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Acta Agronomica Sinica ›› 2024, Vol. 50 ›› Issue (3): 669-685.doi: 10.3724/SP.J.1006.2024.34055


Identification of candidate genes implicated in low-nitrogen-stress tolerance based on RNA-Seq in sorghum

WANG Rui1(), ZHANG Fu-Yao1, ZHAN Peng-Jie1, CHU Jian-Qiang1, JIN Min-Shan2, ZHAO Wei-Jun1, CHENG Qing-Jun1,*()   

  1. 1Institute of Sorghum, Shanxi Agricultural University / Key Laboratory of Genetic and Germplasm Innovation in Sorghum for Shanxi, Jinzhong 030600, Shanxi, China
    2College of Agronomy, Northwest A&F University, Yangling 712100, Shaanxi, China
  • Received:2023-03-16 Accepted:2023-10-23 Online:2024-03-12 Published:2023-11-17
  • Contact: *E-mail: chqj7002@163.com
  • Supported by:
    National Natural Science Foundation of China(32272164);Shanxi Scholarship Council of China(2020-161);“14th Five-Year Plan” Biological Breeding Project(YZGC058)


The objective of this study is to explore gene differential expression between different sorghum materials under low nitrogen stress conditions and to provide the references for probing into the breeding of low-nitrogen-tolerant sorghum varieties and the molecular mechanism of low-nitrogen-stress tolerance in sorghum. Two low-nitrogen-tolerant sorghum varieties (BSX44 and BTx378) were selected as experimental materials, and both of them were subjected to normal-growth treatment and low-nitrogen-stress treatment respectively before the gene expression of sorghum was detected at seedling stage, heading stage and flowering stage via RNA-Seq technology. The biological functions and metabolic pathways of the differentially expressed genes (DEGs) were analyzed by bioinformatics to screen genes that may be involved in the low-nitrogen regulation, and to understand the possible molecular pathways for nitrogen efficient materials in the process of nitrogen absorption and utilization. The results showed that: For BTx378 and BSX44, under normal-growth and low-nitrogen-stress treatments, 937 and 787 DEGs were detected at the seedling stage, 1305 and 935 at the heading stage, and 1402 and 963 at the flowering stage, for BTx378 and BSX44 respectively. Then the converged DEGs at the three stages were identified, and it was found that 246 genes were differentially expressed in the two low-nitrogen-tolerant sorghum varieties at the seedling stage, 371 at the heading stage, and 306 at the flowering stage. Furthermore, a total of 28 genes were consistently detected as DEGs at all three stages in the two low-nitrogen tolerant varieties, among which 5 genes were up-regulated and 23 genes were down-regulated. The KEGG analysis of the 28 common DEGs showed that they were mainly enriched in nitrogen metabolism, alanine, aspartic acid and glutamic acid metabolism, glycerophospholipid metabolism, and amino acid biosynthesis. This suggested that regulation of the genes in these pathways mainly affects the low nitrogen stress tolerance in sorghum.

Key words: sorghum, transcriptome sequencing, low nitrogen stress, differentially expressed genes (DEGs)

Table 1

Transcriptome sample"

Growth stage
正常氮Normal nitrogen 低氮Low nitrogen
BTx378 苗期 Seedling stage T1 (NN-R1-S1) T4 (LN-R1-S1)
抽穗期 Heading stage T2 (NN-R1-S2) T5 (LN-R1-S2)
开花期 Flowering stage T3 (NN-R1-S3) T6 (LN-R1-S3)
BSX44 苗期 Seedling stage T7 (NN-R2-S1) T10 (LN-R2-S1)
抽穗期 Heading stage T8 (NN-R2-S2) T11 (LN-R2-S2)
开花期 Flowering stage T9 (NN-R2-S3) T12 (LN-R2-S3)

Table 2

Groups of transcriptome sample"

