Growth-promoting bacteria and arbuscular mycorrhizal fungus enhance maize tolerance to saline stress

Climate change intensifies soil salinization and jeopardizes the development of crops worldwide. The accumulation of salts in plant tissue activates the defense system and triggers ethylene production thus restricting cell division. We hypothesize that the inoculation of plant growth-promoting bacte...

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Veröffentlicht in:Microbiological research 2024-07, Vol.284, p.127708-127708, Article 127708
Hauptverfasser: de Carvalho Neta, Stella Jorge, Araújo, Victor Lucas Vieira Prudêncio, Fracetto, Felipe José Cury, da Silva, Cintia Caroline Gouveia, de Souza, Edivan Rodrigues, Silva, William Ramos, Lumini, Erica, Fracetto, Giselle Gomes Monteiro
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container_title Microbiological research
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creator de Carvalho Neta, Stella Jorge
Araújo, Victor Lucas Vieira Prudêncio
Fracetto, Felipe José Cury
da Silva, Cintia Caroline Gouveia
de Souza, Edivan Rodrigues
Silva, William Ramos
Lumini, Erica
Fracetto, Giselle Gomes Monteiro
description Climate change intensifies soil salinization and jeopardizes the development of crops worldwide. The accumulation of salts in plant tissue activates the defense system and triggers ethylene production thus restricting cell division. We hypothesize that the inoculation of plant growth-promoting bacteria (PGPB) producing ACC (1-aminocyclopropane-1-carboxylate) deaminase favors the development of arbuscular mycorrhizal fungi (AMF), promoting the growth of maize plants under saline stress. We investigated the efficacy of individual inoculation of PGPB, which produce ACC deaminase, as well as the co-inoculation of PGPB with Rhizophagus clarus on maize plant growth subjected to saline stress. The isolates were acquired from the bulk and rhizospheric soil of Mimosa bimucronata (DC.) Kuntze in a temporary pond located in Pernambuco State, Brazil. In the first greenhouse experiment, 10 halophilic PGPB were inoculated into maize at 0, 40 and 80 mM of NaCl, and in the second experiment, the PGPB that showed the best performance were co-inoculated with R. clarus in maize under the same conditions as in the first experiment. Individual PGPB inoculation benefited the number of leaves, stem diameter, root and shoot dry mass, and the photosynthetic pigments. Inoculation with PGPB 28–10 Pseudarthrobacter enclensis, 24–1 P. enclensis and 52 P. chlorophenolicus increased the chlorophyll a content by 138%, 171%, and 324% at 0, 40 and 80 mM NaCl, respectively, comparing to the non-inoculated control. We also highlight that the inoculation of PGPB 28–10, 28–7 Arthrobacter sp. and 52 increased the content of chlorophyll b by 72%, 98%, and 280% and carotenoids by 82%, 98%, and 290% at 0, 40 and 80 mM of NaCl, respectively. Co-inoculation with PGPB 28–7, 46–1 Leclercia tamurae, 70 Artrobacter sp., and 79–1 Micrococcus endophyticus significantly increased the rate of mycorrhizal colonization by roughly 50%. Furthermore, co-inoculation promoted a decrease in the accumulation of Na and K extracted from plant tissue, with an increase in salt concentration, from 40 mM to 80 mM, also favoring the establishment and development of R. clarus. In addition, co-inoculation of these PGPB with R. clarus promoted maize growth and increased plant biomass through osmoregulation and protection of the photosynthetic apparatus. The tripartite symbiosis (plant-fungus-bacterium) is likely to reprogram metabolic pathways that improve maize growth and crop yield, suggesting that the AMF-PGPB consortium c
