盐碱胁迫下的紫花苜蓿幼苗蛋白组差异分析

doi:10.3864/j.issn.0578-1752.2025.21.019

摘要/Abstract

摘要：

【目的】土壤盐碱化是紫花苜蓿（Medicago sativa L.）生长和产量的重要限制因素。为解析紫花苜蓿幼苗响应盐碱胁迫的分子机理，通过蛋白质组学分析，揭示盐碱胁迫下关键差异蛋白及其参与的代谢通路，为其耐盐碱机制研究提供理论依据。【方法】以中苜4号紫花苜蓿为材料，对其种子分别进行盐（30 mmol·L^-1NaCl和30 mmol·L^-1 Na₂SO₄）和碱（10 mmol·L^-1 Na₂CO₃和10 mmol·L^-1 NaHCO₃）处理，利用TMT标记结合液相色谱-质谱联用技术，对胁迫后的幼苗进行了蛋白组差异分析。【结果】蛋白组共鉴定到6 829个蛋白，其中碱、盐胁迫下分别有489个（274个上调，215个下调）和376个差异蛋白（218个上调，158个下调）。GO注释分析发现，差异蛋白主要注释于细胞代谢、有机物代谢、胁迫响应等生物过程，以及细胞内细胞器、细胞质和膜等细胞组分。KEGG通路富集分析发现，碱胁迫下差异蛋白显著富集于光合作用、苯丙烷生物合成和异黄酮生物合成等通路，盐胁迫下差异蛋白主要富集于光合作用、异黄酮生物合成及谷胱甘肽代谢等通路。对富集到的蛋白进一步分析发现，紫花苜蓿幼苗通过上调异黄酮生物合成途径关键酶（HI4OMT和CYP81E），增强抗氧化能力和渗透调节能力，从而抵御盐碱胁迫。HI4OMT和CYP81E等关键酶的上调显著促进了异黄酮类化合物的积累，帮助植物清除活性氧并维持细胞稳态。此外，苯丙烷生物合成途径关键酶（PAL、CAD和COMT）在碱胁迫下显著上调，促进了木质素和类黄酮的合成，增强了细胞壁强度和抗氧化能力，帮助植物适应高pH环境，以应对碱胁迫。在盐胁迫下，紫花苜蓿幼苗通过上调谷胱甘肽代谢途径关键酶（PRDX6、GPX和GST），维持氧化还原稳态并清除活性氧，增强对盐胁迫的耐受性。【结论】通过蛋白组学分析，揭示了紫花苜蓿幼苗响应盐碱胁迫的关键蛋白及代谢通路，为解析紫花苜蓿耐盐碱分子机制提供了重要的理论依据，同时也为紫花苜蓿的耐盐碱育种提供了潜在的候选蛋白和代谢通路。后续可进一步验证这些关键蛋白的功能，并通过一系列生物育种的技术手段，培育具有更高耐盐碱性的紫花苜蓿新品种，以应对土壤盐碱化对苜蓿生产带来的挑战。

关键词: 紫花苜蓿, 盐碱胁迫, 蛋白质组, 苯丙烷生物合成途径, 谷胱甘肽代谢途径

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

杨永念, 曾祥翠, 刘青松, 李如月, 龙瑞才, 陈林, 王雪, 何飞, 康俊梅, 李明娜. 盐碱胁迫下的紫花苜蓿幼苗蛋白组差异分析[J]. 中国农业科学, 2025, 58(21): 4512-4527.

YANG YongNian, ZENG XiangCui, LIU QingSong, LI RuYue, LONG RuiCai, CHEN Lin, WANG Xue, HE Fei, KANG JunMei, LI MingNa. Differential Proteomic Analysis of Alfalfa Seedlings Under Salt- Alkaline Stress[J]. Scientia Agricultura Sinica, 2025, 58(21): 4512-4527.

