Signaling pathways underlying nitrogen-dependent changes in root system architecture: from model to crop species

Abstract

Among all essential mineral elements, nitrogen (N) is required in the largest amounts and thus is often a limiting factor for plant growth. N is taken up by plant roots in the form of water-soluble nitrate, ammonium, and, depending on abundance, low-molecular weight organic N. In soils, the availability and composition of these N forms can vary over space and time, which exposes roots to various local N signals that regulate root system architecture in combination with systemic signals reflecting the N nutritional status of the shoot. Uncovering the molecular mechanisms underlying N-dependent signaling provides great potential to optimize root system architecture for the sake of higher N uptake efficiency in crop breeding. In this review, we summarize prominent signaling mechanisms and their underlying molecular players that derive from external N forms or the internal N nutritional status and modulate root development including root hair formation and gravitropism. We also compare the current state of knowledge of these pathways between Arabidopsis and graminaceous plant species.

Integration of A Nitrate-Related Signaling Pathway in Rhizobia-Induced Responses During Interactions with Non-Legume Host Arabidopsis thaliana

“…It is well documented that nitrate starvation is accompanied by stimulated lateral root emergence and primary root elongation, while excess nitrate leads to root growth inhibition (Jia & Wiren, 2020). In line with this, the presence of PGPRs on Arabidopsis roots stimulates a low-nitrate response.…”

“…Auxin accumulates in nitrate-rich patches of lateral roots and induces root emergence and elongation, whereas auxin depleted in sites with low nitrate availability resulting in reduced overall root growth (Remans et al, 2006;Mounier et al, 2014). Notably, root system architecture, and here primarily lateral-and primary-root length, are stimulated during moderate but homogenous nitrate availability, but inhibited under excess conditions (Jia & Wiren, 2020). This indicates that different signaling cascades are activated in fluctuating nitrate conditions resulting in adaptive physiological and morphological processes.…”

Modulation of root growth by nutrient-defined fine-tuning of polar auxin transport

“…Since the distribution of these N sources in the soil is very heterogeneous 58 , plants tend to maximize the N exploitation by flexible modulation of root system architecture 59 . Although distinct impacts of NH 4 + and NO 3 - on the root system growth and development have been already demonstrated 6 , molecular mechanisms how spatio-temporal changes in N resource impact on root growth are scarcely described.…”

“…For example; wheat, maize, canola, beans, sugar beet, Arabidopsis and tobacco grow preferentially on NO 3 − nutrition, whereas, rice and pine grow on NH 4 + nutrition. Fluctuations in both concentrations and the form of nitrogen sources available in the soil have prominent effects on root system growth and development 6,7 . Deficiency in nitrogen severely interferes with root elongation growth and development; low to medium availability of nitrogen enhances root growth and branching to promote the exploitation of this macronutrient, whereas high levels of availability might inhibit the elongation growth of primary and lateral roots 8 .…”

Improving coordination of plant growth and nitrogen metabolism for sustainable agriculture

“…In the past decade, a lot of transporting and metabolism genes that provide better access to the biological processes of N uptake, transport, assimilation and redistribution have been identified in model plants (Li et al 2017;Wang et al 2018d;Vidal et al 2020). In addition, a number of N-responsive genes and relevant regulatory elements in the control of N uptake and plant architecture in response to changes in N availability have also been investigated (Li et al 2017;Wang et al 2018d;Jia and Wiren 2020;Luo et al 2020). Although many efforts have been focused how to improve grain yield and NUE, the molecular mechanisms underlying N sensing and signaling networks are still elusive, and the NUE improvements in crops have a limited success.…”