Scientia Agricultura Sinica ›› 2025, Vol. 58 ›› Issue (21): 4512-4527.doi: 10.3864/j.issn.0578-1752.2025.21.019

• EXPLORATION OF SALT-ALKALI AND DROUGHT RESISTANT GENES FOR ALFALFA BREEDING • Previous Articles     Next Articles

Differential Proteomic Analysis of Alfalfa Seedlings Under Salt- Alkaline Stress

YANG YongNian1,2(), ZENG XiangCui1, LIU QingSong3, LI RuYue1, LONG RuiCai1, CHEN Lin1, WANG Xue1, HE Fei1, KANG JunMei1, LI MingNa1()   

  1. 1 Institute of Animal Science, Chinese Academy of Agricultural Sciences, Beijing 100193
    2 College of Forestry and Landscape Architecture, South China Agricultural University, Guangzhou 510642
    3 Cangzhou Academy of Agriculture and Forestry Sciences, Cangzhou 061001, Hebei
  • Received:2025-03-04 Accepted:2025-04-09 Online:2025-11-01 Published:2025-11-06
  • Contact: LI MingNa

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Abstract:

【Objective】Soil salinization and alkalization are significant limiting factors for the growth and yield of alfalfa (Medicago sativa L.). To elucidate the molecular mechanisms underlying the response of alfalfa seedlings to salt or alkali stress, this study employed proteomic analysis to identify key differentially expressed proteins and their associated metabolic pathways under saline-alkali stress, so as to provide a theoretical foundation for elucidating the mechanisms of saline-alkali tolerance. 【Method】This study used Zhongmu No. 4 alfalfa as the experimental material. Seeds were subjected to salt stress (30 mmol·L-1 NaCl and 30 mmol·L-1 Na2SO4) and alkali stress (10 mmol·L-1 Na2CO3 and 10 mmol·L-1 NaHCO3). TMT labeling combined with liquid chromatography- mass spectrometry (LC-MS/MS) was employed to analyze the proteomic changes in alfalfa seedlings after stress treatments. 【Result】In total, 6 829 proteins were identified, including 489 differentially expressed proteins (DEPs) (274 up-regulated and 215 down-regulated) under alkali stress and 376 DEPs (218 up-regulated and 158 down-regulated) under salt stress. GO annotation analysis revealed that the DEPs were primarily associated with biological processes, such as cellular metabolism, organic metabolism, and stress response, as well as cellular components including intracellular organelles, cytoplasm, and membranes. KEGG pathway enrichment analysis indicated that under alkali stress, DEPs were significantly enriched in pathways, such as photosynthesis, phenylpropanoid biosynthesis, and isoflavonoid biosynthesis, while under salt stress, they were mainly enriched in photosynthesis, isoflavonoid biosynthesis, and glutathione metabolism. Further analysis of the enriched proteins demonstrated that alfalfa seedlings enhanced their resistance to salt-alkali stress by up-regulating key proteins in the isoflavonoid biosynthesis pathway (HI4OMT and CYP81E). The upregulation of key enzymes such as HI4OMT and CYP81E significantly enhanced the accumulation of isoflavonoids, which facilitated reactive oxygen species scavenging and maintained cellular homeostasis in plants. Furthermore, under alkaline stress, key enzymes (PAL, CAD, and COMT) in the phenylpropanoid biosynthesis pathway were markedly upregulated, promoting the synthesis of lignin and flavonoids. This process strengthened cell wall integrity and antioxidant capacity, enabling plants to adapt to high-pH environments and cope with alkaline stress. Under salt stress, alfalfa seedlings upregulated critical enzymes (PRDX6, GPX, and GST) in the glutathione metabolism pathway, maintaining redox homeostasis and enhancing ROS scavenging, thereby improving salt stress tolerance. 【Conclusion】In summary, this proteomic study elucidated key proteins and metabolic pathways involved in the response of alfalfa seedlings to salt-alkali stress, providing a theoretical foundation for understanding the molecular mechanisms of salt-alkali tolerance in alfalfa. Simultaneously, this study provided potential candidate proteins and metabolic pathways for breeding salt-alkali tolerant alfalfa. Subsequent research could further validate the functions of these key proteins and employ advanced biotechnological breeding approaches to develop new alfalfa varieties with enhanced salt-alkali tolerance, thereby addressing the challenges posed by soil salinization-alkalization to alfalfa production.

