异形根孢囊霉对镉胁迫下番茄生长和基因表达的影响

doi:10.3969/j.issn.1004-1524.20250366

浙江农业学报 ›› 2026, Vol. 38 ›› Issue (1): 54-66.DOI: 10.3969/j.issn.1004-1524.20250366

异形根孢囊霉对镉胁迫下番茄生长和基因表达的影响

刘俊丽¹(), 江建锋², 董祥伟², 杨海峻², 包晓琪¹^,³, 付晨曦¹, 郭彬¹, 童文彬²^,^*()

1.浙江省农业科学院环境资源与土壤肥料研究所,农产品质量安全全国重点实验室,浙江杭州 310021
2.衢州市衢江区农业技术推广中心,浙江衢州 324022
3.浙江工业大学环境学院,浙江杭州 310014

收稿日期:2025-03-14 出版日期:2026-01-25 发布日期:2026-02-11
作者简介:*童文彬,E-mail:zjqztwb@163.com
刘俊丽,研究方向为微生物与植物互作机制及其生态应用。E-mail:liujunli@zaas.ac.cn
通讯作者: 童文彬
基金资助:
国家自然科学基金(42007120);农产品质量安全全国重点实验室财政专项(10417000024CE0601G)

The influence of Rhizophagus irregularis on the growth and gene expression of tomato under cadmium stress

LIU Junli¹(), JIANG Jianfeng², DONG Xiangwei², YANG Haijun², BAO Xiaoqi¹^,³, FU Chenxi¹, GUO Bin¹, TONG Wenbin²^,^*()

1. Institute of Environment, Resource, Soil and Fertilizer, State Key Laboratory for Quality and Safety of Agro-Products, Zhejiang Academy of Agricultural Sciences, Hangzhou 310021, China
2. Qujiang District Agricultural Technology Promotion Center, Quzhou 324022, Zhejiang, China
3. College of Environment, Zhejiang University of Technology, Hangzhou 310014, China

Received:2025-03-14 Online:2026-01-25 Published:2026-02-11
Contact: TONG Wenbin

摘要/Abstract

摘要：

丛枝菌根真菌(arbuscular mycorrhizal fungi, AMF)在调控植物镉(cadmium, Cd)耐性中具有重要作用,但其对番茄生长与Cd积累的分子机制尚不明确。为探究接种AMF提高番茄Cd耐性的机制,采用砂培试验,研究100 μmol·L^-1 Cd胁迫下接种异形根孢囊霉(Rhizophagus irregularis, Ri)对番茄生长、Cd含量、抗氧化酶活性、根组织细胞超微结构与基因表达的影响,并通过GO(Gene Ontology)和KEGG(Kyoto Encyclopedia of Genes and Genomes)分析差异表达基因(differential expressed gene, DEG)的富集特征。结果表明,Cd胁迫抑制番茄生长,显著降低根部过氧化物酶(POD)和超氧化物歧化酶(SOD)的活性,并导致细胞超微结构严重损伤。与未接种Ri相比,Cd胁迫下接种Ri的番茄地上部生物量显著增加27%,根部和地上部Cd含量分别显著降低40%与38%,根部抗坏血酸过氧化物酶(APX)和SOD活性分别显著提高45.27%与46.35%,同时细胞超微结构损伤得到缓解。GO富集分析显示,对照处理与单独Cd处理、单独Cd处理与Cd+Ri共处理2个比较组的差异表达基因在生物学过程(代谢、应激响应等)、细胞组分(膜、细胞器等)和分子功能(催化、转运、抗氧化活性等)3个分支均显著富集,且接种Ri组在各分支中涉及的DEG数量更多。KEGG富集分析表明,对照处理与单独Cd处理的DEG显著富集于110条代谢通路,单独Cd处理与Cd+Ri共处理的DEG显著富集于118条代谢通路,主要包括苯丙氨酸代谢、植物激素信号转导和ABC转运蛋白等关键途径。热图分析显示,含有LysM结构域基因(上调14倍)、PDR基因(上调12.6倍)与多个激酶基因(上调倍数>9)的特异性高表达,是AMF介导重金属解毒的重要分子特征。本研究表明,Ri可能通过协同调控苯丙氨酸代谢、ABC转运蛋白、植物激素信号转导和防御反应等多个关键通路,构建系统的重金属胁迫响应网络,增强番茄对Cd胁迫的生理适应性,从而促进生长并提高抗逆性。研究结果可为利用AMF降低作物Cd累积的技术应用提供理论基础与候选基因资源。

