Interacting TCP and NLP transcription factors control plant responses to nitrate availability

Abstract

Plants have evolved adaptive strategies that involve transcriptional networks to cope with and survive environmental challenges. Key transcriptional regulators that mediate responses to environmental fluctuations in nitrate have been identified; however, little is known about how these regulators interact to orchestrate nitrogen (N) responses and cell-cycle regulation. Here we report that teosinte branched1/cycloidea/proliferating cell factor1-20 (TCP20) and NIN-like protein (NLP) transcription factors NLP6 and NLP7, which act as activators of nitrate assimilatory genes, bind to adjacent sites in the upstream promoter region of the nitrate reductase gene, , and physically interact under continuous nitrate and N-starvation conditions. Regions of these proteins necessary for these interactions were found to include the type I/II Phox and Bem1p (PB1) domains of NLP6&7, a protein-interaction module conserved in animals for nutrient signaling, and the histidine- and glutamine-rich domain of TCP20, which is conserved across plant species. Under N starvation, TCP20-NLP6&7 heterodimers accumulate in the nucleus, and this coincides with TCP20 and NLP6&7-dependent up-regulation of nitrate assimilation and signaling genes and down-regulation of the G/M cell-cycle marker gene, TCP20 and NLP6&7 also support root meristem growth under N starvation. These findings provide insights into how plants coordinate responses to nitrate availability, linking nitrate assimilation and signaling with cell-cycle progression.

Nitrate acts at the Arabidopsis thaliana shoot apical meristem to regulate flowering time

“…NLP7 is known as the master regulator of nitrate signaling and is controlled at a subcellular level by a nitrate‐dependent nuclear retention mechanism (Marchive et al ., ). NLP6 function is described as partially redundant to NLP7 (Guan et al ., ). A late‐flowering phenotype has been observed for the nlp7 mutants (Castaings et al ., ).…”

“…Both SPL3 and SPL5 carry two and five functional NRE sequences in their upstream intergenic regions, respectively. These elements are targeted by NLP6 and NLP7 upon activation and nuclear retention in the presence of nitrate (Marchive et al ., ; Guan et al ., ). NLP6 and NLP7 belong to a family of nine nitrate‐regulated transcription factors present in the A. thaliana genome, and all nine members can potentially bind to NREs (Konishi & Yanagisawa, ).…”

“…These genes encode proteins required for nitrate transport and assimilation, and the reprogramming of carbon (C) and N metabolism, as well as transcription factors and regulatory proteins, triggering a cascade of changes that support increased growth. An early event in nitrate responses involves the accumulation of the transcription factor NIN‐LIKE PROTEIN 7 (NLP7) and its close homolog, NLP6, in the nucleus (Marchive et al ., ; Guan et al ., ), where they bind to nitrate‐responsive elements (NREs) in promoter regions of target genes (Konishi & Yanagisawa, ) and regulate their expression.…”

Evolving Tale of TCPs: New Paradigms and Old Lacunae

“…For example, TCP8 may activate or repress ISOCHORISMATE SYNTHASE 1 ( ICS1 ), a key gene involved in salicylic acid biosynthesis, by interacting with the transcriptional activators, WRKY28 and SAR DEFICIENT 1 or the NAC family repressor NAC109, respectively (Wang X. et al, 2015). Interactions between TCP20 and NIN-like TFs has been recently demonstrated to regulate nitrate assimilation and signaling (Guan et al, 2017). Overall, these studies highlight that TCP proteins are at the center of plant molecular networks and control diverse range of processes and signaling networks by recruiting specific interaction partners.…”

The long noncoding RNA T5120 regulates nitrate response and assimilation in Arabidopsis

“…Several pathways have been characterised for NLP7's regulation of nitrate signalling. NLP7 directly binds to some nitrate‐related genes, including NIR , NRT2.1 , and NRT2.2 , controlling their transcription levels and then modulating nitrate transport and assimilation (Castaings et al ., ; Konishi & Yanagisawa, ; Marchive et al ., ; Guan et al ., ). Moreover, NLP7 also regulates the nitrate signalling by directly binding to the promoter and controlling the expression of NIGT1 , which encodes the GARP‐type transcriptional repressor 1 proteins and affects the expression of some target genes involved in nitrate regulation (Maeda et al ., ).…”