TGA1/4 transcription factors are critical for plant survival under a temporally fluctuating nitrogen environment

Unlike plants in laboratory environments, plants in the field experience marked temporal fluctuations in environmental conditions. Consequently, transcription factors that are essential for survival in fluctuating environments, not in stable environments, often escape functional identification. Here, we show that TGA1 and TGA4 act as hub transcription factors through which the expression of genes involved in high-affinity nitrate uptake are regulated in response to shoot-derived, nitrogen (N) deficiency signals CEP DOWNSTREAM 1 (CEPD1), CEPD2 and CEPD-like 2 (CEPDL2) and N sufficiency signals Glutaredoxin S1 (GrxS1) to GrxS8. CEPD1/2/CEPDL2 and GrxS1-S8 competitively bind to TGA1/4, with the former acting as transcription coactivators that enhance the uptake of nitrate, while the latter function as corepressor complexes together with TOPLESS to limit nitrate uptake. Arabidopsis plants deficient in TGA1/4 maintain basal nitrate uptake, but were impaired in the demand-dependent regulation of nitrate acquisition, leading to defective growth under temporally fluctuating N environments where rhizosphere nitrate ions switch periodically between deficient and sufficient states. TGA1/4 are crucial transcription factors that enable plants to survive under challenging N environmental conditions.