0
/ / 推荐

导出引用管理器 EndNote|Reference Manager|ProCite|BibTeX|RefWorks

链接本文: https://www.chinaagrisci.com/CN/10.3864/j.issn.0578-1752.2025.21.019

https://www.chinaagrisci.com/CN/Y2025/V58/I21/4512

图/表 9

图1

图2

图3

图4

图5

表1

盐碱胁迫下重要候选蛋白信息与差异变化"

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

表1

图6

图7

图8

参考文献 45

[1]	FANG S M, HOU X, LIANG X L. Response mechanisms of plants under saline-alkali stress. Frontiers in Plant Science, 2021, 12: 667458.
[2]	FAO (Food and Agriculture Organization of the United Nations), ITPS (Intergovernmental Technical Panel on Soils). Global map of salt-affected soils. 2021.
[3]	杨劲松, 姚荣江, 王相平, 谢文萍, 张新, 朱伟, 张璐, 孙瑞娟. 中国盐渍土研究: 历程、现状与展望. 土壤学报, 2022, 59(1): 10-27.
	YANG J S, YAO R J, WANG X P, XIE W P, ZHANG X, ZHU W, ZHANG L, SUN R J. Research on salt-affected soils in China: History, status quo and prospect. Acta Pedologica Sinica, 2022, 59(1): 10-27. (in Chinese)
[4]	SU K Q, MU L, ZHOU T, KAMRAN M, YANG H M. Intercropped alfalfa and spring wheat reduces soil alkali-salinity in the arid area of northwestern China. Plant and Soil, 2024, 499(1): 275-292.
[5]	MUNNS R, TESTER M. Mechanisms of salinity tolerance. Annual Review of Plant Biology, 2008, 59: 651-681. doi: 10.1146/annurev.arplant.59.032607.092911 pmid: 18444910
[6]	ZHU J K. Plant salt tolerance. Trends in Plant Science, 2001, 6(2): 66-71. doi: 10.1016/s1360-1385(00)01838-0 pmid: 11173290
[7]	王瀚祥, 李广存, 徐建飞, 王万兴, 金黎平. 植物耐盐机理研究进展. 作物杂志, 2022(5): 1-12.
	WANG H X, LI G C, XU J F, WANG W X, JIN L P. Advances in research on salt tolerance mechanism of plants. Crops, 2022(5): 1-12. (in Chinese)
[8]	ZHANG H, LIU X L, ZHANG R X, YUAN H Y, WANG M M, YANG H Y, MA H Y, LIU D, JIANG C J, LIANG Z W. Root damage under alkaline stress is associated with reactive oxygen species accumulation in rice (Oryza sativa L.). Frontiers in Plant Science, 2017, 8: 1580.
[9]	GUO K W, XU Z S, HUO Y Z, SUN Q, WANG Y, CHE Y H, WANG J C, LI W, ZHANG H H. Effects of salt concentration, pH, and their interaction on plant growth, nutrient uptake, and photochemistry of alfalfa (Medicago sativa) leaves. Plant Signaling & Behavior, 2020, 15(12): 1832373.
[10]	李小冬, 舒健虹, 于二汝, 吴佳海, 蔡一鸣, 王小利. 高羊茅在低氮胁迫下的蛋白组学分析. 草业学报, 2016, 25(3): 67-76. doi: 10.11686/cyxb2015470
	LI X D, SHU J H, YU E R, WU J H, CAI Y M, WANG X L. Proteomic analysis of nitrogen stress-responsive proteins in the leaves of tall fescue. Acta Prataculturae Sinica, 2016, 25(3): 67-76. (in Chinese)
[11]	WANG Y, YANG P, ZHOU Y, HU T, ZHANG P, WU Y. A proteomic approach to understand the impact of nodulation on salinity stress response in alfalfa (Medicago sativa L.). Plant Biology, 2022, 24(2): 323-332.
[12]	裴翠明, 张振亚, 马进. 南方型紫花苜蓿苗期叶片盐胁迫差异蛋白分析. 农业生物技术学报, 2016, 24(11): 1629-1642.
	PEI C M, ZHANG Z Y, MA J. Differentially expressed proteins analysis of seedling leaf of southern type alfalfa (Medicago sativa 'Millenium') under salt stress. Journal of Agricultural Biotechnology, 2016, 24(11): 1629-1642. (in Chinese)
