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

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.

Enhanced Cd-Accumulation in Typha latifolia by Interaction with Pseudomonas rhodesiae GRC140 under Axenic Hydroponic Conditions

“…We observed that CAT activity increased two-fold in T. latifolia roots exposed to 10 mg/L of Cd, but no significant changes were detected in shoots and roots exposed to 20 or 40 mg/L of Cd ( Figure 3 a). Similar results were observed in Sassafras tzumu and Triticum aestivum plants exposed to Cd [ 34 , 35 ]. The increase in CAT activity at low Cd levels (10 mg/L) may be attributed to increased ROS production induced by Cd oxidative stress, similar to that observed in T. aestivum [ 35 ].…”

“…Similar results were observed in Sassafras tzumu and Triticum aestivum plants exposed to Cd [ 34 , 35 ]. The increase in CAT activity at low Cd levels (10 mg/L) may be attributed to increased ROS production induced by Cd oxidative stress, similar to that observed in T. aestivum [ 35 ]. On the other hand, the low CAT activity at high Cd concentrations could result from Cd ions interacting with amino acids of the CAT active center, preventing CAT binding to H 2 O 2 by steric hindrance conditions [ 36 ].…”

Metabolome and transcriptome association analysis revealed key factors involved in melatonin mediated cadmium-stress tolerance in cotton

“…This was due to ascorbic acid acted as a special electron donor for APX to reduce the content of H 2 O 2 and O 2− , and was oxidized to dehydroascorbic acid (DHAA) and then non-enzymatically reduced by GSH to form an AsA-GSH cycle, which eliminates reactive oxygen species (ROS) produced under heavy metal stress by redox regulation ( Intarasit & Saengnil, 2021 ). Studies have found that Cd toxicity reprogrammed the gene transcription profile of the AsA-GSH cycle, the expression level of the corresponding DEGs was greater especially in Cd-tolerant wheat varieties ( Zhang et al., 2021b ), and the addition of exogenous MT increased the content of ascorbic acid and GSH in safflower seedlings ( Amjadi et al., 2021 ), which was consistent with the up-regulated of genes related to the ascorbic acid metabolism pathway in this study, and the pretreatment with 2-OHMT ( Shah et al., 2020b ) and MT ( Shah et al., 2020c ) increased the accumulation of glutathione in Cucumis sativus seedlings, indicating that plant seedlings can improve the tolerance to Cd toxicity by accelerating the AsA-GSH cycle.…”

Exogenous hydrogen sulfide and methylglyoxal alleviate cadmium-induced oxidative stress in Salix matsudana Koidz by regulating glutathione metabolism

“…Moreover, exogenous supplementation of NaHS and MG maintained the redox status of AsA and GSH through regulating the AsA–GSH cycle enzymes (Figs. 2 and 5 ) [ 26 ], thereby triggering the tolerance of plants to Cd [ 12 ].…”

“…In plants, GSH is a water-soluble non-protein thiol compound and performs a wide range of biochemical functions [ 9 ]. Many studies have found that GSH accumulates in response to increased levels of ROS or to compensate for a decrease in the defense capability of other antioxidants [ 10 , 11 ], and GSH levels are constitutively higher in plants subjected to Cd [ 12 ], drought [ 13 ], and heat [ 14 ] stress conditions. On the one hand, GSH can directly scavenge free radical by reacting with 1 O 2 , O 2 .- , and ∙OH [ 15 ]; and on the other hand, GSH is able to induce signal transduction and defense against ROS under stress conditions through regulating the enzymes related to GSH metabolism [ 10 , 15 ].…”