# Gravisensing in plants

Nicole Brunel-Michac, François Bizet, Valérie Legué, Bruno Moulia, Antoine

Bérut, Hugo Chauvet-Thiry, Nicolas Levernier, Yoel Forterre, Olivier

Pouliquen

## ► To cite this version:

Nicole Brunel-Michac, François Bizet, Valérie Legué, Bruno Moulia, Antoine Bérut, et al. Gravisensing in plants. 28th European Low Gravity Research Association Biennial Symposium, European Low Gravity Research Association (ELGRA), Sep 2024, Liverpool United Kingdom, United Kingdom. hal-04906222

HAL Id: hal-04906222

https://uca.hal.science/hal-04906222v1

Submitted on 22 Jan 2025

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<figure><img src="image_1.png" /></figure>

Distributed under a Creative Commons Attribution 4.0 International License
# Gravisensing in plants: the contribution of ground and space experiments. Unresolved questions

Valérie Legué

<figure><img src="image_2.png" /></figure>

N. Brunel-Michac, F. Bizet, V. Legué, B. Moulia

INRAe and Université Clermont Auvergne, PIAF, France

A. Bérut, H. Chauvet, N. Levernier, Y. Forterre, O. Pouliquen

CNRS & Aix Marseille Université, IUSTI, France
At the beginning of gravitropism response...gravisensing

<figure><img src="image_3.png" /></figure>

Amyloplasts: a sensor made of starch-rich grains

Hormone flux (auxin)

↓

Differential growth and
bending of organ
# Amyloplasts: a star in the gravisensing!

## A series of successful studies

<figure><img src="image_4.png" /><figcaption>### Deformation of the Endoplasmic Reticulum</figcaption></figure>

(Leitz et al 2009)

<figure><img src="image_5.png" /><figcaption>### Interaction/Deformation of actin cytoskeleton</figcaption></figure>

(Perbal and Driss-Ecole, 2003)

<figure><img src="image_6.png" /><figcaption>### Protein interactions and translocation</figcaption></figure>

<figure><img src="image_7.png" /></figure>

(Strohm et al 2014)

<figure><img src="image_8.png" /></figure>

(Chen et al, 2023; Nishimura et al, 2023)
Amyloplasts: a star in the gravisensing!

- How does the sensor work? Pressure ? Contact ? Displacement/motion ?

- Role of the granular nature of the sensor?
How could the relevant measurements of gravi-response
help us for
understanding the cellular events of gravi-sensing?

➤ Using the relevant measurements of gravi-response
# Relevant Measurements of Gravitropic response

<figure><img src="image_9.png" /></figure>

<figure><img src="image_10.png" /></figure>

Dynamics of the response:

* Dynamics of Tip angle velocity (linear phase)

* Growth rate

* Radius of organ

$$ \text{The relevant measure for the gravitropic response} = \frac{\Delta \dot{\varepsilon}}{\dot{\varepsilon}} = \frac{R}{\dot{\varepsilon}} \frac{dC}{dt} \approx R \frac{d\theta_{tip}}{dL} \frac{d\theta_{tip}}{dt} $$
What is detected (gravity, angle) at cellular level ?

<figure><img src="image_11.png" /></figure>
# One classical result: the sine-law

**At organ scale:**

The response is proportional to the sine of
the inclinaison (in permanent inclinaison)

► **The sin-law**

see also Sacks 1882, Audus 1964....

**At cellular scale:**

Gravitropic signal comes from the weight
of the statoliths on the lateral side of the
cell

► **Statoliths: a force sensor ?**

<figure><img src="image_12.png" /></figure>

lino et al. 1996

<figure><img src="image_13.png" /></figure>
One classical result: the sine-law

Biological explanation: The statocyte sense the statolith (amyloplast) pressure

<figure><img src="image_14.png" /><figcaption>Deformation of actin cytoskeleton
(Perbal and Driss-Ecole, 2003)</figcaption></figure>

<figure><img src="image_15.png" /></figure>
If statolith: a force sensor

The response should be proportional to the gravity (intensity) ? influence of “g”?

<figure><img src="image_16.png" /></figure>
# Test of the Force sensor hypothesis

wheat coleoptiles, grown in dark

<figure><img src="image_17.png" /></figure>

$$ \text{The relevant measure for the gravitropic response} = \frac{\Delta \dot{\varepsilon}}{\dot{\varepsilon}} = \frac{R}{\dot{\varepsilon}} \frac{dC}{dt} \approx R \frac{d\theta_{tip}}{dt} \frac{dL}{dt} $$

<figure><img src="image_18.png" /></figure>

## ➤ Gravi-sensitivity to permanent inclination: the sine-law
Test of the Force sensor hypothesis

<figure><img src="image_19.png" /></figure>

Chauvet et al. 2016

<figure><img src="image_20.png" /></figure>

The sine-law does not depend on g !

