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Acta Agronomica Sinica ›› 2025, Vol. 51 ›› Issue (5): 1230-1247.doi: 10.3724/SP.J.1006.2025.41072

• CROP GENETICS & BREEDING·GERMPLASM RESOURCES·MOLECULAR GENETICS • Previous Articles     Next Articles

Differences in transcriptomic responses to cadmium stress in high/low-Cd- accumulation wheat

WANG Qing(), WANG Yi-Xiu, LI Yue-Nan, LYU Yong-Hui, ZHANG Hai-Bo, LIU Na*(), CHENG Hong-Yan*()   

  1. College of Resource and Environment, Shanxi Agricultural University, Taigu 030801, Shanxi, China
  • Received:2024-10-27 Accepted:2025-01-23 Online:2025-05-12 Published:2025-02-11
  • Contact: *E-mail: liuna@sxau.edu.cn; E-mail: ndchenghy@163.com
  • Supported by:
    National Natural Science Foundation of China(42107044);Distinguished and Excellent Young Scholar Cultivation Project of Shanxi Agricultural University(2022YQPYGC07);Shanxi Province Excellent Doctor Award Fund(SXBYKY2021038);Shanxi Province Major Science and Technology Special Plan “Rank-Listed Project” titled “Research and Application Demonstration of Key Technologies in the Super Quality Edible Mushroom Industry”(202301140601015);Shanxi Agricultural University “Special” and “Excellent” Agricultural High Quality Development Science and Technology Support Project(TYGC24-03)

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Abstract:

Cadmium (Cd) is readily absorbed by wheat, posing a significant threat to human health. However, the molecular mechanisms underlying wheat’s response to Cd stress remain poorly understood. Investigating these mechanisms is essential for developing low-Cd-accumulating wheat varieties through genetic improvement. In this study, hydroponic culture combined with transcriptome sequencing was used to analyze gene regulatory network changes in two wheat varieties with differing Cd accumulation capacities (Jimai 22 and Zhoumai 32) under Cd stress at concentrations of 0, 0.05 mmol L-1, and 0.10 mmol L-1. Functional enrichment analyses using the Kyoto Encyclopedia of Genes and Genomes (KEGG), Gene Ontology (GO), and Protein-Protein Interaction (PPI) networks revealed that Cd stress induced the expression of defense-related genes. The endoplasmic reticulum protein processing pathway was the most significantly enriched upregulated pathway in Jimai 22 under 0.05 mmol L-1 Cd stress, while the benzoxazinoid biosynthesis pathway was highly enriched in Jimai 22 under 0.10 mmol L-1 Cd stress. Additionally, the ribosomal protein uL13 family was identified as a central hub in the PPI network under Cd stress, highlighting its importance in maintaining ribosomal function. Key transporters, including TaNRAMP1, TaNRAMP2, TaNRAMP5, TaZIP6, and TaABCG36, were found to play pivotal roles in Cd uptake and accumulation. Moreover, transcription factors such as WRKY, MYB, bHLH, and bZIP were upregulated under Cd stress, contributing to the alleviation of Cd-induced damage. Weighted gene co-expression network analysis (WGCNA) identified LOC123168319 and LOC123145825 as potential candidate genes associated with Cd accumulation. The differentially expressed genes and metabolic pathways identified in this study provide valuable resources for genetic improvement of wheat. Technologies such as CRISPR/Cas9 can be employed to reduce Cd absorption and accumulation, offering insights into wheat’s Cd resistance mechanisms and supporting the breeding of low-Cd wheat varieties.

