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Comparative Study
. 2021 Oct 8;21(1):459.
doi: 10.1186/s12870-021-03225-w.

Comparative physiological and transcriptomic analyses reveal ascorbate and glutathione coregulation of cadmium toxicity resistance in wheat genotypes

Tao Zhang #  1 , Jingui Xiao #  1 , Yongsheng Zhao #  1 , Yifan Zhang #  1 , Yaqi Jie #  1 , Dandan Shen  2 , Caipeng Yue  2 , Jinyong Huang  2 , Yingpeng Hua  3 , Ting Zhou  4
Affiliations
Free PMC article
Comparative Study

Comparative physiological and transcriptomic analyses reveal ascorbate and glutathione coregulation of cadmium toxicity resistance in wheat genotypes

Tao Zhang et al. BMC Plant Biol. .
Free PMC article

Abstract

Background: Cadmium (Cd) is a heavy metal with high toxicity that severely inhibits wheat growth and development. Cd easily accumulates in wheat kernels and enters the human food chain. Genetic variation in the resistance to Cd toxicity found in wheat genotypes emphasizes the complex response architecture. Understanding the Cd resistance mechanisms is crucial for combating Cd phytotoxicity and meeting the increasing daily food demand.

Results: Using two wheat genotypes (Cd resistant and sensitive genotypes T207 and S276, respectively) with differing root growth responses to Cd, we conducted comparative physiological and transcriptomic analyses and exogenous application tests to evaluate Cd detoxification mechanisms. S276 accumulated more H2O2, O2-, and MDA than T207 under Cd toxicity. Catalase activity and levels of ascorbic acid (AsA) and glutathione (GSH) were greater, whereas superoxide dismutase (SOD) and peroxidase (POD) activities were lower in T207 than in S276. Transcriptomic analysis showed that the expression of RBOHA, RBOHC, and RBOHE was significantly increased under Cd toxicity, and two-thirds (22 genes) of the differentially expressed RBOH genes had higher expression levels in S276 than inT207. Cd toxicity reshaped the transcriptional profiling of the genes involving the AsA-GSH cycle, and a larger proportion (74.25%) of the corresponding differentially expressed genes showed higher expression in T207 than S276. The combined exogenous application of AsA and GSH alleviated Cd toxicity by scavenging excess ROS and coordinately promoting root length and branching, especially in S276.

Conclusions: The results indicated that the ROS homeostasis plays a key role in differential Cd resistance in wheat genotypes, and the AsA-GSH cycle fundamentally and vigorously influences wheat defense against Cd toxicity, providing insight into the physiological and transcriptional mechanisms underlying Cd detoxification.

Keywords: AsA-GSH cycle; Cd resistance; Genotypic diversity; ROS; Wheat.

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Conflict of interest statement

