Identification of common genes for salt and cadmium tolerance in soybean

doi:10.3969/j.issn.1004-1524.20250086

Acta Agriculturae Zhejiangensis ›› 2026, Vol. 38 ›› Issue (1): 1-16.DOI: 10.3969/j.issn.1004-1524.20250086

• Crop Science • Previous Articles Next Articles

Identification of common genes for salt and cadmium tolerance in soybean

XU Yan¹^,²(), LI Sujuan³, CHEN Guang², XU Shengchun¹^,²^,⁴, WANG Jian²^,^*()

1. College of Advanced Agricultural Science, Zhejiang A&F University, Hangzhou 311300, China
2. Institute of Digital Agriculture, Zhejiang Academy of Agricultural Sciences, Hangzhou 310021, China
3. State Key Laboratory for Quality and Safety of Agro-Products, Zhejiang Academy of Agricultural Sciences, Hangzhou 310021, China
4. Xianghu Laboratory, Hangzhou 311258, China

Received:2025-02-07 Online:2026-01-25 Published:2026-02-11

Abstract

Abstract:

Saline-alkali land is occasionally accompanied by heavy metal pollution. Studying plant growth and physiological responses to combined salt and cadmium stress and identifying their common tolerance genes and regulatory pathways are of great significance for the genetic improvement of crop stress resistance. In this study, 50 soybean cultivars and wild soybean accessions were used as materials. They were cultivated under salt stress (200 mmol·L^-1 NaCl), cadmium stress (0.3 mmol·L^-1 CdCl₂), and normal conditions, respectively. Six indexes, including germination rate, plant height, root length, root-shoot ratio, and fresh weights of the aboveground and underground parts, were measured. Key tolerance indicators were screened through principal component analysis. The wild soybean accession W-3-12-90, which exhibited the strongest tolerance, was used to construct a full-length cDNA yeast expression library. Combined with the Full-length cDNA Over-expressor (FOX) gene hunting system and second-generation sequencing, genes related to co-tolerance to salt and cadmium were identified. Principal component analysis revealed that plant height, root length, aboveground fresh weight, and germination rate were the four key indexes for evaluating soybean tolerance to salt and cadmium. The wild soybean accession W-3-12-90 demonstrated the strongest tolerance under salt and cadmium stress. Using this material, a total of 109 common responsive genes to salt and cadmium were identified. Subcellular localization prediction showed that 39 of these genes encoded extracellular proteins, which respond rapidly and account for a high proportion. Proteins encoded by another 51 genes were distributed in the nucleus, cytoplasm, and cell membrane, and were primarily involved in pathways related to protein metabolism, cellular signal transduction, defense and stress responses, and oxidoreductase activity. Gene expression analysis indicated that six candidate co-tolerance genes were significantly upregulated under both salt and cadmium stress. In summary, genes responding to salt and cadmium stress in plants primarily function by encoding extracellular proteins and coordinately regulate plant tolerance through interactions of these proteins with the plasma membrane, nucleus, and cytoplasm. This study provides new insights for elucidating the molecular mechanism of soybean tolerance to salt and cadmium, and provides gene resources and theoretical basis for breeding new salt- and cadmium-tolerant germplasms.

Key words: soybean, salt stress, cadmium stress, germplasm screening, gene mining

CLC Number:

S565.1

XU Yan, LI Sujuan, CHEN Guang, XU Shengchun, WANG Jian. Identification of common genes for salt and cadmium tolerance in soybean[J]. Acta Agriculturae Zhejiangensis, 2026, 38(1): 1-16.

