Foliar Applications of <i>Bacillus subtilis</i> HA1 Culture Filtrate Enhance Tomato Growth and Induce Systemic Resistance against <i>Tobacco mosaic virus</i> Infection

The application of microbial products as natural biocontrol agents for inducing systemic resistance against plant viral infections represents a promising strategy for sustainable and eco-friendly agricultural applications. Under greenhouse conditions, the efficacy of the culture filtrate of <i>...

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Main Authors: Hamada El-Gendi, Abdulaziz A. Al-Askar, Lóránt Király, Marwa A. Samy, Hassan Moawad, Ahmed Abdelkhalek
Format: Article
Language:English
Published: MDPI AG 2022-03-01
Series:Horticulturae
Subjects:
Online Access:https://www.mdpi.com/2311-7524/8/4/301
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author Hamada El-Gendi
Abdulaziz A. Al-Askar
Lóránt Király
Marwa A. Samy
Hassan Moawad
Ahmed Abdelkhalek
author_facet Hamada El-Gendi
Abdulaziz A. Al-Askar
Lóránt Király
Marwa A. Samy
Hassan Moawad
Ahmed Abdelkhalek
author_sort Hamada El-Gendi
collection DOAJ
description The application of microbial products as natural biocontrol agents for inducing systemic resistance against plant viral infections represents a promising strategy for sustainable and eco-friendly agricultural applications. Under greenhouse conditions, the efficacy of the culture filtrate of <i>Bacillus subtilis</i> strain HA1 (Acc# OM286889) for protecting tomato plants from <i>Tobacco mosaic virus</i> (TMV) infection was assessed. The results showed that the dual foliar application of this culture filtrate (HA1-CF) 24 h before and 24 h after TMV inoculation was the most effective treatment for enhancing tomato plant development, with substantial improvements in shoot and root parameters. Furthermore, compared to non-treated plants, HA1-CF-treated tomato had a significant increase in total phenolic and flavonoid contents of up to 27% and 50%, respectively. In addition, a considerable increase in the activities of reactive oxygen species scavenging enzymes (PPO, SOD, and POX) and a significant decrease in non-enzymatic oxidative stress markers (H<sub>2</sub>O<sub>2</sub> and MDA) were reported. In comparison to untreated control plants, all HA1-CF-treated plants showed a significant reduction in TMV accumulation in systemically infected tomato leaves, up to a 91% reduction at 15 dpi. The qRT-PCR results confirmed that HA1-CF stimulated the transcription of several defense-related tomato genes (<i>PR-1, PAL, CHS, and HQT</i>), pointing to their potential role in induced resistance against TMV. GC–MS analysis showed that phenol, 2,4-bis (1,1-dimethylethyl)-, Pyrrolo [1,2-a] pyrazine-1,4-dione, hexahydro-3-(2-methylpropyl)- and eicosane are the primary ingredient compounds in the HA1-CF ethyl acetate extract, suggesting that these molecules take part in stimulating induced systemic resistance in tomato plants. Our results imply that HA1-CF is a potential resistance inducer to control plant viral infections, a plant growth promoter, and a source of bioactive compounds for sustainable disease management.
