Proton exudation mediated by GmVP2 has widespread effects on plant growth, remobilization of soil phosphorus, and the structure of the rhizosphere microbial community

Increased root secretion of H+ is a known strategy in plant adaption to low phosphorus (P) stress as it enhances mobilization of sparingly soluble P sources in the soil. However, our knowledge of the full effects induced by this enhanced acidification of the rhizosphere remains incomplete. In this s...

Ausführliche Beschreibung

Gespeichert in:
Bibliographische Detailangaben
Veröffentlicht in:Journal of experimental botany 2023-02, Vol.74 (3), p.1140-1156
Hauptverfasser: Xie, Baoxing, Chen, Qianqian, Lu, Xing, Chen, Kang, Yang, Yuesheng, Tian, Jiang, Liang, Cuiyue
Format: Artikel
Sprache:eng
Schlagworte:
Online-Zugang:Volltext
Tags: Tag hinzufügen
Keine Tags, Fügen Sie den ersten Tag hinzu!
container_end_page 1156
container_issue 3
container_start_page 1140
container_title Journal of experimental botany
container_volume 74
creator Xie, Baoxing
Chen, Qianqian
Lu, Xing
Chen, Kang
Yang, Yuesheng
Tian, Jiang
Liang, Cuiyue
description Increased root secretion of H+ is a known strategy in plant adaption to low phosphorus (P) stress as it enhances mobilization of sparingly soluble P sources in the soil. However, our knowledge of the full effects induced by this enhanced acidification of the rhizosphere remains incomplete. In this study we found that P deficiency increased the net H+ flux rate from soybean (Glycine max) roots. Among the eight H+-pyrophosphatase (GmVP) genes in the soybean genome, GmVP2 showed the highest expression level under low P conditions. Transient expression of a GmVP2-GFP construct in tobacco (Nicotiana tabacum) leaves, together with functional characterization of GmVP2 in transgenic soybean hairy roots demonstrated that it encodes a plasma-membrane transporter that mediates H+ exudation. Overexpression of GmVP2 in Arabidopsis resulted in enhanced root H+ exudation, promoted root growth, and improved the utilization of sparingly soluble Ca-P. The improved root growth caused by GmVP2-overexpression might be due to the differential expression of genes related to hormone and flavonoid metabolism, and to root development. Overexpression of GmVP2 also changed the structure of the rhizospheric microbial community, as reflected by a preferential accumulation of Acidobacteria. Overall, our results suggest that GmVP2 mediates H+ exudation in the root response to Pi starvation, and that this influences plant growth, the mobilization sparingly soluble P-sources, and the structure of the microbial community in a coordinated manner.
doi_str_mv 10.1093/jxb/erac476
format Article
fullrecord <record><control><sourceid>pubmed_cross</sourceid><recordid>TN_cdi_crossref_primary_10_1093_jxb_erac476</recordid><sourceformat>XML</sourceformat><sourcesystem>PC</sourcesystem><sourcerecordid>36455868</sourcerecordid><originalsourceid>FETCH-LOGICAL-c256t-cc5acf5a9b1590374d37d203f1c36679eadb89569848a6713ef9f495b1d472703</originalsourceid><addsrcrecordid>eNo9kF1LwzAUhoMobk6vvJfcu7qkadLmUoZOQXAX6m1J82Ez2rUkKfv4Qf5OMza9OJzDy8PL4QHgFqMHjDiZrbbVTDshs5ydgTHOGErSjOBzMEYoTRPEaT4CV96vEEIUUXoJRoRllBasGIOfpetCt4Z6OygRbLxarawIWsFqBxft1zKFtfBwY5X2vdNCQW2MlsHDyPaNWAf47bpNqKfQ6barbGP3x6LOQN_ZBvZ15-O4wU-hWCsYag19cIMMg9MH6hC42u4PmI5Ra6WLRaKBsmvbYW3D7hpcGNF4fXPaE_D5_PQxf0ne3hev88e3RKaUhURKKqShgleYckTyTJFcpYgYLAljOY_vVwWnjBdZIViOiTbcZJxWWGV5miMyAffH3viB906bsne2FW5XYlQebJfRdnmyHem7I90PVdT2z_7pJb8GnYCo</addsrcrecordid><sourcetype>Aggregation Database</sourcetype><iscdi>true</iscdi><recordtype>article</recordtype></control><display><type>article</type><title>Proton exudation mediated by GmVP2 has widespread effects on plant growth, remobilization of soil phosphorus, and the structure of the rhizosphere microbial community</title><source>Oxford University Press Journals All Titles (1996-Current)</source><source>MEDLINE</source><source>Elektronische Zeitschriftenbibliothek - Frei zugängliche E-Journals</source><source>Alma/SFX Local Collection</source><creator>Xie, Baoxing ; Chen, Qianqian ; Lu, Xing ; Chen, Kang ; Yang, Yuesheng ; Tian, Jiang ; Liang, Cuiyue</creator><creatorcontrib>Xie, Baoxing ; Chen, Qianqian ; Lu, Xing ; Chen, Kang ; Yang, Yuesheng ; Tian, Jiang ; Liang, Cuiyue</creatorcontrib><description>Increased root secretion of H+ is a known strategy in plant adaption to low phosphorus (P) stress as it enhances mobilization of sparingly soluble P sources in the soil. However, our knowledge of the full effects induced by this enhanced acidification of the rhizosphere remains incomplete. In this study we found that P deficiency increased the net H+ flux rate from soybean (Glycine max) roots. Among the eight H+-pyrophosphatase (GmVP) genes in the soybean genome, GmVP2 showed the highest expression level under low P conditions. Transient expression of a GmVP2-GFP construct in tobacco (Nicotiana tabacum) leaves, together with functional characterization of GmVP2 in transgenic soybean hairy roots demonstrated that it encodes a plasma-membrane transporter that mediates H+ exudation. Overexpression of GmVP2 in Arabidopsis resulted in enhanced root H+ exudation, promoted root growth, and improved the utilization of sparingly soluble Ca-P. The improved root growth caused by GmVP2-overexpression might be due to the differential expression of genes related to hormone and flavonoid metabolism, and to root development. Overexpression of GmVP2 also changed the structure of the rhizospheric microbial community, as reflected by a preferential accumulation of Acidobacteria. Overall, our results suggest that GmVP2 mediates H+ exudation in the root response to Pi starvation, and that this influences plant growth, the mobilization sparingly soluble P-sources, and the structure of the microbial community in a coordinated manner.</description><identifier>ISSN: 0022-0957</identifier><identifier>EISSN: 1460-2431</identifier><identifier>DOI: 10.1093/jxb/erac476</identifier><identifier>PMID: 36455868</identifier><language>eng</language><publisher>England</publisher><subject>Arabidopsis - physiology ; Phosphorus - metabolism ; Plant Roots - metabolism ; Protons ; Rhizosphere ; Soil - chemistry</subject><ispartof>Journal of experimental botany, 2023-02, Vol.74 (3), p.1140-1156</ispartof><rights>The Author(s) 2022. Published by Oxford University Press on behalf of the Society for Experimental Biology. All rights reserved. For permissions, please email: journals.permissions@oup.com.</rights><lds50>peer_reviewed</lds50><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c256t-cc5acf5a9b1590374d37d203f1c36679eadb89569848a6713ef9f495b1d472703</citedby><cites>FETCH-LOGICAL-c256t-cc5acf5a9b1590374d37d203f1c36679eadb89569848a6713ef9f495b1d472703</cites><orcidid>0000-0002-2962-1500 ; 0000-0001-9587-0030 ; 0000-0001-7136-5531</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><link.rule.ids>314,776,780,27901,27902</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/36455868$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Xie, Baoxing</creatorcontrib><creatorcontrib>Chen, Qianqian</creatorcontrib><creatorcontrib>Lu, Xing</creatorcontrib><creatorcontrib>Chen, Kang</creatorcontrib><creatorcontrib>Yang, Yuesheng</creatorcontrib><creatorcontrib>Tian, Jiang</creatorcontrib><creatorcontrib>Liang, Cuiyue</creatorcontrib><title>Proton exudation mediated by GmVP2 has widespread effects on plant growth, remobilization of soil phosphorus, and the structure of the rhizosphere microbial community</title><title>Journal of experimental botany</title><addtitle>J Exp Bot</addtitle><description>Increased root secretion of H+ is a known strategy in plant adaption to low phosphorus (P) stress as it enhances mobilization of sparingly soluble P sources in the soil. However, our knowledge of the full effects induced by this enhanced acidification of the rhizosphere remains incomplete. In this study