Vacuolar H+-Pyrophosphatase and Cytosolic Soluble Pyrophosphatases Cooperatively Regulate Pyrophosphate Levels in Arabidopsis thaliana

Inorganic pyrophosphate (PPi) is a phosphate donor and energy source. Many metabolic reactions that generate PPi are suppressed by high levels of PPi. Here, we investigated how proper levels of cytosolic PPi are maintained, focusing on soluble pyrophosphatases (AtPPa1 to AtPPa5; hereafter PPa1 to PP...

Full description

Saved in:
Bibliographic Details
Published in:The Plant cell 2018-05, Vol.30 (5), p.1040-1061
Main Authors: Segami, Shoji, Tomoyama, Takaaki, Sakamoto, Shingo, Gunji, Shizuka, Fukuda, Mayu, Kinoshita, Satoru, Mitsuda, Nobutaka, Ferjani, Ali, Maeshima, Masayoshi
Format: Article
Language:English
Subjects:
Arabidopsis thaliana
Cell walls
Cellulose
Cytosol
Dwarfism
Homeostasis
Hydrogen
Inorganic pyrophosphatase
Isoenzymes
Metabolism
Mutants
Nuclei
Phenotypes
Pyrophosphatase
Starch
Yeast
Citations: Items that cite this one
Online Access:Get full text
Tags: Add Tag
No Tags, Be the first to tag this record!
cited_by cdi_FETCH-LOGICAL-c500t-c11f1f77d1c5ff1cefa5c75c6ee600c1d594e46f63e41c08f3d9f72c7dbef4f83
cites
container_end_page 1061
container_issue 5
container_start_page 1040
container_title The Plant cell
container_volume 30
creator Segami, Shoji
Tomoyama, Takaaki
Sakamoto, Shingo
Gunji, Shizuka
Fukuda, Mayu
Kinoshita, Satoru
Mitsuda, Nobutaka
Ferjani, Ali
Maeshima, Masayoshi
description Inorganic pyrophosphate (PPi) is a phosphate donor and energy source. Many metabolic reactions that generate PPi are suppressed by high levels of PPi. Here, we investigated how proper levels of cytosolic PPi are maintained, focusing on soluble pyrophosphatases (AtPPa1 to AtPPa5; hereafter PPa1 to PPa5) and vacuolar H+-pyrophosphatase (H+-PPase, AtVHP1/FUGU5) in Arabidopsis thaliana. In planta, five PPa isozymes tagged with GFP were detected in the cytosol and nuclei. Immunochemical analyses revealed a high abundance of PPa1 and the absence of PPa3 in vegetative tissue. In addition, the heterologous expression of each PPa restored growth in a soluble PPase-defective yeast strain. Although the quadruple knockout mutant plant ppa1 ppa2 ppa4 ppa5 showed no obvious phenotypes, H+-PPase and PPa1 double mutants (fugu5 ppa1) exhibited significant phenotypes, including dwarfism, high PPi concentrations, ectopic starch accumulation, decreased cellulose and callose levels, and structural cell wall defects. Altered cell arrangements and weakened cell walls in the root tip were particularly evident in fugu5 ppa1 and were more severe than in fugu5. Our results indicate that H+-PPase is essential for maintaining adequate PPi levels and that the cytosolic PPa isozymes, particularly PPa1, prevent increases in PPi concentrations to toxic levels. We discuss fugu5 ppa1 phenotypes in relation to metabolic reactions and PPi homeostasis.