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spelling doaj.art-af5d73789f4a407d830d26637a231f8b2023-11-30T21:12:50ZengMDPI AGHorticulturae2311-75242022-03-018430110.3390/horticulturae8040301Foliar Applications of <i>Bacillus subtilis</i> HA1 Culture Filtrate Enhance Tomato Growth and Induce Systemic Resistance against <i>Tobacco mosaic virus</i> InfectionHamada El-Gendi0Abdulaziz A. Al-Askar1Lóránt Király2Marwa A. Samy3Hassan Moawad4Ahmed Abdelkhalek5Bioprocess Development Department, Genetic Engineering and Biotechnology Research Institute, City of Scientific Research and Technological Applications, Alexandria 21934, EgyptDepartment of Botany and Microbiology College of Science, King Saud University, P.O. Box 2455, Riyadh 11451, Saudi ArabiaCentre for Agricultural Research, Plant Protection Institute, ELKH, 15 Herman Ottó Str., H-1022 Budapest, HungaryPlant Protection and Biomolecular Diagnosis Department, ALCRI, City of Scientific Research and Technological Applications, Alexandria 21934, EgyptAgriculture Microbiology Department, National Research Centre, Cairo 12622, EgyptPlant Protection and Biomolecular Diagnosis Department, ALCRI, City of Scientific Research and Technological Applications, Alexandria 21934, EgyptThe application of microbial products as natural biocontrol agents for inducing systemic resistance against plant viral infections represents a promising strategy for sustainable and eco-friendly agricultural applications. Under greenhouse conditions, the efficacy of the culture filtrate of <i>Bacillus subtilis</i> strain HA1 (Acc# OM286889) for protecting tomato plants from <i>Tobacco mosaic virus</i> (TMV) infection was assessed. The results showed that the dual foliar application of this culture filtrate (HA1-CF) 24 h before and 24 h after TMV inoculation was the most effective treatment for enhancing tomato plant development, with substantial improvements in shoot and root parameters. Furthermore, compared to non-treated plants, HA1-CF-treated tomato had a significant increase in total phenolic and flavonoid contents of up to 27% and 50%, respectively. In addition, a considerable increase in the activities of reactive oxygen species scavenging enzymes (PPO, SOD, and POX) and a significant decrease in non-enzymatic oxidative stress markers (H<sub>2</sub>O<sub>2</sub> and MDA) were reported. In comparison to untreated control plants, all HA1-CF-treated plants showed a significant reduction in TMV accumulation in systemically infected tomato leaves, up to a 91% reduction at 15 dpi. The qRT-PCR results confirmed that HA1-CF stimulated the transcription of several defense-related tomato genes (<i>PR-1, PAL, CHS, and HQT</i>), pointing to their potential role in induced resistance against TMV. GC–MS analysis showed that phenol, 2,4-bis (1,1-dimethylethyl)-, Pyrrolo [1,2-a] pyrazine-1,4-dione, hexahydro-3-(2-methylpropyl)- and eicosane are the primary ingredient compounds in the HA1-CF ethyl acetate extract, suggesting that these molecules take part in stimulating induced systemic resistance in tomato plants. Our results imply that HA1-CF is a potential resistance inducer to control plant viral infections, a plant growth promoter, and a source of bioactive compounds for sustainable disease management.https://www.mdpi.com/2311-7524/8/4/301<i>Bacillus subtilis</i><i>Tobacco mosaic virus</i>oxidative stressantioxidative enzymesgene expressionGC–MS
spellingShingle Hamada El-Gendi
Abdulaziz A. Al-Askar
Lóránt Király
Marwa A. Samy
Hassan Moawad
Ahmed Abdelkhalek
Foliar Applications of <i>Bacillus subtilis</i> HA1 Culture Filtrate Enhance Tomato Growth and Induce Systemic Resistance against <i>Tobacco mosaic virus</i> Infection
Horticulturae
<i>Bacillus subtilis</i>
<i>Tobacco mosaic virus</i>
oxidative stress
antioxidative enzymes
gene expression
GC–MS
title Foliar Applications of <i>Bacillus subtilis</i> HA1 Culture Filtrate Enhance Tomato Growth and Induce Systemic Resistance against <i>Tobacco mosaic virus</i> Infection
title_full Foliar Applications of <i>Bacillus subtilis</i> HA1 Culture Filtrate Enhance Tomato Growth and Induce Systemic Resistance against <i>Tobacco mosaic virus</i> Infection
title_fullStr Foliar Applications of <i>Bacillus subtilis</i> HA1 Culture Filtrate Enhance Tomato Growth and Induce Systemic Resistance against <i>Tobacco mosaic virus</i> Infection
title_full_unstemmed Foliar Applications of <i>Bacillus subtilis</i> HA1 Culture Filtrate Enhance Tomato Growth and Induce Systemic Resistance against <i>Tobacco mosaic virus</i> Infection
title_short Foliar Applications of <i>Bacillus subtilis</i> HA1 Culture Filtrate Enhance Tomato Growth and Induce Systemic Resistance against <i>Tobacco mosaic virus</i> Infection
title_sort foliar applications of i bacillus subtilis i ha1 culture filtrate enhance tomato growth and induce systemic resistance against i tobacco mosaic virus i infection
topic <i>Bacillus subtilis</i>
<i>Tobacco mosaic virus</i>
oxidative stress
antioxidative enzymes
gene expression
GC–MS
url https://www.mdpi.com/2311-7524/8/4/301
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