Low Concentrations of Propyzamide and Oryzalin Alter Microtubule Dynamics in Arabidopsis Epidermal Cells

Nakamura, Masayoshi; Naoi, Kuniko; Shoji, Tsubasa; Hashimoto, Takashi

doi:10.1093/pcp/pch300

Cited by 131 publications

(130 citation statements)

References 21 publications

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“…Factors other than simple dynamicity, however, may additionally contribute to the microtubule array organization. Low concentrations of microtubule depolymerization drugs cause less dynamic but more destabilized microtubules and right-handed helical arrays (17). Whether the microtubule population is biased toward polymerization or depolymerization would be another key to the array formation.…”

Section: Discussionmentioning

confidence: 99%

“…Fourday-old seedlings expressing GFP-TUB6 or GFP-EB1 were used for dynamic analysis in the epidermal cells of upper hypocotyls. Microscopy was done as described (16,17), using a DMRE microscope (Leica, Allendale, NJ) equipped with a CSU10 scanning head (Yokogawa, Tokyo, Japan) and ORCA-ER CCD camera (Hamamatsu Photonics, Shizuoka, Japan). Images were taken in the 16-bit tiff format every 4 sec during the course of 6 min for the analysis of GFP-TUB6 and during the course of 4 min for the analysis of GFP-EB1.…”

Section: Methodsmentioning

confidence: 99%

“…The GFP-TUB6 marker line (17) was used to analyze the dynamic behavior of cortical microtubules in the wild type and two select ␣-tubulin mutants. It should be noted that elongating epidermal cells of the light-grown upper hypocotyls, which were used for observation, had a more variable microtubule orientation than elongating root epidermal cells.…”

Section: Molecular Modeling Of Mutations On a Tubulin Heterodimermentioning

confidence: 99%

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Helical microtubule arrays in a collection of twisting tubulin mutants of Arabidopsis thaliana

Ishida

Kaneko

Iwano

et al. 2007

Proc. Natl. Acad. Sci. U.S.A.

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Anisotropic expansion of plant cells requires organized arrays of cortical microtubules. Mutations in microtubule-associated proteins and a particular mutation in ␣-tubulins were reported to cause abnormal microtubule arrays and result in helical growth in Arabidopsis thaliana. However, the way in which these mutations affect the organization of microtubules remains unknown. We here identified 32 Arabidopsis twisting mutants that have either missense or amino acid deletion mutations in ␣-or ␤-tubulins. Mutations were mapped to the GTPase-activating region in ␣-tubulin, intra-and interdimer interfaces of tubulin heterodimers, and lateral contact regions among adjacent protofilaments. These dominant-negative tubulin mutants were incorporated into the microtubule polymer and formed shallow helical arrays of distinct handedness along the long axis of the root epidermal cells. A striking correlation exists between the direction in which cortical helical arrays are skewed and the growth direction of elongating roots. The GTPase-activating-region mutant had left-handed helical arrays composed of highly stabilized microtubules, which could be decorated along the entire microtubule lattices with the otherwise tip-localized End Binding 1 protein. A mutation at the intradimer interface, on the other hand, generated highly dynamic microtubules and right-handed helical arrays. Cortical microtubules in wild type and these two tubulin mutants were composed mainly of 13 protofilaments. This comprehensive analysis of tubulin mutations provides insights into the mechanism by which tubulin structures influence microtubule dynamics and organization.dynamic instability ͉ GTPase-activating region ͉ helix D ifferentiated plant cells show a striking diversity of shapes that are important to their functions. As a plant cell expands under the force of turgor pressure, cellulose microfibrils in the wall function as the primary load-bearing structure, and their spatial arrangement generally determines the direction of cell expansion and final cell shape (1). A long-standing paradigm proposes that plasma membrane-associated microtubules direct or constrain the movement of the cellulose-synthesizing complex and thus dictate the deposition patterns of cellulose microfibrils, although the relationship between the cortical microtubules and cell morphogenesis may be more complicated (1, 2).Rapidly expanding cells in the roots and the etiolated hypocotyls grow longitudinally to form highly elongated cylindrical cells and possess arrays of cortical microtubules that are arranged largely perpendicular to the cell's long axis (3). The importance of transverse arrays for straight growth has been indicated by pharmacological studies and experiments with helical growth mutants of Arabidopsis thaliana. The rapidly elongating cells of these mutants skew consistently either to the right or to the left and exhibit cortical microtubule arrays that form shallow helices with fixed handedness (4). Plant-specific microtubule-associated proteins are mutated in t...

