Integration of nutrient signaling pathways | Institut des Sciences des Plantes de Montpellier

Nitrate signaling and regulation by the environment

Group leader: Antoine Martin
Senior Scientist CNRS

Key words

nitrogen nutrition, transport and sensing of nitrate, N and C signaling, root development, climate change

Presentation

Our group investigates the mechanisms governing the uptake of nitrate by plant roots.

Nitrate (NO₃^–) is the main nitrogen (N) source for the nutrition of most plant species. Its uptake by the roots is the first step of the inorganic nitrogen assimilation process, which is, as photosynthesis, a fundamental function at the basis of plant autotrophy. Moreover, it constitutes a key factor of crop productivity that now must take into account the urgent needs for lower nitrogen fertilizer input and adaptation to global climate change. These considerations are at the heart of the development of sustainable and environmentally-friendly agriculture.

Our work focuses on two main components controlling root nitrate acquisition: the membrane transport systems for nitrate and the root system architecture. The main aim is to identify molecular mechanisms allowing the plants to modulate root nitrate uptake in response to changes in external nitrate availability or in their own nutritional status (N starvation or satiety, fluctuations of photosynthesis, CO2 elevation).

We mostly study, in Arabidopsis thaliana, mechanisms involved in the sensing of nitrate, in the regulation of nitrate transport systems, and in the control of root development.

Our approach is integrative as it aims to understand (i) how one specific signaling pathway allows the coordination between physiological and developmental responses (nitrate transport and root development, respectively), (ii) how various regulatory mechanisms acting at separate levels (transcription factors, chromatin dynamics, protein expression and trafficking, protein/protein interactions, posttranslational modifications) contribute to the same functional response, and (ii) how different signaling pathways interact to trigger an integrated response of the roots to separate signals (e.g., nitrogen and carbon signals).

We use molecular physiology, functional genomics and systems biology approaches: transcriptomics, gene networks modeling, proteomics, reverse genetics, functional phenotyping, root architecture analysis, imaging, isotope labeling.

Team members

Main results

For more than 15 years, our group has been at the forefront of the functional characterization of membrane nitrate transporters (e.g., NRT2.1), and of the identification of their regulatory mechanisms (regulation by nitrate, by whole plant N status, and by photosynthesis).
See: Lejay et al. 1999, Cerezo et al. 2001, Lejay et al. 2003, Wirth et al. 2007, Lejay et al. 2008, Widiez et al. 2011, Laugier et al. 2012, de Jong et al. 2014, Alvarez et al. 2014.
We have unravelled a novel mechanism of nitrate sensing involving the dual transport/sensing function of the nitrate transporter (transceptor) NRT1.1/NPF6.3. NRT1.1/NPF6.3 triggers many different responses of the plant to nitrate, including regulation of other nitrate transporters and regulation of lateral root growth.
See: Muños et al. 2004, Remans et al. 2006, Krouk et al. 2010, Gojon et al. 2011, Bouguyon et al. 2015, Bouguyon et al. 2016.

See also : prize of the French Academy of sciences: Nitrogen nutrition in plants: root growth guided by protein, and press releases: Les stratégies des plantes pour optimiser l’utilisation des nitrates (in French), Détection des ions minéraux par les plantes : du nouveau pour le nitrate et le phosphate (in French).
Our group has organized the EMBO Conference Nitrogen2016 (Third International Symposium on the Nitrogen Nutrition of Plants, August 2016, Montpellier, France), and has edited a special issue of the Journal of Experimental Botany associated with this conference (Special Issue: Nitrogen Nutrition in Plants: Rapid Progress and New Challenges).

Significant publications

Charoensawan V✉, Cortijo S✉, Domijan M✉, Negrão S✉ (2022) Multi-disciplinary approaches to plant responses to climate change. Front. Plant Sci., 13:876432

Hachiya T✉, Inaba J, Wakazaki M, Sato M, Toyooka K, Miyagi A, Kawai-Yamada M, Sugiura D, Nakagawa T, Kiba T, Gojon A, Sakakibara H (2021) Excessive ammonium assimilation by plastidic glutamine synthetase causes ammonium toxicity in Arabidopsis thaliana. Nat. Commun., 12:4944

Ruffel S*, Chaput V*, Przybyla-Toscano J, Fayos I, Ibarra C, Moyano TC, Fizames C, Tillard P, O’Brien JA, Gutiérrez RA, Gojon A, Lejay L✉ (2021) Genome-wide analysis in response to nitrogen and carbon identifies regulators for root AtNRT2 transporters. Plant Physiol., 186(1):696-714

Cassan O✉, Lèbre S, Martin A (2021) Inferring and analyzing gene regulatory networks from multi-factorial expression data: a complete and interactive suite. BMC Genomics, 22:387

Chu L-C, Offenborn JN, Steinhorst L, Wu XN, Xi L, Li Z, Jacquot A, Lejay L, Kudla J, Schulze W✉ (2021) Plasma membrane calcineurin B-like calcium-ion sensor proteins function in regulating primary root growth and nitrate uptake by affecting global phosphorylation patterns and microdomain protein distribution. New Phytol., 229(4):2223-2237