关键词: 番茄, 丛枝菌根真菌, 生长, 镉, 差异表达基因

Abstract:

Arbuscular mycorrhizal fungi (AMF) play a significant role in regulating plant cadmium (Cd) tolerance, but the molecular mechanisms underlying their effects on tomato growth and Cd accumulation remain unclear. To investigate the mechanisms by which AMF inoculation enhances tomato Cd tolerance, a sand culture experiment was conducted to study the effects of inoculating Rhizophagus irregularis (Ri) under 100 μmol·L^-1 Cd stress on tomato growth, Cd content, antioxidant enzyme activities, root cell ultrastructure, and gene expression. The enrichment characteristics of differentially expressed genes (DEGs) were analyzed through GO (Gene Ontology) and KEGG (Kyoto Encyclopedia of Genes and Genomes) analyses. The results showed that Cd stress inhibited tomato growth, significantly reduced root peroxidase (POD) and superoxide dismutase (SOD) activities, and caused severe damage to cell ultrastructure. Compared with non-inoculated Ri treatment, under Cd stress, Ri inoculation significantly increased tomato aboveground biomass by 27%, significantly reduced root and shoot Cd content by 40% and 38%, respectively, significantly enhanced root ascorbate peroxidase (APX) and SOD activities by 45.27% and 46.35%, respectively, and alleviated cell ultrastructure damage. GO enrichment analysis revealed that DEGs from both comparison groups (control vs. Cd treatment alone and Cd treatment alone vs. Cd+Ri co-treatment) were significantly enriched in three branches: biological processes (metabolism, stress response, etc.), cellular components (membrane, organelles, etc.), and molecular functions (catalysis, transport, antioxidant activity, etc.). Cd+Ri co-treatment group involved a greater number of DEGs across all branches. KEGG enrichment analysis indicated that DEGs from the control vs. Cd treatment alone comparison were significantly enriched in 110 metabolic pathways, while DEGs from the Cd treatment alone vs. Cd+Ri co-treatment comparison were significantly enriched in 118 metabolic pathways, primarily including key pathways such as phenylalanine metabolism, plant hormone signal transduction, and ABC transporters. Heatmap analysis showed that the specific high expression of genes containing LysM domains (upregulated 14-fold), PDR genes (upregulated 12.6-fold), and multiple kinase genes (upregulated>9-fold) were important molecular features of AMF-mediated heavy metal detoxification. This study suggests that Ri might enhance tomato physiological adaptation to Cd stress, thereby promoting growth and improving stress resistance, by coordinately regulating multiple key pathways such as phenylalanine metabolism, ABC transporters, plant hormone signal transduction, and defense responses, thereby constructing a systematic heavy metal stress response network. The findings provided a theoretical basis and candidate gene resources for the technical application of AMF in reducing Cd accumulation in crops.

Key words: tomato, arbuscular mycorrhizal fungi, growth, cadmium, differentially expressed gene

中图分类号:

S641.2

刘俊丽, 江建锋, 董祥伟, 杨海峻, 包晓琪, 付晨曦, 郭彬, 童文彬. 异形根孢囊霉对镉胁迫下番茄生长和基因表达的影响[J]. 浙江农业学报, 2026, 38(1): 54-66.

LIU Junli, JIANG Jianfeng, DONG Xiangwei, YANG Haijun, BAO Xiaoqi, FU Chenxi, GUO Bin, TONG Wenbin. The influence of Rhizophagus irregularis on the growth and gene expression of tomato under cadmium stress[J]. Acta Agriculturae Zhejiangensis, 2026, 38(1): 54-66.

