Physiological and Transcriptomic Analysis of Soybean under Waterlogging Stress

doi:10.7668/hbnxb.20195959

Abstract

Abstract:

Waterlogging stress severely impacts soybean production.To investigate the effects of waterlogging stress on soybean growth and development and elucidate its response mechanisms,this study employed four soybean germplasms cultivated in the Huaibei region as experimental materials.Through simulated waterlogging treatment at the V2 stages,combined with yield analysis,physiological indices,and transcriptomic profiling,the study explores the waterlogging tolerance mechanisms in soybean.The results demonstrated that waterlogging stress significantly reduced dry matter accumulation and nitrogen uptake efficiency in the waterlogging-sensitive cultivar Xudou 18,resulting in a yield loss of 30.23%.In contrast,the waterlogging-tolerant cultivar Huaidou 13 exhibited stronger adaptability with only a 16.77% yield loss,attributed to stabilized root nitrogen absorption and maintained root dry matter accumulation.Transcriptomic analysis revealed that differentially expressed genes(DEGs)in Huaidou 13 under waterlogging stress were significantly enriched in pathways that related to the biosynthesis of secondary metabolites,photosynthetic systems,and antioxidant activity.Conversely,DEGs in Xudou 18 were predominantly associated with hormone transduction,photosynthesis,and peroxisome-related pathways.A total of 148 genotype-specific DEGs were identified between cultivars with contrasting waterlogging tolerance,primarily enriched in photosynthesis,secondary metabolite biosynthesis,and fatty acid metabolism.Identified transcription factors included members of the AP2/ERF-ERF,C3H,ARR-B,NAC,and WRKY families.In summary,transcription factors or genes in secondary metabolic pathways that may be related to waterlogging tolerance were screened.

Key words: Soybean, Waterlogging stress, Physiological metabolism, Transcriptome

CLC Number:

ZHAO Zhixin, LIU Ningning, XU Haifeng, WANG Yaqi, FU Mengmeng, LI Shuguang, YU Xiwen. Physiological and Transcriptomic Analysis of Soybean under Waterlogging Stress[J]. Acta Agriculturae Boreali-Sinica, 2025, 40(S1): 9-19. doi: 10.7668/hbnxb.20195959.

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Figures/Tables 13

Tab.1 Treatment combination of test materials

品种名称 Test materials	正常水分处理 (CK) Normal treatment of water(CK)	涝害处理(LH) Waterlogging treatment (LH)
淮豆13 Huaidou 13	CK-G01	LH-G01
淮豆4号Huaidou 4	CK-G02	LH-G02
Forrest	CK-G03	LH-G03
徐豆18 Xudou 18	CK-G04	LH-G04

Tab.2 Effects of water logging stress on soybean yield and yield-related factors

品种 Test materials	对照处理CK			涝害处理LH
品种 Test materials	百粒质量/g 100-seed weight	单株粒数 Seed number per plant	单株产量/g Yield per plant	百粒质量/g 100-seed weight	单株粒数 Seed number per plant	单株产量/g Yield per plant
G01	18.36±2.56a	67.25±11.69a	12.22±3.15a	18.24±4.98a	57.00±9.24b	10.17±4.26ab
G02	20.42±3.54a	79.80±13.59a	14.62±3.24a	20.40±3.47a	57.75±10.66b	10.18±4.12b
G03	16.05±2.72a	71.00±11.32a	11.35±2.87a	16.57±3.68a	53.40±8.63b	8.53±3.47b
G04	19.47±3.16a	81.00±17.65a	14.75±3.87a	16.58±3.29b	69.92±14.23b	10.29±2.69b

Fig.1 Effects of water logging stress on dry matter accumulation of soybean The different lowercase letters indicate significant differences among materials and treatments(P<0.05).The same as Fig.2-3.

