Water, signaling and hydraulic architecture (Aqua)

Group leader : Christophe Maurel
CNRS Research Director

 

 

Key words

Aquaporin, Cell signaling, Hydraulics, Phosphorylation, Roots, Water stress, Water transport

Presentation

The Aqua team studies the different modes of water transport in plant tissues. The main objective is to understand how these processes are regulated by water availability, and linked to plant growth and responses to environmental stresses. Supported by national (ANR) and European (ERC) funding, the team combines studies on the model plant Arabidopsis thaliana and maize.

A first axis concerns cell signalling processes. The early mechanisms of plant response to water stress are investigated through molecular (interactomics, proteomics) and high-resolution microscopy approaches. A particular focus is made on the role of membrane nanodomains, reactive oxygen species and protein phosphorylation. These processes are linked to the regulation of aquaporins, membrane channel proteins that facilitate the transport of water across cell membranes.

A second axis concerns the hydraulic architecture of roots. Quantitative genetics, root phenotyping and mathematical modelling are combined to describe the dynamics of root growth and hydraulics. The aim is to understand how they adapt to environmental constraints and water stress in particular, by integrating local and systemic signalling processes.

 

Team members
Main results

In the last few years, the team has uncovered novel functions and regulations of plant aquaporins. Proteins that physically interact with and regulate root aquaporins have been identified (Bellati et al., 2016). A novel post-translational mechanism that accounts for circadian oscillations of leaf hydraulic conductivity was described (Prado et al., 2019). We also uncovered a dual hydraulic and signaling role of aquaporins during the closing response of stomata to abscisic acid (ABA) (Grondin et al., 2015; Rodrigues et al., 2017). Here, aquaporins contribute to the signalling pathway of this stress hormone by facilitating the entry of hydrogen peroxide in the guard cell. The reactive oxygen species are also crucial during the early signalling responses of root cells to osmotic stress (Martinière et al., 2019).  

Quantitative genetic approaches have revealed new components of root hydraulics. A gene that encodes a protein kinase and regulates the root water permeability in response to combined oxygen limitation and potassium sufficiency identifies a novel mechanism for plant response to flooding stress (Shahzad et al., 2016). In addition, a transcription factor controls xylem vessel differentiation and determines a trade-off between abiotic and biotic stress resistance in Arabidopsis (Tang et al., 2018). These results reveal an unsuspected capability of plants to perceive and adapt to multiple environmental constraints. Finally, a coordinating role of ABA in the response of root hydraulic architecture to water deficit was recently uncovered (Rosales et al., 2019).

Significant publications

More than 30 articles in 5 years such as….

Rosales MA, Maurel C, Nacry P✉ (2019) Abscisic acid coordinates dose-dependent developmental and hydraulic responses of roots to water deficit. Plant Physiol., 180(4):2198-2211

Martinière A*✉, Fiche J-B*, Smokvarska M, Mari S, Alcon C, Dumont X, Hematy K, Jaillais Y, Nollmann M, Maurel C (2019) Osmotic stress activates two reactive oxygen species pathways with distinct effects on protein nanodomains and diffusion. Plant Physiol., 179(4):1581-1593

Prado K, Cotelle V, Li G, Bellati J, Tang N, Tournaire-Roux C, Martinière A, Santoni V, Maurel C✉ (2019) Oscillating aquaporin phosphorylations and 14-3-3 proteins mediate the circadian regulation of leaf hydraulics. Plant Cell, 31(2):417-429

Tang N, Shahzad Z, Lonjon F, Loudet O, Vailleau F, Maurel C✉ (2018) Natural variation at XND1 impacts root hydraulics and trade-off for stress responses in Arabidopsis. Nat. Commun., 9:3884

Rodrigues O, Reshetnyak G, Grondin A, Saijo Y, Leonhardt N, Maurel C, Verdoucq L✉ (2017) Aquaporins facilitate hydrogen peroxide entry into guard cells to mediate ABA- and pathogen-triggered stomatal closure. Proc. Natl. Acad. Sci. USA, 114(34):9200-9205

Shahzad Z, Canut M, Tournaire-Roux C, Martinière A, Boursiac Y, Loudet O, Maurel C✉ (2016) A potassium-dependent oxygen sensing pathway regulates plant root hydraulics. Cell, 167(1):87-98.e14

Bellati J, Champeyroux C, Hem S, Rofidal V, Krouk G, Maurel C, Santoni V✉ (2016) Novel aquaporin regulatory mechanisms revealed by interactomics. Mol. Cell. Proteomics, 15(11):3473-3487

Grondin A, Rodrigues O, Verdoucq L, Merlot S, Leonhardt N, Maurel C✉ (2015) Aquaporins contribute to ABA-triggered stomatal closure through OST1-mediated phosphorylation. Plant Cell, 27(7):1945-1954

Maurel C✉, Boursiac Y, Luu D-T, Santoni V, Shahzad Z, Verdoucq L (2015) Aquaporins in plants. Physiol. Rev., 95(4):1321-1358

Prado K, Boursiac Y, Tournaire-Roux C, Monneuse J-M, Postaire O, Da Ines O, Schäffner AR, Hem S, Santoni V, Maurel C✉ (2013) Regulation of Arabidopsis leaf hydraulics involves light-dependent phosphorylation of aquaporins in veins. Plant Cell, 25(3):1029-1039