图/表 8

图1 Cd胁迫下丛枝菌根真菌与番茄的共生关系 A~C,番茄根部菌丝、泡囊与丛枝等结构的显微观察;红色箭头指示泡囊,黄色箭头指示丛枝,绿色箭头指示根外菌丝,标尺=100 μm。D,番茄根部的总侵染率;数据为平均值±标准误(n=3),无相同小写字母表示处理间差异显著(p<0.05,Duncan检验)。-CdNM,未添加Cd、不接种菌根真菌;-CdAM,未添加Cd、接种菌根真菌;+CdAM,添加Cd、接种菌根真菌。下同。

Fig.1 Symbiotic relationship between arbuscular mycorrhizal fungi and tomato under cadmium stress A-C, Microscopic observation of structures such as hyphae, vesicles and arbuscular branches in tomato roots; red arrows indicate vesicles, yellow arrows indicate arbuscular branches, green arrows indicate extraradical hyphae, scale bar=100 μm. D, Total colonization rate of tomato roots; data were mean±standard error (n=3), data marked without the same lowercase letter indicated significant differences (p<0.05, Duncan’s test).-CdNM, no Cd added, no mycorrhizal fungi inoculated;-CdAM, no Cd added, mycorrhizal fungi inoculated;+CdAM, Cd added, mycorrhizal fungi inoculated. The same as below.

表1 不同处理下番茄单株生物量(干重)

Table 1 Biomass (dry weight) per plant of tomato under different treatments

处理 Teatment	根部生物量/g Root biomass/g	地上部生物量/g Shoot biomass/g	根冠比 Root shoot ratio
-CdNM	0.014±0.001 b	0.221±0.011 b	0.061±0.003 a
-CdAM	0.020±0.001 a	0.304±0.028 a	0.067±0.004 a
+CdNM	0.014±0.002 b	0.164±0.016 c	0.089±0.022 a
+CdAM	0.012±0.001 b	0.208±0.002 b	0.058±0.004 a

表2 不同处理下番茄植株镉含量与转运系数

Table 2 Cd content and transfer coefficient in tomato plants under different treatments

处理 Teatment	根部Cd含量/ (mg·g^-1) Cd content in root/(mg·g^-1)	地上部Cd含量/ (mg·g^-1) Cd content in shoot/(mg·g^-1)	镉转运系数 Transfer coefficient of cadmium
-CdNM	0.004±0 c	0.001±0 c	—
-CdAM	0.003±0.001 c	0.001±0 c	—
+CdNM	3.473±0.530 a	0.118±0.013 a	0.035±0.003 a
+CdAM	2.073±0.236 b	0.073±0.007 b	0.036±0.001 a

图2 不同处理下番茄根系的抗氧化酶活性

Fig.2 Antioxidant enzyme activities in tomato roots under different treatments

图3 不同处理下番茄根组织细胞的超微结构 MT,线粒体;CW,细胞壁;ICS,细胞间隙;Va,液泡。白色箭头指示质壁分离,黄色箭头指示线粒体空泡化。

Fig.3 Ultrastructure of tomato root tissue cells under different treatments MT, Mitochondria; CW, Cell wall; ICS, Intercellular space; Va, Vacuole. White arrows indicate plasmolysis, yellow arrows indicate mitochondrial vacuolization.

图4 不同处理番茄根系中的差异表达基因 A,不同处理番茄根系差异表达基因的韦恩图;G0、G1、G2和G3分别表示+CdAM与-CdAM、-CdAM与-CdNM、+CdNM与-CdNM,以及+CdAM与+CdNM对比组间的差异表达基因。B,G2与G3两个对比组差异表达基因的韦恩图。C和D分别为-CdNM vs+CdNM与+CdNM vs+CdAM对比组的基因表达火山图。FC,差异倍数。

Fig.4 Differentially expressed genes in tomato roots under different treatments A, Venn diagram of differentially expressed genes in tomato roots under different treatments; G0, G1, G2, and G3 represent differentially expressed genes between the comparison groups+CdAM vs-CdAM,-CdAM vs-CdNM,+CdNM vs-CdNM, and+CdAM vs+CdNM, respectively. B, Venn diagram of differentially expressed genes in the two comparison groups G2 and G3. C and D are gene expression volcano plots for the comparison groups-CdNM vs+CdNM and+CdNM vs+CdAM, respectively. FC, Fold change.