Fig.2 Effects of water logging stress on nitrogen accumulation in soybean

Fig.3 Effects of water logging stress on MDA content in soybean

Tab.3 Effect of water logging stress on antioxidant enzyme activity of soybean

品种 Test materials	SOD/(U/g)		POD/(U/g)		CAT/(nmol/mg)
品种 Test materials	CK	LH	CK	LH	CK	LH
G01	129.88±20.00a	102.40±26.90b	8 054.67±886.39a	6 153.33±416.64b	688.36±211.60a	571.56±136.17b
G02	197.93±10.62b	220.50±40.63a	10 066.67±3 035.85a	10 625.30±1 945.02a	723.48±6.28a	807.72±198.62a
G03	147.87±10.66a	122.98±6.83a	10 256.00±1 385.93a	10 524.33±682.64a	1 844.13±97.17b	2 136.88±99.06a
G04	354.25±6.02b	371.48±15.72a	6 096.00±75.70b	7 128.00±1 509.57a	347.58±17.69b	528.46±136.55a

Tab.4 Statistical table of sequencing data quality evaluation

样品 Samples	过滤后数据 Clean reads	匹配到的数据 Total mapped reads	匹配率/% Total mapped reads	GC含量/% GC content	Q30碱基比例/% Q30 content
CK-G01-1	44 387 312	42 697 614	96.19	44.54	96.70
CK-G01-2	53 714 074	51 809 156	96.45	44.60	96.84
CK-G04-1	45 732 788	43 709 270	95.58	43.78	97.04
CK-G04-2	55 330 950	53 427 847	96.56	44.56	95.04
LH-G01-1	52 922 238	48 273 942	91.22	45.05	90.34
LH-G01-2	41 479 404	36 768 240	88.64	46.38	96.91
LH-G04-1	40 252 692	38 244 336	95.01	44.07	96.84
LH-G04-2	50 595 966	48 542 084	95.94	43.98	96.65

Fig.4 Differentially expressed analysis of Huaidou 13 and Xudou 18 of leaf transcriptomic A.Heatmap of sample;B.Histogram of the number of differentially expressed genes;C.Venn.

Fig.5 GO enrichment analysis of DEGs in Huaidou 13(A)and Xudou 18(B) A:1.Cellular process;2.Metabolic process;3.Single-organism process;4.Biological regulation;5.Localization;6.Regulation of biological process;7.Rresponse to stimulus;8.Cellular component organization or biogenesis;9.Multicellular organismal process;10.Multi-organism process;11.Signaling;12.Reproduction;13.Developmental process;14.Reproductive process;15.Detoxification;16.Negative regulation of biological process;17.Locomotion;18.Positive regulation of biological process;19.Immune system process;20.Behavior;21.Biological adhesion;22.Growth;23.Cell killing;24.Rhythmic process;25.Catalytic activity;26.Binding;27.Transporter activity;28.Nucleic acid binding transcription factor activity;29.Electron carrier activity;30.Structural molecule activity;31.Antioxidant activity;32.Molecular function regulator;33.Signal transducer activity;34.Molecular transducer activity;35.Translation regulator activity;36.Transcription factor activity,protein binding;37.Metallochaperone activity;38.Cell part;39.Cell;40.Membrane;41.Membrane part;42.Macromolecular complex;43.Organelle;44.Organelle part;45.Extracellular region;46.Membrane-enclosed lumen;47.Virion;48.Virion part;49.Synapse;50.Viral occlusion body;51.Supramolecular fiber;52.Extracellular region part;53.Synapse part;54.Nucleoid;55.Extracellular matrix;56.Symplast;57.Cell junction.B:1.Ccellular process;2.Metabolic process;3.Single-organism process;4.Localization;5.Response to stimulus;6.Biological regulation;7.Regulation of biological process;8.Cellular component organization or biogenesis;9.Multi-organism process;10.Signaling;11.Reproduction;12.Multicellular organismal process;13.Developmental process;14.Reproductive process;15.Negative regulation of biological process;16.Detoxification;17.Positive regulation of biological process;18.Locomotion;19.Immune system process;20.Growth;21.Biological adhesion;22.Rhythmic process;23.Behavior;24.Presynaptic process involved in synaptic transmission;25.Cell killing;26.Catalytic activity;27.Binding;28.Transporter activity;29.Nucleic acid binding transcription factor activity;30.Structural molecule activity;31.Antioxidant activity;32.Molecular function regulator;33.Electron carrier activity;34.Signal transducer activity;35.Molecular transducer activity;36.Transcription factor activity,protein binding;37.Metallochaperone activity;38.Protein tag;39.Translation regulator activity;40.Cell;41.Cell part;42.Membrane;43.Mcromolecular complex;44.Organelle;45.Membrane part;46.Organelle part;47.Extracellular region;48.Membrane-enclosed lumen;49.Virion;50.Virion part;51.Extracellular region part;52.Supramolecular fiber;53.Extracellular matrix;54.Viral occlusion body;55.Symplast;56.Cell junction;57.Other organism;58.Other organism part;59.Synapse;60.Synapse part.

