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

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.

Nitrogen–phosphorus interplay: old story with molecular tale

“…This is supported by the recent work in Arabidopsis showing that AtNRT1.1 also plays an important role in the nitrateactivated phosphate starvation response in an AtPHR1-dependent manner (Medici et al, 2019). This is supported by the recent work in Arabidopsis showing that AtNRT1.1 also plays an important role in the nitrateactivated phosphate starvation response in an AtPHR1-dependent manner (Medici et al, 2019).…”

“…The N-regulated P response has been well described by recent studies, while the Pregulated N response remains largely obscure. Phosphate availability can dramatically regulate the expression of nitrate responsive genes in both Arabidopsis and rice (Maeda et al, 2018;Hu et al, 2019;Medici et al, 2019). AtNRT1.5, a nitrate transporter responsible for root-toshoot nitrate transport, is also reported to be involved in regulating the phosphate starvation response in Arabidopsis (Cui et al, 2019).…”

“…Based on current knowledge, the signaling network for the NRT1.1-SPX cascade and NIGT1s involved in N-P balance can be understood (Fig. It has been observed that nitrate-induced expression of PSI genes is greatly enhanced under phosphate starvation (Hu et al, 2019;Medici et al, 2019). Under low nitrate conditions, regardless of phosphate availability, the SPX protein accumulates to a relatively high level, thus retaining both PHR and NLP in the cytoplasm and repressing the expression of both PSI genes and nitrate-responsive genes (Fig.…”

“…Under control of the NLP and PHR transcription factors, NIGT1 further regulates the expression of both nitrate responsive genes and PSI genes, through which the N-P balance is modulated in a more precise manner in response to changing nutritional conditions. It has been observed that nitrate-induced expression of PSI genes is greatly enhanced under phosphate starvation (Hu et al, 2019;Medici et al, 2019). This contributes to implementing an N-P balance with higher phosphate utilization ability under low phosphate conditions.…”

A reevaluation of the contribution of NRT1.1 to nitrate uptake in Arabidopsis under low‐nitrate supply

“…Keywords: Arabidopsis thaliana; dual-affinity nitrate transporter; nitrate uptake; NRT1.1; NRT2.1; NRT2.2 Nitrate (NO À 3 ) is the major form of nitrogen absorbed by the roots of most terrestrial plants [1]. It not only acts an N source for growth and development but has also been proposed to act as a signal regulating several physiological processes, such as seed germination [2], root development [3], and flowering time [4,5], among others [6][7][8][9]. To better adapt to fluctuating nitrate availability, plants have evolved two uptake systems: one operating at low external nitrate concentrations, where nitrate is absorbed by high-affinity transport systems (HATS), the other acting at high nitrate concentrations through low-affinity transport systems (LATS) [10][11][12].…”