Ötvös K, Marconi M, Vega A, O’Brien JA, Johnson A, Abualia R, Antonielli L, Montesinos JC, Zhang Y, Tan S-T, Cuesta C, Artner C, Bouguyon E, Gojon A, Friml J, Gutiérrez RA, Wabnik K, Benková E✉ (2021) Modulation of plant root growth by nitrogen source-defined regulation of polar auxin transport. EMBO J., 40(3):e106862

Cortijo S, Bhattarai M, Locke JCW✉, Ahnert SE✉ (2020) Co-expression networks from gene expression variability between genetically identical seedlings can reveal novel regulatory relationships. Front. Plant Sci., 11:599464

Jacquot A, Chaput V, Mauriès A, Li Z, Tillard P, Fizames C, Bonillo P, Bellegarde F, Laugier E, Santoni V, Hem S, Martin A, Gojon A, Schulze W, Lejay L✉ (2020) NRT2.1 C-terminus phosphorylation prevents root high affinity nitrate uptake activity in Arabidopsis thaliana. New Phytol., 228(3):1038-1054

Maghiaoui A, Gojon A, Bach L✉ (2020) NRT1.1-centered nitrate signaling in plants. J. Exp. Bot., 71(20):6226-6237

Vidal EA, Alvarez JM, Araus V, Riveras E, Brooks MD, Krouk G, Ruffel S, Lejay L, Crawford NM, Coruzzi GM, Gutiérrez RA✉ (2020) Nitrate 2020: Thirty years from transport to signaling networks. Plant Cell, 32(7):2094-2119

Maghiaoui A*, Bouguyon E*, Cuesta C, Perrine-Walker F, Alcon C, Krouk G, Benková E, Nacry P, Gojon A, Bach L✉ (2020) The Arabidopsis NRT1.1 transceptor coordinately controls auxin biosynthesis and transport to regulate root branching in response to nitrate. J. Exp. Bot., 71(15):4480-4494

Chaput V, Martin A, Lejay L✉ (2020) Redox metabolism: the hidden player in carbon and nitrogen signaling? J. Exp. Bot., 71(13):3816-3826

Bellegarde F, Maghiaoui A, Boucherez J, Krouk G, Lejay L, Bach L, Gojon A, Martin A✉ (2019) The chromatin factor HNI9 and ELONGATED HYPOCOTYL 5 maintain ROS homeostasis under high nitrogen provision. Plant Physiol., 180(1):582-592

Bellegarde F, Herbert L, Séré D, Caillieux E, Boucherez J, Fizames C, Roudier F, Gojon A, Martin A✉ (2018) Polycomb Repressive Complex 2 attenuates the very high expression of the Arabidopsis gene NRT2.1. Sci. Rep.-UK, 8:7905

Bellegarde F, Gojon A, Martin A✉ (2017) Signals and players in the transcriptional regulation of root responses by local and systemic N signaling in Arabidopsis thaliana. J. Exp. Bot., 68(10):2553-2565

Jacquot A, Li Z, Gojon A, Schulze W, Lejay L✉ (2017) Post-translational regulation of nitrogen transporters in plants and microorganisms. J. Exp. Bot., 68(10):2567-2580

Ruffel S✉, Gojon A✉ (2017) Systemic nutrient signalling: On the road for nitrate. Nat. Plants, 3:17040

Bouguyon E, Perrine-Walker F, Pervent M, Rochette J, Cuesta C, Benková E, Martinière A, Bach L, Krouk G, Gojon A, Nacry P✉ (2016) Nitrate controls root development through post-transcriptional regulation of the NRT1.1/NPF6.3 transporter/sensor. Plant Physiol., 172(2):1237-1248

O’Brien JA, Vega A, Bouguyon E, Krouk G, Gojon A, Coruzzi GM, Gutiérrez RA✉ (2016) Nitrate transport, sensing and responses in plants. Mol. Plant, 9(6):837-856

Bouguyon E, Brun F, Meynard D, Kubeš M, Pervent M, Léran S, Lacombe B, Krouk G, Guiderdoni E, Zažímalová E, Hoyerová K, Nacry P, Gojon A✉ (2015) Multiple mechanisms of nitrate sensing by Arabidopsis nitrate transceptor NRT1.1. Nat. Plants, 1:15015

Alvarez JM, Riveras E, Vidal EA, Gras DE, Contreras-López O, Tamayo KP, Aceituno F, Gómez I, Ruffel S, Lejay L, Jordana X, Gutiérrez RA✉ (2014) Systems approach identifies TGA1 and TGA4 transcription factors as important regulatory components of the nitrate response of Arabidopsis thaliana roots. Plant J., 80(1):1-13

de Jong F, Thodey K, Lejay L, Bevan MW✉ (2014) Glucose elevates NITRATE TRANSPORTER2.1 protein levels and nitrate transport activity independently of its HEXOKINASE1-mediated stimulation of NITRATE TRANSPORTER2.1 expression. Plant Physiol., 164(1):308-320