Fig.6 The top 20 functional classification of GO enrichment analysis of Huaidou 13(A)and Xudou 18(B) A:1.GO:0016020 Membrane;2.GO:0009535 Chloroplast thylakoid membrane;3.GO:0055035 Plastid thylakoid membrane;4.GO:0045156 Electron transporter,transferring electrons within the cyclic electron transport pathway of photosynthesis activity;5.GO:0016168 Chlorophyll binding;6.GO:0016491 Oxidoreductase activity;7.GO:0009534 Chloroplast thylakoid;8.GO:0003700 Transcription factor activity,sequence-specific DNA binding;9.GO:0001071 Nucleic acid binding transcription factor activity;10.GO:0031976 Plastid thylakoid;11.GO:0015267 Channel activity;12.GO:0022803 Passive transmembrane transporter activity;13.GO:0009772 Photosynthetic electron transport in photosystem Ⅱ;14.GO:0009539 Photosystem Ⅱ reaction center;15.GO:0016021 Integral component of membrane;16.GO:0031224 Intrinsic component of membrane;17.GO:0005216 Ion channel activity;18.GO:0055114 Oxidation-reduction process;19.GO:0022838 Substrate-specific channel activity;20.GO:0004421 Hydroxymethylglutaryl-CoA synthase activity.B:1.GO:0006468 Protein phosphorylation;2.GO:0016310 Phosphorylation;3.GO:0004672 Protein kinase activity;4.GO:0016301 Kinase activity;5.GO:0016773 Phosphotransferase activity,alcohol group as acceptor;6.GO:0003824 Catalytic activity;7.GO:0016740 Transferase activity;8.GO:0003700 Transcription factor activity,sequence-specific DNA binding;9.GO:0001071 Nucleic acid binding transcription factor activity;10.GO:0016772 Transferase activity,transferring phosphorus-containing groups;11.GO:0016798 Hydrolase activity,acting on glycosyl bonds;12.GO:0016667 Oxidoreductase activity,acting on a sulfur group of donors;13.GO:0006629 Lipid metabolic process;14.GO:0006464 Cellular protein modification process;15.GO:0036211 Protein modification process;16.GO:0004553 Hydrolase activity,hydrolyzing O-glycosyl compounds;17.GO:0006793 Phosphorus metabolic process;18.GO:0009654 Photosystem Ⅱ oxygen evolving complex;19.GO:0015035 Protein disulfide oxidoreductase activity;20.GO:0042221 Response to chemical.

