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Enhancing spinach (Spinacia oleracea L.) resilience in pesticide-contaminated soil: Role of pesticide-tolerant Ciceribacter azotifigens and Serratia marcescens in root architecture, leaf gas exchange attributes and antioxidant response restoration
This study unveils the detoxification potential of insecticide-tolerant plant beneficial bacteria (PBB), i.e., Ciceribacter azotifigens SF1 and Serratia marcescens SRB1, in spinach treated with fipronil (FIP), profenofos (PF) and chlorantraniliprole (CLP) insecticides. Increasing insecticide doses (...
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Published in: | Chemosphere (Oxford) 2024-08, Vol.361, p.142487, Article 142487 |
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description | This study unveils the detoxification potential of insecticide-tolerant plant beneficial bacteria (PBB), i.e., Ciceribacter azotifigens SF1 and Serratia marcescens SRB1, in spinach treated with fipronil (FIP), profenofos (PF) and chlorantraniliprole (CLP) insecticides. Increasing insecticide doses (25–400 μg kg−1 soil) significantly curtailed germination attributes and growth of spinach cultivated at both bench-scale and in greenhouse experiments. Profenofos at 400 μg kg−1 exhibited maximum inhibitory effects and reduced germination by 55%; root and shoot length by 78% and 81%, respectively; dry matter accumulation in roots and shoots by 79% and 62%, respectively; leaf number by 87% and leaf area by 56%. Insecticide application caused morphological distortion in root tips/surfaces, increased levels of oxidative stress, and cell death in spinach. Application of insecticide-tolerant SF1 and SRB1 strains relieved insecticide pressure resulting in overall improvement in growth and physiology of spinach grown under insecticide stress. Ciceribacter azotifigens improved germination rate (10%); root biomass (53%); shoot biomass (25%); leaf area (10%); Chl-a (45%), Chl-b (36%) and carotenoid (48%) contents of spinach at 25 μg CLP kg−1 soil. PBB inoculation reinvigorated the stressed spinach and modulated the synthesis of phytochemicals, proline, malondialdehyde (MDA), superoxide anions (O2•–), and hydrogen peroxide (H2O2). Scanning electron microscopy (SEM) revealed recovery in root tip morphology and stomatal openings on abaxial leaf surfaces of PBB-inoculated spinach grown with insecticides. Ciceribacter azotifigens inoculation significantly increased intrinsic water use efficiency, transpiration rate, vapor pressure deficit, intracellular CO2 concentration, photosynthetic rate, and stomatal conductance in spinach exposed to 25 μg FIP kg−1. Also, C. azotifigens and S. marcescens modulated the antioxidant defense systems of insecticide-treated spinach. Bacterial strains were strongly colonized to root surfaces of insecticide-stressed spinach seedlings as revealed under SEM. The identification of insecticide-tolerant PBBs such as C. azotifigens and S. marcescens hold the potential for alleviating abiotic stress to spinach, thereby fostering enhanced and safe production within polluted agroecosystems.
[Display omitted]
•Insecticides showed differential toxicity to Spinacia oleracea (L.) seedlings.•Insecticide-tolerant PGPR strains-mediated phytotoxicity alleviation |
doi_str_mv | 10.1016/j.chemosphere.2024.142487 |
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[Display omitted]
•Insecticides showed differential toxicity to Spinacia oleracea (L.) seedlings.•Insecticide-tolerant PGPR strains-mediated phytotoxicity alleviation was reported.•PGPR improved leaf gas-exchange attributes and stomatal behavior under stress.•PGPR-mediated reduction in insecticide-induced oxidative stress and ROS generation in spinach.•Successful colonization and establishment of strains in stressed spinach rhizosphere.