doi_str_mv 10.1105/tpc.17.00911
format article
fullrecord <record><control><sourceid>jstor_pubme</sourceid><recordid>TN_cdi_pubmedcentral_primary_oai_pubmedcentral_nih_gov_6002195</recordid><sourceformat>XML</sourceformat><sourcesystem>PC</sourcesystem><jstor_id>90022329</jstor_id><sourcerecordid>90022329</sourcerecordid><originalsourceid>FETCH-LOGICAL-c500t-c11f1f77d1c5ff1cefa5c75c6ee600c1d594e46f63e41c08f3d9f72c7dbef4f83</originalsourceid><addsrcrecordid>eNpdkU-LFDEUxIMo7rp686oEPGqPeelOZ3IRlkFdYUDxH95CJv2ykyHbaZP0wnwBP7dZZx1cT-9B_agqKEKeAlsAMPG6THYBcsGYArhHTkG0vOFq-eN-_VnHmq4XcEIe5bxjjIEE9ZCccNUraKE9Jb--GzvHYBK9eNl82qc4bWOetqaYjNSMA13tS8wxeEu_xDBvAtL_qExXMU6YTPHXGPb0M17OwZS7HNI1VjVTP9LzZDZ-iFP2mZatCd6M5jF54EzI-OT2npFv795-XV0064_vP6zO140VjJXGAjhwUg5ghXNg0RlhpbA9Ys-YhUGoDrve9S12YNnStYNykls5bNB1btmekTcH32neXOFgcSzJBD0lf2XSXkfj9V1l9Ft9Ga91teegRDV4cWuQ4s8Zc9G7OKexdtacCS5AcriJeXWgbIo5J3THBGD6ZjVdV9Mg9Z_VKv7831ZH-O9MFXh2AHa5xHTUVS3FW67a3xjuojc</addsrcrecordid><sourcetype>Open Access Repository</sourcetype><iscdi>true</iscdi><recordtype>article</recordtype><pqid>2052517218</pqid></control><display><type>article</type><title>Vacuolar H+-Pyrophosphatase and Cytosolic Soluble Pyrophosphatases Cooperatively Regulate Pyrophosphate Levels in Arabidopsis thaliana</title><source>JSTOR Archival Journals and Primary Sources Collection</source><source>Oxford Journals - Connect here FIRST to enable access</source><creator>Segami, Shoji ; Tomoyama, Takaaki ; Sakamoto, Shingo ; Gunji, Shizuka ; Fukuda, Mayu ; Kinoshita, Satoru ; Mitsuda, Nobutaka ; Ferjani, Ali ; Maeshima, Masayoshi</creator><creatorcontrib>Segami, Shoji ; Tomoyama, Takaaki ; Sakamoto, Shingo ; Gunji, Shizuka ; Fukuda, Mayu ; Kinoshita, Satoru ; Mitsuda, Nobutaka ; Ferjani, Ali ; Maeshima, Masayoshi</creatorcontrib><description>Inorganic pyrophosphate (PPi) is a phosphate donor and energy source. Many metabolic reactions that generate PPi are suppressed by high levels of PPi. Here, we investigated how proper levels of cytosolic PPi are maintained, focusing on soluble pyrophosphatases (AtPPa1 to AtPPa5; hereafter PPa1 to PPa5) and vacuolar H+-pyrophosphatase (H+-PPase, AtVHP1/FUGU5) in Arabidopsis thaliana. In planta, five PPa isozymes tagged with GFP were detected in the cytosol and nuclei. Immunochemical analyses revealed a high abundance of PPa1 and the absence of PPa3 in vegetative tissue. In addition, the heterologous expression of each PPa restored growth in a soluble PPase-defective yeast strain. Although the quadruple knockout mutant plant ppa1 ppa2 ppa4 ppa5 showed no obvious phenotypes, H+-PPase and PPa1 double mutants (fugu5 ppa1) exhibited significant phenotypes, including dwarfism, high PPi concentrations, ectopic starch accumulation, decreased cellulose and callose levels, and structural cell wall defects. Altered cell arrangements and weakened cell walls in the root tip were particularly evident in fugu5 ppa1 and were more severe than in fugu5. Our results indicate that H+-PPase is essential for maintaining adequate PPi levels and that the cytosolic PPa isozymes, particularly PPa1, prevent increases in PPi concentrations to toxic levels. We discuss fugu5 ppa1 phenotypes in relation to metabolic reactions and PPi homeostasis.</description><identifier>ISSN: 1040-4651</identifier><identifier>EISSN: 1532-298X</identifier><identifier>DOI: 10.1105/tpc.17.00911</identifier><identifier>PMID: 29691313</identifier><language>eng</language><publisher>United States: American Society of Plant Biologists</publisher><subject>Arabidopsis thaliana ; Cell walls ; Cellulose ; Cytosol ; Dwarfism ; Homeostasis ; Hydrogen ; Inorganic pyrophosphatase ; Isoenzymes ; Metabolism ; Mutants ; Nuclei ; Phenotypes ; Pyrophosphatase ; Starch ; Yeast</subject><ispartof>The Plant cell, 2018-05, Vol.30 (5), p.1040-1061</ispartof><rights>2018 American Society of Plant Biologists</rights><rights>2018 American Society of Plant Biologists. All rights reserved.</rights><rights>Copyright American Society of Plant Biologists May 2018</rights><rights>2018 American Society of Plant Biologists. All rights reserved. 