Abstract
Nitrate is the main source of nitrogen for plants and an essential component of fertilizers. Rapid transcriptional activation of genes encoding the high-affinity nitrate transport system (HATS) is an important strategy that plants use to cope with nitrogen deficiency. However, the specific transcriptional machineries involved in this process and the detailed transcriptional regulatory mechanism of the core HATS remain poorly understood. ZmCHB101 is the core subunit of the SWI/SNF-type ATP-dependent chromatin remodeling complex in maize. RNA-interference transgenic plants (ZmCHB101-RNAi) display abaxially curling leaves and impaired tassel and cob development. Here, we demonstrate that ZmCHB101 plays a pivotal regulatory role in nitrate-responsive gene expression. ZmCHB101-RNAi lines showed accelerated root growth and increased biomass under low nitrate conditions. An RNA sequencing analysis revealed that ZmCHB101 regulates the expression of genes involved in nitrate transport, including ZmNRT2.1 and ZmNRT2.2. The NIN-like protein (NLP) of maize, ZmNLP3.1, recognized the consensus nitrate-responsive cis-elements (NREs) in the promoter regions of ZmNRT2.1 and ZmNRT2.2, and activated the transcription of these genes in response to nitrate. Intriguingly, well-positioned nucleosomes were detected at NREs in the ZmNRT2.1 and ZmNRT2.2 gene promoters, and nucleosome densities were lower in ZmCHB101-RNAi lines than in wild-type plants, both in the absence and presence of nitrate. The ZmCHB101 protein bound to NREs and was involved in the maintenance of nucleosome occupancies at these sites, which may impact the binding of ZmNLP3.1 to NREs in the absence of nitrate. However, in the presence of nitrate, the binding affinity of ZmCHB101 for NREs decreased dramatically, leading to reduced nucleosome density at NREs and consequently increased ZmNLP3.1 binding. Our results provide novel insights into the role of chromatin remodeling proteins in the regulation of nitrate-responsive gene expression in plants.
Highlights
Maize (Zea mays) is one of the most important crops in the world
Our results demonstrate that the NIN-like protein (NLP) in maize, ZmNLP3.1, recognizes nitrate-responsive cis-elements (NREs) in the promoters of the ZmNRT2.1 and ZmNRT2.2 genes, and it activates the expression of these genes in response to nitrate
The full-length GST-tagged ZmNLP3.1 protein (GSTZmNLP3.1) was capable of binding to probes containing consensus ZmNLP3.1-binding motifs; mutations of the NREs in the ZmNRT2.1 or ZmNRT2.2 gene promoter abolished the binding of ZmNLP3.1 to these regions (Figure 5E). These results indicate that ZmNLP3.1 binds to NREs located in the promoter regions of ZmNRT2.1 and ZmNRT2.2, and activates the expression of these genes in response to nitrate
Summary
Maize (Zea mays) is one of the most important crops in the world. To maximize the yield of maize crop in the field, large quantities of nitrogenous fertilizers are added to the soil during cultivation. Over the past several decades, application of nitrogen (N) fertilizer has significantly increased maize production (Zhang et al, 2011; Sun and Zheng, 2015; Alvarez et al, 2019). N deficiency limits plant growth and development, thereby reducing crop yield (Chen et al, 2016). Crops utilize only approximately 30% of the applied N fertilizer (Raun and Johnson, 1999; Sultan, 2003), while the remaining N causes environmental pollution via gaseous emission, fertilizer leaching, surface runoff, and denitrification (Good et al, 2004)
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