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

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 t...

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Main Authors: Yu Wang, Jin-Li Cao, Abeer Hashem, Elsayed Fathi Abd_Allah, Qiang-Sheng Wu
Format: Article
Language:English
Published: Frontiers Media S.A. 2023-10-01
Series:Frontiers in Plant Science
Subjects:
Online Access:https://www.frontiersin.org/articles/10.3389/fpls.2023.1247342/full
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author Yu Wang
Jin-Li Cao
Abeer Hashem
Elsayed Fathi Abd_Allah
Qiang-Sheng Wu
author_facet Yu Wang
Jin-Li Cao
Abeer Hashem
Elsayed Fathi Abd_Allah
Qiang-Sheng Wu
author_sort Yu Wang
collection DOAJ
description 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.
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spelling doaj.art-2d525183e39346e0af747e60f680d1d92023-10-04T10:00:38ZengFrontiers Media S.A.Frontiers in Plant Science1664-462X2023-10-011410.3389/fpls.2023.12473421247342Serendipita indica mitigates drought-triggered oxidative burst in trifoliate orange by stimulating antioxidant defense systemsYu Wang0Jin-Li Cao1Abeer Hashem2Elsayed Fathi Abd_Allah3Qiang-Sheng Wu4College of Horticulture and Gardening, Yangtze University, Jingzhou, Hubei, ChinaCollege of Horticulture and Gardening, Yangtze University, Jingzhou, Hubei, ChinaBotany and Microbiology Department, College of Science, King Saud University, Riyadh, Saudi ArabiaPlant Production Department, College of Food and Agricultural Sciences, King Saud University, Riyadh, Saudi ArabiaCollege of Horticulture and Gardening, Yangtze University, Jingzhou, Hubei, ChinaSoil 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.https://www.frontiersin.org/articles/10.3389/fpls.2023.1247342/fullantioxidationcitrusendophytic fungusgas exchangeoxidative damage
spellingShingle Yu Wang
Jin-Li Cao
Abeer Hashem
Elsayed Fathi Abd_Allah
Qiang-Sheng Wu
Serendipita indica mitigates drought-triggered oxidative burst in trifoliate orange by stimulating antioxidant defense systems
Frontiers in Plant Science
antioxidation
citrus
endophytic fungus
gas exchange
oxidative damage
title Serendipita indica mitigates drought-triggered oxidative burst in trifoliate orange by stimulating antioxidant defense systems
title_full Serendipita indica mitigates drought-triggered oxidative burst in trifoliate orange by stimulating antioxidant defense systems
title_fullStr Serendipita indica mitigates drought-triggered oxidative burst in trifoliate orange by stimulating antioxidant defense systems
title_full_unstemmed Serendipita indica mitigates drought-triggered oxidative burst in trifoliate orange by stimulating antioxidant defense systems
title_short Serendipita indica mitigates drought-triggered oxidative burst in trifoliate orange by stimulating antioxidant defense systems
title_sort serendipita indica mitigates drought triggered oxidative burst in trifoliate orange by stimulating antioxidant defense systems
topic antioxidation
citrus
endophytic fungus
gas exchange
oxidative damage
url https://www.frontiersin.org/articles/10.3389/fpls.2023.1247342/full
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