Peizhu Guan, Juan-José Ripoll, Renhou Wang, Lam Vuong, Lindsay J. Bailey-Steinitz, Dening Ye, and Nigel M. Crawford

Significance

Nitrate is an essential nutrient and a critical signal for plant growth, development, and stress responses. Nitrate signaling underlies a myriad of physiological, morphological, and developmental processes. Here we report that interacting teosinte branched1/cycloidea/proliferating cell factor and NIN-like protein transcription factors constitute a molecular link between nitrate signaling and the control of the cell-cycle progression gene CYCB1;1 and root meristem growth. Our findings shed light on the regulatory mechanisms underlying an important plant adaptive process for coping with and surviving environmental challenges.

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, NIA1, 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 G₂/M cell-cycle marker gene, CYCB1;1. 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.

See http://www.pnas.org/content/114/9/2419.abstract.html?etoc

PNAS February 28 2017; vol.114; no.9: 2419–2424

Fig. 1.

Binding of TCP20 DNA-binding domain (DB), NLP6-DB, and NLP7-DB to the fragments of NIA1 (109 bp) DNA was determined by EMSA. (A) Diagram of probes. Red and green triangles represent TCP20 (red) and NLP6/7(green) binding sites, respectively. (B–D) Binding of TCP20DB, NLP6DB, and NLP7DB to A, B, C, D, and E probes. The probes are listed in SI Appendix, Table S1.