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Acta Agronomica Sinica ›› 2020, Vol. 46 ›› Issue (10): 1526-1538.doi: 10.3724/SP.J.1006.2020.94197

• CROP GENETICS & BREEDING · GERMPLASM RESOURCES · MOLECULAR GENETICS • Previous Articles     Next Articles

Expression profile analysis of low nitrogen stress in Brassica napus

XIAO Yan(), YAO Jun-Yue(), LIU Dong, SONG Hai-Xing, ZHANG Zhen-Hua*()   

  1. College of Resource and Environment, Hunan Agricultural University / Southern Regional Collaborative Innovation Center for Grain and Oil Crops in China, Changsha 410128, Hunan, China
  • Received:2019-12-16 Accepted:2020-04-15 Online:2020-10-12 Published:2020-05-07
  • Contact: Zhen-Hua ZHANG E-mail:xiaoxiaoY8432@163.com;yjy950606@126.com;zhzh1468@163.com
  • Supported by:
    National Key Research and Development Program of China(2017YFD0200100);National Key Research and Development Program of China(2017YFD0200103)

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Abstract:

The nitrogen fertilizer was overapplied with people’s increased demand for crop yield, but the nitrogen utilization efficiency (NUE) of crops was decreasing. In this study, the differentially expressed genes (DEGs) including the nitrogen absorption, transport, distribution and transcription factors were screened under low nitrogen treatment of 0, 3, and 72 h by the physiological changes and RNA-Seq in rapeseed. The results showed that nitrogen were preferentially allocated to the shoots with the increased glutamine?synthetase (GS) and NUE activities and the decreased nitrate reductase (NR) activity and the total nitrogen concentration under low nitrogen treatment. The analysis of Gene Ontology (GO) enrichment and the Kyoto encyclopedia of genes and genomes (KEGG) metabolic pathway showed that DEGs of the shoots were mainly involved in metabolic process, protein binding, ion binding, and anion binding, while DEGs of the roots were mainly involved in molecular function, primary metabolic process, ion binding, and anion binding. The gene expression profile analysis indicated that after low nitrogen treatment for 72 h, the expression of most genes in BnaGLNs increased; the expression of BnaWRKY33s and BnaWRKY70s showed significantly decreased in roots; the expression of most genes in BnaMYB4s, BnaMYB44s, and BnaMYB51s decreased in the roots; the expression of most genes in BnaNIAs family was up-regulated in roots; and in the subfamily of BnaNRT2.1s and BnaNRT3.1s, the expression of BnaA6NRT2.1 (BnaA06g04560D), BnaA6NRT2.1 (BnaA06g04570D), BnaA2NRT3.1 (BnaA02g11760D), and BnaC2NRT3.1 (BnaC02g16150D) increased significantly in roots. At the same time, skipped exon (SE) and mutually exclusive exons (MXE) type occurred in shoots and roots in order to have a better adaptation under low nitrogen stress. In conclusion, the NUE activity was increased by regulating BnaNRTs, BnaGLNs and BnaNIAs genes, and the BnaMYBs, BnaWRKYs genes and alternative splicing favored Brassica napus to adapt the low nitrogen stress.

Key words: Brassica napus, low nitrogen stress, NO3-, alternative splicing

Fig. 1

Physiological responses to nitrogen (N) stress in oilseed rape A: the ratio of root NO3- concentration to shoot NO3- concentration; B: the total N concentration; C: the nitrogen use efficiency (NUE) value, NUE = total dry weight / total N content; D: the total biomass (per plant dry weight DW); E: the nitrate reductase (NR) activity in shoots and roots; F: glutamine synthase (GS) activity in shoots and roots. Data present means (n = 5), the error bars denote the standard error (SE) value."

Table 1

Overview of the digital gene expression (DGE) profiling sequencing data"

样本名
Sample name		 下机原始reads数目
Raw reads		 高质量
reads数目
Clean reads		 过滤后高质量
数据碱基总数
Clean bases		 测序错误率
Error rate (%)		 碱基质量值达到Q20以上的碱基
Q20 (%)		 碱基质量值达到
Q30以上的碱基
Q30 (%)		 过滤前(后)的序列
碱基GC比例
GC content (%)
S0 596,35,738 57,043,591 8.55 0.01 97.05 92.59 47.49
R0 49,108,674.67 47,000,152 7.05 0.02 97.13 92.83 46.14
S3 58,163,928.67 55,612,390 8.34 0.02 97.15 92.79 47.61
R3 44,434,570 42,606,356 6.39 0.02 96.85 92.17 45.61
S72 55,942,618 53,982,678 8.10 0.02 96.72 91.64 47.07
R72 50,080,180 48,523,315 7.28 0.02 97.05 92.46 46.26

Fig. 2

Heatmap of Pearson correlation coefficient values in the shoots and roots of Brassica napus seedlings S0 and R0 represent the shoots and roots without low nitrogen treatment, respectively; S3 and R3 indicate the shoots and roots after 3 h under low nitrogen treatment, respectively; S72 and R72 denote the shoots and roots after 72 h under low nitrogen treatment, respectively."