Péret B*, Li G*, Zhao J*, Band LR*, Voß U, Postaire O, Luu D-T, Da Ines O, Casimiro I, Lucas M, Wells DM, Lazzerini L, Nacry P, King JR, Jensen OE, Schäffner AR✉, Maurel C✉, Bennett MJ✉ (2012) Auxin regulates aquaporin function to facilitate lateral root emergence. Nat. Cell Biol., 14(10):991-998

Collaborations
Funding

MIRGA « Architecture et croissance du système racinaire de maïs » (2016-2020).
An ANR project that involves, in addition to the Aqua team, the laboratory of Agroecology (INRA Dijon) and the plant biotechnology company Biogemma.

APLIM “Advanced Plant Life Imaging and Metrology” (2016-2020).
This contract is financed by the Agropolis Foundation. It aims to develop nuclear magnetic resonance techniques (NMR, MRI, nanoprobes) in plants and investigate their responses to abiotic and biotic stresses. It involves several institutes of Montpellier, specialized in plant sciences, physics and chemistry.

HyArchi “Targeting Root Hydraulic Architecture to improve Crops under Drought”(2018-2023)
This ERC Advanced project uses maize as a model cereal to study how root system architecture, its hydraulic properties and its environmental plasticity contribute to water uptake and plant resistance to drought.

TURGOMAP “Towards a mapping of turgor pressure in plant tissues “ (2018 – 2020)
A CNRS interdisciplinary program assembling several research groups from Montpellier, Lyon and Grenoble.

ABAqua “ABA-dependent control of plant hydraulics in plant acclimation to water deficit” (2019- 2022)
An ANR-DFG project that involves, in addition to the Aqua team, the Technische Universität München (Prof. Erwin Grill’s group).

CellOsmo “ Membrane nanodomains: Role in osmotic signaling” (2020-2024)
An ANR project supporting early stage researchers.

Former team members

Guowei Li, Shandong Academy of Agricultural Sciences, Jinan, China : swzxliguowei@shandong.cn

Karine Prado, Carnegie Institution for Science, Stanford, USA : kprado@carnegiescience.edu

Alexandre Grondin, IRD, Montpellier :                            alexandre.grondin@ird.fr

Olivier Rodrigues, Texas A&M University, USA:            olivier-rodrigues@laposte.net

Zaigham Shahzad, University of Glasgow, UK :               Zaigham.Shahzad@glasgow.ac.uk

Jorge Bellati, Montpellier :                                                jbellati@gmail.com

Ning Tang, Wuhan University, China:                               tangningwww@163.com

Chloé Champeyroux, ETH, Zürich, Switzerland:             chloe.champeyroux@biol.ethz.ch

Monica Calvo, Montpellier :                                              mcalvopolanco@gmail.com

Miguel Rosales, IRNAS-CSIC, Sevilla, Spain:                   mrosales@irnas.csic.es

Developmental control of plant Rho GTPase nano-organization by the lipid phosphatidylserine

Phosphatidylserine is required for the clustering of ROP6, a small guanosine triphosphatase (GTPase), in membranes in response to signals from the plant hormone auxin. Changes in phosphatidylserine concentration altered the clustering of ROP6 and thus the auxin signaling response

Georges Morel Prize (French Academy of Sciences)

The Georges Morel 2018 prize was awarded to Christophe Maurel, deputy director of BPMP and head of the Aquaporin team. This biennial prize was created in 2013. It rewards a scientist who conducted an outstanding research work in plant biology in a French laboratory.

Natural variation at XND1 impacts root hydraulics and trade-off for stress responses in Arabidopsis

Tang N, Shahzad Z, Lonjon F, Loudet O, Vailleau F, Maurel C (2018) Natural variation at XND1 impacts root hydraulics and trade-off for stress responses in Arabidopsis. Nat. Commun., 9:3884 This work shows that, by inhiting the differentiation of xylem vessels in root...

How drought affects plant roots

Crops may face increasing levels of drought due to a changing climate. Plant scientists funded by the EU investigated the molecular and physiological mechanisms underlying root water transport function during drought conditions. [ Lire l’article ]

Root architecture discoveries could help breed drought-resistant crops

Roots and plant resistance to drought, flagship progress of UMR B&PMP at the European level. A freesia’s root architecture helps the plant store food to survive seasonal weather conditions. Image credit – Brian Atkinson We should breed new varieties of crops...

MISTRAL 2018

July 2-13, 2018 – Montpellier International School on ion and water TRAnsport in PLant

Logo du ERC

Christophe Maurel (B&PMP, Aquaporins team), grantee of the ” ERC Advanced Grant 2017 “!

The project, named “HyArchi”, will use maize as a model cereal to investigate how the architecture of the root system, its hydraulic properties and its environmental plasticity contribute to water uptake and to plant resistance to drought.

Thesis defended by Thi Thu Huyen Chu

April 4, 2018 – Cell biology of aquaporins in rice (Oryza sativa L.)

Thesis defended by Chloé Champeyroux

Nov. 29, 2017 – Functional characterisation of proteins interacting with the aquaporin PIP2;1