Fig.7 The top 20 pathways of KEGG enrichment analysis of Huaidou 13(A)and Xudou 18(B) A:1.Ko04626 Plant-pathogen interaction;2.Ko00195 Photosynthesis;3.Ko00909 Sesquiterpenoid and triterpenoid biosynthesis;4.Ko04141 Protein processing in endoplasmic reticulum;5.Ko01100 Metabolic pathways;6.Ko00380 Tryptophan metabolism;7.Ko00561 Glycerolipid metabolism;8.Ko01110 Biosynthesis of secondary metabolites;9.Ko02010 ABC transporters;10.Ko00901 Indole alkaloid biosynthesis;11.Ko00073 Cutin,suberine and wax biosynthesis;12.Ko00591 Linoleic acid metabolism;13.Ko00062 Fatty acid elongation;14.Ko00903 Limonene degradation;15.Ko00941 Flavonoid biosynthesis;16.Ko00750 Vitamin B6 metabolism;17.Ko00053 Ascorbate and aldarate metabolism;18.Ko00250 Alanine,aspartate and glutamate metabolism;19.Ko00071 Fatty acid degradation;20.Ko00330 Arginine and proline metabolism.B:1.Ko04075 Plant hormone signal transduction;2.Ko00196 Photosynthesis-antenna proteins;3.Ko00860 Porphyrin metabolism;4.Ko04016 MAPK signaling pathway-plant;5.Ko00592 alpha-Linolenic acid metabolism;6.Ko01110 Biosynthesis of secondary metabolites;7.Ko04626 Plant-pathogen interaction;8.Ko01212 Fatty acid metabolism;9.Ko00195 Photosynthesis;10.Ko00061 Fatty acid biosynthesis;11.Ko00430 Taurine and hypotaurine metabolism;12.Ko00071 Fatty acid degradation;13.Ko00941 Flavonoid biosynthesis;14.Ko00410 beta-Alanine metabolism;15.Ko00945 Stilbenoid,diarylheptanoid and gingerol biosynthesis;16.Ko04146 Peroxisome;17.Ko04136 Autophagy-other;18.Ko00480 Glutathione metabolism;19.Ko00280 Valine,leucine and isoleucine degradation;20.Ko01040 Biosynthesis of unsaturated fatty acids.

Fig.8 Family classification of transcription factors of differential expression genes

Fig.9 GO and KEGG enrichment analysis of 148 response genes to water logging stress A:1.GO:0015035 Protein disulfide oxidoreductase activity;2.GO:0004364 Glutathione transferase activity;3.GO:0004784 Superoxide dismutase activity;4.GO:0016721 Oxidoreductase activity,acting on superoxide radicals as acceptor;5.GO:0008686 3,4-dihydroxy-2-butanone-4-phosphate synthase activity;6.GO:0015542 Sugar efflux transmembrane transporter activity;7.GO:0001871 Pattern binding;8.GO:0030247 Polysaccharide binding;9.GO:0030729 Acetoacetate-CoA ligase activity;10.GO:0050218 Propionate-CoA ligase activity;11.GO:0008668(2,3-dihydroxybenzoyl)adenylate synthase activity;12.GO:0008756 O-succinylbenzoate-CoA ligase activity;13.GO:0003987 Acetate-CoA ligase activity;14.GO:0047473 D-alanine-poly(phosphoribitol)ligase activity;15.GO:0005351 Sugar:proton symporter activity;16.GO:0030246 Carbohydrate binding;17.GO:0003700 Transcription factor activity,sequence-specific DNA binding;18.GO:0001071 Nucleic acid binding transcription factor activity;19.GO:0016405 CoA-ligase activity;20.GO:0016878 Acid-thiol ligase activity.B:1.Ko04141 Protein processing in endoplasmic reticulum;2.Ko04626 Plant-pathogen interaction;3.Ko00591 Linoleic acid metabolism;4.Ko04146 Peroxisome;5.Ko00061 Fatty acid biosynthesis;6.Ko00592 alpha-Linolenic acid metabolism;7.Ko00250 Alanine,aspartate and glutamate metabolism;8.Ko00195 Photosynthesis;9.Ko03420 Nucleotide excision repair;10.Ko01212 Fatty acid metabolism;11.Ko00909 Sesquiterpenoid and triterpenoid biosynthesis;12.Ko00480 Glutathione metabolism;13.Ko00062 Fatty acid elongation;14.Ko00053 Ascorbate and aldarate metabolism;15.Ko00280 Valine,leucine and isoleucine degradation;16.Ko00130 Ubiquinone and other terpenoid-quinone biosynthesis;17.Ko00071 Fatty acid degradation;18.Ko00260 Glycine,serine and threonine metabolism;19.Ko04070 Phosphatidylinositol signaling system;20.Ko00562 Inositol phosphate metabolism.

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