Journal Article

Low nitrogen stress-induced transcriptome changes revealed the molecular response and tolerance characteristics in maintaining the C/N balance of sugar beet (Beta vulgaris L.)

Liu, Xinyu, Yao, Qi, Xing, Wang, Yin, Xilong, Li, Jiajia, Tan, Wenbo, Xu, Lingqing, Liu, Dali, Li, Wangsheng, Wang, Qiuhong

2023

Overview

Nitrogen (N) is an essential macronutrient for plants, acting as a common limiting factor for crop yield. The application of nitrogen fertilizer is related to the sustainable development of both crops and the environment. To further explore the molecular response of sugar beet under low nitrogen (LN) supply, transcriptome analysis was performed on the LN-tolerant germplasm ‘780016B/12 superior’. In total, 580 differentially expressed genes (DEGs) were identified in leaves, and 1,075 DEGs were identified in roots (log 2 |FC| ≥ 1; q value < 0.05). Gene Ontology (GO), protein−protein interaction (PPI), and Kyoto Encyclopedia of Genes and Genomes (KEGG) analyses clarified the role and relationship of DEGs under LN stress. Most of the downregulated DEGs were closely related to “photosynthesis” and the metabolism of “photosynthesis-antenna proteins”, “carbon”, “nitrogen”, and “glutathione”, while the upregulated DEGs were involved in flavonoid and phenylalanine biosynthesis. For example, GLUDB (glutamate dehydrogenase B) was identified as a key downregulated gene, linking carbon, nitrogen, and glutamate metabolism. Thus, low nitrogen-tolerant sugar beet reduced energy expenditure mainly by reducing the synthesis of energy-consuming amino acids, which in turn improved tolerance to low nitrogen stress. The glutathione metabolism biosynthesis pathway was promoted to quench reactive oxygen species (ROS) and protect cells from oxidative damage. The expression levels of nitrogen assimilation and amino acid transport genes, such as NRT2.5 (high-affinity nitrate transporter), NR (nitrate reductase [NADH]), NIR (ferredoxin-nitrite reductase), GS (glutamine synthetase leaf isozyme), GLUDB, GST (glutathione transferase) and GGT3 (glutathione hydrolase 3) at low nitrogen levels play a decisive role in nitrogen utilization and may affect the conversion of the carbon skeleton. DFRA (dihydroflavonol 4-reductase) in roots was negatively correlated with NIR in leaves (coefficient = −0.98, p < 0.05), suggesting that there may be corresponding remote regulation between “flavonoid biosynthesis” and “nitrogen metabolism” in roots and leaves. FBP (fructose 1,6-bisphosphatase) and PGK (phosphoglycerate kinase) were significantly positively correlated (p < 0.001) with Ci (intercellular CO 2 concentration). The reliability and reproducibility of the RNA-seq data were further confirmed by real-time fluorescence quantitative PCR (qRT−PCR) validation of 22 genes (R 2 = 0.98). This study reveals possible pivotal genes and metabolic pathways for sugar beet adaptation to nitrogen-deficient environments.

• Publisher: Frontiers Media SA,Frontiers Media S.A
• Subject: Agricultural production / Amino acids / Biosynthesis / Carbon / carbon and nitrogen balance / Carbon dioxide / Carbon dioxide concentration / Crop yield / Down-regulation / Energy expenditure / Enzymes / Ferredoxin / Ferredoxin-nitrite reductase / Flavonoids / Genes / Genomes / Germplasm / Glutamate dehydrogenase / Glutamate-ammonia ligase / Glutamine / Glutathione / Glutathione transferase / Kinases / Leaves / Lignin / low nitrogen stress / Metabolic pathways / Metabolism / Metabolites / Nicotinamide adenine dinucleotide / Nitrate reductase / Nitrite reductase / Nitrogen / nitrogen assimilation and transport / Nitrogen metabolism / Phenylalanine / Phosphoglycerate kinase / Photosynthesis / Physiology / Plant growth / Plant Science / Protected species / Proteins / Reactive oxygen species / Real time / Reductases / Roots / Software / Sugar / sugar beet / Sugar beets / Sulfuric acid / Sustainable development / transcriptome / Transcriptomes