Ruffel S, Gojon A, Lejay L✉ (2014) Signal interactions in the regulation of root nitrate uptake. J. Exp. Bot., 65(19):5509-5517

Nacry P✉, Bouguyon E, Gojon A (2013) Nitrogen acquisition by roots: physiological and developmental mechanisms ensuring plant adaptation to a fluctuating resource. Plant Soil, 370(1-2):1-29

Laugier E, Bouguyon E, Mauriès A, Tillard P, Gojon A, Lejay L✉ (2012) Regulation of high-affinity nitrate uptake in roots of Arabidopsis depends predominantly on post-transcriptional control of the NRT2.1/NAR2.1 transport system . Plant Physiol., 158(2):1067-1078

Gojon A✉, Krouk G, Perrine-Walker F, Laugier E (2011) Nitrate transceptor(s) in plants. J. Exp. Bot., 62(7):2299-2308

Widiez T*, El Kafafi ES*, Girin T, Berr A, Ruffel S, Krouk G, Vayssières A, Shen WH, Coruzzi GM, Gojon A, Lepetit M✉ (2011) HIGH NITROGEN INSENSITIVE 9 (HNI9)-mediated systemic repression of root NO₃^– uptake is associated with changes in histone methylation. P. Natl. Acad. Sci. USA, 108(32):13329-13334

Krouk G, Lacombe B, Bielach A, Perrine-Walker F, Malinska K, Mounier E, Hoyerová K, Tillard P, Leon S, Ljung K, Zažímalová E, Benková E, Nacry P, Gojon A✉ (2010) Nitrate-regulated auxin transport by NRT1.1 defines a mechanism for nutrient sensing in plants. Dev. Cell, 18(6):927-937

Gojon A✉, Nacry P✉, Davidian J-C✉ (2009) Root uptake regulation: a central process for NPS homeostasis in plants. Curr. Opin. Plant Biol., 12(3):328-338

Krouk G, Tranchina D, Lejay L, Cruikshank AA, Shasha DE, Coruzzi GM, Gutiérez RA✉ (2009) A systems approach uncovers restrictions for signal interactions regulating genome-wide responses to nutritional cues in Arabidopsis. PloS Comput. Biol., 5:e1000326

Lejay L✉*, Wirth J*, Pervent M, Cross J M-F, Tillard P, Gojon A (2008) Oxidative Pentose Phosphate Pathway-dependent sugar sensing as a mechanism for regulation of root ion transporters by photosynthesis. Plant Physiol., 146(4):2036-2053

Wirth J*, Chopin F*, Santoni V, Viennois G, Tillard P, Krapp A, Lejay L✉, Daniel-Vedele F, Gojon A (2007) Regulation of root nitrate uptake at the NRT2.1 protein level in Arabidopsis thaliana. J. Biol. Chem., 282(32):23541-23552

Remans T, Nacry P✉, Pervent M, Filleur S, Diatloff E, Mounier E, Tillard P, Forde BG, Gojon A (2006) The Arabidopsis NRT1.1 transporter participates in the signaling pathway triggering root colonization of nitrate-rich patches. P. Natl. Acad. Sci. USA, 103(50):19206-19211

Muños S, Cazettes C, Fizames C, Gaymard F, Tillard P, Lepetit M, Lejay L, Gojon A✉ (2004) Transcript profiling in the chl1-5 mutant of Arabidopsis reveals a role of the nitrate transporter NRT1.1 in the regulation of another nitrate transporter, NRT2.1. Plant Cell, 16:2433-2447

Lejay L, Gansel X, Cerezo M, Tillard P, Müller C, Krapp A, von Wirén N, Daniel-Vedele F, Gojon A✉ (2003) Regulation of root ion transporters by photosynthesis: functional importance and relation with hexokinase. Plant Cell, 15:2218-2232

Cerezo M, Tillard P, Filleur S, Muños S, Daniel-Vedele F, Gojon A✉ (2001) Major alterations of the regulation of root NO3- uptake are associated with the mutation of Nrt2.1 and Nrt2.2 genes in Arabidopsis. Plant Physiol., 127(1):262-271

Lejay L, Tillard P, Lepetit M, Olive FD, Filleur S, Daniel-Vedele F, Gojon A✉ (1999) Molecular and functional regulation of two NO3- uptake systems by N- and C-status of Arabidopsis plants. Plant J., 18(5):509-519

Collaborations

Nationales
- Nourollah Ahmadi / Emmanuel Guiderdoni, UMR AGAP, Cirad, Montpellier
- Anne Krapp / Christian Meyer, IJPB, INRA, Versailles
- François Roudier, UMR RDP, ENS, Lyon
- Christophe Salon, UMR Agro-écologie, INRA, Dijon
Internationales
- Rodrigo Gutiérrez, Université catholique du Chili
- Waltraud Schulze, Université Hohenheim, Allemagne
- Dennis Shasha, New York University, Etats Unis
- Yi-Fang Tsay, Academia Sinica, Taiwan
- Eva Zazimalova, Czech Academy of Sciences, République Tchèque