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Identification of Molecular Integrators Shows that Nitrogen Actively Controls the Phosphate Starvation Response in Plants

Anna Medici, Wojciech Szponarski, Pierre Dangeville, Alaeddine Safi, Indeewari Madhubhashini Dissanayake, Chorpet Saenchai, Amélie Emanuel, Vicente Rubio, Benoît Lacombe, Sandrine Ruffel, Milos Tanurdzic, Hatem Rouached, Gabriel Krouk
Anna Medici
BPMP, Univ Montpellier, CNRS, INRA, SupAgro, Montpellier, France
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  • ORCID record for Anna Medici
  • For correspondence: anna.medici@supagro.fr
Wojciech Szponarski
BPMP, Univ Montpellier, CNRS, INRA, SupAgro, Montpellier, France
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  • ORCID record for Wojciech Szponarski
Pierre Dangeville
BPMP, Univ Montpellier, CNRS, INRA, SupAgro, Montpellier, France
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  • ORCID record for Pierre Dangeville
Alaeddine Safi
BPMP, Univ Montpellier, CNRS, INRA, SupAgro, Montpellier, France
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  • ORCID record for Alaeddine Safi
Indeewari Madhubhashini Dissanayake
School of Biological Sciences, University of Queensland, Brisbane 4072, Queensland, Australia
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  • ORCID record for Indeewari Madhubhashini Dissanayake
Chorpet Saenchai
BPMP, Univ Montpellier, CNRS, INRA, SupAgro, Montpellier, France
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  • ORCID record for Chorpet Saenchai
Amélie Emanuel
BPMP, Univ Montpellier, CNRS, INRA, SupAgro, Montpellier, France
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  • ORCID record for Amélie Emanuel
Vicente Rubio
Centro Nacional de Biotecnología-Consejo Superior de Investigaciones Cientificas, Darwin 3, Campus de la Universidad Autónoma Madrid, Cantoblanco, 28049, Madrid, Spain
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Benoît Lacombe
BPMP, Univ Montpellier, CNRS, INRA, SupAgro, Montpellier, FranceInstitut Claude Grignon, Biochime et Physiologie Moleculaire des Plantes, Centre National de la Recherche Scientifique, 34060 Montpellier, France
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Sandrine Ruffel
BPMP, Univ Montpellier, CNRS, INRA, SupAgro, Montpellier, France
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  • ORCID record for Sandrine Ruffel
Milos Tanurdzic
School of Biological Sciences, University of Queensland, Brisbane 4072, Queensland, Australia
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Hatem Rouached
BPMP, Univ Montpellier, CNRS, INRA, SupAgro, Montpellier, France
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Gabriel Krouk
BPMP, Univ Montpellier, CNRS, INRA, SupAgro, Montpellier, FranceInstitut Claude Grignon, Biochime et Physiologie Moleculaire des Plantes, Centre National de la Recherche Scientifique, 34060 Montpellier, France
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  • ORCID record for Gabriel Krouk
  • For correspondence: anna.medici@supagro.fr

Published May 2019. DOI: https://doi.org/10.1105/tpc.18.00656

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  • © 2019 American Society of Plant Biologists. All rights reserved.

Abstract

Nitrogen (N) and phosphorus (P) are key macronutrients sustaining plant growth and crop yield and ensuring food security worldwide. Understanding how plants perceive and interpret the combinatorial nature of these signals thus has important agricultural implications within the context of (1) increased food demand, (2) limited P supply, and (3) environmental pollution due to N fertilizer usage. Here, we report the discovery of an active control of P starvation response (PSR) by a combination of local and long-distance N signaling pathways in plants. We show that, in Arabidopsis (Arabidopsis thaliana), the nitrate transceptor CHLORINA1/NITRATE TRANSPORTER1.1 (CHL1/NRT1.1) is a component of this signaling crosstalk. We also demonstrate that this crosstalk is dependent on the control of the accumulation and turnover by N of the transcription factor PHOSPHATE STARVATION RESPONSE1 (PHR1), a master regulator of P sensing and signaling. We further show an important role of PHOSPHATE2 (PHO2) as an integrator of the N availability into the PSR since the effect of N on PSR is strongly affected in pho2 mutants. We finally show that PHO2 and NRT1.1 influence each other’s transcript levels. These observations are summarized in a model representing a framework with several entry points where N signal influence PSR. Finally, we demonstrate that this phenomenon is conserved in rice (Oryza sativa) and wheat (Triticum aestivum), opening biotechnological perspectives in crop plants.

  • Received August 30, 2018.
  • Revised February 26, 2019.
  • Accepted March 13, 2019.
  • Published March 14, 2019.
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Identification of Molecular Integrators Shows that Nitrogen Actively Controls the Phosphate Starvation Response in Plants
Anna Medici, Wojciech Szponarski, Pierre Dangeville, Alaeddine Safi, Indeewari Madhubhashini Dissanayake, Chorpet Saenchai, Amélie Emanuel, Vicente Rubio, Benoît Lacombe, Sandrine Ruffel, Milos Tanurdzic, Hatem Rouached, Gabriel Krouk
The Plant Cell May 2019, 31 (5) 1171-1184; DOI: 10.1105/tpc.18.00656

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Identification of Molecular Integrators Shows that Nitrogen Actively Controls the Phosphate Starvation Response in Plants
Anna Medici, Wojciech Szponarski, Pierre Dangeville, Alaeddine Safi, Indeewari Madhubhashini Dissanayake, Chorpet Saenchai, Amélie Emanuel, Vicente Rubio, Benoît Lacombe, Sandrine Ruffel, Milos Tanurdzic, Hatem Rouached, Gabriel Krouk
The Plant Cell May 2019, 31 (5) 1171-1184; DOI: 10.1105/tpc.18.00656
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The Plant Cell: 31 (5)
The Plant Cell
Vol. 31, Issue 5
May 2019
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