Increase in demand for our primary foodstuffs is outstripping increase in yields, an expanding gap that indicates large potential food shortages by mid-century. This comes at a time when yield improvements are slowing or stagnating as the approaches of the Green Revolution reach their biological limits. Photosynthesis, which has been improved little in crops and falls far short of its biological limit, emerges as the key remaining route to increase the genetic yield potential of our major crops. Thus, there is a timely need to accelerate our understanding of the photosynthetic process in crops to allow informed and guided improvements via in-silico-assisted genetic engineering. Potential and emerging approaches to improving crop photosynthetic efficiency are discussed, and the new tools needed to realize these changes are presented.

Nitrogen and phosphorus are among the most widely used fertilizers worldwide. Nitrate (NO3−) and phosphate (PO43−) are also signaling molecules whose respective transduction pathways are being intensively studied. However, plants are continuously challenged with combined nutritional deficiencies, yet very little is known about how these signaling pathways are integrated. Here we report the identification of a highly NO3−-inducible NRT1.1-controlled GARP transcription factor, HRS1, document its genome-wide transcriptional targets, and validate its cis-regulatory-elements. We demonstrate that this transcription factor and a close homolog repress primary root growth in response to P deficiency conditions, but only when NO3− is present. This system defines a molecular logic gate integrating P and N signals. We propose that NO3− and P signaling converge via double transcriptional and post-transcriptional control of the same protein, HRS1

SignificanceOur study exploits time—the relatively unexplored fourth dimension of gene regulatory networks (GRNs)—to learn the temporal transcriptional logic underlying dynamic nitrogen (N) signaling in plants. We introduce several conceptual innovations to the analysis of time-series data in the area of predictive GRNs. Our resulting network now provides the “transcriptional logic” for transcription factor perturbations aimed at improving N-use efficiency, an important issue for global food production in marginal soils and for sustainable agriculture. More broadly, the combination of the time-based approaches we develop and deploy can be applied to uncover the temporal “transcriptional logic” for any response system in biology, agriculture, or medicine.

Significance Cellular signals evoke rapid and broad changes in gene regulatory networks. To uncover these network dynamics, we developed an approach able to monitor primary targets of a transcription factor (TF) based solely on gene regulation, in the absence of detectable binding. This enabled us to follow the transient propagation of a nitrogen (N) nutrient signal as a direct impact of the master TF Basic Leucine Zipper 1 (bZIP1). Unexpectedly, the largest class of primary targets that exhibit transient associations with bZIP1 is uniquely relevant to the rapid and dynamic propagation of the N signal. Our ability to uncover this transient network architecture has revealed the “dark matter” of dynamic N nutrient signaling in plants that has previously eluded detection.