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The accumulation of salts in plant tissue activates the defense system and triggers ethylene production thus restricting cell division. We hypothesize that the inoculation of plant growth-promoting bacteria (PGPB) producing ACC (1-aminocyclopropane-1-carboxylate) deaminase favors the development of arbuscular mycorrhizal fungi (AMF), promoting the growth of maize plants under saline stress. We investigated the efficacy of individual inoculation of PGPB, which produce ACC deaminase, as well as the co-inoculation of PGPB with Rhizophagus clarus on maize plant growth subjected to saline stress. The isolates were acquired from the bulk and rhizospheric soil of Mimosa bimucronata (DC.) Kuntze in a temporary pond located in Pernambuco State, Brazil. In the first greenhouse experiment, 10 halophilic PGPB were inoculated into maize at 0, 40 and 80 mM of NaCl, and in the second experiment, the PGPB that showed the best performance were co-inoculated with R. clarus in maize under the same conditions as in the first experiment. Individual PGPB inoculation benefited the number of leaves, stem diameter, root and shoot dry mass, and the photosynthetic pigments. Inoculation with PGPB 28–10 Pseudarthrobacter enclensis, 24–1 P. enclensis and 52 P. chlorophenolicus increased the chlorophyll a content by 138%, 171%, and 324% at 0, 40 and 80 mM NaCl, respectively, comparing to the non-inoculated control. We also highlight that the inoculation of PGPB 28–10, 28–7 Arthrobacter sp. and 52 increased the content of chlorophyll b by 72%, 98%, and 280% and carotenoids by 82%, 98%, and 290% at 0, 40 and 80 mM of NaCl, respectively. Co-inoculation with PGPB 28–7, 46–1 Leclercia tamurae, 70 Artrobacter sp., and 79–1 Micrococcus endophyticus significantly increased the rate of mycorrhizal colonization by roughly 50%. Furthermore, co-inoculation promoted a decrease in the accumulation of Na and K extracted from plant tissue, with an increase in salt concentration, from 40 mM to 80 mM, also favoring the establishment and development of R. clarus. In addition, co-inoculation of these PGPB with R. clarus promoted maize growth and increased plant biomass through osmoregulation and protection of the photosynthetic apparatus. The tripartite symbiosis (plant-fungus-bacterium) is likely to reprogram metabolic pathways that improve maize growth and crop yield, suggesting that the AMF-PGPB consortium can minimize damages caused by saline stress. [Display omitted] •PGPB from temporary ponds in the tropical semiarid alleviate salt stress in maize.•PGPB protected the photosynthetic apparatus of maize under saline stress.•PGPB enhanced the development of mycorrhiza in maize under saline stress.•Co-inoculation of PGPB with R. clarus promoted maize growth through osmoregulation.</description><identifier>ISSN: 0944-5013</identifier><identifier>EISSN: 1618-0623</identifier><identifier>DOI: 10.1016/j.micres.2024.127708</identifier><identifier>PMID: 38599021</identifier><language>eng</language><publisher>Germany: Elsevier GmbH</publisher><subject>Bacteria - classification ; Bacteria - isolation &amp; purification ; Bacteria - metabolism ; Carbon-Carbon Lyases - metabolism ; Chlorophyll - metabolism ; Glomeromycota - physiology ; Mycorrhizae - physiology ; Photosynthesis ; Plant Leaves - microbiology ; Plant Roots - growth &amp; development ; Plant Roots - microbiology ; Rhizosphere ; Salt Stress ; Salt Tolerance ; Sodium Chloride - metabolism ; Soil - chemistry ; Soil Microbiology ; Soil salinity. 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All rights reserved.</rights><lds50>peer_reviewed</lds50><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c362t-37fae5b62cf863b94fdb132c3f31958634910697b3d202c9577f71f4ddb38f4a3</citedby><cites>FETCH-LOGICAL-c362t-37fae5b62cf863b94fdb132c3f31958634910697b3d202c9577f71f4ddb38f4a3</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktohtml>$$Uhttps://dx.doi.org/10.1016/j.micres.2024.127708$$EHTML$$P50$$Gelsevier$$H</linktohtml><link.rule.ids>315,782,786,3552,27931,27932,46002</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/38599021$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>de Carvalho Neta, Stella Jorge</creatorcontrib><creatorcontrib>Araújo, Victor Lucas Vieira