Key words: Alfalfa, salt-alkali stress, proteomics, phenylpropanoid biosynthesis, glutathione metabolism pathway

Fig. 1

Protein function annotation and differentially expressed protein identification A: Protein functional annotation chart; B: Differential protein chart; C: Venn diagram of up-regulated differential expressed proteins; D: Venn diagram of down-regulated differentially expressed proteins"

Fig. 2

GO functional classification of differentially expressed proteins A: Functional classification of differentially expressed proteins in the alkaline stress comparison group (AM3 vs SM1); B: Functional classification of differentially expressed proteins in the salt stress comparison group (SM3 vs SM1). The abscissa represents the number of differential proteins in the classification, the ordinate represents the secondary functional classification of GO; the different colors represent the primary classification of GO (Biological process/Cellular component/Molecular function)"

Fig. 3

Heatmap of GO functional cluster analysis of differentially expressed proteins under salt stress A: Enrichment of differentially expressed proteins in biological processes; B: Enrichment of differentially expressed proteins in cellular components; C: Enrichment of differentially expressed proteins in molecular functions. The horizontal representation represents different comparison groups, the longitudinal representation represents the related functions of differentially expressed protein enrichment in different comparison groups; The color gradient indicates the significance of enrichment, dark blue represents high enrichment significance, light blue and white represent low enrichment significance; *:P < 0.05, **:P < 0.01, and ***:P < 0.001"

Fig. 4

KEGG bubble diagram of functional enrichment analysis of differential proteins A: Functional enrichment of differentially expressed proteins in the alkaline stress comparison group (AM3 vs SM1); B: Functional enrichment of differentially expressed proteins in the salt stress comparison group (SM3 vs SM1). The horizontal axis is the enrichment degree of differential proteins in this function, and the greater the value, the higher the enrichment degree of differential proteins; The vertical axis is the KEGG path description information; The color of the point indicates the enrichment significance P value, and the bluer the color, the stronger the enrichment significance; The size of the dot indicates the number of differential proteins in the KEGG pathway, and the larger the dot, the more differential proteins there are"

Fig. 5

Schematic presentation of salinity stress-responsive proteins involved in photosystem and electron transport in Medicago sativa A: Changes in Differentially Expressed Proteins in the alkaline stress comparison group (AM3 vs SM1); B: Changes in Differentially Expressed Proteins in the salt stress comparison group (SM3 vs SM1)"

Table 1

Information and differential changes of important candidate proteins under saline-alkali stress"