[13]	马进, 郑钢, 裴翠明, 张振亚. 基于iTRAQ质谱分析技术筛选南方型紫花苜蓿根部响应盐胁迫差异表达蛋白. 农业生物技术学报, 2016, 24(4): 497-509.
	MA J, ZHENG G, PEI C M, ZHANG Z Y. Screening differentially expressed proteins in southern type alfalfa (Medicago sativa 'Millenium') root upon salt stress by iTRAQ protein mass spectrometry. Journal of Agricultural Biotechnology, 2016, 24(4): 497-509. (in Chinese)
[14]	LONG R C, SUN H, CAO C Y, ZHANG T J, KANG J M, WANG Z, LI M N, GAO Y L, LI X, YANG Q C. Identification of alkali- responsive proteins from early seedling stage of two contrasting Medicago species by iTRAQ-based quantitative proteomic analysis. Environmental and Experimental Botany, 2019, 157: 26-34.
[15]	李波, 方志坚, 邬婷婷, 李红, 杨曌, 赵宇佳. 盐碱胁迫下紫花苜蓿叶片蛋白组的初步分析. 草地学报, 2019, 27(3): 574-580. doi: 10.11733/j.issn.1007-0435.2019.03.008
	LI B, FANG Z J, WU T T, LI H, YANG Z, ZHAO Y J. Preliminary analysis of alfalfa leaf proteome under salt-alkali stress. Acta Agrestia Sinica, 2019, 27(3): 574-580. (in Chinese) doi: 10.11733/j.issn.1007-0435.2019.03.008
[16]	LING L, AN Y M, WANG D, TANG L, DU B H, SHU Y J, BAI Y, GUO C H. Proteomic analysis reveals responsive mechanisms for saline-alkali stress in alfalfa. Plant Physiology and Biochemistry, 2022, 170: 146-159.
[17]	CARDONA T, SHAO S X, NIXON P J. Enhancing photosynthesis in plants: the light reactions. Essays in Biochemistry, 2018, 62(1): 85-94. doi: 10.1042/EBC20170015 pmid: 29563222
[18]	CHAVES M M, FLEXAS J, PINHEIRO C. Photosynthesis under drought and salt stress: regulation mechanisms from whole plant to cell. Annals of Botany, 2009, 103(4): 551-560. doi: 10.1093/aob/mcn125 pmid: 18662937
[19]	KHAING E P, ZHONG V, EATON-RYE J J. An updated system for the targeted mutagenesis of the psbDI: psbC operon in Synechocystis sp. PCC 6803: Mutations targeting Asp460 in CP43 of Photosystem II reduce oxygen-evolving activity and perturb electron transfer in the quinone-Fe-acceptor complex. New Zealand Journal of Botany, 2020, 58(4): 389-405.
[20]	LUO W, DENG X X, HUO J, RUAN T, GONG Z W, YAN J B, YANG Z H, QUAN C, CUI Z F. Strengthening NADPH regeneration for improving photo-biocatalytic ketones asymmetric reduction reaction by Synechocystis through overexpression of FNR. Catalysis Letters, 2018, 148(6): 1714-1722.
[21]	ZHAO L L, ZHAO X, HUANG L, LIU X Y, WANG P C. Transcriptome analysis of Pennisetum americanum × Pennisetum purpureum and Pennisetum americanum leaves in response to high-phosphorus stress. BMC Plant Biology, 2024, 24(1): 635.
[22]	OKOOBOH G O, HAFERKAMP I, RÜHLE T, LEISTER D, NEUHAUS H E. Expression of the plastocyanin gene PETE2 in Camelina sativa improves seed yield and salt tolerance. Journal of Plant Physiology, 2023, 290: 154103.
[23]	VALENTINE R C. Bacterial ferredoxin. Bacteriological Reviews, 1964, 28(4): 497-517.
