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.

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1 nitrate and phosphate supply reveal functional divergence of 2 genetic factors involved in nitrate and phosphate signaling 3 Running title: Wheat transcriptional responses to nitrate and 4 phosphate 5 6 7 Abstract 42 43 Nitrate (N) and phosphate (P) levels are sensed by plant cells and signaled via local and 44 systemic signaling pathways to modulate plant growth and development. Understanding the 45 genetic basis of these signaling mechanisms is key to future improvement of nutrient use 46 efficiency. While major progress has been made in understanding N and P signaling 47 pathways and their interaction in the model plant Arabidopsis, understanding of 48 transcriptional responses to N and P in a major monocot crop wheat is lacking. Therefore, 49we investigated gene expression dynamics of wheat roots in response to N and/or P provision 50 using RNA-Seq. We found that nitrate presence is the major trigger for most of the 51 transcriptional response to occur within 24 h, however, we also identified a large array of 52 synergistic transcriptional responses to concomitant supply of N and P. Through gene co-53 expression analysis, we identified gene co-expression modules prominent in nitrate signaling 54 and metabolism in wheat. Importantly, we identified likely instances of functional 55 divergence in major N-responsive transcription factors families HRS1/HHO and TGA of 56 wheat from their rice/Arabidopsis homologues. Our work broadens the understanding of 57 wheat N and P transcriptional responses and aids in prioritizing gene candidates for 58 production of wheat varieties that are efficient in nitrogen usage. 59 60 61

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