Nitrogen economics of root foraging: Transitive closure of the nitrate-cytokinin relay and distinct systemic signaling for N supply vs. demand

Sandrine Ruffel, Gabriel Krouk, Daniela Ristova, Dennis Shasha, Kenneth Birnbaum, Gloria Coruzzi

Research output: Contribution to journalArticle

Abstract

As sessile organisms, root plasticity enables plants to forage for and acquire nutrients in afluctuating underground environment.Here,we use genetic and genomic approaches in a "split-root" framework - in which physically isolated root systems of the same plant are challengedwith different nitrogen (N) environments - to investigate how systemic signaling affects genome-wide reprogramming and root development. The integration of transcriptome and root phenotypes enables us to identify distinct mechanisms underlying "N economy"(i.e.,Nsupply and demand) of plants as a system.Under nitrate-limited conditions, plant roots adopt an "active-foraging strategy", characterized by lateral root outgrowth and a shared pattern of transcriptome reprogramming, in response to either local or distal nitrate deprivation. By contrast, in nitrate-replete conditions, plant roots adopt a "dormant strategy", characterized by a repression of lateral root outgrowth and a shared pattern of transcriptome reprogramming, in response to either local or distal nitrate supply. Sentinel genes responding to systemic N signaling identified by genome-wide comparisons of heterogeneous vs. homogeneous split-root N treatments were used to probe systemic N responses in Arabidopsis mutants impaired in nitrate reduction and hormone synthesis and also in decapitated plants. This combined analysis identified genetically distinct systemic signaling underlying plant N economy: (i) N supply, corresponding to a long-distance systemic signaling triggered by nitrate sensing; and (ii) N demand, experimental support for the transitive closure of a previously inferred nitrate-cytokinin shoot-root relay system that reports the nitrate demand of the whole plant, promoting a compensatory root growth in nitrate-rich patches of heterogeneous soil.

Original languageEnglish (US)
Pages (from-to)18524-18529
Number of pages6
JournalProceedings of the National Academy of Sciences of the United States of America
Volume108
Issue number45
DOIs
StatePublished - Nov 8 2011

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Cytokinins
Nitrates
Nitrogen
Economics
Transcriptome
Plant Roots
Genome
Arabidopsis
Soil
Hormones
Phenotype
Food

Keywords

  • Hormone
  • Root morphology
  • Systems analysis

ASJC Scopus subject areas

  • General

Cite this

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title = "Nitrogen economics of root foraging: Transitive closure of the nitrate-cytokinin relay and distinct systemic signaling for N supply vs. demand",
abstract = "As sessile organisms, root plasticity enables plants to forage for and acquire nutrients in afluctuating underground environment.Here,we use genetic and genomic approaches in a {"}split-root{"} framework - in which physically isolated root systems of the same plant are challengedwith different nitrogen (N) environments - to investigate how systemic signaling affects genome-wide reprogramming and root development. The integration of transcriptome and root phenotypes enables us to identify distinct mechanisms underlying {"}N economy{"}(i.e.,Nsupply and demand) of plants as a system.Under nitrate-limited conditions, plant roots adopt an {"}active-foraging strategy{"}, characterized by lateral root outgrowth and a shared pattern of transcriptome reprogramming, in response to either local or distal nitrate deprivation. By contrast, in nitrate-replete conditions, plant roots adopt a {"}dormant strategy{"}, characterized by a repression of lateral root outgrowth and a shared pattern of transcriptome reprogramming, in response to either local or distal nitrate supply. Sentinel genes responding to systemic N signaling identified by genome-wide comparisons of heterogeneous vs. homogeneous split-root N treatments were used to probe systemic N responses in Arabidopsis mutants impaired in nitrate reduction and hormone synthesis and also in decapitated plants. This combined analysis identified genetically distinct systemic signaling underlying plant N economy: (i) N supply, corresponding to a long-distance systemic signaling triggered by nitrate sensing; and (ii) N demand, experimental support for the transitive closure of a previously inferred nitrate-cytokinin shoot-root relay system that reports the nitrate demand of the whole plant, promoting a compensatory root growth in nitrate-rich patches of heterogeneous soil.",
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T2 - Transitive closure of the nitrate-cytokinin relay and distinct systemic signaling for N supply vs. demand

AU - Ruffel, Sandrine

AU - Krouk, Gabriel

AU - Ristova, Daniela

AU - Shasha, Dennis

AU - Birnbaum, Kenneth

AU - Coruzzi, Gloria

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