蛋白编号
Protein accession		 蛋白名称
Protein name		 比值/Ratio AM3/SM1 比值/Ratio SM3/SM1 上调/下调
Up/Down
光合作用途径 Photosynthesis
Msa.H.0037330 光合系统 I 亚基 IV Photosystem I subunit IV，PsaE 0.70 0.70 Down
Msa.H.0077410 光合系统 I 亚基 III Photosystem I subunit III，PsaF 0.70 0.70 Down
Msa.H.0064710 铁氧还蛋白 Ferredoxin，PetF 0.76 0.75 Down
Msa.H.0099480 光合系统 II 10 kDa 蛋白 Photosystem II 10kDa protein，PsbR 0.75 0.73 Down
Msa.H.0138280 光合系统 II 析氧增强蛋白 2 Pphotosystem II oxygen-evolving enhancer protein 2，PsbP 0.67 0.70 Down
Msa.H.0119220 质体蓝蛋白 Plastocyanin，PetE 0.70 0.74 Down
Msa.H.0183910 光合系统II CP43叶绿素载脂蛋白 Photosystem II CP43 chlorophyll apoprotein，PsbC 0.77 - Down
Msa.H.0250550 光合系统 I 亚基 II Photosystem I subunit II，PsaD 0.74 0.73 Down
Msa.H.0261110 铁氧还蛋白 - NADP+ 还原酶 Ferredoxin--NADP+ reductase，PetH 0.77 - Down
Msa.H.0259150 光合系统 II 析氧增强子蛋白1 Photosystem II oxygen-evolving enhancer protein 1，PsbO 0.70 0.74 Down
Msa.H.0298590 光合系统 II 析氧增强蛋白 2 Photosystem II oxygen-evolving enhancer protein 2，PsbP 0.62 0.63 Down
Msa.H.0472080 光合系统 II 析氧增强子蛋白 1 Photosystem II oxygen-evolving enhancer protein 1，PsbO 0.68 0.70 Down
Msa.H.0466450 光合系统I P700叶绿素a载脂蛋白A2 Photosystem I P700 chlorophyll a apoprotein A2，PsaB 0.71 0.74 Down
异黄酮生物合成 Isoflavonoid biosynthesis
Msa.H.0226800 2-羟基异黄烷酮合酶 2-hydroxyisoflavanone synthase，CYP93C 1.34 1.39 Up
Msa.H.0232170 异黄酮/4'-甲氧基异黄酮 2'-羟化酶 Isoflavone/4'-methoxyisoflavone 2'-hydroxylase，CYP81E 1.59 - Up
Msa.H.0226810 2,7,4'-三羟基异黄烷酮 4'-O-甲基转移酶/异黄酮 4'-O-甲基转移酶 2,7,4'-trihydroxyisoflavanone 4'-O-methyltransferase / isoflavone 4'-O-methyltransferase，HI4OMT 1.38 1.20 Up
Msa.H.0199640 2,7,4'-三羟基异黄烷酮 4'-O-甲基转移酶/异黄酮 4'-O-甲基转移酶 2,7,4'-trihydroxyisoflavanone 4'-O-methyltransferase / isoflavone 4'-O-methyltransferase，HI4OMT 1.56 1.35 Up
Msa.H.0260210 2'-羟基异黄酮还原酶 2'-hydroxyisoflavone reductase，IFR 1.71 1.44 Up
Msa.H.0406540 维斯提酮还原酶 Vestitone reductase，VR 1.68 1.44 Up
苯丙烷生物合成途径 Phenylpropanoid biosynthesis
Msa.H.0001220 肉桂醇脱氢酶Cinnamyl-alcohol dehydrogenase，CAD 1.37 - Up
Msa.H.0077680 过氧化物酶 Peroxidase，POD 0.74 - Down
Msa.H.0107820 过氧化物酶 Peroxidase，POD 0.73 - Down
Msa.H.0077670 过氧化物酶 Peroxidase，POD 1.48 - Up
Msa.H.0077610 过氧化物酶 Peroxidase，POD 1.83 - Up
Msa.H.0065700 过氧化物酶 Peroxidase，POD 1.92 - Up
Msa.H.0077620 过氧化物酶 Peroxidase，POD 1.56 - Up
Msa.H.0155080 过氧化物酶 Peroxidase，POD 0.71 - Down
Msa.H.0167830 过氧化物酶 Peroxidase，POD 2.82 - Up
Msa.H.0300450 苯丙氨酸解氨酶 Phenylalanine ammonia-lyase-PAL 1.72 - Up
Msa.H.0332160 过氧化物酶 Peroxidase，POD 1.90 - Up
Msa.H.0421520 苯丙氨酸解氨酶 Phenylalanine ammonia-lyase-PAL 1.37 - Up
Msa.H.0425430 过氧化物酶 Peroxidase，POD 1.39 - Up
Msa.H.0404990 过氧化物酶 Peroxidase，POD 1.54 - Up
Msa.H.0431280 咖啡酸 3-O-甲基转移酶 / 乙酰血清素 O-甲基转移
Caffeic acid 3-O-methyltransferase / acetylserotonin O-methyltransferase，COMT		 1.31 - Up
Msa.H.0489830 过氧化物酶 Peroxidase，POD 0.64 - Down
Msa.H.0445400 咖啡酸 3-O-甲基转移酶 / 乙酰血清素 O-甲基转移
Caffeic acid 3-O-methyltransferase / acetylserotonin O-methyltransferase，COMT		 0.66 - Down
Msa.H.0473540 咖啡酰辅酶 A O-甲基转移酶 Caffeoyl-CoA O-methyltransferase，CCoAOMT 0.74 - Down
谷胱甘肽代谢途径 Glutathione metabolism
Msa.H.0047790 谷胱甘肽 S-转移酶 Glutathione S-transferase，GST - 1.33 Up
Msa.H.0039470 谷胱甘肽过氧化物酶 Glutathione peroxidase，GPX, btuE, bsaA - 0.37 Down
Msa.H.0202400 过氧化物还原蛋白 6 Peroxiredoxin 6，PRDX6 - 1.42 Up
Msa.H.0241880 谷胱甘肽过氧化物酶 Glutathione peroxidase，GPX, btuE, bsaA - 1.43 Up
Msa.H.0235120 谷胱甘肽 S-转移酶 Glutathione S-transferase，GST - 1.36 Up
Msa.H.0271410 谷胱甘肽 S-转移酶 Glutathione S-transferase，GST - 1.37 Up
Msa.H.0271450 谷胱甘肽 S-转移酶 Glutathione S-transferase，GST - 1.39 Up
Msa.H.0282830 L-抗坏血酸过氧化物酶 L-ascorbate peroxidase，APX - 0.74 Down

Fig. 6

KEGG enrichment pathway diagram of phenylpropanoid biosynthesis pathway under alkaline salt stress The red fill in the figure represents differentially upregulated proteins, the blue fill represents differentially downregulated proteins, the yellow fill represents nodes that contain both differentially upregulated and downregulated proteins"

Fig. 7

KEGG enrichment pathway diagram of differential glutathione metabolic pathway under neutral salt stress The red fill in the figure represents differentially upregulated proteins, the blue fill represents differentially downregulated proteins, the yellow fill represents nodes that contain both differentially upregulated and downregulated proteins"

Fig. 8

Schematic diagram of the changes of important differential proteins under saline-alkali stress A: Schematic diagram of salt or alkali treatment; B: Schematic diagram of key differential proteins and pathways under salt or alkali stress. Fill the top-left blue box to represent proteins altered under alkali stress, fill the top-right green box for salt-stress responsive proteins, and use silver fill for the two bottom boxes indicating proteins changed under both salt and alkali stresses. Within the boxes, protein names in red indicate up-regulated proteins, while protein names in blue indicate down-regulated proteins"

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