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We discuss how both nitrogen and water availability combine to impact plant biological responses at the molecular, transcriptomic, and physiological level., Nitrogen (N) and water (W) are crucial inputs for plant survival as well as costly resources for agriculture. Given their importance, the molecular mechanisms that plants rely on to signal changes in either N or W status have been under intense scrutiny. However, how plants sense and respond to the combination of N and W signals at the molecular level has received scant attention. The purpose of this review is to shed light on what is currently known about how plant responses to N are impacted by W status. We review classic studies which detail how N and W combinations have both synergistic and antagonistic effects on key plant traits, such as root architecture and stomatal aperture. Recent molecular studies of N and W interactions show that mutations in genes involved in N metabolism affect drought responses, and vice versa. Specifically, perturbing key N signaling genes may lead to changes in drought-responsive gene expression programs, which is supported by a meta-analysis we conduct on available transcriptomic data. Additionally, we cite studies that show how combinatorial transcriptional responses to N and W status might drive crop phenotypes. Through these insights, we suggest research strategies that could help to develop crops adapted to marginal soils depleted in both N and W, an important task in the face of climate change.

The Atacama Desert in Chile—hyperarid and with high–ultraviolet irradiance levels—is one of the harshest environments on Earth. Yet, dozens of species grow there, including Atacama-endemic plants. Herein, we establish the Talabre–Lejia transect (TLT) in the Atacama as an unparalleled natural laboratory to study plant adaptation to extreme environmental conditions. We characterized climate, soil, plant, and soil–microbe diversity at 22 sites (every 100 m of altitude) along the TLT over a 10-y period. We quantified drought, nutrient deficiencies, large diurnal temperature oscillations, and pH gradients that define three distinct vegetational belts along the altitudinal cline. We deep-sequenced transcriptomes of 32 dominant plant species spanning the major plant clades, and assessed soil microbes by metabarcoding sequencing. The top-expressed genes in the 32 Atacama species are enriched in stress responses, metabolism, and energy production. Moreover, their root-associated soils are enriched in growth-promoting bacteria, including nitrogen fixers. To identify genes associated with plant adaptation to harsh environments, we compared 32 Atacama species with the 32 closest sequenced species, comprising 70 taxa and 1,686,950 proteins. To perform phylogenomic reconstruction, we concatenated 15,972 ortholog groups into a supermatrix of 8,599,764 amino acids. Using two codon-based methods, we identified 265 candidate positively selected genes (PSGs) in the Atacama plants, 64% of which are located in Pfam domains, supporting their functional relevance. For 59/184 PSGs with an Arabidopsis ortholog, we uncovered functional evidence linking them to plant resilience. As some Atacama plants are closely related to staple crops, these candidate PSGs are a “genetic goldmine” to engineer crop resilience to face climate change.

International audience; Nitrogen (N) is an essential macronutrient for plants, and a major limiting factor for plant growth and crop production. Nitrate is the main source of N available for plants in agricultural soils and in many natural environments. Sustaining agricultural productivity is of paramount importance in the current scenario of increasing world population, diversification of crop uses, and climate change. Plant productivity for major crops around the world is still supported by excess application of N-based fertilizers with detrimental economic and environmental impacts. Thus, understanding how plants regulate nitrate uptake and metabolism is key for developing new crops with enhanced N use efficiency (NUE) and to cope with future world food demands. The study of plant responses to nitrate has gained considerable interest over the last thirty years. This review provides an overview of key findings in nitrate research, spanning biochemistry, molecular genetics, genomics and systems biology. We discuss how we reached our current understanding of nitrate transport, local and systemic nitrate sensing/signaling, and the regulatory networks underlying nitrate-controlled outputs in plants. We hope this summary serves not only as a time-line and information repository, but also as a base to outline important open questions for future research.

An increase in nutrient dose leads to proportional increases in crop biomass and agricultural yield. However, the molecular underpinnings of this nutrient dose–response are largely unknown. To investigate, we assayed changes in the Arabidopsis root transcriptome to different doses of nitrogen (N)—a key plant nutrient—as a function of time. By these means, we found that rate changes of genome-wide transcript levels in response to N-dose could be explained by a simple kinetic principle: the Michaelis–Menten (MM) model. Fitting the MM model allowed us to estimate the maximum rate of transcript change ( V max ), as well as the N-dose at which one-half of V max was achieved ( K m ) for 1,153 N-dose–responsive genes. Since transcription factors (TFs) can act in part as the catalytic agents that determine the rates of transcript change, we investigated their role in regulating N-dose–responsive MM-modeled genes. We found that altering the abundance of TGA1, an early N-responsive TF, perturbed the maximum rates of N-dose transcriptomic responses ( V max ), K m , as well as the rate of N-dose–responsive plant growth. We experimentally validated that MM-modeled N-dose–responsive genes included both direct and indirect TGA1 targets, using a root cell TF assay to detect TF binding and/or TF regulation genome-wide. Taken together, our results support a molecular mechanism of transcriptional control that allows an increase in N-dose to lead to a proportional change in the rate of genome-wide expression and plant growth.