</description><identifier>ISSN: 0045-6535</identifier><identifier>ISSN: 1879-1298</identifier><identifier>EISSN: 1879-1298</identifier><identifier>DOI: 10.1016/j.chemosphere.2024.142487</identifier><identifier>PMID: 38821129</identifier><language>eng</language><publisher>England: Elsevier Ltd</publisher><subject>Antioxidant defence enzymes ; Antioxidants - metabolism ; Bacillaceae - metabolism ; Bacillaceae - physiology ; Biodegradation, Environmental ; Gas exchange attributes ; Germination - drug effects ; Insecticide-tolerant PGPR ; Insecticides - toxicity ; Oxidative Stress - drug effects ; Pesticides - metabolism ; Pesticides - toxicity ; Photosynthesis - drug effects ; Plant Leaves - drug effects ; Plant Roots - drug effects ; Plant Roots - microbiology ; Root colonization and biofilm formation ; Serratia marcescens - drug effects ; Serratia marcescens - metabolism ; Serratia marcescens - physiology ; Soil - chemistry ; Soil Microbiology ; Soil Pollutants - metabolism ; Soil Pollutants - toxicity ; Spinacia oleracea (L.) ; Spinacia oleracea - drug effects ; Spinacia oleracea - metabolism ; Spinacia oleracea - physiology ; Stomatal behavior</subject><ispartof>Chemosphere (Oxford), 2024-08, Vol.361, p.142487, Article 142487</ispartof><rights>2024 Elsevier Ltd</rights><rights>Copyright © 2024 Elsevier Ltd. All rights reserved.</rights><lds50>peer_reviewed</lds50><woscitedreferencessubscribed>false</woscitedreferencessubscribed><cites>FETCH-LOGICAL-c1669-fce7cf5bd6ff354c6e5d69ec315bc429f4b863a2bf93a31cda618d0e20bf7e4a3</cites><orcidid>0000-0002-2443-9451</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><link.rule.ids>314,780,784,27924,27925</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/38821129$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Shahid, Mohammad</creatorcontrib><creatorcontrib>Singh, Udai B.</creatorcontrib><title>Enhancing spinach (Spinacia oleracea L.) resilience in pesticide-contaminated soil: Role of pesticide-tolerant Ciceribacter azotifigens and Serratia marcescens in root architecture, leaf gas exchange attributes and antioxidant response restoration</title><title>Chemosphere (Oxford)</title><addtitle>Chemosphere</addtitle><description>This study unveils the detoxification potential of insecticide-tolerant plant beneficial bacteria (PBB), i.e., Ciceribacter azotifigens SF1 and Serratia marcescens SRB1, in spinach treated with fipronil (FIP), profenofos (PF) and chlorantraniliprole (CLP) insecticides. Increasing insecticide doses (25–400 μg kg−1 soil) significantly curtailed germination attributes and growth of spinach cultivated at both bench-scale and in greenhouse experiments. Profenofos at 400 μg kg−1 exhibited maximum inhibitory effects and reduced germination by 55%; root and shoot length by 78% and 81%, respectively; dry matter accumulation in roots and shoots by 79% and 62%, respectively; leaf number by 87% and leaf area by 56%. Insecticide application caused morphological distortion in root tips/surfaces, increased levels of oxidative stress, and cell death in spinach. Application of insecticide-tolerant SF1 and SRB1 strains relieved insecticide pressure resulting in overall improvement in growth and physiology of spinach grown under insecticide stress. Ciceribacter azotifigens improved germination rate (10%); root biomass (53%); shoot biomass (25%); leaf area (10%); Chl-a (45%), Chl-b (36%) and carotenoid (48%) contents of spinach at 25 μg CLP kg−1 soil. PBB inoculation reinvigorated the stressed spinach and modulated the synthesis of phytochemicals, proline, malondialdehyde (MDA), superoxide anions (O2•–), and hydrogen peroxide (H2O2). Scanning electron microscopy (SEM) revealed recovery in root tip morphology and stomatal openings on abaxial leaf surfaces of PBB-inoculated spinach grown with insecticides. Ciceribacter azotifigens inoculation significantly increased intrinsic water use efficiency, transpiration rate, vapor pressure deficit, intracellular CO2 concentration, photosynthetic rate, and stomatal conductance in spinach exposed to 25 μg FIP kg−1. Also, C. azotifigens and S. marcescens modulated the antioxidant defense systems of insecticide-treated spinach. Bacterial strains were strongly colonized to root surfaces of insecticide-stressed spinach seedlings as revealed under SEM. The identification of insecticide-tolerant PBBs such as C. azotifigens and S. marcescens hold the potential for alleviating abiotic stress to spinach, thereby fostering enhanced and safe production within polluted agroecosystems.