[24]	WANG Y, WANG J C, GUO D D, ZHANG H B, CHE Y H, LI Y Y, TIAN B, WANG Z H, SUN G Y, ZHANG H H. Physiological and comparative transcriptome analysis of leaf response and physiological adaption to saline alkali stress across pH values in alfalfa (Medicago sativa). Plant Physiology and Biochemistry, 2021, 167: 140-152. doi: 10.1016/j.plaphy.2021.07.040 pmid: 34352517
[25]	DASTMALCHI M, DHAUBHADEL S. Proteomic insights into synthesis of isoflavonoids in soybean seeds. PROTEOMICS, 2015, 15(10): 1646-1657.
[26]	GARCÍA-CALDERÓN M, PÉREZ-DELGADO C M, PALOVE- BALANG P, BETTI M, MÁRQUEZ A J. Flavonoids and isoflavonoids biosynthesis in the model legume Lotus japonicus; connections to nitrogen metabolism and photorespiration. Plants, 2020, 9(6): 774.
[27]	LIU J Y, AHMAD N, HONG Y Q, ZHU M H, ZAMAN S, WANG N, YAO N, LIU X M. Molecular characterization of an isoflavone 2’-hydroxylase gene revealed positive insights into flavonoid accumulation and abiotic stress tolerance in safflower. Molecules, 2022, 27(22): 8001.
[28]	GAO Y L, LONG R C, KANG J M, WANG Z, ZHANG T J, SUN H, LI X, YANG Q C. Comparative proteomic analysis reveals that antioxidant system and soluble sugar metabolism contribute to salt tolerance in alfalfa (Medicago sativa L.) leaves. Journal of Proteome Research, 2019, 18(1): 191-203.
[29]	ZANG Y, JIANG T, CONG Y, ZHENG Z J, OUYANG J. Molecular characterization of a recombinant Zea mays Phenylalanine Ammonia- Lyase (ZmPAL2) and its application in trans-Cinnamic acid production from l-Phenylalanine. Applied Biochemistry and Biotechnology, 2015, 176(3): 924-937.
[30]	DIXON R A, PAIVA N L. Stress-induced phenylpropanoid metabolism. The Plant Cell, 1995, 7(7): 1085-1097. doi: 10.1105/tpc.7.7.1085 pmid: 12242399
[31]	REN W, WANG Y Z, XU A K, ZHAO Y G. Genome-wide identification and characterization of the Phenylalanine Ammonia- lyase (PAL) gene family in Medicago truncatula. Legume Research - an International Journal, 2019, 42(4): 461-466.
[32]	曾祥翠, 杨永念, 李如月, 蒋学乾, 蒋旭, 徐嫣然, 刘忠宽, 龙瑞才, 康俊梅, 杨青川, 李明娜. 紫花苜蓿MsCEP基因家族的鉴定及其调控根系生长发育功能的分析. 中国农业科学, 2024, 57(24): 4839-4853. doi: 10.3864/j.issn.0578-1752.2024.24.002.
	ZENG X C, YANG Y N, LI R Y, JIANG X Q, JIANG X, XU Y R, LIU Z K, LONG R C, KANG J M, YANG Q C, LI M N. Identification of alfalfa(Medicago sativa) MsCEP genes and functional analysis of its regulation in root growth and development. Scientia Agricultura Sinica, 2024, 57(24): 4839-4853. doi: 10.3864/j.issn.0578-1752.2024.24.002. (in Chinese)
[33]	FAN L J, SHI G F, YANG J, LIU G L, NIU Z Q, YE W B, WU S Q, WANG L, GUAN Q J. A protective role of phenylalanine ammonia-lyase from Astragalus membranaceus against saline-alkali stress. International Journal of Molecular Sciences, 2022, 23(24): 15686.
[34]	ZHAI L, XUE Y F, SONG Y H, XIAN M J, YIN L, ZHONG N Q, XIA G X, MA Y H. Overexpression of AaPal, a peptidoglycan- associated lipoprotein from Alkalomonas amylolytica, improves salt and alkaline tolerance of Escherichia coli and Arabidopsis thaliana. Biotechnology Letters, 2014, 36(3): 601-607.
