Scientia Agricultura Sinica ›› 2025, Vol. 58 ›› Issue (24): 5128-5142.doi: 10.3864/j.issn.0578-1752.2025.24.003

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

Study on the Function of Soybean Nicotinamide Enzyme GmNIC1 Gene Under Saline Alkali Stress

ZHANG Qi1(), XUE FuZhen1(), YANG XiuJie1, JIANG SuYang1, HUANG XueJuan1, MA JiaYi1, ZHANG ZheWen1, XU JieFei2,*()   

  1. 1 School of Bioengineering, Daqing Normal University/Daqing Research Base of Wetland Center, Chinese Academy of Sciences, Daqing 163712, Heilongjiang
    2 Jiamusi Branch of Heilongjiang Academy of Agricultural Sciences/Jiamusi Comprehensive Experimental Station of National Soybean Industry Technology System, Jiamusi 154002, Heilongjiang
  • Received:2025-07-02 Accepted:2025-09-03 Online:2025-12-16 Published:2025-12-22
  • Contact: XU JieFei

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Abstract:

【Objective】Saline-alkali stress is one of the significant abiotic stresses that restrict soybean production. Nicotinamide enzyme gene GmNIC1 is a key enzyme gene involved in the synthesis of NAD+ in soybeans. It has been previously established that this gene participates in abiotic stress responses. Investigating the function of GmNIC1 under saline-alkali stress lays the foundation for soybean breeding for saline-alkali tolerance.【Method】Using the soybean cultivar Hefeng 25 as the receptor, GmNICl-OE (overexpression) and GmNICl-KO (knockout) transgenic T3 generation soybean plants were generated, and their growth and physiological indicators under saline-alkali stress were measured. Transcriptome sequencing was performed on wild-type (WT), GmNICl-OE, and GmNICl-KO plants, followed by GO functional enrichment and KEGG pathway enrichment analysis. A protein-protein interaction network was constructed based on the differentially expressed genes of the three comparative combinations, and proteins interacting with GmNIC1 were identified and validated using quantitative real-time PCR.【Result】After saline-alkali stress, GmNICl-OE plants exhibited yellowing of newly grown leaves but erect petioles and increased plant height; GmNICl-KO plants showed wilted and dried leaves, severed yellowing of stems and near-death: WT plants had yellowish-brown stems and leaves that were less yellowed and wilted than those of the GmNICl-KO plants. Compared to WT and GmNICl-KO plants, GmNIC1-OE plants showed increased NAD+ content and decreased NADP+ content, leading to glucose accumulation, increased activity of SOD and CAT enzymes, and reduced O2- and H2O2 content. Transcriptome sequencing revealed a total of 747 differentially expressed genes in the OE-1 vs KO-1 comparative combination, including 622 upregulated and 125 downregulated differentially expressed genes. The number of differentially expressed genes in this combination was significantly higher than that in the other two groups. The functions of differentially expressed genes in the three comparative combinations were mainly concentrated in lactase activity, transcriptional regulation activity, and oxidoreductase activity (acting on NADP (H)); metabolic pathways were mainly involved in the biosynthesis of secondary metabolites, exogenous substance metabolism, glucosinolate biosynthesis, galactose metabolism, MAPK signaling pathway, glutathione metabolism, etc. Four proteins related to GmNIC1 were identified, suggesting that Glyma.04G055000.1 positively interacts with GmNICl, and Glyma.12G086500.1 negatively interacts with GmNIC1.【Conclusion】GmNIC1 increases NAD+ content and reduces NADP+ content to accumulate glucose and enhance antioxidant enzyme activity to eliminate ROS, thereby strengthening the plant's resistance to salt and alkali stress. The GmNIC1 protein can also collaborate with Glyma.04G055000.1 and Glyma.12G086500.1 to jointly regulate the growth of soybean seedlings under salt and alkali stress.

