Carbon Monoxide Alleviates Salt-Induced Oxidative Damage in Sorghum bicolor by Inducing the Expression of Proline Biosynthesis and Antioxidant Genes

Ikebudu, Vivian Chigozie; Nkuna, Mulisa; Ndou, Nzumbululo; Ajayi, Rachel Fanelwa; Chivasa, Stephen; Cornish, Katrina; Mulaudzi, Takalani

Abstract

Crop growth and yield are affected by salinity, which causes oxidative damage to plant cells. Plants respond to salinity by maintaining cellular osmotic balance, regulating ion transport, and enhancing the expression of stress-responsive genes, thereby inducing tolerance. As a byproduct of heme oxygenase (HO)-mediated degradation of heme, carbon monoxide (CO) regulates plant responses to salinity. This study investigated a CO-mediated salt stress tolerance mechanism in sorghum seedlings during germination. Sorghum seeds were germinated in the presence of 250 mM NaCl only, or in combination with a CO donor (1 and 1.5 μM hematin), HO inhibitor (5 and 10 μM zinc protoporphyrin IX; ZnPPIX), and hemoglobin (0.1 g/L Hb). Salt stress decreased the germination index (47.73%) and root length (74.31%), while hydrogen peroxide (H2O2) (193.5%), and proline (475%) contents increased. This increase correlated with induced HO (137.68%) activity and transcripts of ion-exchanger and antioxidant genes. Salt stress modified vascular bundle structure, increased metaxylem pit size (42.2%) and the Na+/K+ ratio (2.06) and altered primary and secondary metabolites. However, exogenous CO (1 μM hematin) increased the germination index (63.01%) and root length (150.59%), while H2O2 (21.94%) content decreased under salt stress. Carbon monoxide further increased proline (147.62%), restored the vascular bundle structure, decreased the metaxylem pit size (31.2%) and Na+/K+ ratio (1.46), and attenuated changes observed on primary and secondary metabolites under salt stress. Carbon monoxide increased HO activity (30.49%), protein content, and antioxidant gene transcripts. The alleviatory role of CO was abolished by Hb, whereas HO activity was slightly inhibited by ZnPPIX under salt stress. These results suggest that CO elicited salt stress tolerance by reducing oxidative damage through osmotic adjustment and by regulating the expression of HO1 and the ion exchanger and antioxidant transcripts.

Citation

Ikebudu, V. C., Nkuna, M., Ndou, N., Ajayi, R. F., Chivasa, S., Cornish, K., & Mulaudzi, T. (2024). Carbon Monoxide Alleviates Salt-Induced Oxidative Damage in Sorghum bicolor by Inducing the Expression of Proline Biosynthesis and Antioxidant Genes. Plants, 13(6), Article 782. https://doi.org/10.3390/plants13060782

• Journal Article Type: Article
• Acceptance Date: Mar 5, 2024
• Online Publication Date: Mar 10, 2024
• Publication Date: Mar 10, 2024
• Deposit Date: May 16, 2024
• Publicly Available Date: May 16, 2024
• Journal: Plants
• Electronic ISSN: 2223-7747
• Publisher: MDPI
• Peer Reviewed: Peer Reviewed
• Volume: 13
• Issue: 6
• Article Number: 782
• DOI: https://doi.org/10.3390/plants13060782
• Public URL: https://durham-repository.worktribe.com/output/2379143