Prudêncio</creatorcontrib><creatorcontrib>Fracetto, Felipe José Cury</creatorcontrib><creatorcontrib>da Silva, Cintia Caroline Gouveia</creatorcontrib><creatorcontrib>de Souza, Edivan Rodrigues</creatorcontrib><creatorcontrib>Silva, William Ramos</creatorcontrib><creatorcontrib>Lumini, Erica</creatorcontrib><creatorcontrib>Fracetto, Giselle Gomes Monteiro</creatorcontrib><title>Growth-promoting bacteria and arbuscular mycorrhizal fungus enhance maize tolerance to saline stress</title><title>Microbiological research</title><addtitle>Microbiol Res</addtitle><description>Climate change intensifies soil salinization and jeopardizes the development of crops worldwide. The accumulation of salts in plant tissue activates the defense system and triggers ethylene production thus restricting cell division. We hypothesize that the inoculation of plant growth-promoting bacteria (PGPB) producing ACC (1-aminocyclopropane-1-carboxylate) deaminase favors the development of arbuscular mycorrhizal fungi (AMF), promoting the growth of maize plants under saline stress. We investigated the efficacy of individual inoculation of PGPB, which produce ACC deaminase, as well as the co-inoculation of PGPB with Rhizophagus clarus on maize plant growth subjected to saline stress. The isolates were acquired from the bulk and rhizospheric soil of Mimosa bimucronata (DC.) Kuntze in a temporary pond located in Pernambuco State, Brazil. In the first greenhouse experiment, 10 halophilic PGPB were inoculated into maize at 0, 40 and 80 mM of NaCl, and in the second experiment, the PGPB that showed the best performance were co-inoculated with R. clarus in maize under the same conditions as in the first experiment. Individual PGPB inoculation benefited the number of leaves, stem diameter, root and shoot dry mass, and the photosynthetic pigments. Inoculation with PGPB 28–10 Pseudarthrobacter enclensis, 24–1 P. enclensis and 52 P. chlorophenolicus increased the chlorophyll a content by 138%, 171%, and 324% at 0, 40 and 80 mM NaCl, respectively, comparing to the non-inoculated control. We also highlight that the inoculation of PGPB 28–10, 28–7 Arthrobacter sp. and 52 increased the content of chlorophyll b by 72%, 98%, and 280% and carotenoids by 82%, 98%, and 290% at 0, 40 and 80 mM of NaCl, respectively. Co-inoculation with PGPB 28–7, 46–1 Leclercia tamurae, 70 Artrobacter sp., and 79–1 Micrococcus endophyticus significantly increased the rate of mycorrhizal colonization by roughly 50%. Furthermore, co-inoculation promoted a decrease in the accumulation of Na and K extracted from plant tissue, with an increase in salt concentration, from 40 mM to 80 mM, also favoring the establishment and development of R. clarus. In addition, co-inoculation of these PGPB with R. clarus promoted maize growth and increased plant biomass through osmoregulation and protection of the photosynthetic apparatus. The tripartite symbiosis (plant-fungus-bacterium) is likely to reprogram metabolic pathways that improve maize growth and crop yield, suggesting that the AMF-PGPB consortium can minimize damages caused by saline stress. [Display omitted] •PGPB from temporary ponds in the tropical semiarid alleviate salt stress in maize.•PGPB protected the photosynthetic apparatus of maize under saline stress.•PGPB enhanced the development of mycorrhiza in maize under saline stress.•Co-inoculation of PGPB with R. clarus promoted maize growth through osmoregulation.