Figures/Tables 12

Table 1 Primers for qRT-PCR analysis of candidate genes associated with salt- and cadmium-tolerance

基因Gene	正向引物序列(5'→3') Forward primer sequence(5'→3')	反向引物序列(5'→3') Reverse primer sequence(5'→3')
GmEF1b	CCACTGCTGAAGAAGATGATGATG	AAGGACAGAAGACTTGCCACTC
GmDehydrin	AGGAAGGAACATCGTCAGCA	TGACAAGACACTGTACGTACG
GmSSP	CCACCTCAGGAGTCTCAGAA	CCCGCAAAAGTTTCGTGACT
GmGF14	ACGTTGGGAGAGGAATCATACA	GCATTCAACACCTTCTCCCT
GmPAP85	AGCAGAAAGAGGAGGGGAAC	AGCAGACAGTTGAAGTACACA
GmHUP54	ATGCCTAGGATTGACAGCGA	AGCAGAGTCAGCACCATCAT
GmMET2	TCGAGAGTGCTGAAATGGGT	ACACACCCATCACAAGTCCA

Fig.1 Physiological performance of different soybean seedlings under salt or cadmium stress Physiological responses of soybean seedlings of salt/Cd-tolerant and salt/Cd-sensitive varieties under salt/Cd stress for 8 days. NaCl, Salt stress; Cd, Cadmium stress; Control, Normal growth.

Table 2 Physiological performance of 50 soybean germplasms during seedling stage under normal conditions and salt/cadmium stress

处理 Treatment	PL/cm		RL/cm		RL/PL		SW/g		RW/g		GR
处理 Treatment	均值 Mean	CV/%	均值 Mean	CV/%	均值 Mean	CV/%	均值 Mean	CV/%	均值 Mean	CV/%	均值 Mean	CV/%
正常条件 CK	10.26± 0.31 a	24.91	7.52± 0.16 a	18.27	0.81± 0.02 b	23.83	0.76± 0.02 a	24.14	0.24± 0.01 a	31.58	0.97± 0.01 a	6.15
盐胁迫 Salt stress	1.03± 0.02 b	16.75	1.86± 0.05 b	23.06	1.92± 0.05 a	24.63	0.41± 0.01 b	31.97	0.05± 0.00 b	46.62	0.92± 0.01 b	10.56
镉胁迫 Cd stress	0.88± 0.03 b	37.75	0.30± 0.04 c	133.61	0.30± 0.04 c	134.28	0.41± 0.01 b	30.95	0.03± 0.01 b	353.39	0.75± 0.02 c	31.25

Table 3 Contribution of variables to principal components under salt stress across 50 soybean germplasms

性状 Trait	主成分1 PC1	主成分2 PC2	主成分3 PC3
PL	0.86	-0.12	0.08
RL	0.35	0.82	-0.12
GR	-0.49	0.84	-0.09
RL/PL	0.42	0.67	0.24
RW	0.84	-0.04	0.20
SW	-0.37	0.04	0.90
特征值Eigenvalue	2.09	1.81	0.93
贡献率/%Contribution rate/%	34.85	30.12	15.52
累计贡献率/%	34.85	64.97	80.49
Cumulative contribution rate/%

Table 4 Contribution of variables to principal components under cadmium stress across 50 soybean germplasms

性状 Trait	主成分1 PC1	主成分2 PC2	主成分3 PC3
PL	0.76	-0.19	0.52
RL	0.94	0.25	-0.16
RL/PL	0.55	-0.30	-0.14
GR	0.65	0.53	-0.51
RW	0.62	-0.48	0.20
SW	0.05	0.70	0.66
特征值Eigenvalue	2.56	1.20	1.05
贡献率/%Contribution rate/%	42.68	20.01	17.51
累计贡献率/%	42.68	62.69	80.20
Cumulative contribution rate/%

Fig.2 Growth performance of yeast strains transformed with soybean library under different growth conditions A, The survival performance of yeast strain G19 transformed with full-length soybean cDNA library on SD-His-Ura medium supplemented with 500 mmol·L-1 NaCl; B, The survival performance of yeast strain Δycf1 transformed with full-length soybean cDNA library on SD-Ura medium supplemented with 50 μmol·L-1 CdCl2. The photos were taken three days after plating.

