Serendipita indica mitigates drought-triggered oxidative burst in trifoliate orange by stimulating antioxidant defense systems

Yu Wang; Jin-Li Cao; Abeer Hashem; Elsayed Fathi Abd Allah; Qiang-Sheng Wu

doi:10.3389/fpls.2023.1247342

Serendipita indica mitigates drought-triggered oxidative burst in trifoliate orange by stimulating antioxidant defense systems

Front Plant Sci. 2023 Oct 4:14:1247342. doi: 10.3389/fpls.2023.1247342. eCollection 2023.

Authors

Yu Wang¹, Jin-Li Cao¹, Abeer Hashem², Elsayed Fathi Abd Allah³, Qiang-Sheng Wu¹

Affiliations

¹ College of Horticulture and Gardening, Yangtze University, Jingzhou, Hubei, China.
² Botany and Microbiology Department, College of Science, King Saud University, Riyadh, Saudi Arabia.
³ Plant Production Department, College of Food and Agricultural Sciences, King Saud University, Riyadh, Saudi Arabia.

Abstract

Soil drought is detrimental to plant growth worldwide, particularly by triggering reactive oxygen species (ROS) burst. Serendipita indica (Si), a culturable root-associated endophytic fungus, can assist host plants in dealing with abiotic stresses; however, it is unknown whether and how Si impacts the drought tolerance of citrus plants. To unravel the effects and roles of Si on drought-stressed plants, trifoliate orange (Poncirus trifoliata L. Raf.; a citrus rootstock) seedlings were inoculated with Si and exposed to soil drought, and growth, gas exchange, ROS levels, antioxidant defense systems, and expression of genes encoding antioxidant enzymes and fatty acid desaturases in leaves were measured. Soil drought suppressed plant biomass, whereas Si inoculation significantly increased plant biomass (10.29%-22.47%) and shoot/root ratio (21.78%-24.68%) under ample water and drought conditions, accompanied by improved net photosynthetic rate (105.71%), water use efficiency (115.29%), chlorophyll index (55.34%), and nitrogen balance index (63.84%) by Si inoculation under soil drought. Soil drought triggered an increase in leaf hydrogen peroxide and superoxide anion levels, while Si inoculation significantly reduced these ROS levels under soil drought, resulting in lower membrane lipid peroxidation with respect to malondialdehyde changes. Furthermore, Si-inoculated seedlings under soil drought had distinctly higher levels of ascorbate and glutathione, as well as catalase, peroxidase, and glutathione peroxidase activities, compared with no-Si-inoculated seedlings. Si inoculation increased the expression of leaf PtFAD2, PtFAD6, PtΔ9, PtΔ15, PtFe-SOD, PtCu/Zn-SOD, PtPOD, and PtCAT1 genes under both ample water and soil drought conditions. Overall, Si-inoculated trifoliate orange plants maintained a low oxidative burst in leaves under drought, which was associated with stimulation of antioxidant defense systems. Therefore, Si has great potential as a biostimulant in enhancing drought tolerance in plants, particularly citrus.

Keywords: antioxidation; citrus; endophytic fungus; gas exchange; oxidative damage.

Grants and funding

This study was supported by the Plan in Scientific and Technological Innovation Team of Outstanding Young Scientists, Hubei Provincial Department of Education (T201604). The authors would like to extend their sincere appreciation to the Researchers Supporting Project Number (RSP2023R356), King Saud University, Riyadh, Saudi Arabia.