we found that P deficiency increased the net H+ flux rate from soybean (Glycine max) roots. Among the eight H+-pyrophosphatase (GmVP) genes in the soybean genome, GmVP2 showed the highest expression level under low P conditions. Transient expression of a GmVP2-GFP construct in tobacco (Nicotiana tabacum) leaves, together with functional characterization of GmVP2 in transgenic soybean hairy roots demonstrated that it encodes a plasma-membrane transporter that mediates H+ exudation. Overexpression of GmVP2 in Arabidopsis resulted in enhanced root H+ exudation, promoted root growth, and improved the utilization of sparingly soluble Ca-P. The improved root growth caused by GmVP2-overexpression might be due to the differential expression of genes related to hormone and flavonoid metabolism, and to root development. Overexpression of GmVP2 also changed the structure of the rhizospheric microbial community, as reflected by a preferential accumulation of Acidobacteria. Overall, our results suggest that GmVP2 mediates H+ exudation in the root response to Pi starvation, and that this influences plant growth, the mobilization sparingly soluble P-sources, and the structure of the microbial community in a coordinated manner.</description><subject>Arabidopsis - physiology</subject><subject>Phosphorus - metabolism</subject><subject>Plant Roots - metabolism</subject><subject>Protons</subject><subject>Rhizosphere</subject><subject>Soil - chemistry</subject><issn>0022-0957</issn><issn>1460-2431</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2023</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNo9kF1LwzAUhoMobk6vvJfcu7qkadLmUoZOQXAX6m1J82Ez2rUkKfv4Qf5OMza9OJzDy8PL4QHgFqMHjDiZrbbVTDshs5ydgTHOGErSjOBzMEYoTRPEaT4CV96vEEIUUXoJRoRllBasGIOfpetCt4Z6OygRbLxarawIWsFqBxft1zKFtfBwY5X2vdNCQW2MlsHDyPaNWAf47bpNqKfQ6barbGP3x6LOQN_ZBvZ15-O4wU-hWCsYag19cIMMg9MH6hC42u4PmI5Ra6WLRaKBsmvbYW3D7hpcGNF4fXPaE_D5_PQxf0ne3hev88e3RKaUhURKKqShgleYckTyTJFcpYgYLAljOY_vVwWnjBdZIViOiTbcZJxWWGV5miMyAffH3viB906bsne2FW5XYlQebJfRdnmyHem7I90PVdT2z_7pJb8GnYCo</recordid><startdate>20230205</startdate><enddate>20230205</enddate><creator>Xie, Baoxing</creator><creator>Chen, Qianqian</creator><creator>Lu, Xing</creator><creator>Chen, Kang</creator><creator>Yang, Yuesheng</creator><creator>Tian, Jiang</creator><creator>Liang, Cuiyue</creator><scope>CGR</scope><scope>CUY</scope><scope>CVF</scope><scope>ECM</scope><scope>EIF</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><orcidid>https://orcid.org/0000-0002-2962-1500</orcidid><orcidid>https://orcid.org/0000-0001-9587-0030</orcidid><orcidid>https://orcid.org/0000-0001-7136-5531</orcidid></search><sort><creationdate>20230205</creationdate><title>Proton exudation mediated by GmVP2 has widespread effects on plant growth, remobilization of soil phosphorus, and the structure of the rhizosphere microbial community</title><author>Xie, Baoxing ; Chen, Qianqian ; Lu, Xing ; Chen, Kang ; Yang, Yuesheng ; Tian, Jiang ; Liang, Cuiyue</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c256t-cc5acf5a9b1590374d37d203f1c36679eadb89569848a6713ef9f495b1d472703</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2023</creationdate><topic>Arabidopsis - physiology</topic><topic>Phosphorus - metabolism</topic><topic>Plant Roots - metabolism</topic><topic>Protons</topic><topic>Rhizosphere</topic><topic>Soil - chemistry</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Xie, Baoxing</creatorcontrib><creatorcontrib>Chen, Qianqian</creatorcontrib><creatorcontrib>Lu, Xing</creatorcontrib><creatorcontrib>Chen, Kang</creatorcontrib><creatorcontrib>Yang, Yuesheng</creatorcontrib><creatorcontrib>Tian, Jiang</creatorcontrib><creatorcontrib>Liang, Cuiyue</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><jtitle>Journal of experimental botany</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Xie, Baoxing</au><au>Chen, Qianqian</au><au>Lu, Xing</au><au>Chen, Kang</au><au>Yang, Yuesheng</au><au>Tian, Jiang</au><au>Liang, Cuiyue</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Proton