图5 差异表达基因的GO与KEGG富集分析 Metabolic process,代谢过程;Single-organism process,单生物过程;Cellular process,细胞过程;Response to stimulus,刺激响应;Biological regulation,生物调节;Localization,定位;Detoxification,解毒;Multi-organism process,多生物过程;Signaling,信号传导;Reproduction,繁殖;Reproductive process,生殖过程;Developmental process,发育过程;Immune system process,免疫系统过程;Rhythmic process,节律过程;Growth,生长;Membrane,膜;Membrane part,膜部分;Cell,细胞;Cell part,细胞部分;Organelle part,细胞器部分;Extracellular region,细胞外区域;Macromolecular complex,大分子复合物;Membrane-enclosed lumen,膜包被腔;Cell junction,细胞连接;Nucleoid,类核;Symplast,共质体;Other organism,其他生物体;Other organism part,其他生物体部分;Supramolecular complex,超分子复合物;Synapse,突触;Synapse part,突触部分;Extracellular region part,细胞外区域部分;Catalytic activity,催化活性;Binding,结合;Transporter activity,转运蛋白活性;Antioxidant activity,抗氧化活性;Molecular transducer activity,分子转导活性;Signal transducer activity,信号转导活性;Molecular function regulator,分子功能调节因子;Structural molecule activity,结构分子活性;Electron carrier activity,电子载体活性;Nutrient reservoir activity,营养储存活性。Phenylpropanoid biosynthesis,苯丙烷类生物合成;Flavonoid biosynthesis,类黄酮生物合成;Isoquinoline alkaloid biosynthesis,异喹啉类生物碱生物合成;Sulfur metabolism,硫代谢;Circadian rhythm-plant,植物昼夜节律;Starch and sucrose metabolism,淀粉和蔗糖代谢;Thiamine metabolism,硫胺素代谢;ABC transporters,ABC转运蛋白;Biosynthesis of unsaturated fatty acids,不饱和脂肪酸生物合成;Mannose type O-glycan biosynthesis,甘露糖型O-聚糖生物合成;Monoterpenoid biosynthesis,单萜类生物合成;Plant-pathogen interaction,植物-病原体互作;Isoflavonoid biosynthesis,异黄酮类生物合成;Flavone and flavonol biosynthesis,黄酮与黄酮醇生物合成;Pentose and glucuronate interconversions,戊糖与葡萄糖醛酸相互转化;Cyanoamino acid metabolism,氰基氨基酸代谢;Cutin, suberine and wax biosynthesis,角质、木栓质与蜡生物合成;Benzoxazinoid biosynthesis,苯并恶嗪类生物合成;Plant hormone signal transduction,植物激素信号转导;Pyruvate metabolism,丙酮酸代谢;Fatty acid biosynthesis,脂肪酸生物合成;Glycolysis/Gluconeogenesis,糖酵解/糖异生;Carbon metabolism,碳代谢; Glycosaminoglycan degradation,糖胺聚糖降解; Fatty acid metabolism,脂肪酸代谢;MAPK signaling pathway-plant,植物MAPK信号通路;Phenylalanine metabolism,苯丙氨酸代谢;Diterpenoid biosynthesis,二萜类生物合成;Biotin metabolism,生物素代谢;Pantothenate and CoA biosynthesis,泛酸与辅酶A生物合成;Arginine and proline metabolism,精氨酸与脯氨酸代谢;Citrate cycle (TCA cycle),柠檬酸循环。 A和B分别为-CdNM vs+CdNM比较组与+CdNM vs+CdAM比较组差异表达基因的GO富集分析。CCO/CCB,细胞组分组成或生物发生;MOP,多细胞生物过程;NABTFA,核酸结合转录因子活性;TFAPB,转录因子活性、蛋白质结合。C和D分别为-CdNM vs+CdNM比较组与+CdNM vs+CdAM比较组差异表达基因的KEGG富集分析。图中展示了q值最小的前20个通路;TPPAB,托烷类、哌啶类和吡啶类生物碱的生物合成;SDGB,二苯乙烯类、二芳基庚烷类和姜酚类物质的生物合成;VLID,缬氨酸、亮氨酸和异亮氨酸的降解。