Transcriptional regulation, determined by chromatin structure and regulatory elements interacting at promoter regions, is a key step in plant responses to environmental cues. Nitrate (NO3-) is a nutrient signal that regulates the expression of hundreds of genes in Arabidopsis thaliana. Here we integrate mRNA-seq, genome-wide RNA polymerase II (RNPII), ChIP-Seq and DNase-seq data sets to establish the relationship between RNPII occupancy and chromatin accessibility in response to NO3- treatments in Arabidopsis root organs. Genomic footprinting allowed us to identify in vivo regulatory elements controlling gene expression in response to NO3- treatments. NO3--modulated TF footprints are important for a rapid increase in RNPII occupancy and transcript accumulation over time. We mapped key TF regulatory interactions and functionally validated the role of NAP, a NAC-domain containing TF, as a new regulatory factor in NO3- transport. Our strategy provides a comprehensive view of transcriptional networks in response to a nutrient signal in Arabidopsis roots. Fil: Alvarez, José M.. Pontificia Universidad Católica de Chile; Chile Fil: Moyano, Tomás C.. Pontificia Universidad Católica de Chile; Chile Fil: Zhang, Tao. Yangzhou University; China Fil: Gras, Diana Ester. Consejo Nacional de Investigaciones Científicas y Técnicas. Centro Científico Tecnológico Conicet - Santa Fe. Instituto de Agrobiotecnología del Litoral. Universidad Nacional del Litoral. Instituto de Agrobiotecnología del Litoral; Argentina Fil: Herrera, Francisco J.. University of California at Berkeley; Estados Unidos Fil: Araus, Viviana. Pontificia Universidad Católica de Chile; Chile Fil: OBrien, José A.. Pontificia Universidad Católica de Chile; Chile Fil: Carrillo, Laura. Universidad Politécnica de Madrid; España Fil: Medina, Joaquín. Universidad Politécnica de Madrid; España Fil: Vicente-Carbajosa, Jesús. Universidad Politécnica de Madrid; España Fil: Jiang, Jiming. University Of Wisconsin-madison; Estados Unidos Fil: Gutiérrez, Rodrigo A.. Pontificia Universidad Católica de Chile; Chile

One of the most striking examples of plant developmental plasticity to changing environmental conditions is the modulation of root system architecture (RSA) in response to nitrate supply. Despite the fundamental and applied significance of understanding this process, the molecular mechanisms behind nitrate-regulated changes in developmental programs are still largely unknown. Small RNAs (sRNAs) have emerged as master regulators of gene expression in plants and other organisms. To evaluate the role of sRNAs in the nitrate response, we sequenced sRNAs from control and nitrate-treated Arabidopsis seedlings using the 454 sequencing technology. miR393 was induced by nitrate in these experiments. miR393 targets transcripts that code for a basic helix-loop-helix (bHLH) transcription factor and for the auxin receptors TIR1, AFB1, AFB2, and AFB3. However, only AFB3 was regulated by nitrate in roots under our experimental conditions. Analysis of the expression of this miR393/ AFB3 module, revealed an incoherent feed-forward mechanism that is induced by nitrate and repressed by N metabolites generated by nitrate reduction and assimilation. To understand the functional role of this N-regulatory module for plant development, we analyzed the RSA response to nitrate in AFB3 insertional mutant plants and in miR393 overexpressors. RSA analysis in these plants revealed that both primary and lateral root growth responses to nitrate were altered. Interestingly, regulation of RSA by nitrate was specifically mediated by AFB3 , indicating that miR393/ AFB3 is a unique N-responsive module that controls root system architecture in response to external and internal N availability in Arabidopsis .

Development of crops with improved nitrogen use efficiency (NUE) is essential for sustainable agriculture. However, achieving this goal has proven difficult since NUE is a complex trait encompassing physiological and developmental processes. We thought to tackle this problem by taking a systems biology approach to identify candidate target genes. First, we used a supervised machine-learning algorithm to predict a NUE gene network in Arabidopsis (Arabidopsis thaliana). Second, we identified BT2, a member of the Bric-a-Brac/Tramtrack/Broad gene family, as the most central and connected gene in the NUE network. Third, we experimentally tested BT2 for a role in NUE. We found NUE decreased in plants overexpressing BT2 gene compared to wild-type plants under limiting nitrate conditions. In addition, NUE increased compared to wild-type plants under low nitrate conditions in double mutant plants in bt2 and its closely related homolog bt1, indicating a functional redundancy of BT1 and BT2 for NUE. Expression of the nitrate transporter genes NRT2.1 and NRT2.4 increased in the bt1/bt2 double mutant compared to wild-type plants, with a concomitant 65% increase in nitrate uptake under low nitrate conditions. Similar to Arabidopsis, we found that mutation of the BT1/BT2 ortholog gene in rice (Oryza sativa) OsBT increased NUE by 20% compared to wild-type rice plants under low nitrogen conditions. These results indicate BT gene family members act as conserved negative regulators of nitrate uptake genes and NUE in plants and highlight them as prime targets for future strategies to improve NUE in crops.