Compare group
Control group vs Treatment group
A 1 T1 vs T4 NN-R1-S1 vs LN-R1-S1 正常氮-BTx378-苗期 vs低氮-BTx378-苗期
Normal nitrogen-BTx378-Seedling stage vs Low nitrogen-BTx378-Seedling stage
2 T7 vs T10 NN-R2-S1 vs LN-R2-S1 正常氮-BSX44-苗期 vs低氮-BSX44-苗期
Normal nitrogen-BSX44-Seedling stage vs Low nitrogen-BSX44-Seedling stage
B 3 T2 vs T5 NN-R1-S2 vs LN-R1-S2 正常氮-BTx378-抽穗期 vs低氮-BTx378-抽穗期
Normal nitrogen-BTx378-Heading stage vs Low nitrogen-BTx378-Heading stage
4 T8 vs T11 NN-R2-S2 vs LN-R2-S2 正常氮-BSX44-抽穗期 vs低氮-BSX44-抽穗期
Normal nitrogen-BSX44-Heading stage vs Low nitrogen-BSX44-Heading stage
C 5 T3 vs T6 NN-R1-S3 vs LN-R1-S3 正常氮-BTx378-开花期 vs低氮-BTx378-开花期
Normal nitrogen-BTx378-Flowering stage vs Low nitrogen-BTx378-Flowering stage
6 T9 vs T12 NN-R2-S3 vs LN-R2-S3 正常氮-BSX44-开花期 vs低氮-BSX44-开花期
Normal nitrogen-BSX44-Flowering stage vs Low nitrogen-BSX44-Flowering stage

Table 3

Information of the primers"

Primer ID
Sequence (5′-3′)
Product length (bp)

Table 4

Quality evaluation of RNA sequencing data"

Clean reads
Clean bases
GC 含量
GC content (%)
T1 NN-R1-S1 16,868,217 4,978,049,154 55.45 92.73
T2 NN-R1-S2 19,294,220 5,706,447,154 56.06 92.41
T3 NN-R1-S3 19,051,651 5,623,880,026 57.58 92.19
T4 LN-R1-S1 16,490,988 4,854,433,778 56.78 91.65
T5 LN-R1-S2 15,070,044 4,433,027,812 56.47 92.03
T6 LN-R1-S3 15,956,808 4,691,702,406 56.77 92.72
T7 NN-R2-S1 14,343,423 4,221,379,930 57.01 92.55
T8 NN-R2-S2 15,743,754 4,605,121,084 56.21 92.98
T9 NN-R2-S3 13,847,707 4,095,501,214 56.07 92.13
T10 LN-R2-S1 14,905,380 4,407,032,326 56.80 91.53
T11 LN-R2-S2 13,986,375 4,119,603,114 56.65 92.66
T12 LN-R2-S3 17,798,466 5,262,344,634 56.17 91.74

Fig. 1

qRT-PCR validation of partially differentially expressed genes NN: normal nitrogen; LN: low nitrogen. S1: seedling stage; S2: heading stage; S3: flowering stage. R1: BTx378; R2: BSX44. TPM: transcripts per million"

Table 5

Statistics of differentially expressed genes (DEGs)"

Compare group
Compare group
Up-regulated genes
Down-regulated genes
DEG number
A 1 NN-R1-S1 vs LN-R1-S1 464 473 937
2 NN-R2-S1 vs LN-R2-S1 264 523 787
B 3 NN-R1-S2 vs LN-R1-S2 637 668 1305
4 NN-R2-S2 vs LN-R2-S2 432 503 935
C 5 NN-R1-S3 vs LN-R1-S3 394 1008 1402
6 NN-R2-S3 vs LN-R2-S3 384 579 963

Fig. 2

Venn diagram of differentially expressed genes R1: BTx378; R2: BSX44. NN-R1 vs LN-R1: normal nitrogen-BTx378 vs low nitrogen-BTx378; NN-R2 vs LN-R2: normal nitrogen-BSX44 vs low nitrogen-BSX44."

Fig. 3

Enrichment analysis of differentially expressed genes at seedling stage A: GO enrichment annotation of differentially expressed genes at seedling stage; B: the KEGG pathway enrichment map of differentially expressed genes at seedling stage."