<figure><img src="image_21.png" /></figure>

The plant gravisensor is NOT a force sensor

<figure><img src="image_22.png" /></figure>

Chauvet et al. 2016
Another hypothesis:

The final position of the statoliths being independent of gravity
(only inclination)

<figure><img src="image_23.png" /></figure>

Statolith: A position sensor?

<figure><img src="image_24.png" /></figure>

implies that the statoliths have to move and change position to induce a signal.

<figure><img src="image_25.png" /></figure>
# Test of the position sensor hypothesis
## Visualizing *in vivo* statolith motion

<figure><img src="image_26.png" /><figcaption>Statolith motion: granular avalanche?</figcaption></figure>

<figure><img src="image_27.png" /><figcaption>Wheat coleoptiles cuts and observed on horizontal microscope</figcaption></figure>

<figure><img src="image_28.png" /></figure>

<figure><img src="image_29.png" /></figure>

g↓

<figure><img src="image_30.png" /></figure>
# Statolith avalanche dynamics

<figure><img src="image_31.png" /></figure>

<figure><img src="image_32.png" /></figure>

Bérut et al, 2018

- The statolith pile angle relaxes to zero... as a liquid like-behaviour

- Two different regimes: granular avalanche (2 min) + slow creep (10-20 min)

Unlike a classical granular material, statoliths move as **liquid-like behaviour on long time**
Studies support this hypothesis ?
# Results from microgravity... Analysis of statolith positioning

<figure><img src="image_33.png" /></figure>

<figure><img src="image_34.png" /><figcaption>Microgravity:
Statoliths form a cluster</figcaption></figure>

<figure><img src="image_35.png" /></figure>

<figure><img src="image_36.png" /><figcaption>Following gravistimuli:
Statolith complex occupies an identical space and move collectively</figcaption></figure>

<figure><img src="image_37.png" /></figure>
# Results from microgravity...Analysis of calcium precipitates

## Density of calcium precipitates

<table><thead><tr><td>Condition</td><td>Number of precipitates /10 µm²</td></tr></thead><tbody><tr><td>µg</td><td>1.0 ± 0.2 (6)</td></tr><tr><td>µg + 0.01g-9h</td><td>1.0 ± 0.2 (6)</td></tr><tr><td>µg + 2g-5min</td><td>0.9 ± 0.1 (12)</td></tr><tr><td>µg + 2g-15min</td><td>1.1 ± 0.1 (12)</td></tr></tbody></table>

<figure><img src="image_38.png" /></figure>

The displacement of amyloplasts-complex:

No impact on the number of calcium precipitates density and neither of their localisation

<figure><img src="image_39.png" /></figure>

Supports the position sensor hypothesis ?
Interaction protein on amyloplasts

<figure><img src="image_40.png" /><figcaption>Protein interactions
(Strohm et al 2014)</figcaption></figure>

<figure><img src="image_41.png" /></figure>

Amyloplast sedimentation repolarizes LAZYs
(Chen et al, 2023)

LZY translocation from statoliths to the plasma
membrane (Nishimura et al, 2023)

« LZY appears to act as a signal molecule that transmits the positional information of statoliths to the PM » (Nishimura et al, 2023)
Origin of the liquid-like behavior? Agitation!

<figure><img src="image_42.png" /></figure>

Relaxation of the heap slope to zero angle because of
the random motion of the statoliths ?

Where does agitation come from ?
## Individual Statolith agitation

<figure><img src="image_43.png" /></figure>

<figure><img src="image_44.png" /></figure>

## Individual Statoliths Exhibit Random Motion
Origin of the liquid-like behavior? Agitation!

<figure><img src="image_45.png" /></figure>

Relaxation of the heap slope to zero angle
because of the random motion of the statoliths ?

<figure><img src="image_46.png" /></figure>

<figure><img src="image_47.png" /></figure>

Cytoskeleton activity ?
Home message

- Statocyte: a **position sensor** and not a stress/force sensor

- Sensitivity due to the **agitation** of the statoliths pile induced by the activity of cytoskeleton...

= a highly sensitive position sensor thanks to the cytoskeleton-induced statolith agitation
And now

What's missing in our gravisensing story ?

Link statoliths position to auxin transport

From proposed models:
Levernier et al Front. Plant Sci. 2021
Meroz's team

Permanent and transient stimuli
Thanks

<figure><img src="image_48.png" /></figure>

PIAF

N. Brunel-Michac, F. Bizet, V. Legué, B. Moulia

INRAe and Université Clermont Auvergne, PIAF, France

A. Bérut, H. Chauvet, N. Levernier, Y. Forterre, O. Pouliquen

CNRS & Aix Marseille Université, IUSTI, France