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Section: Discussionmentioning

confidence: 99%

Section: Methodsmentioning

confidence: 99%

Section: Molecular Modeling Of Mutations On a Tubulin Heterodimermentioning

confidence: 99%

See 1 more Smart Citation

Helical microtubule arrays in a collection of twisting tubulin mutants of Arabidopsis thaliana

Ishida

Kaneko

Iwano

et al. 2007

Proc. Natl. Acad. Sci. U.S.A.

Self Cite

150

184

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“…Enhanced rightward root skewing is observed when wild-type Landsberg erecta seedlings are grown on media containing 3 mM propyzamide, a b-tubulinbinding pronamide that affects microtubule dynamics and reorients microtubules in elongating epidermal cells to right-handed helices (Furutani et al, 2000;Nakamura et al, 2004). The latter observation was used to support a role for the alignment of cortical microtubules in CEZ epidermal cells in the control of root skewing on hard-agar surfaces (Furutani et al, 2000).…”

Section: Effects Of Propyzamide On Root Skewing and Cortical Microtubmentioning

confidence: 99%

Loss-of-Function Mutations of ROOT HAIR DEFECTIVE3 Suppress Root Waving, Skewing, and Epidermal Cell File Rotation in Arabidopsis

et al. 2005

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Wild-type Arabidopsis (Arabidopsis thaliana L. Heynh.) roots growing on a tilted surface of impenetrable hard-agar media adopt a wave-like pattern and tend to skew to the right of the gravity vector (when viewed from the back of the plate through the medium). Reversible root-tip rotation often accompanies the clockwise and counterclockwise curves that form each wave. These rotations are manifested by epidermal cell file rotation (CFR) along the root. Loss-of-function alleles of ROOT HAIR DEFECTIVE3 (RHD3), a gene previously implicated in the control of vesicle trafficking between the endoplasmic reticulum and the Golgi compartments, resulted in an almost complete suppression of epidermal CFR, root skewing, and waving on hard-agar surfaces. Several other root hair defective mutants (rhd2-1, rhd4-1, and rhd6-1) did not exhibit dramatic alterations in these root growth behaviors, suggesting that a generalized defect in root hair formation is not responsible for the surfacedependent phenotypes of rhd3. However, similar alterations in root growth behavior were observed in a variety of mutants characterized by defects in cell expansion (cob-1, cob-2, eto1-1, eto2-1, erh2-1, and erh3-1). The erh2-1 and rhd3-1 mutants differed from other anisotropic cell expansion mutants, though, by an inability to respond to low doses of the microtubule-binding drug propyzamide, which normally causes enhanced left-handed CFR and right skewing. We hypothesize that RHD3 may control epidermal CFR, root skewing, and waving on hard-agar surfaces by regulating the traffic of wall-or plasma membraneassociated determinants of anisotropic cell expansion.The primary roots of Arabidopsis (Arabidopsis thaliana L. Heynh.) seedlings display different growth behaviors depending on the conditions to which they are exposed. If grown within a homogenous environment (such as liquid or penetrable agar media), primary roots will grow downward in response to gravity (Blancaflor and Masson, 2003). When forced to grow on the surface of impenetrable hard-agar media, they will display more complex growth behaviors with characteristics dictated by the angle of the surface (Okada and Shimura, 1990). On surfaces tilted slightly forward, the roots of commonly used ecotypes will skew their growth to the right of the vertical when viewed through the agar medium, as per the established convention (Rutherford and Masson, 1996;Simmons et al., 1996). If the surface is tilted backward, roots will form waves in addition to skewing. This pattern results from the root tip pressing on the surface when gravitropism directs downward growth Shimura, 1990, 1992;Rutherford and Masson, 1996;Simmons et al., 1996;Thompson and Holbrook, 2004). Root waving is usually accompanied by a reversible rotation of the tip about its axis, which manifests itself by a twisting of epidermal cell files (cell file rotation [CFR]) along the root (Okada and Shimura, 1990). While curving to the right, roots tend to display left-handed CFR. By contrast, roots curving to the left display right-handed C...