Fig. 4

Enrichment analysis of differentially expressed genes at heading stage A: GO enrichment annotation of differentially expressed genes at heading stage; B: the KEGG pathway enrichment map of differentially expressed genes at heading stage."

Fig. 5

Enrichment analysis of differentially expressed genes at anthesis stage A: GO enrichment annotation of differentially expressed genes at flowering stage; B: the KEGG pathway enrichment map of differentially expressed genes at flowering stage."

Fig. 6

Venn diagram of differentially expressed genes R1: BTx378; R2: BSX44."

Fig. 7

Heatmap of common differentially expressed genes LN-R2-S1: low nitrogen-BSX44-seedling stage; LN-R2-S2: low nitrogen-BSX44-heading stage; LN-R2-S3: low nitrogen-BSX44- flowering stage; LN-R1-S1: low nitrogen-BTx378-seedling stage; LN-R1-S2: low nitrogen-BTx378-heading stage; LN-R1-S3: low nitrogen- BTx378-flowering stage; NN-R1-S1: normal nitrogen-BTx378-seedling stage; NN-R1-S2: normal nitrogen-BTx378-heading stage; NN-R1- S3: normal nitrogen-BTx378-flowering stage; NN-R2-S1: normal nitrogen-BSX44-seedling stage; NN-R2-S2: normal nitrogen-BSX44- heading stage; NN-R2-S3: normal nitrogen-BSX44-flowering stage."

Table 6

Related information of common differentially expressed genes"

序号 基因编号 基因功能注释
Number Gene ID Gene function annotation
1 Sb01g006100 铁氧还蛋白——NADP还原酶, 根同工酶, 叶绿体
Ferredoxin—NADP reductase, root isozyme, chloroplastic
2 Sb01g007010 PAC2家族 PAC2 family
3 Sb01g015190 异天冬酰胺肽酶/L-天冬酰胺酶1亚基β
Isoaspartyl peptidase/L-asparaginase 1 subunit beta
4 Sb01g023750 丙氨酸转氨酶2 Alanine aminotransferase 2
5 Sb01g029470 硝酸盐转运蛋白1.1 POT家族
Nitrate transporter 1.1 POT family
6 Sb01g032250 二酰基甘油激酶1 Diacylglycerol kinase 1
7 Sb02g006060 抗病蛋白RPM1 Disease resistance protein RPM1
8 Sb02g042310 磷脂酶A1-Igamma2, 叶绿体
Phospholipase A1-Igamma2, chloroplastic
9 Sb03g012720 磷脂酶D p1 Phospholipase D p1
10 Sb03g036210 紫色酸性磷酸酶2 Purple acid phosphatase 2
11 Sb03g045170 蛋白SRG1 Protein SRG1
12 Sb04g005740 细胞色素P450 71D10 Cytochrome P450 71D10
13 Sb04g006250 氯通道样蛋白CLC-g
Putative chloride channel-like protein CLC-g
14 Sb04g006740 枯草杆菌蛋白酶Subtilisin-like protease
15 Sb04g021010 甘油磷酸二酯磷酸二酯酶家族
Glycerophosphoryl diester phosphodiesterase family
16 Sb04g032280 分歧的CRAL/TRIO域 Divergent CRAL/TRIO domain
17 Sb04g034160 铁氧还蛋白——亚硝酸盐还原酶, 叶绿体
Ferredoxin—nitrite reductase, chloroplastic
18 Sb04g035040 20 kD伴侣蛋白, 叶绿体20 kD chaperonin, chloroplastic
19 Sb05g016820 精氨酸/丝氨酸蛋白45 Arginine/serine-rich protein 45
20 Sb06g016540 脱落胁迫成熟蛋白2 Abscisic stress-ripening protein 2
21 Sb06g025950 含SPX结构域的膜蛋白 SPX domain-containing membrane protein
22 Sb06g031460 谷氨酰胺合成酶, 叶绿体Glutamine synthetase, chloroplastic
23 Sb07g008300 紫色酸性磷酸酶15 Purple acid phosphatase 15
24 Sb07g026000 营养细胞壁蛋白gp1 Vegetative cell wall protein gp1
25 Sb07g028630 含BTB/POZ结构域的蛋白 BTB/POZ domain-containing protein
26 Sb08g003180 转录因子GLK2 Probable transcription factor GLK2
27 Sb09g028090 营养细胞壁蛋白gp1 Vegetative cell wall protein gp1
28 Sorghum_bicolor_newGene_166 未知蛋白Unknown protein

