Hydrogen sulfide priming enhanced salinity tolerance in sunflower by modulating ion hemostasis, cellular redox balance, and gene expression

Abstract

Background The salinity threat represents an environmental challenge that drastically affects plant growth and yield. Besides salinity stress, the escalating world population will greatly influence the world’s food security in the future. Therefore, searching for effective strategies to improve crop salinity resilience and sustain agricultural productivity under high salinity is a must. Seed priming is a reliable, simple, low-risk, and low-cost technique. Therefore, this work aimed to evaluate the impact of seed priming with 0.5 mM NaHS, as a donor of H2S, in mitigating salinity effects on sunflower seedlings. Primed and nonprime seeds were established in nonsaline soil irrigated with tape water for 14 d, and then exposed to 150 mM NaCl for 7 d. Results Salinity stress significantly reduced the seedling growth, biomass accumulation, K+, Ca2+, and salinity tolerance index while elevating Na+ uptake and translocation. Salinity-induced adverse effects were significantly alleviated by H2S priming. Upregulation in gene expression (HaSOS2, HaGST) under NaCl stress was further enhanced by H2S priming. Also, H2S reduced lipid peroxidation, electrolyte leakage, and H2O2 content, but elevated the antioxidant defense system. NaCl-induced levels of ascorbate, glutathione, and α tocopherol, as well as the activities of AsA-GSH cycle enzymes: ascorbate peroxidase, monodehydroascorbate reductase, dehydroascorbate reductase, glutathione reductase, and glutathione S-transferase, were further enhanced by H2S priming. Increased level of H2S and total thiol by NaCl was also further stimulated by H2S priming. Conclusion H2S priming has proved to be an efficient strategy to improve sunflower seedlings’ salinity tolerance by retaining ion homeostasis, detoxifying oxidative damage, modulating gene expression involved in ion homeostasis and ROS scavenging, and boosting endogenous H2S. These findings suggested that H2S acts as a regulatory molecule activating the functional processes responsible for sunflower adaptive mechanisms and could be adopted as a crucial crop management strategy to combat saline conditions. However, it would be of great interest to conduct further studies in the natural saline field to broaden our understanding of crop adaptive mechanisms and to support our claims.

Hydrogen sulfide-mitigated salinity stress impact in sunflower seedlings was associated with improved photosynthesis performance and osmoregulation

“…The reduction in growth parameters and the higher R/S ratio were also reported in different crop species in response to saline conditions [ 40 – 44 ]. On the other hand, the mitigative effect of H 2 S on salinity-induced growth reduction most probably is interpreted as H 2 S modulation of ion hemostasis, elevation of osmolyte levels (total soluble proteins and total soluble sugars observed in this study), signaling molecule role, and scavenging of ROS under saline imposition [ 34 , 35 , 45 – 48 ]. Reduced toxic ions and elevated beneficial ones as well as ROS detoxification by H 2 S priming under saline conditions have been reported as adaptive mechanisms for sunflower salinity tolerance [ 35 ].…”

“…On the other hand, the mitigative effect of H 2 S on salinity-induced growth reduction most probably is interpreted as H 2 S modulation of ion hemostasis, elevation of osmolyte levels (total soluble proteins and total soluble sugars observed in this study), signaling molecule role, and scavenging of ROS under saline imposition [ 34 , 35 , 45 – 48 ]. Reduced toxic ions and elevated beneficial ones as well as ROS detoxification by H 2 S priming under saline conditions have been reported as adaptive mechanisms for sunflower salinity tolerance [ 35 ]. Also, H 2 S priming followed by NaCl stress resulted in a remarkable reduction in the R/S ratio might be explained by the impact of H 2 S in reducing Na + uptake and accumulation in both the root and shoot as previously reported by Younis and Mansour [ 35 ].…”

“…In this study, the fresh weight, dry weight, and leaf area of sunflower seedlings were significantly suppressed under NaCl stress. This salinity-induced decrease in the growth can be attributed to the osmotic action of salinity (i.e., water stress), ionic stress due to excessive ion accumulation, nutritional disequilibrium, reduced photosynthetic capacity (observed in this research), and/or oxidative stress [ 35 – 37 ]. However, salinity-stressed seedlings showed a marked increase in root-to-shoot dry weight ratio which might imply a higher reduction in the shoot dry weight [ 35 ] as well as an increase in root biomass production, which may favor the retention of Na + in the root as an adaptive response [ 6 , 35 ].…”

“…This salinity-induced decrease in the growth can be attributed to the osmotic action of salinity (i.e., water stress), ionic stress due to excessive ion accumulation, nutritional disequilibrium, reduced photosynthetic capacity (observed in this research), and/or oxidative stress [ 35 – 37 ]. However, salinity-stressed seedlings showed a marked increase in root-to-shoot dry weight ratio which might imply a higher reduction in the shoot dry weight [ 35 ] as well as an increase in root biomass production, which may favor the retention of Na + in the root as an adaptive response [ 6 , 35 ]. We also speculate that the extensive root growth could compensate for their absorption function loss resulting from salinity treatment by dry weight accumulation [ 38 , 39 ].…”

“…Reduced toxic ions and elevated beneficial ones as well as ROS detoxification by H 2 S priming under saline conditions have been reported as adaptive mechanisms for sunflower salinity tolerance [ 35 ]. Also, H 2 S priming followed by NaCl stress resulted in a remarkable reduction in the R/S ratio might be explained by the impact of H 2 S in reducing Na + uptake and accumulation in both the root and shoot as previously reported by Younis and Mansour [ 35 ].…”