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“…Microtubules are cytoskeletal polymers composed of α-and β-tubulin heterodimers. Microtubules are polarized with a fast growing plus end and a slow growing minus end, and exhibit dynamic behaviors such as rapid growth and shrinkage both in vivo and in vitro (Mitchison and Kirschner 1984; Horio and Hotani 1986; Sammak and Borisy 1988; Shaw et al 2003;Nakamura et al 2004). Cortical microtubules are specifically found in plant cells during interphase and are localized close to the cell cortex (Ledbetter and Porter 1963).…”

Section: Introductionmentioning

confidence: 99%

Structure, function, and evolution of plant NIMA-related kinases: implication for phosphorylation-dependent microtubule regulation

et al. 2015

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1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 59 IntroductionThe growth and morphogenesis of plant cells relies on the orientation of cellulose microfibrils and cortical microtubules. Microtubules are cytoskeletal polymers composed of α-and β-tubulin heterodimers. Microtubules are polarized with a fast growing plus end and a slow growing minus end, and exhibit dynamic behaviors such as rapid growth and shrinkage both in vivo and in vitro (Mitchison and Kirschner 1984; Horio and Hotani 1986; Sammak and Borisy 1988; Shaw et al. 2003;Nakamura et al. 2004). Cortical microtubules are specifically found in plant cells during interphase and are localized close to the cell cortex (Ledbetter and Porter 1963). Cortical microtubules align perpendicularly to the growth direction and regulate anisotropic growth and morphogenesis of rapidly expanding cells (Green 1962; Shibaoka 1994;Wasteneys 2002; Fig. 1). Findings from genetic studies of Arabidopsis thaliana mutants strongly support the essential roles of cortical microtubule arrays on directional cell growth (Whittington et al. 2001; Thitamadee et al. 2002; Abe et al. 2004; Ishida et al. 2007a; Ishida et al. 2007b; Sedbrook and Kaloriti 2008;Wasteneys and Ambrose 2009). In addition, microtubules regulate cell division and chromosome segregation. In the mitotic phase, microtubules form a series of arrays; a preprophase band that determines the future cell division plane, mitotic spindle that segregate chromosomes, and a phragmoplast that constructs the new cell plate ( 1 2 3 4 5 6 7 8 9 10 11 12 13 14 15 16 17 18 19 20 21 22 23 24 25 26 27 28 29 30 31 32 33 34 35 36 37 38 39 40 41 42 43 44 45 46 47 48 49 50 51 52 53 54 55 56 57 58 59 suggesting that cortical microtubules could also regulate directional cell growth independently of cellulose microfibrils (Sugimoto et al. 2003). Fujita et al. (2011) have shown that cortical microtubule abundance affects cellulose crystallinity to promote directional cell growth.Microtubules might regulate the mobility and stability of cellulose synthase complexes to affect physical properties of cellulose microfibrils. Because it is beyond the scope of this review, Interested readers could consult the recent literature and references therein (Bringmann et al. 2012; Fujita et al. 2012; Lei et al. 2014). In this review, we will summarize recent findings on microtubule regulation with focus on phosphorylation-dependent regulatory mechanisms. Microtubule regulationMicrotubule-associated proteins (MAPs) play pivotal roles in the regulation of microtubule dynamics (Hamada 2014). MAPs affect microtubule assembly and bundling and regulate their geometry and organization. Because the function and regulation of MAPs have been well described in detail, we show here a few examples from a cellular and developmen...

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Low Concentrations of Propyzamide and Oryzalin Alter Microtubule Dynamics in Arabidopsis Epidermal Cells

Cited by 131 publications

References 21 publications

Helical microtubule arrays in a collection of twisting tubulin mutants of Arabidopsis thaliana

Helical microtubule arrays in a collection of twisting tubulin mutants of Arabidopsis thaliana

Loss-of-Function Mutations of ROOT HAIR DEFECTIVE3 Suppress Root Waving, Skewing, and Epidermal Cell File Rotation in Arabidopsis

Structure, function, and evolution of plant NIMA-related kinases: implication for phosphorylation-dependent microtubule regulation

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