The role of Arabidopsis Actin-Related Protein 3 in amyloplast sedimentation and polar auxin transport in root gravitropism

Zou, Junjie; Zheng, Zhongyu; Xue, Shan; Li, Han-Hai; Wang, Yuren; Le, Jie

doi:10.1093/jxb/erw294

Cited by 35 publications

(30 citation statements)

References 84 publications

(128 reference statements)

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“…This last hypothesis is supported by studies using actin inhibitors or actin mutants showing a decrease of saltation motion in Arabidopsis thaliana stems ( 14 , 17 ). However, disrupting actin also decreases the cytoplasm viscosity and speeds up the diffusion of statoliths in other systems (roots) ( 18 , 23 ), making the interpretation of these mutant or drug-based experiments difficult.…”

Section: Resultsmentioning

confidence: 99%

“…Experiments using actin inhibitors and mutants inducing a fragmentation of AFs also reported a reduction of the saltatory motion of statoliths ( 17 ), suggesting a key role of actin in statolith agitation. However, actin inhibitors also decrease the cytoskeleton viscosity, making statoliths more mobile ( 18 , 23 ). Our study shows that it is possible to disentangle both effects.…”

Section: Discussionmentioning

confidence: 99%

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Gravisensors in plant cells behave like an active granular liquid

Bérut

Chauvet

Legué

et al. 2018

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

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SignificanceThe sensor of gravity in plants consists of tiny starch-rich grains called statoliths that sediment and form miniature granular piles at the bottom of the gravisensing cells. How such a sensor could be a reliable clinometer is unclear, as granular materials are known to display jamming and finite avalanche angles. Here we address this issue by comparing statolith avalanches in plant cells to microfluidic avalanches of Brownian particles in biomimetic cells. We reveal that statoliths behave like a liquid, not a granular material, due to the cell activity that strongly agitates statoliths. Our study elucidates the physical grounds of the high sensitivity of plants to gravity and bridges the active microrheology of statoliths to the macroscopic response of the plant.

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Section: Resultsmentioning

confidence: 99%

Section: Discussionmentioning

confidence: 99%

Gravisensors in plant cells behave like an active granular liquid

Bérut

Chauvet

Legué

et al. 2018

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

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“…The sgr9 mutant of Arabidopsis exhibited reduced stem gravitropism and amyloplast sedimentation because of denser network of actin filaments enmeshed amyloplasts and reduced their normal sedimentation (Nakamura et al, 2011). In central columella cells of Arabidopsis root it was also found that ARP3 mutants display thick actin bundles surrounding amyloplasts that possibly affect amyloplast kinetics, indicating that actin cytoskeleton may regulate amyloplast movement through regulating local viscosity of the cells (Zou et al, 2016). However, the intracellular environments in shoot and root endodermal cells differ considerably (Blancaflor, 2013).…”

Section: Discussionmentioning

confidence: 99%

Arabidopsis Myosins XI1, XI2, and XIK Are Crucial for Gravity-Induced Bending of Inflorescence Stems

et al. 2016

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Myosins and actin filaments in the actomyosin system act in concert in regulating cell structure and dynamics and are also assumed to contribute to plant gravitropic response. To investigate the role of the actomyosin system in the inflorescence stem gravitropism, we used single and multiple mutants affecting each of the 17 Arabidopsis myosins of class VIII and XI. We show that class XI but not class VIII myosins are required for stem gravitropism. Simultaneous loss of function of myosins XI1, XI2, and XIK leads to impaired gravitropic bending that is correlated with altered growth, stiffness, and insufficient sedimentation of gravity sensing amyloplasts in stem endodermal cells. The gravitropic defect of the corresponding triple mutant xi1 xi2 xik could be rescued by stable expression of the functional XIK:YFP in the mutant background, indicating a role of class XI myosins in this process. Altogether, our results emphasize the critical contributions of myosins XI in stem gravitropism of Arabidopsis.

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“…Several papers also indicated that actin in the cytoskeleton has a significant role in gravity signaling, as pressure exerted by sedimentation of statoliths on actin polymers could conduct a physical pressure signal toward the plasma membrane or ER membrane, causing ion channels to open (Yoder et al, 2001;Perbal and Driss-Ecole, 2003). Additionally, the ARP3 subunit of the Actin-Related Protein 2/3 (ARP2/3) complex is involved in regulating amyloplast sedimentation kinetics, as Arabidopsis distorted1 (dis1) mutants lacking ARP3 display a delayed response to gravitropic stimulation (Zou et al, 2016). However, the exact role of the cytoskeleton deserves more attention, as pharmacological experiments gave contradictory results, showing both inhibition and promotion of gravitropism (Ma and Hasenstein, 2006;Blancaflor, 2013).…”

Section: Gravitropismmentioning

confidence: 99%

Root Tropisms: Investigations on Earth and in Space to Unravel Plant Growth Direction

et al. 2020

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Root tropisms are important responses of plants, allowing them to adapt their growth direction. Research on plant tropisms is indispensable for future space programs that envisage plant-based life support systems for long-term missions and planet colonization. Root tropisms encompass responses toward or away from different environmental stimuli, with an underexplored level of mechanistic divergence. Research into signaling events that coordinate tropistic responses is complicated by the consistent coincidence of various environmental stimuli, often interacting via shared signaling mechanisms. On Earth the major determinant of root growth direction is the gravitational vector, acting through gravitropism and overruling most other tropistic responses to environmental stimuli. Critical advancements in the understanding of root tropisms have been achieved nullifying the gravitropic dominance with experiments performed in the microgravity environment. In this review, we summarize current knowledge on root tropisms to different environmental stimuli. We highlight that the term tropism must be used with care, because it can be easily confused with a change in root growth direction due to asymmetrical damage to the root, as can occur in apparent chemotropism, electrotropism, and magnetotropism. Clearly, the use of Arabidopsis thaliana as a model for tropism research contributed much to our understanding of the underlying regulatory processes and signaling events. However, pronounced differences in tropisms exist among species, and we argue that these should be further investigated to get a more comprehensive view of the signaling pathways and sensors. Finally, we point out that the Cholodny-Went theory of asymmetric auxin distribution remains to be the central and unifying tropistic mechanism after 100 years. Nevertheless, it becomes increasingly clear that the theory is not applicable to all root tropistic responses, and we propose further research to unravel commonalities and differences in the molecular and physiological processes orchestrating root tropisms.

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The role of Arabidopsis Actin-Related Protein 3 in amyloplast sedimentation and polar auxin transport in root gravitropism

Abstract: HighlightArabidopsis actin-related protein ARP3 plays a role in amyloplast sedimentation and polar auxin redistribution during root gravitropism.

Cited by 35 publications

References 84 publications

Gravisensors in plant cells behave like an active granular liquid

Gravisensors in plant cells behave like an active granular liquid

Arabidopsis Myosins XI1, XI2, and XIK Are Crucial for Gravity-Induced Bending of Inflorescence Stems

Root Tropisms: Investigations on Earth and in Space to Unravel Plant Growth Direction

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