</description><subject>Bacteria - classification</subject><subject>Bacteria - isolation &amp; purification</subject><subject>Bacteria - metabolism</subject><subject>Carbon-Carbon Lyases - metabolism</subject><subject>Chlorophyll - metabolism</subject><subject>Glomeromycota - physiology</subject><subject>Mycorrhizae - physiology</subject><subject>Photosynthesis</subject><subject>Plant Leaves - microbiology</subject><subject>Plant Roots - growth &amp; development</subject><subject>Plant Roots - microbiology</subject><subject>Rhizosphere</subject><subject>Salt Stress</subject><subject>Salt Tolerance</subject><subject>Sodium Chloride - metabolism</subject><subject>Soil - chemistry</subject><subject>Soil Microbiology</subject><subject>Soil salinity. Bioprotection. Tripartite interaction. ACC deaminase</subject><subject>Zea mays - growth &amp; development</subject><subject>Zea mays - microbiology</subject><issn>0944-5013</issn><issn>1618-0623</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2024</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNp9kE1rGzEQhkVJaVy3_6AEHXNZV1_7oUuhmCQNGHppz0IrjWKZ3VUiaRucXx8l6-aY0zDD-87M-yD0jZINJbT5ftiM3kRIG0aY2FDWtqT7gFa0oV1FGsbP0IpIIaqaUH6OPqd0IIQK2bFP6Jx3tZSE0RWyNzE85n11H8MYsp_ucK9Nhug11pPFOvZzMvOgIx6PJsS49096wG6e7uaEYdrryQAetX8CnMMA8bXPASc9-AlwyuXD9AV9dHpI8PVU1-jv9dWf7a9q9_vmdvtzVxnesFzx1mmo-4YZ1zW8l8LZnnJmuONU1mUkJCWNbHtuS2Yj67Z1LXXC2p53Tmi-RpfL3pLmYYaU1eiTgWHQE4Q5KU54y0twURepWKQmhpQiOHUf_ajjUVGiXviqg1r4qhe-auFbbBenC3M_gn0z_QdaBD8WAZSc_zxElYyHAsX6CCYrG_z7F54BOyyPVQ</recordid><startdate>202407</startdate><enddate>202407</enddate><creator>de Carvalho Neta, Stella Jorge</creator><creator>Araújo, Victor Lucas Vieira Prudêncio</creator><creator>Fracetto, Felipe José Cury</creator><creator>da Silva, Cintia Caroline Gouveia</creator><creator>de Souza, Edivan Rodrigues</creator><creator>Silva, William Ramos</creator><creator>Lumini, Erica</creator><creator>Fracetto, Giselle Gomes Monteiro</creator><general>Elsevier GmbH</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></search><sort><creationdate>202407</creationdate><title>Growth-promoting bacteria and arbuscular mycorrhizal fungus enhance maize tolerance to saline stress</title><author>de Carvalho Neta, Stella Jorge ; Araújo, Victor Lucas Vieira Prudêncio ; Fracetto, Felipe José Cury ; da Silva, Cintia Caroline Gouveia ; de Souza, Edivan Rodrigues ; Silva, William Ramos ; Lumini, Erica ; Fracetto, Giselle Gomes Monteiro</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c362t-37fae5b62cf863b94fdb132c3f31958634910697b3d202c9577f71f4ddb38f4a3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2024</creationdate><topic>Bacteria - classification</topic><topic>Bacteria - isolation &amp; purification</topic><topic>Bacteria - metabolism</topic><topic>Carbon-Carbon Lyases - metabolism</topic><topic>Chlorophyll - metabolism</topic><topic>Glomeromycota - physiology</topic><topic>Mycorrhizae - physiology</topic><topic>Photosynthesis</topic><topic>Plant Leaves - microbiology</topic><topic>Plant Roots - growth &amp; development</topic><topic>Plant Roots - microbiology</topic><topic>Rhizosphere</topic><topic>Salt Stress</topic><topic>Salt Tolerance</topic><topic>Sodium Chloride - metabolism</topic><topic>Soil - chemistry</topic><topic>Soil Microbiology</topic><topic>Soil salinity. 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ACC deaminase</topic><topic>Zea mays - growth &amp; development</topic><topic>Zea mays - microbiology</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>de Carvalho Neta, Stella Jorge</creatorcontrib><creatorcontrib>Araújo, Victor Lucas Vieira Prudêncio</creatorcontrib><creatorcontrib>Fracetto, Felipe José Cury</creatorcontrib><creatorcontrib>da Silva, Cintia Caroline Gouveia</creatorcontrib><creatorcontrib>de Souza, Edivan Rodrigues</creatorcontrib><creatorcontrib>Silva, William Ramos</creatorcontrib><creatorcontrib>Lumini, Erica</creatorcontrib><creatorcontrib>Fracetto, Giselle Gomes Monteiro</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>Microbiological research</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>de Carvalho Neta, Stella Jorge</au><au>Araújo, Victor Lucas Vieira Prudêncio</au><au>Fracetto, Felipe José Cury</au><au>da Silva, Cintia Caroline Gouveia</au><au>de Souza, Edivan Rodrigues</au><au>Silva, William Ramos</au><au>Lumini, Erica</au><au>Fracetto, Giselle Gomes Monteiro</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Growth-promoting bacteria and arbuscular mycorrhizal fungus enhance maize tolerance to saline stress</atitle><jtitle>Microbiological research</jtitle><addtitle>Microbiol