Nitrogen economics of root foraging: transitive closure of the nitrate-cytokinin relay and distinct systemic signaling for N supply vs. demand.
As sessile organisms, root plasticity enables plants to forage for and acquire nutrients in a fluctuating 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 challenged with 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., N supply 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.
Center for Genomics and Systems Biology, New York University, New York, NY 10003, USA. sandrine.ruffel@supagro.inra.fr
Sandrine
S
Ruffel
Gabriel
G
Krouk
Daniela
D
Ristova
Dennis
D
Shasha
Kenneth D
KD
Birnbaum
Gloria M
GM
Coruzzi
D017360:Arabidopsis / Q000235:genetics / Q000378:metabolism; D003583:Cytokinins / Q000096:biosynthesis / Q000378:metabolism*; D017343:Genes, Plant; D009566:Nitrates / Q000378:metabolism*; D009584:Nitrogen / Q000378:metabolism*; D018517:Plant Roots / Q000378:metabolism*; D015398:Signal Transduction
D003583:Cytokinins; D009566:Nitrates; D009584:Nitrogen