Research Article: DEP1 is involved in regulating the carbon–nitrogen metabolic balance to affect grain yield and quality in rice (Oriza sativa L.)

Date Published: March 11, 2019

Publisher: Public Library of Science

Author(s): Mingzhu Zhao, Minghui Zhao, Shuang Gu, Jian Sun, Zuobin Ma, Lili Wang, Wenjing Zheng, Zhengjin Xu, Qian Qian.

http://doi.org/10.1371/journal.pone.0213504

Abstract

The DEP1 (dense and erect panicle 1) gene, which corresponds to the erect panicle architecture, shows a pleiotropic effect in increasing grain yield and nitrogen use efficiency (NUE) in rice. Nevertheless, it remains unclear whether the carbon−nitrogen metabolic balance changes as the dep1 allele enhances nitrogen uptake and assimilation. In this study, we generated transgenic Akitakomati plants by overexpressing dep1 and analyzed the carbon−nitrogen metabolic status, gene expression profiles, and grain yield and quality. Under either low or high nitrogen growth conditions, the carbon−nitrogen metabolic balance of dep1-overexpressed lines was broken in stem sheaths and leaves but not in grains; the dep1-overexpressed plants showed higher expressions of glutamine synthetase (GS) and glutamate synthase (GOGAT) genes than the wildtype, along with increased total nitrogen and soluble protein content in the straw at maturity. However, the ribulose-1,5-bisphosphate carboxylase/oxygenase (RUBISCO) and phosphoenolpyruvate carboxylase (PEPC) genes were downregulated in dep1-overexpressed plants, leading to a decreased carbohydrate content and carbon/nitrogen ratio. Although the unbalanced carbon−nitrogen metabolism decreased the grain-filling rate, grain setting percentage, 1000 grain weight, and grain quality in dep1-overexpressed lines, it led to increased grain numbers per panicle and consequently increased grain yield. Our results suggest that an unbalanced carbon−nitrogen metabolic status is a major limiting factor for further improving grain yield and quality in erect panicle varieties.

Partial Text

Nitrogen is an essential nutrient in the growth and development of plants [1]. A great deal of nitrogen fertilizer is applied to fields to maximize grain yield for its significant effect on crop productivity [2]. However, excessive nitrogen fertilizer application results in severe environmental pollution, particularly in aquatic ecosystems [3]. Thus, it is important to optimize the use of nitrogen fertilizers to make agriculture more sustainable. One method of optimization is to increase nitrogen use efficiency (NUE) through genetic improvement, particularly in rice (Oryza sativa L.), which would increase grain yield with less nitrogen fertilizer [4].

Rice plants carrying the dominant DEP1 allele (dep1) have higher expression levels of GS1;1 and GS activity, exhibiting nitrogen-insensitive vegetative growth coupled with increased nitrogen uptake and assimilation [16]. However, many studies have found that the balance of carbon−nitrogen metabolism can be broken if the nitrogen metabolism activity is increased in GS-overexpressed plants [8–10]. In this study, the carbon/nitrogen ratio of dep1-overexpressed lines was lower in stem sheaths and leaves than that of the wildtype under either LN or HN conditions, which was not only attributed to the increased total nitrogen content but also decreased total carbon content. Similar results in previous studies have also shown that more carbohydrate or nitrogen accumulating in plants automatically results in lower concentrations of other components [31–34]. However, the carbon/nitrogen ratio is sometimes considered to be a poor indicator of the carbon and nitrogen metabolism status of plant tissues [34]. Thus, to provide evidence of unbalanced carbon−nitrogen metabolism in dep1-overexpressed lines, we showed an increase in soluble protein content and decreases in starch, sucrose, and soluble sugar content in the straw of these lines. The gene expression patterns involved in carbon-nitrogen metabolism were further analyzed. The dep1-overexpressed lines had higher expressions of GS and GOGAT genes, and thus showed higher nitrogen metabolic activity than the wildtype under either LN or HN conditions. Meanwhile, the genes involved in carbon metabolism, such as RUBISCO and PEPC, were suppressed, which caused unbalanced carbon−nitrogen metabolism in stem sheaths and leaves under both LN and HN conditions.

 

Source:

http://doi.org/10.1371/journal.pone.0213504

 

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