Res</addtitle><date>2024-07</date><risdate>2024</risdate><volume>284</volume><spage>127708</spage><epage>127708</epage><pages>127708-127708</pages><artnum>127708</artnum><issn>0944-5013</issn><eissn>1618-0623</eissn><abstract>Climate change intensifies soil salinization and jeopardizes the development of crops worldwide. The accumulation of salts in plant tissue activates the defense system and triggers ethylene production thus restricting cell division. We hypothesize that the inoculation of plant growth-promoting bacteria (PGPB) producing ACC (1-aminocyclopropane-1-carboxylate) deaminase favors the development of arbuscular mycorrhizal fungi (AMF), promoting the growth of maize plants under saline stress. We investigated the efficacy of individual inoculation of PGPB, which produce ACC deaminase, as well as the co-inoculation of PGPB with Rhizophagus clarus on maize plant growth subjected to saline stress. The isolates were acquired from the bulk and rhizospheric soil of Mimosa bimucronata (DC.) Kuntze in a temporary pond located in Pernambuco State, Brazil. In the first greenhouse experiment, 10 halophilic PGPB were inoculated into maize at 0, 40 and 80 mM of NaCl, and in the second experiment, the PGPB that showed the best performance were co-inoculated with R. clarus in maize under the same conditions as in the first experiment. Individual PGPB inoculation benefited the number of leaves, stem diameter, root and shoot dry mass, and the photosynthetic pigments. Inoculation with PGPB 28–10 Pseudarthrobacter enclensis, 24–1 P. enclensis and 52 P. chlorophenolicus increased the chlorophyll a content by 138%, 171%, and 324% at 0, 40 and 80 mM NaCl, respectively, comparing to the non-inoculated control. We also highlight that the inoculation of PGPB 28–10, 28–7 Arthrobacter sp. and 52 increased the content of chlorophyll b by 72%, 98%, and 280% and carotenoids by 82%, 98%, and 290% at 0, 40 and 80 mM of NaCl, respectively. Co-inoculation with PGPB 28–7, 46–1 Leclercia tamurae, 70 Artrobacter sp., and 79–1 Micrococcus endophyticus significantly increased the rate of mycorrhizal colonization by roughly 50%. Furthermore, co-inoculation promoted a decrease in the accumulation of Na and K extracted from plant tissue, with an increase in salt concentration, from 40 mM to 80 mM, also favoring the establishment and development of R. clarus. In addition, co-inoculation of these PGPB with R. clarus promoted maize growth and increased plant biomass through osmoregulation and protection of the photosynthetic apparatus. The tripartite symbiosis (plant-fungus-bacterium) is likely to reprogram metabolic pathways that improve maize growth and crop yield, suggesting that the AMF-PGPB consortium can minimize damages caused by saline stress. [Display omitted] •PGPB from temporary ponds in the tropical semiarid alleviate salt stress in maize.•PGPB protected the photosynthetic apparatus of maize under saline stress.•PGPB enhanced the development of mycorrhiza in maize under saline stress.•Co-inoculation of PGPB with R. clarus promoted maize growth through osmoregulation.</abstract><cop>Germany</cop><pub>Elsevier GmbH</pub><pmid>38599021</pmid><doi>10.1016/j.micres.2024.127708</doi><tpages>1</tpages></addata></record>
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subjects Bacteria - classification
Bacteria - isolation & purification
Bacteria - metabolism
Carbon-Carbon Lyases - metabolism
Chlorophyll - metabolism
Glomeromycota - physiology
Mycorrhizae - physiology
Photosynthesis
Plant Leaves - microbiology
Plant Roots - growth & development
Plant Roots - microbiology
Rhizosphere
Salt Stress
Salt Tolerance
Sodium Chloride - metabolism
Soil - chemistry
Soil Microbiology
Soil salinity. Bioprotection. Tripartite interaction. ACC deaminase
Zea mays - growth & development
Zea mays - microbiology
title Growth-promoting bacteria and arbuscular mycorrhizal fungus enhance maize tolerance to saline stress
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