Table 7

KEGG enrichment pathway of common differentially expressed genes"

KEGG pathway
KEGG同源基因KEGG orthology 基因编号
Gene ID
ko00910 氮代谢Nitrogen metabolism K00366+K01915 Sb04g034160; Sb06g031460
ko00250 丙氨酸、天冬氨酸和谷氨酸代谢
Alanine, aspartate and glutamate metabolism
K00814+K01915 Sb01g023750; Sb06g031460
ko00564 甘油磷脂代谢Glycerophospholipid metabolism K00901+K01115 Sb01g032250; Sb03g012720
ko01230 氨基酸的生物合成Biosynthesis of amino acids K00814+K01915 Sb01g023750; Sb06g031460
ko00565 醚脂代谢Ether lipid metabolism K01115 Sb03g012720
ko01210 2-氧羧酸代谢2-Oxocarboxylic acid metabolism K00814 Sb01g023750
ko00630 乙醛酸和二羧酸代谢Glyoxylate and dicarboxylate metabolism K01915 Sb06g031460
ko04070 磷脂酰肌醇信号系统Phosphatidylinositol signaling system K00901 Sb01g032250
ko00195 光合作用Photosynthesis K02641 Sb01g006100
ko00561 甘油脂代谢Glycerolipid metabolism K00901 Sb01g032250
ko00330 精氨酸和脯氨酸代谢Arginine and proline metabolism K01915 Sb06g031460
ko00710 光合生物的碳固定
Carbon fixation in photosynthetic organisms
K00814 Sb01g023750
ko04144 内吞作用Endocytosis K01115 Sb03g012720
ko01200 碳代谢Carbon metabolism K00814 Sb01g023750

Fig. 8

KEGG enrichment analysis of common differentially expressed genes"

Table 8

15 genes in the nitrogen uptake and mobilization pathway of orthologous maize and rice genes during different periods"

Genome ID
Orthologous genes
Seedling stage
Heading stage
Flowering stage
T1 vs T4 T7 vs T10 T2 vs T5 T8 vs T11 T3 vs T6 T9 vs T12
Sb01g001970 铵转运蛋白 AMT2 GRMZM2G338809 Os03g62200
Sb01g010270 谷氨酰胺合成酶 GS GRMZM2G024104 Os03g50490 -- --
Sb01g029470 低亲和硝酸盐转运蛋白 NRT1/PTR GRMZM2G161459 Os10g40600
Sb02g025100 谷氨酰胺合成酶 GS GRMZM2G036783 Os09g25610 -- --
Sb02g033100 谷氨酰胺合成酶 GS GRMZM2G459854
Sb03g035270 低亲和硝酸盐转运蛋白 NRT1/PTR GRMZM2G035790 -- -- --
Sb03g039530 亚硝酸还原酶 NiR GRMZM2G367668 --
Sb03g041190 低亲和硝酸盐转运蛋白 NRT1/PTR GRMZM2G470454 Os01g65100 --
Sb03g043020 低亲和硝酸盐转运蛋白 NRT1/PTR GRMZM2G419328 --
Sb04g002810 谷草转氨酶 AST Os02g04170 --
Sb04g031320 硝酸盐转运蛋白 NRT1/PTR Os02g46460 --
Sb05g002760 亚硝酸还原酶 NiR --
Sb06g020180 高亲和硝酸盐转运蛋白 NRT3 GRMZM2G163494 Os04g40410 --
Sb06g028990 谷氨酸合成酶 GOGAT GRMZM2G076239 Os04g53210 --
Sb10g026090 低亲和硝酸盐转运蛋白 NRT1/PTR
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