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White lupin (Lupinus albus L.) is a legume that produces seeds recognized for their high protein content and good nutritional value (lowest glycemic index of all grains, high dietary fiber content, and zero gluten or starch)1–5. White lupin can form nitrogen-fixing nodules but has lost the ability to form mycorrhizal symbiosis with fungi6. Nevertheless, its root system is well adapted to poor soils: it produces cluster roots, constituted of dozens of determinate lateral roots that improve soil exploration and phosphate remobilization7. As phosphate is a limited resource that comes from rock reserves8, the production of cluster roots is a trait of interest to improve fertilizers efficiency. Using long reads sequencing technologies, we provide a high-quality genome sequence of a modern variety of white lupin (2n=50, 451 Mb), as well as de novo assemblies of a landrace and a wild relative. We describe how domestication impacted soil exploration capacity through the early establishment of lateral and cluster roots. We identify the APETALA2 transcription factor LaPUCHI-1, homolog of the Arabidopsis morphogenesis coordinator9, as a potential regulator of this trait. Our high-quality genome and companion genomic and transcriptomic resources enable the development of modern breeding strategies to increase and stabilize yield and to develop new varieties with reduced allergenic properties (caused by conglutins10), which would favor the deployment of this promising culture.

Plants are subjected to variable nitrogen (N) availability including frequent spatial nitrate (NO3-) heterogeneity in soil. Thus, plants constantly adapt their genome expression and root physiology in order to optimize N acquisition from this heterogeneous source. These adaptations rely on a complex and long distance root-shoot-root signaling network that is still largely unknown. Here, we used a combination of reverse genetics, transcriptomic analysis, NO3- uptake experiments and hormone profiling under conditions of homogeneous or heterogeneous NO3- availability to characterize the systemic signaling involved. We demonstrate the important role of the trans-zeatin form of cytokinin (CK) in shoots, in particular using a mutant altered for ABCG14-mediated trans-zeatin-translocation from the root to the shoot, in mediating: (i) rapid long distance N-demand signaling and (ii) long term functional adaptations to heterogeneous NO3- supply, including changes in NO3- transport capacity and root growthmodifications. We also provide insights into the potential CK-dependent and independent shoot-to-root signals involved in root adaptation to heterogeneous N availability.

Plants need to cope with strong variations in the nitrogen content of the soil solution. Although many molecular actors are being discovered concerning how plants perceive NO3- provision, it is less clear how plants recognize a lack of Nitrogen. Indeed, following N removal plants activate their Nitrogen Starvation Response (NSR) being characterized in particular by the activation of very high affinity nitrate transport systems (NRT2.4, NRT2.5) and other sentinel genes such as GDH3. Here we show using a combination of functional genomics (via TF perturbation) and molecular physiology studies, that the GARP Transcription Factors (TFs) belonging the HHO sub-family are important regulators of the NSR through two potential mechanisms. First, HHOs directly repress NRT2.4 and NRT2.5 high-affinity nitrate transporters. Genotypes affected in HHO genes (mutants and overexpressors) display modified high-affinity nitrate transport activities opening interesting perspectives in biotechnology applications. Second, we show that Reactive Oxygen Species (ROS) are important to control NSR in wild type plants and that HRS1 and HHO1 overexpressors are affected in their ROS content, defining a potential feedforward branch of the signaling pathway. Taken together our results define two new classes of molecular actors in the control of NSR including ROS and the first transcription factors to date. This work (i) opens perspectives on a poorly understood nutrient related signaling pathway, and (ii) defines targets for molecular breeding of plants with enhanced NO3- uptake.