Fig.5 GO and KEGG enrichment analysis of differentially expressed genes A and B, Gene Ontology (GO) enrichment analysis of differentially expressed genes (DEGs) from the comparison groups -CdNM vs +CdNM and +CdNM vs +CdAM, respectively. CCO/CCB, Cellular component organization or biogenesis; MOP, Multicellular organismal process; NABTFA, Nucleic acid binding transcription factor activity; TFAPB, Transcription factor activity, protein binding. C and D, KEGG pathway enrichment analysis of DEGs from the same comparison groups. The figure shows the top 20 pathways with the smallest q-values. TPPAB, Tropane, piperidine and pyridine alkaloid biosynthesis; SDGB, Stilbenoid, diarylheptanoid and gingerol biosynthesis; VLID, Valine, leucine and isoleucine degradation.

图6 苯丙氨酸代谢途径(A)、ABC转运蛋白家族基因(B)、植物激素信号转导(C)和植物-病原菌互作(D)相关差异表达基因热图 A,苯丙氨酸代谢途径差异表达基因热图。PAL,苯丙氨酸解氨酶基因;HDC,组氨酸脱羧酶基因;AG,酰胺酶基因;PAO,初级胺氧化酶基因;TAT2,氨基酸转移酶基因;Other,其他基因。B,ABC家族基因差异表达基因热图。ABCA、ABCB、ABCC、ABCG分别表示ABC家族A、B、C和G亚家族基因;PDR,多效药物耐性基因,属于ABCG亚家族。C,植物激素信号转导差异表达基因热图。ABA,脱落酸相关基因;AUX,生长素相关基因;Brs,油菜素内酯相关基因;CK,细胞分裂素相关基因;Et,乙烯相关基因;GA,赤霉素相关基因;JA,茉莉酸相关基因;SA,水杨酸相关基因。D,植物-病原菌互作差异表达基因热图。CLP,钙结合蛋白家族基因;NLR,NLR家族基因;RLP,受体类似蛋白基因;PK,蛋白激酶基因;PR,病程相关蛋白基因;WRKY,WRKY转录因子基因;Other,其他基因。数据为log2|FPKM平均值+1|(n=3),标尺表示颜色对应的数值范围。

Fig.6 Heatmap of differentially expressed genes related to phenylalanine metabolism (A), ABC transporter family gene (B), plant hormone signal transduction (C) and plant-pathogen interaction (D) A, Heatmap of differentially expressed genes (DEGs) related to phenylalanine metabolism pathway. PAL, Phenylalanine ammonia-lyase gene; HDC, Histidine decarboxylase gene; AG, Amidase gene; PAO, Primary amine oxidase gene; TAT2, Aminotransferase gene; Other, Other genes. B, Heatmap of DEGs associated with ABC transporter family genes. ABCA/B/C/G represent subfamilies A, B, C and G of ABC transporter family genes, respectively; PDR, Pleiotropic drug resistance gene (belonging to ABCG subfamily). C, Heatmap of DEGs involved in plant hormone signal transduction. ABA, Abscisic acid gene; AUX, Auxin gene; Brs, Brassinosteroids gene; CK, Cytokinins gene; Et, Ethylene gene; GA, Gibberellins gene; JA, Jasmonic acid gene; SA, Salicylic acid gene. D, Heatmap of DEGs related to plant-pathogen interaction. CLP, Calmodulin-like protein gene; NLR, NLR family gene; RLP, Receptor-like protein gene; PK, Protein kinase gene; PR, Pathogenesis-related protein gene; WRKY, WRKY transcription factor gene; Other, Other genes. Data are presented as log2|FPKM mean+1| (n=3), the scale bar is the numerical range corresponding to the color in the heatmap.

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异形根孢囊霉对镉胁迫下番茄生长和基因表达的影响

The influence of Rhizophagus irregularis on the growth and gene expression of tomato under cadmium stress

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