Integration of shoot-derived polypeptide signals by root TGA transcription factors is essential for survival under fluctuating nitrogen environments

• Published in: Nature communications Vol. 15; no. 1; pp. 6903 - 12
• Main Authors: Kobayashi, Ryutaro, Ohkubo, Yuri, Izumi, Mai, Ota, Ryosuke, Yamada, Keiko, Hayashi, Yoko, Yamashita, Yasuko, Noda, Saki, Ogawa-Ohnishi, Mari, Matsubayashi, Yoshikatsu
• Format: Journal Article
• Language: English
• Published: London Nature Publishing Group 23.08.2024; Nature Portfolio
• Subjects: Environmental conditions; Gene expression; Gene regulation; Genes; Glutaredoxin; Nitrates; Nitrogen; Polypeptides; Rhizosphere; Sessile species; Shoots; Survival; Transcription factors
• ISSN: 2041-1723; 2041-1723
• DOI: 10.1038/s41467-024-51091-5

Unlike plants in the field, which experience significant temporal fluctuations in environmental conditions, plants in the laboratory are typically grown in controlled, stable environments. Therefore, signaling pathways evolved for survival in fluctuating environments often remain functionally latent in laboratory settings. 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 phloem mobile polypeptides, CEP DOWNSTREAM 1 (CEPD1), CEPD2 and CEPD-like 2 (CEPDL2) as nitrogen (N) deficiency signals, and Glutaredoxin S1 (GrxS1) to GrxS8 as N sufficiency signals. CEPD1/2/CEPDL2 and GrxS1-S8 competitively bind to TGA1/4 in roots, with the former acting as transcription coactivators that enhance the uptake of nitrate, while the latter function as corepressor complexes together with TOPLESS (TPL), TPL-related 1 (TPR1) and TPR4 to limit nitrate uptake. Arabidopsis plants deficient in TGA1/4 maintain basal nitrate uptake and exhibit growth similar to wild-type plants in a stable N environment, but are impaired in regulation of nitrate acquisition in response to shoot N demand, leading to defective growth under 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 fluctuating and challenging N environmental conditions.As sessile organisms, plants grow under continuously fluctuating nitrogen (N) nutrient environments. Here, the authors uncovered that root TGA1/4, as key transcription factors, regulate the expression of nitrate uptake genes by binding to shoot-derived transcriptional cofactors that reflect shoot N demand.