Key words: Cd stress, wheat, differentially expressed gene, protein-protein interaction, weighted gene co-expression network

Table S1

Effects of Cd stress on root and plant length, and biomass of different wheat varieties"

品种
Variety		 Cd浓度
Cd concentration
(mmol L-1)		 株高
Plant height
(cm)		 根长
Root length
(cm)		 地上部干重
Dry weight of the
aboveground parts (g)		 根干重
Dry weight of the roots
(g)
济麦22 Jimai 22 0 22.4 Aa 27.3 Aa 2.42 Aa 1.01 Aa
泰山24 Taishan 24 0 21.0 Aab 26.8 Aa 2.11 Aab 0.92 Aa
周麦27 Zhoumai 27 0 19.2 Ab 26.6 Aa 1.90 Ab 0.89 Aa
周麦32 Zhoumai 32 0 20.7 Aab 26.2 Aa 1.95 Ab 0.91 Aa
济麦22 Jimai 22 0.05 17.2 Ba 25.5 Aa 1.18 Ba 0.43 Ba
泰山24 Taishan 24 0.05 16.2 Ba 22.8 Bab 1.15 Bab 0.43 Bab
周麦27 Zhoumai 27 0.05 12.4 Bb 23.5 Bab 1.06 Bbc 0.41 Bab
周麦 32 Zhoumai 32 0.05 13.9 Bb 22.2 Bb 0.95 Bc 0.40 Bb
济麦22 Jimai 22 0.10 13.0 Ba 21.2 Ba 0.83 Ca 0.36 Ba
泰山24 Taishan 24 0.10 11.6 Cab 20.3 Bab 0.78 Ca 0.35 Cab
周麦27 Zhoumai 27 0.10 9.9 Cc 18.3 Cab 0.66 Cb 0.31 Cc
周麦32 Zhoumai 32 0.10 10.5 Cbc 16.9 Bb 0.63 Cb 0.32 Cbc

Fig. S1

Antioxidant enzyme activities of different wheat cultivars under different Cd stress A-D represent malondialdehyde (MDA), superoxide dismutase (SOD), catalase (CAT), and peroxidase (POD) activities, respectively. Different lowercase letters indicate significant differences (Tukey’s test; P < 0.05)."

Fig. S2

Sulfhydryl substance contents of different wheat cultivars under different Cd stress A-C represent contents of glutathione (GSH), non-protein thiol (NPT), and phytochelatins (PCs), respectively. Different lowercase letters indicate significant differences (Tukey’s test; P < 0.05)."

Fig. 1

Cd contents in the aboveground (A) and roots (B) of different wheat cultivars under different Cd stress Different lowercase letters indicate significant differences among different varieties at the same concentration (Tukey’s test; P < 0.05)."

Fig. 2

Principal component analysis (PCA) and differentially expressed genes (DEG) of Jimai 22 and Zhoumai 32 under different Cd stress A: principal component analysis of DEG in Jimai 22 and Zhoumai 32 samples under Cd stress. Cd-22 and Cd-32 represent the wheat varieties Jimai 22 and Zhoumai 32, respectively. The numbers 0, 0.05, and 0.10 indicate Cd stress levels of 0, 0.05, and 0.10 mmol L-1, respectively. B-D: volcano plots of DEG under CK, 0.05, and 0.10 mmol L-1 Cd stress, respectively (Zhoumai 32 is the control). X-axis represents the fold change of the comparison group, and Y-axis represents the significance of the differential expression, which indicates the P-value. FC indicates fold change; blue circles indicate insignificant differences; green and red circles indicate down and up regulated genes, respectively."

Fig. 3

GO and KEGG enrichment analyses of DEG in the aboveground parts of Jimai 22 and Zhoumai 32 under different Cd stress GO and KEGG enrichment analyses of DEG in the CK group (A and B), under 0.05 mmol L-1 Cd stress (C and D), and under 0.10 mmol L-1 Cd stress (E and F). The vertical axis in the figure represents the pathway entry, and the horizontal axis represents the ratio of the DEG annotated in the entry to the number of all DEG annotated to the entry. The size of the circle represents the number of DEG enriched in the pathway. The larger the circle, the greater the number. The color of the circle represents the P-value of the hypergeometric test. The closer the P-value is to 0 (indicated by red), the more significant the enrichment is."