Fig.3 GO and KEGG analysis of candidate genes for salt tolerance in soybean A, GO function clustering analysis; B, KEGG pathway enrichment analysis. The annotation names of Fig. A from top to bottom are as follows: Translational initiation; Translation initiation factor activity; RNA binding; Response to stress; Protein domain specific binding; Photosynthesis, light harvesting; Oxidoreductase activity, acting on single donors with incorporation of molecular oxygen, incorporation of two atoms of oxygen; Nutrient reservoir activity; Monolayer-surrounded lipid storage body; Glycolytic process. The annotation names of Fig. B from top to bottom are as follows: Spliceosome; RNA transport; Ribosome; Photosynthesis-antenna proteins; Metabolic pathways; Linoleic acid metabolism; Carbon metabolism; Carbon fixation in photosynthetic organisms; Biosynthesis of secondary metabolites; Biosynthesis of amino acids.

Fig.4 GO and KEGG enrichment analysis of candidate genes for cadmium tolerance in soybean A, GO function clustering analysis; B, KEGG pathway enrichment analysis. The annotation names of Fig. A from top to bottom are as follows: Serine-type endopeptidase inhibitor activity; S-adenosylmethionine biosynthetic process; RNA binding; Response to stress; Protein domain specific binding; Photosynthesis, light harvesting; Oxidoreductase activity, acting on the aldehyde or oxo group of donors, NAD or NADP as acceptor; Nutrient reservoir activity; Methionine adenosyltransferase activity; Heat shock protein binding. The annotation names of Fig. B from top to bottom are as follows: Ribosome; Photosynthesis-antenna proteins; Metabolic pathways; Glyoxylate and dicarboxylate metabolism; Glycolysis/Gluconeogenesis; Cysteine and methionine metabolism; Carbon metabolism; Carbon fixation in photosynthetic organisms; Biosynthesis of secondary metabolites; Biosynthesis of amino acids.

Fig.5 Subcellular localization of proteins encoded by soybean salt and cadmium tolerance candidate genes A, Subcellular localization of proteins encoded by known genes; B, Subcellular localization of proteins encoded by unknown genes.

Fig.6 GO and KEGG analysis of candidate genes for salt-cadmium co-tolerance in soybean A, GO function clustering analysis; B, KEGG pathway enrichment analysis. The annotation names of Fig. A from top to bottom are as follows: Serine-type endopeptidase inhibitor activity; Response to stress; Protein domain specific binding; Photosynthesis, light harvesting; Oxidoreductase activity, acting on the aldehyde or oxo group of donors, NAD or NADP as acceptor; Nutrient reservoir activity; Monolayer-surrounded lipid storage body; Extracellular region; Endopeptidase inhibitor activity; Cysteine-type peptidase activity. The annotation names of Fig. B from top to bottom are as follows: Ribosome; Protein processing in endoplasmic reticulum; Proteasome; Photosynthesis-antenna proteins; Monobactam biosynthesis; Metabolic pathways; Linoleic acid metabolism; Glycolysis/Gluconeogenesis; Carbon metabolism; Carbon fixation in photosynthetic organisms. Gene ratio represents the ratio of differentially expressed genes annotated to a specific term to the total number of differentially expressed genes; Rich factor is the ratio of enriched differentially expressed genes in a pathway to all genes in that pathway. The same as below.

Table 5 Key salt and cadmium tolerant gene information of soybean

基因ID Gene ID	基因名 Gene name	cDNA大小/bp cDNA size/bp	预测功能 Function prediction
Glyma.09G185500	GmDehydrin	681	Dehydrin-like protein
Glyma.03G163533	GmSSP	1 488	Rmlc-like cupins superfamily protein
Glyma.02G208700	GmGF14	789	14-3-3-like protein
Glyma.10G246300	GmPAP85	1 866	Cupin family protein
Glyma.15G072400	GmHUP54	756	Aluminium induced protein with YGL and LRDR motifs
Glyma.07G132000	GmMET2	240	Metallothionein 2A

Fig.7 Relative expression level of candidate genes in soybean roots, stems, and leaves under salt, Cd and salt-Cd stress Bars marked with the same lowercase letters in the figure indicate significant differences (p<0.05) among treatments at the same time.

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Identification of common genes for salt and cadmium tolerance in soybean

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