exudation mediated by GmVP2 has widespread effects on plant growth, remobilization of soil phosphorus, and the structure of the rhizosphere microbial community</atitle><jtitle>Journal of experimental botany</jtitle><addtitle>J Exp Bot</addtitle><date>2023-02-05</date><risdate>2023</risdate><volume>74</volume><issue>3</issue><spage>1140</spage><epage>1156</epage><pages>1140-1156</pages><issn>0022-0957</issn><eissn>1460-2431</eissn><abstract>Increased root secretion of H+ is a known strategy in plant adaption to low phosphorus (P) stress as it enhances mobilization of sparingly soluble P sources in the soil. However, our knowledge of the full effects induced by this enhanced acidification of the rhizosphere remains incomplete. In this study we found that P deficiency increased the net H+ flux rate from soybean (Glycine max) roots. Among the eight H+-pyrophosphatase (GmVP) genes in the soybean genome, GmVP2 showed the highest expression level under low P conditions. Transient expression of a GmVP2-GFP construct in tobacco (Nicotiana tabacum) leaves, together with functional characterization of GmVP2 in transgenic soybean hairy roots demonstrated that it encodes a plasma-membrane transporter that mediates H+ exudation. Overexpression of GmVP2 in Arabidopsis resulted in enhanced root H+ exudation, promoted root growth, and improved the utilization of sparingly soluble Ca-P. The improved root growth caused by GmVP2-overexpression might be due to the differential expression of genes related to hormone and flavonoid metabolism, and to root development. Overexpression of GmVP2 also changed the structure of the rhizospheric microbial community, as reflected by a preferential accumulation of Acidobacteria. Overall, our results suggest that GmVP2 mediates H+ exudation in the root response to Pi starvation, and that this influences plant growth, the mobilization sparingly soluble P-sources, and the structure of the microbial community in a coordinated manner.</abstract><cop>England</cop><pmid>36455868</pmid><doi>10.1093/jxb/erac476</doi><tpages>17</tpages><orcidid>https://orcid.org/0000-0002-2962-1500</orcidid><orcidid>https://orcid.org/0000-0001-9587-0030</orcidid><orcidid>https://orcid.org/0000-0001-7136-5531</orcidid></addata></record>
fulltext fulltext
identifier ISSN: 0022-0957
ispartof Journal of experimental botany, 2023-02, Vol.74 (3), p.1140-1156
issn 0022-0957
1460-2431
language eng
recordid cdi_crossref_primary_10_1093_jxb_erac476
source Oxford University Press Journals All Titles (1996-Current); MEDLINE; Elektronische Zeitschriftenbibliothek - Frei zugängliche E-Journals; Alma/SFX Local Collection
subjects Arabidopsis - physiology
Phosphorus - metabolism
Plant Roots - metabolism
Protons
Rhizosphere
Soil - chemistry
title Proton exudation mediated by GmVP2 has widespread effects on plant growth, remobilization of soil phosphorus, and the structure of the rhizosphere microbial community
url https://sfx.bib-bvb.de/sfx_tum?ctx_ver=Z39.88-2004&ctx_enc=info:ofi/enc:UTF-8&ctx_tim=2025-02-05T03%3A34%3A38IST&url_ver=Z39.88-2004&url_ctx_fmt=infofi/fmt:kev:mtx:ctx&rfr_id=info:sid/primo.exlibrisgroup.com:primo3-Article-pubmed_cross&rft_val_fmt=info:ofi/fmt:kev:mtx:journal&rft.genre=article&rft.atitle=Proton%20exudation%20mediated%20by%20GmVP2%20has%20widespread%20effects%20on%20plant%20growth,%20remobilization%20of%20soil%20phosphorus,%20and%20the%20structure%20of%20the%20rhizosphere%20microbial%20community&rft.jtitle=Journal%20of%20experimental%20botany&rft.au=Xie,%20Baoxing&rft.date=2023-02-05&rft.volume=74&rft.issue=3&rft.spage=1140&rft.epage=1156&rft.pages=1140-1156&rft.issn=0022-0957&rft.eissn=1460-2431&rft_id=info:doi/10.1093/jxb/erac476&rft_dat=%3Cpubmed_cross%3E36455868%3C/pubmed_cross%3E%3Curl%3E%3C/url%3E&disable_directlink=true&sfx.directlink=off&sfx.report_link=0&rft_id=info:oai/&rft_id=info:pmid/36455868&rfr_iscdi=true