[35]	CHENG H, LI L L, XU F, CHENG S Y, CAO F L, WANG Y, YUAN H H, JIANG D Z, WU C H. Expression patterns of a cinnamyl alcohol dehydrogenase gene involved in lignin biosynthesis and environmental stress in Ginkgo biloba. Molecular Biology Reports, 2013, 40(1): 707-721.
[36]	VANHOLME R, DE MEESTER B, RALPH J, BOERJAN W. Lignin biosynthesis and its integration into metabolism. Current Opinion in Biotechnology, 2019, 56: 230-239. doi: S0958-1669(18)30143-5 pmid: 30913460
[37]	MAHMOOD Z, YAMEEN M, JAHANGEER M, RIAZ M, GHAFFAR A, JAVID I. Lignin as natural antioxidant capacity. Lignin-Trends and Applications. InTechOpen, 2018.
[38]	蒋旭, 崔会婷, 王珍, 张铁军, 龙瑞才, 杨青川, 康俊梅. 紫花苜蓿MsNST的克隆及对木质素与纤维素合成的功能分析. 中国农业科学, 2020, 53(18): 3818-3832. doi: 10.3864/j.issn.0578-1752.2020.18.016.
	JIANG X, CUI H T, WANG Z, ZHANG T J, LONG R C, YANG Q C, KANG J M. Cloning and function analysis of MsNST in lignin and cellulose biosynthesis pathway from alfalfa. Scientia Agricultura Sinica, 2020, 53(18): 3818-3832. doi: 10.3864/j.issn.0578-1752.2020.18.016. (in Chinese)
[39]	王静, 周祁, 李丽华, 郝风声, 魏远方, 杨立均, 刘卫群. 烟草的TMV侵染耐受性与谷胱甘肽代谢途径的关系. 河南农业科学, 2017, 46(2): 49-54.
	WANG J, ZHOU Q, LI L H, HAO F S, WEI Y F, YANG L J, LIU W Q. Relationship of tolerance to TMV and glutathione metabolic pathway in tobacco. Journal of Henan Agricultural Sciences, 2017, 46(2): 49-54. (in Chinese)
[40]	PAIVA A L S, PASSAIA G, LOBO A K M, JARDIM-MESSEDER D, SILVEIRA J A G, MARGIS-PINHEIRO M. Mitochondrial glutathione peroxidase (OsGPX3) has a crucial role in rice protection against salt stress. Environmental and Experimental Botany, 2019, 158: 12-21.
[41]	FISHER A B. Peroxiredoxin 6 in the repair of peroxidized cell membranes and cell signaling. Archives of Biochemistry and Biophysics, 2017, 617: 68-83. doi: S0003-9861(16)30541-0 pmid: 27932289
[42]	LI H T, BENIPAL B, ZHOU S P, DODIA C, CHATTERJEE S, TAO J Q, SOROKINA E M, RAABE T, FEINSTEIN S I, FISHER A B. Critical role of peroxiredoxin 6 in the repair of peroxidized cell membranes following oxidative stress. Free Radical Biology and Medicine, 2015, 87: 356-365. doi: 10.1016/j.freeradbiomed.2015.06.009 pmid: 26117327
[43]	DIETZ K J. Peroxiredoxins in plants and cyanobacteria. Antioxidants & Redox Signaling, 2011, 15(4): 1129-1159.
[44]	FROVA C. Glutathione transferases in the genomics era: New insights and perspectives. Biomolecular Engineering, 2006, 23(4): 149-169. pmid: 16839810
[45]	张慧慧, 康晗晔, 刘惠, 张金锐, 霍帆, 郭玮琦, 叶小芳, 季荣, 扈鸿霞. 基于TMT蛋白质组学技术分析蝗虫微孢子虫感染飞蝗后的差异蛋白. 中国农业科学, 2024, 57(24): 4884-4893. doi: 10.3864/j.issn.0578-1752.2024.24.005
	ZHANG H H, KANG H Y, LIU H, ZHANG J R, HUO F, GUO W Q, YE X F, JI R, HU H X. Differentially expressed proteins analysis of Locusta migratoria infected by Paranosema locustae based on TMT proteomics technique. Scientia Agricultura Sinica, 2024, 57(24): 4884-4893. (in Chinese)