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

Figures

Fig. 1
Fig. 1
Characterization of wheat growing under different Cd concentrations. A-B, Images of wheat shoots (A) and roots (B) growing under different Cd concentrations for 12 d. From left to right, represent the phenotypes of plants grow in 0 μM (control), 5 μM, 10 μM, 20 μM, 50 μM, and 100 μM Cd2+. C Shoot height of wheat growing under different Cd concentrations. D Shoot biomass of wheat growing under different Cd concentrations. E, Maximum root length of wheat growing under different Cd concentrations. F, Root biomass of wheat growing under different Cd concentrations. G, Leaf number of wheat growing under different Cd concentrations. Results are means ± SE of six biological replicates
Fig. 2
Fig. 2
Characterization of wheat genotypes T207 and S276 growing under normal or Cd treatment. A Images of T207 and S276 growing under normal or Cd treatment for 12 d. B Shoot biomass of genotypes T207 and S276. C Shoot height of genotypes T207 and S276. D Root biomass of genotypes T207 and S276. E Maximum root length of genotypes T207 and S276. Results are means ± SE of six biological replicates. The black column represents T207 and the white column represents S276. The symbols # and * indicate statistically significant differences between treatments (normal and Cd conditions) (#, P < 0.05, ##, P < 0.01 and ###, P < 0.001) and between genotypes (T207 and S276) (*, P < 0.05, **, P < 0.01 and ***, P < 0.001), respectively. FW, fresh weight
Fig. 3
Fig. 3
MDA, O2−, and H2O2 concentrations of wheat genotypes T207 and S276 roots growing under normal or Cd treatment. A MDA concentration of genotypes T207 and S276. B O2− concentration of genotypes T207 and S276. C H2O2 concentrations of genotypes T207 and S276. Results are means ± SE of four biological replicates. The black column represents T207 and the white column represents S276. The symbols # and * indicate statistically significant differences between treatments (normal and Cd conditions) (#, P < 0.05, ##, P < 0.01 and ###, P < 0.001) and between genotypes (T207 and S276) (*, P < 0.05, **, P < 0.01 and ***, P < 0.001), respectively. FW, fresh weight
Fig. 4
Fig. 4
SOD, POD, CAT, and APX activities of wheat genotypes T207 and S276 roots growing under normal or Cd treatment. A SOD activities of genotypes T207 and S276. B POD activities of genotypes T207 and S276. C CAT activities of genotypes T207 and S276. D APX activities of genotypes T207 and S276. Results are means ± SE of four biological replicates. The black column represents T207 and the white column represents S276. The symbols # and * indicate statistically significant differences between treatments (normal and Cd conditions) (#, P < 0.05, ##, P < 0.01 and ###, P < 0.001) and between genotypes (T207 and S276) (*, P < 0.05, **, P < 0.01 and ***, P < 0.001), respectively. FW, fresh weight
Fig. 5
Fig. 5
AsA and GSH concentrations of wheat genotypes T207 and S276 roots growing under normal or Cd treatment. A AsA concentration of T207 and S276. B GSH concentration of genotypes T207 and S276. Results are means ± SE of four biological replicates. The black column represents T207 and the white column represents S276. The symbols # and * indicate statistically significant differences between treatments (normal and Cd conditions) (#, P < 0.05, ##, P < 0.01 and ###, P < 0.001) and between genotypes (T207 and S276) (*, P < 0.05, **, P < 0.01 and ***, P < 0.001), respectively. FW, fresh weight
Fig. 6
Fig. 6
The expression of genes involved in AsA-GSH cycle. A Genes involved in AsA-GSH cycle in wheat root. The red box indicates the numbers of genes that showed significantly higher expression in T207 than in S276 under Cd treatment. The blue box indicates the numbers of genes that showed significantly higher expression in S276 than in T207 under Cd treatment. B The heatmap of RBOH expression in wheat root. C The heatmap of genes involved in AsA-GSH cycle expression in wheat root
Fig. 7
Fig. 7
Root architecture analysis of wheat genotypes T207 and S276. Root biomass (A), total root length (B), total root tips number (C), root mean diameter (D), total root surface area (E), total root volume (F) of genotypes T207 and S276. Results are means ± SE of four biological replicates. The black column represents T207 and the white column represents S276. The symbols # indicates statistically significant differences between genotypes (T207 and S276) under Cd treatment and * indicate statistically significant differences between treatments (Cd-free and T1–15 to Cd treatment) (#, P < 0.05, ##, P < 0.01 and ###, P < 0.001), respectively. FW, fresh weight
Fig. 8
Fig. 8
The phenotypes of wheat genotypes T207 and S276 in response to exogenous AsA and GSH. A Whole plant phenotypes. B Root phenotypes. Cd: 5 μM Cd2+, T8: 50 μM GSH + 0.1 mM AsA + 5 μM Cd2+, T9: 100 μM GSH + 0.1 mM AsA + 5 μM Cd2+
Fig. 9
Fig. 9
Histochemical detection of H2O2, O2−, and cell death of wheat genotypes T207 and S276 in response to exogenous AsA and GSH. A DAB staining of roots. B NBT staining of roots. C Evan’s blue staining of roots. Cd: 5 μM Cd2+, T8: 50 μM GSH + 0.1 mM AsA + 5 μM Cd2+, T9: 100 μM GSH + 0.1 mM AsA + 5 μM Cd2+
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