Polyamine metabolizing rhizobacteria Pseudomonas sp. GBPI_506 modulates hormone signaling to enhance lateral roots and nicotine biosynthesis in Nicotiana benthamiana
Beneficial rhizobacteria in the soil are important drivers of plant health and growth. In this study, we provide the draft genome of a root colonizing and auxin-producing Pseudomonas sp. strain GBPI_506. The bacterium was investigated for its contribution in the growth of Nicotiana benthamiana (Nb)...
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Veröffentlicht in: | Plant physiology and biochemistry 2023-02, Vol.195, p.193-205 |
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description | Beneficial rhizobacteria in the soil are important drivers of plant health and growth. In this study, we provide the draft genome of a root colonizing and auxin-producing Pseudomonas sp. strain GBPI_506. The bacterium was investigated for its contribution in the growth of Nicotiana benthamiana (Nb) and biosynthesis of nicotine. The bacterium showed chemotaxis towards root exudates potentially mediated by putrescine, a polyamine compound, to colonize the roots of Nb. Application of the bacterium with the roots of Nb, increased plant biomass and total soluble sugars in the leaves, and promoted lateral root (LR) development as compared to the un-inoculated plants. Confocal analysis using transgenic (DR5:GFP) Arabidopsis showed increased auxin trafficking in the LR of inoculated plants. Upregulation of nicotine biosynthesis genes and genes involved in salicylic acid (SA) and jasmonic acid (JA) signaling in the roots of inoculated plants suggested increased nicotine biosynthesis as a result of bacterial application. An increased JA content in roots and nicotine accumulation in leaves provided evidence on JA-mediated upregulation of nicotine biosynthesis in the bacterized plants. The findings suggested that the bacterial root colonization triggered networking between auxin, SA, and JA to facilitate LR development leading to enhanced plant growth and nicotine biosynthesis in Nb.
•Study presents two-way interactions between a Pseudomonas sp. GBPI_506 and N. benthamiana.•Auxin secreting GBPI_506 promoted plant growth and enhanced lateral roots development.•GBPI_506 colonized plant roots through polyamine driven chemotaxis in the rhizosphere.•GBPI_506 regulated jasmonic acid signaling and enhanced nicotine accumulation in plant. |
doi_str_mv | 10.1016/j.plaphy.2023.01.010 |
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•Study presents two-way interactions between a Pseudomonas sp. GBPI_506 and N. benthamiana.•Auxin secreting GBPI_506 promoted plant growth and enhanced lateral roots development.•GBPI_506 colonized plant roots through polyamine driven chemotaxis in the rhizosphere.•GBPI_506 regulated jasmonic acid signaling and enhanced nicotine accumulation in plant.</description><identifier>ISSN: 0981-9428</identifier><identifier>EISSN: 1873-2690</identifier><identifier>DOI: 10.1016/j.plaphy.2023.01.010</identifier><identifier>PMID: 36641943</identifier><language>eng</language><publisher>France: Elsevier Masson SAS</publisher><subject>Arabidopsis - genetics ; Confocal microscopy ; Cyclopentanes ; Hormones ; Indoleacetic Acids ; Nicotiana - genetics ; Nicotine ; Oxylipins ; Phytohormones ; Plant Roots - genetics ; Plant-bacterial interactions ; Polyamines ; Pseudomonas ; Putrescine ; Rhizosphere ; Root architecture ; Salicylic Acid</subject><ispartof>Plant physiology and biochemistry, 2023-02, Vol.195, p.193-205</ispartof><rights>2023 Elsevier Masson SAS</rights><rights>Copyright © 2023 Elsevier Masson SAS. All rights reserved.