Fig. 3

Differentially expressed genes (DEGs) in the shoots (S) and roots (R) of Brassica napus seedlings at 0, 3, and 72 h under low nitrogen treatment A: the venn-graph analysis of the DEGs; B: the number of the DEGs. S0 and R0 represent the shoots and roots without low nitrogen treatment, respectively; S3 and R3 indicate the shoots and roots after 3 h under low nitrogen treatment, respectively; S72 and R72 denote the shoots and roots after 72 h under low nitrogen treatment, respectively."

Fig. 4

Gene Ontology (GO) and Kyoto Encyclopedia of Genes and Genomes (KEGG) enrichment analysis of the digital gene expression (DGE) in the shoots and roots of Brassica napus A: GO enrichment analysis of the differentially expressed genes in the shoots after low nitrogen treatment for 72 h; B: GO enrichment analysis of the differentially expressed genes in the roots after low nitrogen treatment for 72 h; C: KEGG enrichment analysis of the differentially expressed genes in the shoots after low nitrogen treatment for 72 h; D: KEGG enrichment analysis of the differentially expressed genes in the roots after low nitrogen treatment for 72 h."

Fig. 5

Heat maps of the digital gene expression (DGE) profiling of BnaGLNs family genes A: the total DGE profiling of BnaGLNs family genes; B: the DGE profiling of BnaGLN1.1 subfamily genes; C: the DGE profiling of BnaGLN1.2 subfamily genes; D: the DGE profiling of BnaGLN1.3 subfamily genes; E: the DGE profiling of BnaGLN1.4 subfamily genes; F: the DGE profiling of BnaGLN1.5 subfamily genes; G: the DGE profiling of BnaGLN2 subfamily genes. S0 and R0 represent the shoots and roots without low nitrogen treatment, respectively; S3 and R3 indicate the shoots and roots after 3 h of low nitrogen treatment, respectively; S72 and R72 denote the shoots and roots after 72 h of low nitrogen treatment, respectively. The DEGs (S3 vs. S0, S72 vs. S0, R3 vs. R0, and R72 vs. R0) are labelled by asterisks."

Fig. 6

Heat maps of the digital gene expression (DGE) profiling of WRKYs family genes A: the total DGE profiling of BnaWRKY family genes; B the digital gene expression profiling of BnaWRKY33subfamily genes; C the digital gene expression profiling of BnaWRKY70subfamily genes. S0 and R0 represent the shoots and roots without low nitrogen treatment, respectively; S3 and R3 indicate the shoots and roots after 3 h of low nitrogen treatment, respectively; S72 and R72 denote the shoots and roots after 72 h of low nitrogen treatment, respectively. The DEGs (S3 vs. S0, S72 vs. S0; R3 vs. R0, and R72 vs. R0) are labelled by asterisks."

Fig. 7

Heat maps of the digital gene expression (DGE) profiling of MYBs family genes A: the total DGE profiling of BnaMYBs family genes; B: the DGE profiling of BnaMYB4s; C: the DGE profiling of BnaMYB44s; D: the DGE profiling of BnaMYB51ssubfamily genes. S0 and R0 represent the shoots and roots without low nitrogen treatment, respectively; S3 and R3 indicate the shoots and roots after 3 h of low nitrogen treatment, respectively; S72 and R72 denote the shoots and roots after 72 h of low nitrogen treatment, respectively. The DEGs (S3 vs. S0, S72 vs. S0; R3 vs. R0, and R72 vs. R0) are labelled by asterisks."

Fig. 8

Heat maps of the digital gene expression (DGE) profiling of NIAs family genes A: the total DGE profiling of BnaNIAs family genes; B: the DGE profiling of BnaNIA1s; C: the DGE profiling of BnaNIA2ssubfamily genes. S0 and R0 represent the shoots and roots without low nitrogen treatment, respectively; S3 and R3 indicate the shoots and roots after 3 h of low nitrogen treatment, respectively; S72 and R72 denote the shoots and roots after 72 h of low nitrogen treatment, respectively. The DEGs (S3 vs. S0, S72 vs. S0; R3 vs. R0, and R72 vs. R0) are labelled by asterisks."

Fig. 9

Heat maps of the digital gene expression (DGE) profiling of nitrate transporter (NRT) family genes A: the total DGE profiling of BnaNRT2.1 and BnaNRT3.1family genes; B: the DGE profiling of BnaNRT2.1; C: the DGE profiling of BnaNRT3.1 subfamily genes. S0 and R0 represent the shoots and roots without low nitrogen treatment, respectively; S3 and R3 indicate the shoots and roots after 3 h of low nitrogen treatment, respectively; S72 and R72 denote the shoots and roots after 72 h of low nitrogen treatment, respectively. The DEGs (S3 vs. S0, S72 vs. S0; R3 vs. R0, and R72 vs. R0) are labelled by asterisks."

Fig. 10

Alternative splicing classification and quantitative statistics A: the type and number of alternative splicing in shoots after 3 h under low nitrogen treatment; B: the type and number of alternative splicing in shoots after 72 h under low nitrogen treatment; C: the type and number of alternative splicing in roots after 3 h under low nitrogen treatment; D: the type and number of alternative splicing in roots after 72 h under low nitrogen treatment. JC only represent that only Junction Counts are used for AS event detection, and JC + reads OnTarget represent that both Junction Counts and reads on target are used for AS event detection."

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