Fig. 4

Heatmap of DEG related to Cd transporters under different Cd stress"

Fig. 5

Protein-protein interaction (PPI) analysis of network under different Cd stress In the differential protein interaction network diagram, circles represent differential proteins. The shade of the circle indicates the level of connectivity, the darker the color, the higher the connectivity."

Fig. 6

Family statistics of transcription factors (TF) under different Cd stress"

Table 1

Statistics of significant metabolic pathway genes"

通路名称
Pathway name		 基因名称
Gene name		 描述
Description		 差异表达倍数
Fold change
内质网蛋白质加工
Protein processing in the endoplasmic reticulum		 LOC123076941 16.9 kD class I heat shock protein 1-like 255.3
LOC123146971 — 144.6
LOC123065008 17.5 kD class II heat shock protein-like 115.1
LOC123145125 — 93.4
LOC123047559 — 70.1
LOC123045683 Uncharacterized LOC123045683, transcript variant X11 20.7
LOC123092591 Heat shock cognate 70 kD protein 2-like 13.9
LOC123088499 — 11.9
LOC123144151 — 8.0
LOC732706 Small heat shock protein, chloroplastic-like 7.9
苯并噁嗪生物合成
Benzoxazine
biosynthesis		 LOC123117220 — 248.9
LOC123101970 Indolin-2-one monooxygenase-like 43.6
LOC123119086 Indolin-2-one monooxygenase-like 36.4
LOC123043330 DIBOA-glucoside dioxygenase BX6-like 34.7
LOC123110087 Indolin-2-one monooxygenase-like 11.5
LOC123046742 — 9.0
LOC123150283 — 7.4
LOC123147887 — 6.2
LOC123064487 Indole-3-glycerol phosphate lyase, chloroplastic-like 2.8
LOC100682422 DIMBOA UDP-glucosyltransferase BX8 2.6
0.05 mmol L-1 Cd胁迫蛋白-蛋白相互作用
Protein-protein
interaction under
0.05 mmol L-1
Cd stress		 LOC123143519 — 2008.9
LOC123083701 — 1397.5
LOC123154376 V-type proton ATPase subunit C-like, transcript variant X3 1067.2
LOC123047031 Ubiquitin-40S ribosomal protein S27a-2-like 820.5
LOC123159281 — 316.9
LOC123137258 — 264.9
LOC123064314 60S ribosomal protein L9 113.4
LOC123068951 — 80.7
LOC123142574 Uncharacterized 53.5
LOC123039371 — 19.1
0.10 mmol L-1 Cd胁迫蛋白-蛋白相互作用
Protein-protein
interaction under
0.10 mmol L-1
Cd stress		 LOC123142574 — 1223.2
LOC123083701 — 767.6
LOC123091968 — 498.7
LOC123047031 Ubiquitin-40S ribosomal protein S27a-2-like 452.4
LOC123091201 26S proteasome non-ATPase regulatory subunit 13 homolog B-like 354.7
LOC123177030 — 277.2
LOC123129514 Glyoxysomal fatty acid beta-oxidation multifunctional protein MFP-a-like 222.8
LOC123137258 — 186.9
LOC123064314 60S ribosomal protein L9 92.4
LOC123159281 — 63.8

Fig. 7

Correlation heat map between module and phenotype under Cd stress ME: module eigengene; A-Cd: aboveground Cd content; R-Cd: root Cd content; MDA: malondialdehyde; POD : peroxidase; CAT: catalase; SOD: superoxide dismutase; GSH: glutathione; NPT: non-protein thiol; PCs: phytochelatins; ** indicates a highly significant difference (P < 0.01)."

Fig. 8

KEGG enrichment and visualization analyses of Cd-related modules under Cd stress A and B represent the KEGG enrichment analysis of the brown and tan modules under Cd stress, respectively; C and D show the KEGG enrichment analysis and visualization of the lightcyan module; E and F display the KEGG enrichment analysis and visualization of the darkred module; G and H present the KEGG enrichment and visualization results for the blue module. M: metabolism; GIP: genetic information processing; EIP: environmental information processing; OS: organismal systems; CP: cellular processes."

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