Multiscale mechanical signaling in plants

Project Information

MUSIX

Grant agreement ID: 101019515

DOI

10.3030/101019515

EC signature date 13 August 2021

Start date 1 October 2021

End date 30 September 2026

Funded under

• EXCELLENT SCIENCE - European Research Council (ERC)

Total cost

€ 2 176 170,00

EU contribution

€ 2 176 170,00

Coordinated by

INSTITUT NATIONAL DE RECHERCHE POUR L'AGRICULTURE, L'ALIMENTATION ET L'ENVIRONNEMENT
France

Periodic Reporting for period 2 - MUSIX (Multiscale mechanical signaling in plants)

Reporting period: 2023-04-01 to 2024-09-30

Summary of the context and overall objectives of the project

During development, living organisms change shape and thus also change structure. The resulting pattern of force controls cell behavior and thus development. However, the molecular mechanoperception mechanisms involved are only partially understood and how organs integrate local and global patterns of forces is another open question. Plants are ideal systems to study the multicellular implications of mechanotransduction in development because their mechanics is mainly mediated by the cell wall and cells do not move. In past work, we showed that microtubules align with maximal tensile stress direction in planta, thereby guiding the deposition of stiff cellulose microfibrils in cell walls, thus altering organ shape in a feedback loop. Based on our preliminary data, we will test the hypothesis that microtubules are their own mechanosensors, and that wall sensing interferes with this response to account for cell geometry or intercellular cues. The main technical breakthrough behind MUSIX is the introduction of a novel, high-throughput, single cell system in which the wall is replaced by an artificial well, enabling its mechanics and chemistry to be modulated. This simpler approach will allow us to dissect the contribution of wall components in mechanosensing in the absence of interfering global molecular cues. We will then integrate these biophysical mechanisms in multicellular development. Using natural and artificial mosaics (Cre-Lox system) in plant organoids and real organs, we will explore how the autonomous microtubule response to stress integrates mechanical conflicts between adjacent cells in tissues through wall sensing. This work has important implications beyond plant science, including cell signaling (how cells perceive their environment), developmental proprioception (how organs perceive and monitor their own shape and growth), compensation (how organs manage growth-derived mechanical conflicts) and robustness (how tissues manage growth fluctuations).

Beyond the importance for scientific knowledge on mechanotransduction and a central cell biology effector (microtubules) and their many implications in development, the emerging concept of biological robustness has also fed a narrative that is relevant for the much larger question of socio-ecological crisis. As we enter the "polycrisis" world, how cells deal with fluctuations with "suboptimal solutions" can be inspiring, especially when considering that we, humans, tend to favor the most efficient, and thus most fragile, route instead. Biology rather tells us that in a turbulent environment, we should de-optimize to increase robustness. This project thus also fuels a societal debate that goes much beyond microtubules, mechanotransduction and plant morphogenesis, with an increasing societal impact (media coverage, books, etc.)

Work performed from the beginning of the project to the end of the period covered by the report and main results achieved so far

The project is going very well. Today, from this ERC project:

6 research articles are now published:
• Nakayama et al., 2022 Journal of Cell Science
• Asaoka et al., 2023 Development
• Trinh et al., 2023 PNAS
• Correa et al., 2024 Cereal chemistry
• Asaoka et al., 2024 Journal of Plant Research
• Trinh et al., 2024 Biology letters

4 review articles are now published:
• Kirchhelle and Hamant, 2023 Current Opinion Cell Biology
• Malivert and Hamant, 2023 Nature plants
• Arico, Dickmann et al., 2023 The Cell surface
• Hamant, 2024 Anthropocene review

2 research articles are accepted
• Trinh et al., Nature plants
• Melogno, Takatani et al., PNAS

1 research article is under revision:
• Alonso-Serra et al., Nature communications

1 research article is submitted:
• Xu et al., Current Biology

6 research articles are in preparation:
• Trinh et al., (on cell walls in vip3)
• Malivert et al., (on FER and hydraulics)
• Dickmann et al., (on plant filopods)
• Romeiro Motta et al., (on MAP65 and microtubule nucleation)
• Arico et al., (on the molecular bases of Hechtian strands)
• Correa et al., (on quantitative methods for citizen science)

In parallel to this work, I have been involved in several science & society activities, notably on the question of biological robustness (emerging from this ERC project and previous work) with important insights for the socio-ecological crisis. In short, this research project also shows how robustness emerges from suboptimality, i.e. inefficiencies fueling adaptability. On this topic,
I published 4 books:
• La troisième voie du vivant, Ed. Odile Jacob (2022), now translated in English: The benefits of imperfection, Ed. Taylor and Francis (2024)
• Antidote au culte de la performance – la robustesse du vivant, Ed. Gallimard (2023) now translated in English: Antidote to the cult of performance – Robustness from nature, Ed. Gallimard (2024)
• Manifeste pour une santé commune, Ed. Utopia (2023), not translated
• De l’incohérence – Philosophie politique de la robustesse, Ed. Odile Jacob (2024), not translated
These books have met an audience - in particular, 12'000 copies of the "Antidote" have been sold since September 2023 (which is unusual for a systems biology / society book).
I published 4 articles for the science community
• Hamant, 2022 Quantitative Plant Biology
• Hamant, 2024 Quantitative Plant Biology
• Hamant, 2024, Anthropocene review (in press)
• Collste, in prep, Global sustainability
I also published several tribunes in major newspaper (Le Monde, Libération, etc.)
I recorded a MOOC (in French) on “Construire la robustesse” (Sator.fr)
I contributed to the debate in major media (RTBF, Radio France, etc.) and in formations to stakeholders (CEOs, students, politicians, etc.).

Progress beyond the state of the art and expected potential impact (including the socio-economic impact and the wider societal implications of the project so far)

This work is groundbreaking in many ways: we proposed that water acts as a morphogen to define organ boundaries (Alonso-Serra), we discovered a new microtubule organization pre-mitosis, reflecting a mechanism that makes the cell transiently less sensitive to mechanical stress (Melogno), we identified a new animal-like behavior of plant cells exhibiting filopod-like structures (Dickmann), and we demonstraed that the scale at which mechanical conflict occur can increase or decrease organ shape robustness (Trinh). Other results are being consolidated, notably the role of MAP65 in microtubule dynamics, or the role of glutamate in mechanosensing. Last, the bio-inspired question of robustness built against performance also appears ground-breaking in the socio-economic field, and displays strong momentum with many invitations to talk about it in different circles.

meristem-mts2.jpg