[Display omitted]
•Insecticides showed differential toxicity to Spinacia oleracea (L.) seedlings.•Insecticide-tolerant PGPR strains-mediated phytotoxicity alleviation was reported.•PGPR improved leaf gas-exchange attributes and stomatal behavior under stress.•PGPR-mediated reduction in insecticide-induced oxidative stress and ROS generation in spinach.•Successful colonization and establishment of strains in stressed spinach rhizosphere.</description><subject>Antioxidant defence enzymes</subject><subject>Antioxidants - metabolism</subject><subject>Bacillaceae - metabolism</subject><subject>Bacillaceae - physiology</subject><subject>Biodegradation, Environmental</subject><subject>Gas exchange attributes</subject><subject>Germination - drug effects</subject><subject>Insecticide-tolerant PGPR</subject><subject>Insecticides - toxicity</subject><subject>Oxidative Stress - drug effects</subject><subject>Pesticides - metabolism</subject><subject>Pesticides - toxicity</subject><subject>Photosynthesis - drug effects</subject><subject>Plant Leaves - drug effects</subject><subject>Plant Roots - drug effects</subject><subject>Plant Roots - microbiology</subject><subject>Root colonization and biofilm formation</subject><subject>Serratia marcescens - drug effects</subject><subject>Serratia marcescens - metabolism</subject><subject>Serratia marcescens - physiology</subject><subject>Soil - chemistry</subject><subject>Soil Microbiology</subject><subject>Soil Pollutants - metabolism</subject><subject>Soil Pollutants - toxicity</subject><subject>Spinacia oleracea (L.)</subject><subject>Spinacia oleracea - drug effects</subject><subject>Spinacia oleracea - metabolism</subject><subject>Spinacia oleracea - physiology</subject><subject>Stomatal behavior</subject><issn>0045-6535</issn><issn>1879-1298</issn><issn>1879-1298</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2024</creationdate><recordtype>article</recordtype><recordid>eNqNkU-P0zAQxSMEYsvCV0Dmtkik2HHiJtxW1fJHqoTEwtlyxuPGVWoH20ELX5wrTrugPXLyyHpvfjPziuIVo2tGmXh7WMOARx-nAQOuK1rVa1ZXdbt5VKxYu-lKVnXt42JFad2UouHNRfEsxgOl2dx0T4sL3rYVy6JV8fvGDcqBdXsSJ-sUDOTq9lRYRfyIQQEqslu_JgGjHS06QGIdmTAmC1ZjCd4ldcyOhJpEb8d35Es2Em8eiNKplUtkawGD7RUkDET98skau0cXiXKa3GIIKmXwUQXACMt_ZgXvE8k_g00IaQ74hoyoDNmrSPAO8vx7JCql3HdOeG6VWdbfWb0w8-STdxGXIvmF4N3z4olRY8QX9-9l8e39zdftx3L3-cOn7fWuBCZEVxrADZim18IY3tQgsNGiQ-Cs6aGuOlP3reCq6k3HFWeglWCtpljR3mywVvyyuDr3nYL_Pme-PNq82Dgqh36OklPBa8F5x7O0O0sh-BgDGjkFmy_xUzIql9zlQT7IXS65y3Pu2fvyHjP3R9T_nH-DzoLtWYB52R8Wg4xwClPbkI8qtbf_gfkDM93Ntg</recordid><startdate>202408</startdate><enddate>202408</enddate><creator>Shahid, Mohammad</creator><creator>Singh, Udai B.</creator><general>Elsevier Ltd</general><scope>CGR</scope><scope>CUY</scope><scope>CVF</scope><scope>ECM</scope><scope>EIF</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>7X8</scope><orcidid>https://orcid.org/0000-0002-2443-9451</orcidid></search><sort><creationdate>202408</creationdate><title>Enhancing spinach (Spinacia oleracea L.) resilience in pesticide-contaminated soil: Role of pesticide-tolerant Ciceribacter azotifigens and Serratia marcescens in root architecture, leaf gas exchange attributes and antioxidant response restoration</title><author>Shahid, Mohammad ; Singh, Udai B.</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c1669-fce7cf5bd6ff354c6e5d69ec315bc429f4b863a2bf93a31cda618d0e20bf7e4a3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2024</creationdate><topic>Antioxidant defence enzymes</topic><topic>Antioxidants - metabolism</topic><topic>Bacillaceae - metabolism</topic><topic>Bacillaceae - physiology</topic><topic>Biodegradation, Environmental</topic><topic>Gas exchange attributes</topic><topic>Germination - drug effects</topic><topic>Insecticide-tolerant PGPR</topic><topic>Insecticides - toxicity</topic><topic>Oxidative Stress - drug effects</topic><topic>Pesticides - metabolism</topic><topic>Pesticides - toxicity</topic><topic>Photosynthesis - drug effects</topic><topic>Plant Leaves - drug effects</topic><topic>Plant Roots - drug effects</topic><topic>Plant Roots - microbiology</topic><topic>Root colonization and biofilm formation</topic><topic>Serratia marcescens - drug effects</topic><topic>Serratia marcescens - metabolism</topic><topic>Serratia marcescens - physiology</topic><topic>Soil - chemistry</topic><topic>Soil Microbiology</topic><topic>Soil Pollutants - metabolism</topic><topic>Soil Pollutants - toxicity</topic><topic>Spinacia oleracea (L.)</topic><topic>Spinacia oleracea - drug effects</topic><topic>Spinacia oleracea - metabolism</topic><topic>Spinacia oleracea - physiology</topic><topic>Stomatal behavior</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Shahid, Mohammad</creatorcontrib><creatorcontrib>Singh, Udai B.