</rights><lds50>peer_reviewed</lds50><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c362t-89772477827f1eeeec70841ad767ec94329597f49b881118c5cb6500a6733173</citedby><cites>FETCH-LOGICAL-c362t-89772477827f1eeeec70841ad767ec94329597f49b881118c5cb6500a6733173</cites><orcidid>0000-0002-7554-6599 ; 0000-0003-0142-3999</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktohtml>$$Uhttps://dx.doi.org/10.1016/j.plaphy.2023.01.010$$EHTML$$P50$$Gelsevier$$H</linktohtml><link.rule.ids>314,780,784,3550,27924,27925,45995</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/36641943$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Jain, Rahul</creatorcontrib><creatorcontrib>Bhardwaj, Priyanka</creatorcontrib><creatorcontrib>Guleria, Shweta</creatorcontrib><creatorcontrib>Pandey, Anita</creatorcontrib><creatorcontrib>Kumar, Sanjay</creatorcontrib><title>Polyamine metabolizing rhizobacteria Pseudomonas sp. GBPI_506 modulates hormone signaling to enhance lateral roots and nicotine biosynthesis in Nicotiana benthamiana</title><title>Plant physiology and biochemistry</title><addtitle>Plant Physiol Biochem</addtitle><description>Beneficial rhizobacteria in the soil are important drivers of plant health and growth. In this study, we provide the draft genome of a root colonizing and auxin-producing Pseudomonas sp. strain GBPI_506. The bacterium was investigated for its contribution in the growth of Nicotiana benthamiana (Nb) and biosynthesis of nicotine. The bacterium showed chemotaxis towards root exudates potentially mediated by putrescine, a polyamine compound, to colonize the roots of Nb. Application of the bacterium with the roots of Nb, increased plant biomass and total soluble sugars in the leaves, and promoted lateral root (LR) development as compared to the un-inoculated plants. Confocal analysis using transgenic (DR5:GFP) Arabidopsis showed increased auxin trafficking in the LR of inoculated plants. Upregulation of nicotine biosynthesis genes and genes involved in salicylic acid (SA) and jasmonic acid (JA) signaling in the roots of inoculated plants suggested increased nicotine biosynthesis as a result of bacterial application. An increased JA content in roots and nicotine accumulation in leaves provided evidence on JA-mediated upregulation of nicotine biosynthesis in the bacterized plants. The findings suggested that the bacterial root colonization triggered networking between auxin, SA, and JA to facilitate LR development leading to enhanced plant growth and nicotine biosynthesis in Nb.
•Study presents two-way interactions between a Pseudomonas sp. GBPI_506 and N. benthamiana.•Auxin secreting GBPI_506 promoted plant growth and enhanced lateral roots development.•GBPI_506 colonized plant roots through polyamine driven chemotaxis in the rhizosphere.•GBPI_506 regulated jasmonic acid signaling and enhanced nicotine accumulation in plant.</description><subject>Arabidopsis - genetics</subject><subject>Confocal microscopy</subject><subject>Cyclopentanes</subject><subject>Hormones</subject><subject>Indoleacetic Acids</subject><subject>Nicotiana - genetics</subject><subject>Nicotine</subject><subject>Oxylipins</subject><subject>Phytohormones</subject><subject>Plant Roots - genetics</subject><subject>Plant-bacterial interactions</subject><subject>Polyamines</subject><subject>Pseudomonas</subject><subject>Putrescine</subject><subject>Rhizosphere</subject><subject>Root architecture</subject><subject>Salicylic Acid</subject><issn>0981-9428</issn><issn>1873-2690</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2023</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNp9UcFu3CAQRVWrZpP2D6qKYy92AXsBXyq1UZtEito95I4wno1ZYXABR9r8T_8zuJv2GDQSI-bNPN48hD5QUlNC-edDPTs9j8eaEdbUhJYgr9CGStFUjHfkNdqQTtKqa5k8Q-cpHQghrBXNW3TWcN7Srm026M8uuKOerAc8QdZ9cPbR-nscR_sYem0yRKvxLsEyhCl4nXCaa3z1bXejtoTjKQyL0xkSHkMsdcDJ3nvt1hE5YPCj9gbwCona4RhCTlj7AXtrQl5ZexvS0ecRkk3Yevzzb0F7jXsoz-VrJX-H3uy1S_D--b5Adz--311eV7e_rm4uv95WpuEsV7IToigUkok9hXKMILKlehBcgCl6WbftxL7teikppdJsTc-3hGgumoaK5gJ9Oo2dY_i9QMpqssmAc9pDWJJignNSVid4gbYnqIkhpQh7NUc76XhUlKjVH3VQJ3_U6o8itAQpbR-fGZZ-guF_0z9DCuDLCQBF5oOFqJKxUHY42AgmqyHYlxmeAEmSpiM</recordid><startdate>202302</startdate><enddate>202302</enddate><creator>Jain, Rahul</creator><creator>Bhardwaj, Priyanka</creator><creator>Guleria, Shweta</creator><creator>Pandey, Anita</creator><creator>Kumar, Sanjay</creator><general>Elsevier Masson SAS</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/0000-0002-7554-6599</orcidid><orcidid>https://orcid.org/0000-0003-0142-3999</orcidid></search><sort><creationdate>202302</creationdate><title>Polyamine metabolizing rhizobacteria Pseudomonas sp. GBPI_506 modulates hormone signaling to enhance lateral roots and nicotine biosynthesis in Nicotiana benthamiana</title><author>Jain, Rahul ; Bhardwaj, Priyanka ; Guleria, Shweta ; Pandey, Anita ; Kumar, Sanjay</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c362t-89772477827f1eeeec70841ad767ec94329597f49b881118c5cb6500a6733173</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2023</creationdate><topic>Arabidopsis - genetics</topic><topic>Confocal microscopy</topic><topic>Cyclopentanes</topic><topic>Hormones</topic><topic>Indoleacetic Acids</topic><topic>Nicotiana - genetics</topic><topic>Nicotine</topic><topic>Oxylipins</topic><topic>Phytohormones</topic><topic>Plant Roots - genetics</topic><topic>Plant-bacterial interactions</topic><topic>Polyamines</topic><topic>Pseudomonas</topic><topic>Putrescine</topic><topic>Rhizosphere</topic><topic>Root architecture</topic><topic>Salicylic Acid</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Jain, Rahul</creatorcontrib><creatorcontrib>Bhardwaj, Priyanka</creatorcontrib><creatorcontrib>Guleria, Shweta</creatorcontrib><creatorcontrib>Pandey, Anita</creatorcontrib><creatorcontrib>Kumar, Sanjay</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>Plant physiology and biochemistry</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Jain, Rahul</au><au>Bhardwaj, Priyanka</au><au>Guleria, Shweta</au><au>Pandey, Anita</au><au>Kumar, Sanjay</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Polyamine metabolizing rhizobacteria Pseudomonas sp. GBPI_506 modulates hormone signaling to enhance lateral roots and nicotine biosynthesis in Nicotiana benthamiana</atitle><jtitle>Plant physiology and biochemistry</jtitle><addtitle>Plant Physiol Biochem</addtitle><date>2023-02</date><risdate>2023</risdate><volume>195</volume><spage>193</spage><epage>205</epage><pages>193-205</pages><issn>0981-9428</issn><eissn>1873-2690</eissn><abstract>Beneficial rhizobacteria in the soil are important drivers of plant health and growth. In this study, we provide the draft genome of a root colonizing and auxin-producing Pseudomonas sp. strain GBPI_506. The bacterium was investigated for its contribution in the growth of Nicotiana benthamiana (Nb) and biosynthesis of nicotine. The bacterium showed chemotaxis towards root exudates potentially mediated by putrescine, a polyamine compound, to colonize the roots of Nb. Application of the bacterium with the roots of Nb, increased plant biomass and total soluble sugars in the leaves, and promoted lateral root (LR) development as compared to the un-inoculated plants. Confocal analysis using transgenic (DR5:GFP) Arabidopsis showed increased auxin trafficking in the LR of inoculated plants. Upregulation of nicotine biosynthesis genes and genes involved in salicylic acid (SA) and jasmonic acid (JA) signaling in the roots of inoculated plants suggested increased nicotine biosynthesis as a result of bacterial application. An increased JA content in roots and nicotine accumulation in leaves provided evidence on JA-mediated upregulation of nicotine biosynthesis in the bacterized plants. The findings suggested that the bacterial root colonization triggered networking between auxin, SA, and JA to facilitate LR development leading to enhanced plant growth and nicotine biosynthesis in Nb.
•Study presents two-way interactions between a Pseudomonas sp. GBPI_506 and N. benthamiana.•Auxin secreting GBPI_506 promoted plant growth and enhanced lateral roots development.•GBPI_506 colonized plant roots through polyamine driven chemotaxis in the rhizosphere.•GBPI_506 regulated jasmonic acid signaling and enhanced nicotine accumulation in plant.</abstract><cop>France</cop><pub>Elsevier Masson SAS</pub><pmid>36641943</pmid><doi>10.1016/j.plaphy.2023.01.010</doi><tpages>13</tpages><orcidid>https://orcid.org/0000-0002-7554-6599</orcidid><orcidid>https://orcid.org/0000-0003-0142-3999</orcidid></addata></record> |
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subjects | Arabidopsis - genetics Confocal microscopy Cyclopentanes Hormones Indoleacetic Acids Nicotiana - genetics Nicotine Oxylipins Phytohormones Plant Roots - genetics Plant-bacterial interactions Polyamines Pseudomonas Putrescine Rhizosphere Root architecture Salicylic Acid |
title | Polyamine metabolizing rhizobacteria Pseudomonas sp. GBPI_506 modulates hormone signaling to enhance lateral roots and nicotine biosynthesis in Nicotiana benthamiana |
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