarum ◽

10.1034/j.1399-3054.1995.940102.x ◽

1995 ◽

Vol 94 (1) ◽

pp. 7-18

Author(s):

Michael J. Montague

Keyword(s):

Cell Wall ◽

Gibberellic Acid ◽

Cell Expansion ◽

Cell Wall Synthesis

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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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Auxin steers root cell expansion via apoplastic pH regulation in Arabidopsis thaliana

Proceedings of the National Academy of Sciences ◽

10.1073/pnas.1613499114 ◽

2017 ◽

Vol 114 (24) ◽

pp. E4884-E4893 ◽

Cited By ~ 89

Author(s):

Elke Barbez ◽

Kai Dünser ◽

Angelika Gaidora ◽

Thomas Lendl ◽

Wolfgang Busch

Keyword(s):

Arabidopsis Thaliana ◽

Cell Wall ◽

Cell Expansion ◽

Ph Regulation ◽

Root Cell ◽

Auxin Signaling ◽

Acid Growth ◽

Gravitropic Response ◽

Apoplastic Ph ◽

Cellular Resolution

Plant cells are embedded within cell walls, which provide structural integrity, but also spatially constrain cells, and must therefore be modified to allow cellular expansion. The long-standing acid growth theory postulates that auxin triggers apoplast acidification, thereby activating cell wall-loosening enzymes that enable cell expansion in shoots. Interestingly, this model remains heavily debated in roots, because of both the complex role of auxin in plant development as well as technical limitations in investigating apoplastic pH at cellular resolution. Here, we introduce 8-hydroxypyrene-1,3,6-trisulfonic acid trisodium salt (HPTS) as a suitable fluorescent pH indicator for assessing apoplastic pH, and thus acid growth, at a cellular resolution in Arabidopsis thaliana roots. Using HPTS, we demonstrate that cell wall acidification triggers cellular expansion, which is correlated with a preceding increase of auxin signaling. Reduction in auxin levels, perception, or signaling abolishes both the extracellular acidification and cellular expansion. These findings jointly suggest that endogenous auxin controls apoplastic acidification and the onset of cellular elongation in roots. In contrast, an endogenous or exogenous increase in auxin levels induces a transient alkalinization of the extracellular matrix, reducing cellular elongation. The receptor-like kinase FERONIA is required for this physiological process, which affects cellular root expansion during the gravitropic response. These findings pinpoint a complex, presumably concentration-dependent role for auxin in apoplastic pH regulation, steering the rate of root cell expansion and gravitropic response.

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Ectopic expression of LBD15 affects lateral branch development and secondary cell wall synthesis in Arabidopsis thaliana

Plant Growth Regulation ◽

10.1007/s10725-013-9873-9 ◽

2013 ◽

Vol 73 (2) ◽

pp. 111-120 ◽

Cited By ~ 4

Author(s):

Lin Zhu ◽

Jiansheng Guo ◽

Cheng Zhou ◽

Jian Zhu

Keyword(s):

Arabidopsis Thaliana ◽

Cell Wall ◽

Secondary Cell Wall ◽

Ectopic Expression ◽

Lateral Branch ◽

Cell Wall Synthesis ◽

Branch Development ◽

Secondary Cell Wall Synthesis

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Gibberellic acid promotes growth and cell wall synthesis in Avena internodes regardless of the orientation of cell expansion

Physiologia Plantarum ◽

10.1111/j.1399-3054.1995.tb00777.x ◽

1995 ◽

Vol 94 (1) ◽

pp. 7-18 ◽

Cited By ~ 3

Author(s):

Michael J. Montague

Keyword(s):

Cell Wall ◽

Gibberellic Acid ◽

Cell Expansion ◽

Cell Wall Synthesis

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Class A Penicillin-Binding Protein-Mediated Cell Wall Synthesis Promotes Structural Integrity during Peptidoglycan Endopeptidase Insufficiency in Vibrio cholerae

mBio ◽

10.1128/mbio.03596-20 ◽

2021 ◽

Vol 12 (2) ◽

Author(s):

Shannon G. Murphy ◽

Andrew N. Murtha ◽

Ziyi Zhao ◽

Laura Alvarez ◽

Peter Diebold ◽

...

Keyword(s):

Cell Wall ◽

Vibrio Cholerae ◽

Cell Elongation ◽

Cell Expansion ◽

Structural Integrity ◽

Cell Wall Synthesis ◽

Content Type ◽

Class A ◽

Rod System ◽

Mass Increase

ABSTRACT The bacterial cell wall is composed primarily of peptidoglycan (PG), a poly-aminosugar that is essential to sustain cell shape, growth, and structural integrity. PG is synthesized by class A/B penicillin-binding proteins (a/bPBPs) and shape, elongation, division, and sporulation (SEDS) proteins like RodA (as part of the Rod system cell elongation machinery) and degraded by “autolytic” enzymes to accommodate growth processes. It is thought that autolysins (particularly endopeptidases [EPs]) are required for PG synthesis and incorporation by creating gaps that are patched and paved by PG synthases, but the exact relationship between autolysins and PG synthesis remains incompletely understood. Here, we have probed the consequences of EP depletion for PG synthesis in the diarrheal pathogen Vibrio cholerae. We found that EP depletion resulted in severe morphological and division defects, but these cells continued to increase in mass and aberrantly incorporated new cell wall material. Mass increase proceeded in the presence of Rod system inhibitors, but cells lysed upon inhibition of aPBPs, suggesting that aPBPs are required for structural integrity under these conditions. The Rod system, although not essential for the observed mass increase, remained functional even after prolonged EP depletion. Last, heterologous expression of an EP from Neisseria gonorrhoeae fully complemented growth and morphology of an EP-insufficient V. cholerae, highlighting the possibility that the PG synthases may not necessarily function via direct interaction with EPs. Overall, our findings suggest that during EP insufficiency in V. cholerae, aPBPs become essential for structural integrity while the Rod system is unable to promote proper cell expansion. IMPORTANCE Synthesis and turnover of the bacterial cell wall must be tightly coordinated to avoid structural integrity failure and cell death. Details of this coordination are poorly understood, particularly if and how cell wall turnover enzymes are required for the activity of the different cell wall synthesis machines, the aPBPs and the Rod system. Our results suggest that in Vibrio cholerae, one class of turnover enzymes, the endopeptidases, are necessary for proper cell elongation and division. aPBPs become essential for maintaining structural integrity during EP insufficiency, while the Rod system remains active but contributes little to cell expansion under these conditions. Our results suggest that aPBPs are more versatile than the Rod system in their ability to recognize cell wall gaps formed by autolysins other than the major endopeptidases, adding to our understanding of the coordination between autolysins and cell wall synthases. A detailed understanding of autolysin biology may promote the development of antibiotics that target these essential turnover processes.

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