Garo Z. Akmakjian and Julia Bailey-Serres

PNAS June 16, 2020 117 (24) 13196-13198

The wealth of data provided by large-scale -omics studies empowers the discovery of gene regulatory networks and molecular mechanisms that underlie specific phenotypes. Most transcriptomic studies provide a snapshot of how organisms interact with their environment, recording change after a given time or in response to a single environmental variable. Organisms have not evolved in binary states of treatment vs. control and instead experience a continuum of environmental states, from optimal growth conditions to mild and ultimately severe stress. Organismal phenotypes vary along this continuum, but how molecular responses are metered to influence these phenotypes is poorly understood. N is an essential nutrient found in many macromolecules. Plant roots acquire bioavailable N as nitrate or ammonium and assimilate N from these inorganic molecules into amino acids for use in protein synthesis, as well as the synthesis of nucleic acids, chlorophyll, and other secondary metabolites throughout the plant. Here is thus a significant need for innovations that lessen reliance on N fertilizers, including the development of crops with greater nitrogen-use efficiency (NUE) to maximize growth and yield. By incorporating both time and N dosage into their analysis, this work identifies a transcription factor that not only influences N use and growth during low N conditions but also at intermediate and high (subinhibitory) levels of N. The authors’ strategy thereby identifies TGA1 as both a critical component of regulating N assimilation as well as an attractive breeding target for improving crop NUE. This work also demonstrates that not all N-responsive genes fit a classical Michaelis–Menten model, suggesting that additional layers of regulatory complexity underlie N responses that must be understood to even further improve NUE.

See https://www.pnas.org/content/117/24/13196

Figure 1: Role of the transcription factor TGA1 in coordinating proportional transcriptional, metabolic, and growth responses to N availability in roots of A. thaliana. (A) TGA1 target genes fit the Michaelis–Menten model (wild type; black line) as a function of N availability. TGA1 overexpression (TGA1 OX; green line) increases the rate of change of N-responsive gene mRNAs across N concentrations but also raises K_m. Plant growth rates also fit the Michaelis–Menten model, with the growth kinetic changes of TGA1 overexpressing plants mirroring the changes observed for transcripts of TGA1 target genes. (B) Schematic of regulation of N uptake, N reduction, N assimilation, and translation of mRNAs produced by the TGA1 transcriptional network, which is putatively regulated by the nitrate transceptor NRT1.1. TGA1 directly regulates 92 transcription factors in a network that regulates thousands of downstream genes. Enzyme classes are underlined, whereas TGA1-regulated genes are shown in italics and are color coded according to up-regulation (magenta) or down-regulation (green) in the network. Genes shown in bold are direct targets of TGA1. Abbreviations for enzymes: AS, asparagine synthetase; AspAT, aspartate aminotransferase; GDH, glutamate dehydrogenase; GOGAT, glutamine synthase; GS, glutamine synthetase; NIR, nitrite reductase; NR, nitrate reductase. Abbreviations for molecules/metabolites: Asn, asparagine; Asp, aspartate; Gln, glutamine; Glu, glutamate; NH₄⁺, ammonium; NO₂⁻, nitrite; NO₃⁻, nitrate; OAA, oxaloacetate; 2-OG, 2-oxoglutarate.