Key words: soybean, GmNIC1, salt and alkali stress, NAD+, NADP+

Table 1

Sequences of PCR primers"

用途Purpose 引物Primer 序列Sequence (5′-3′)
基因过表达
Gene overexpression		 GmNIC1-OE-F AATTTGGCGCCGAAAGAACC
GmNIC1-OE-R GCCTGAGTGTTGCATTTGGG
基因敲除
Gene knockout		 GmNIC1-KO-F GCATAGTACTTGCTTTGCGTTGG
GmNIC1-KO-R CTCGTGAACAACCTTTGGCTAGG
基因表达分析
Analysis of gene expression		 Actin-F GATCTACCATGTTCCCAAGT
Actin-R ATAGAGCCACCAATCCAGAC
qGmNIC1-F GCGTGGTAAAGATGTTCAAGAGT
qGmNIC1-R CAATATTCGTACTGCCCAAACCA
qGlyma.04G055000-F ATCTGAGGAGATGCGGAGGA
qGlyma.04G055000-R CAGTGCTGGATTAACCCCCT
qGlyma.12G086500-F CGAGTAGAGGAGGAAACAAAACGA
qGlyma.12G086500-R ATTCTCTCTCCCTTCTCTGGCA
qGlyma.13G242100-F CGACAGGGGTCCATATCCAG
qGlyma.13G242100-R CGCTGCAATTCCCCAGTAGA
qGlyma.14G114300-F CGTAGGAACTGGGTTGGTGT
qGlyma.14G114300-R CCGACGAAGATGTAAGCGGA

Fig. 1

Growth of transgenic soybean under salt alkali stress A: T3 generation transgenic soybeans that have grown normally to the V2 stage, bar=5 cm; B: T3 generation transgenic soybeans grown to the V3 stage under saline-alkali stress, bar=5 cm; C: PCR results were obtained from gene overexpression positive seedlings, M: DL2000 DNA Marker; H2O: No template control; -: Negative control; +: Plasmid positive control; D: Sequencing results of gene knockout positive vaccines. WT: Wild Hefeng 25 soybean seedlings; OE-1, OE-2: Transgenic Hefeng 25 soybean with overexpression of GmNIC1 gene; KO-1, KO-2: GmNIC1 knockout transgenic Hefeng 25 soybean"

Fig. 2

Physiological indicators of transgenic soybeans under saline alkali stress A: NAD+ and NADH content; B: NADP+ and NADPH content; C: NAD+/NADH and NADP+/NADPH; D: Glucose content; E: O2- and H2O2 content; F: SOD and CAT enzyme activity; Different lowercase letters indicate significant differences (P<0.05). The same as below"

Table 2

Number of differentially expressed genes in three comparative combinations"

对比组合
Contrast and combination		 上调差异表达基因数
The number of up-regulated genes		 下调差异表达基因数
The number of down-regulated genes
WT vs OE-1 514 39
WT vs KO-1 607 43
OE-1 vs KO-1 622 125

Fig. 3

GO functional enrichment of differentially expressed genes in transgenic soybean under salt alkali stress A：WT vs OE-1；B：WT vs KO-1；C：OE-1 vs KO-1"

Fig. 4

KEGG enrichment of differentially expressed genes in transgenic soybean under salt alkali stress A：WT vs OE-1；B：WT vs KO-1；C：OE-1 vs KO-1"

Fig. 5

Protein interaction network diagram NIT2: Omega-amidase (NIT2); LTP: LTP protein family; MYB63: Transcription factor MYB63; CGI2: CGI2 related proteins; RAB6: Phosphate transport system protein; C6T5S0: AP2/ERF domain-containing protein; CML14: CML14 related calcium binding protein; SMC: SMC family proteins; DDX51: ATP dependent RNA helicase DDX51; CLV1B: Asparagine synthetase protein (CLV1B). The thickness of the lines between each element represents the level of correlation"

Table 3

Protein interaction analysis screened protein information related to GmNIC1"

序号
Number		 交点
Node		 分数
Score		 功能注释
Functional annotation
1 Glyma.04G055000 988 Omega-酰胺酶 Omega-amidase
2 Glyma.12G086500 939 磷酸盐转运系统蛋白 Phosphate transport system protein
5 Glyma.13G242100 959 天冬酰胺合成酶 Asparagine synthetase
6 Glyma.14G114300 954 ATP依赖性RNA解旋酶 ATP dependent RNA helicase

Fig. 6

Expression levels of different interacting protein genes in transgenic soybeans A：Glyma.04G055000；B：Glyma.12G086500；C：Glyma.13G242100；D：Glyma.14G114300"

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