</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>MEDLINE - Academic</collection><jtitle>Chemosphere (Oxford)</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Shahid, Mohammad</au><au>Singh, Udai B.</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Enhancing spinach (Spinacia oleracea L.) resilience in pesticide-contaminated soil: Role of pesticide-tolerant Ciceribacter azotifigens and Serratia marcescens in root architecture, leaf gas exchange attributes and antioxidant response restoration</atitle><jtitle>Chemosphere (Oxford)</jtitle><addtitle>Chemosphere</addtitle><date>2024-08</date><risdate>2024</risdate><volume>361</volume><spage>142487</spage><pages>142487-</pages><artnum>142487</artnum><issn>0045-6535</issn><issn>1879-1298</issn><eissn>1879-1298</eissn><abstract>This study unveils the detoxification potential of insecticide-tolerant plant beneficial bacteria (PBB), i.e., Ciceribacter azotifigens SF1 and Serratia marcescens SRB1, in spinach treated with fipronil (FIP), profenofos (PF) and chlorantraniliprole (CLP) insecticides. Increasing insecticide doses (25–400 μg kg−1 soil) significantly curtailed germination attributes and growth of spinach cultivated at both bench-scale and in greenhouse experiments. Profenofos at 400 μg kg−1 exhibited maximum inhibitory effects and reduced germination by 55%; root and shoot length by 78% and 81%, respectively; dry matter accumulation in roots and shoots by 79% and 62%, respectively; leaf number by 87% and leaf area by 56%. Insecticide application caused morphological distortion in root tips/surfaces, increased levels of oxidative stress, and cell death in spinach. Application of insecticide-tolerant SF1 and SRB1 strains relieved insecticide pressure resulting in overall improvement in growth and physiology of spinach grown under insecticide stress. Ciceribacter azotifigens improved germination rate (10%); root biomass (53%); shoot biomass (25%); leaf area (10%); Chl-a (45%), Chl-b (36%) and carotenoid (48%) contents of spinach at 25 μg CLP kg−1 soil. PBB inoculation reinvigorated the stressed spinach and modulated the synthesis of phytochemicals, proline, malondialdehyde (MDA), superoxide anions (O2•–), and hydrogen peroxide (H2O2). Scanning electron microscopy (SEM) revealed recovery in root tip morphology and stomatal openings on abaxial leaf surfaces of PBB-inoculated spinach grown with insecticides. Ciceribacter azotifigens inoculation significantly increased intrinsic water use efficiency, transpiration rate, vapor pressure deficit, intracellular CO2 concentration, photosynthetic rate, and stomatal conductance in spinach exposed to 25 μg FIP kg−1. Also, C. azotifigens and S. marcescens modulated the antioxidant defense systems of insecticide-treated spinach. Bacterial strains were strongly colonized to root surfaces of insecticide-stressed spinach seedlings as revealed under SEM. The identification of insecticide-tolerant PBBs such as C. azotifigens and S. marcescens hold the potential for alleviating abiotic stress to spinach, thereby fostering enhanced and safe production within polluted agroecosystems.
[Display omitted]
•Insecticides showed differential toxicity to Spinacia oleracea (L.) seedlings.•Insecticide-tolerant PGPR strains-mediated phytotoxicity alleviation was reported.•PGPR improved leaf gas-exchange attributes and stomatal behavior under stress.•PGPR-mediated reduction in insecticide-induced oxidative stress and ROS generation in spinach.•Successful colonization and establishment of strains in stressed spinach rhizosphere.</abstract><cop>England</cop><pub>Elsevier Ltd</pub><pmid>38821129</pmid><doi>10.1016/j.chemosphere.2024.142487</doi><orcidid>https://orcid.org/0000-0002-2443-9451</orcidid></addata></record> |
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subjects | Antioxidant defence enzymes Antioxidants - metabolism Bacillaceae - metabolism Bacillaceae - physiology Biodegradation, Environmental Gas exchange attributes Germination - drug effects Insecticide-tolerant PGPR Insecticides - toxicity Oxidative Stress - drug effects Pesticides - metabolism Pesticides - toxicity Photosynthesis - drug effects Plant Leaves - drug effects Plant Roots - drug effects Plant Roots - microbiology Root colonization and biofilm formation Serratia marcescens - drug effects Serratia marcescens - metabolism Serratia marcescens - physiology Soil - chemistry Soil Microbiology Soil Pollutants - metabolism Soil Pollutants - toxicity Spinacia oleracea (L.) Spinacia oleracea - drug effects Spinacia oleracea - metabolism Spinacia oleracea - physiology Stomatal behavior |
title | Enhancing spinach (Spinacia oleracea L.) resilience in pesticide-contaminated soil: Role of pesticide-tolerant Ciceribacter azotifigens and Serratia marcescens in root architecture, leaf gas exchange attributes and antioxidant response restoration |
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