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

doi:10.3969/j.issn.1004-1524.20250366

Acta Agriculturae Zhejiangensis ›› 2026, Vol. 38 ›› Issue (1): 54-66.DOI: 10.3969/j.issn.1004-1524.20250366

• Horticultural Science • Previous Articles Next Articles

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

Abstract

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

CLC Number:

S641.2

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.

Figures/Tables 8

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.

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

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

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

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.

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.

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.

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

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