2018</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c500t-c11f1f77d1c5ff1cefa5c75c6ee600c1d594e46f63e41c08f3d9f72c7dbef4f83</citedby><orcidid>0000-0003-4687-5630 ; 0000-0002-1611-5481 ; 0000-0003-1157-3261</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.jstor.org/stable/pdf/90022329$$EPDF$$P50$$Gjstor$$H</linktopdf><linktohtml>$$Uhttps://www.jstor.org/stable/90022329$$EHTML$$P50$$Gjstor$$H</linktohtml><link.rule.ids>230,315,786,790,891,27957,27958,58593,58826</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/29691313$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Segami, Shoji</creatorcontrib><creatorcontrib>Tomoyama, Takaaki</creatorcontrib><creatorcontrib>Sakamoto, Shingo</creatorcontrib><creatorcontrib>Gunji, Shizuka</creatorcontrib><creatorcontrib>Fukuda, Mayu</creatorcontrib><creatorcontrib>Kinoshita, Satoru</creatorcontrib><creatorcontrib>Mitsuda, Nobutaka</creatorcontrib><creatorcontrib>Ferjani, Ali</creatorcontrib><creatorcontrib>Maeshima, Masayoshi</creatorcontrib><title>Vacuolar H+-Pyrophosphatase and Cytosolic Soluble Pyrophosphatases Cooperatively Regulate Pyrophosphate Levels in Arabidopsis thaliana</title><title>The Plant cell</title><addtitle>Plant Cell</addtitle><description>Inorganic pyrophosphate (PPi) is a phosphate donor and energy source. Many metabolic reactions that generate PPi are suppressed by high levels of PPi. Here, we investigated how proper levels of cytosolic PPi are maintained, focusing on soluble pyrophosphatases (AtPPa1 to AtPPa5; hereafter PPa1 to PPa5) and vacuolar H+-pyrophosphatase (H+-PPase, AtVHP1/FUGU5) in Arabidopsis thaliana. In planta, five PPa isozymes tagged with GFP were detected in the cytosol and nuclei. Immunochemical analyses revealed a high abundance of PPa1 and the absence of PPa3 in vegetative tissue. In addition, the heterologous expression of each PPa restored growth in a soluble PPase-defective yeast strain. Although the quadruple knockout mutant plant ppa1 ppa2 ppa4 ppa5 showed no obvious phenotypes, H+-PPase and PPa1 double mutants (fugu5 ppa1) exhibited significant phenotypes, including dwarfism, high PPi concentrations, ectopic starch accumulation, decreased cellulose and callose levels, and structural cell wall defects. Altered cell arrangements and weakened cell walls in the root tip were particularly evident in fugu5 ppa1 and were more severe than in fugu5. Our results indicate that H+-PPase is essential for maintaining adequate PPi levels and that the cytosolic PPa isozymes, particularly PPa1, prevent increases in PPi concentrations to toxic levels. We discuss fugu5 ppa1 phenotypes in relation to metabolic reactions and PPi homeostasis.</description><subject>Arabidopsis thaliana</subject><subject>Cell walls</subject><subject>Cellulose</subject><subject>Cytosol</subject><subject>Dwarfism</subject><subject>Homeostasis</subject><subject>Hydrogen</subject><subject>Inorganic pyrophosphatase</subject><subject>Isoenzymes</subject><subject>Metabolism</subject><subject>Mutants</subject><subject>Nuclei</subject><subject>Phenotypes</subject><subject>Pyrophosphatase</subject><subject>Starch</subject><subject>Yeast</subject><issn>1040-4651</issn><issn>1532-298X</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2018</creationdate><recordtype>article</recordtype><recordid>eNpdkU-LFDEUxIMo7rp686oEPGqPeelOZ3IRlkFdYUDxH95CJv2ykyHbaZP0wnwBP7dZZx1cT-9B_agqKEKeAlsAMPG6THYBcsGYArhHTkG0vOFq-eN-_VnHmq4XcEIe5bxjjIEE9ZCccNUraKE9Jb--GzvHYBK9eNl82qc4bWOetqaYjNSMA13tS8wxeEu_xDBvAtL_qExXMU6YTPHXGPb0M17OwZS7HNI1VjVTP9LzZDZ-iFP2mZatCd6M5jF54EzI-OT2npFv795-XV0064_vP6zO140VjJXGAjhwUg5ghXNg0RlhpbA9Ys-YhUGoDrve9S12YNnStYNykls5bNB1btmekTcH32neXOFgcSzJBD0lf2XSXkfj9V1l9Ft9Ga91teegRDV4cWuQ4s8Zc9G7OKexdtacCS5AcriJeXWgbIo5J3THBGD6ZjVdV9Mg9Z_VKv7831ZH-O9MFXh2AHa5xHTUVS3FW67a3xjuojc</recordid><startdate>20180501</startdate><enddate>20180501</enddate><creator>Segami, Shoji</creator><creator>Tomoyama, Takaaki</creator><creator>Sakamoto, Shingo</creator><creator>Gunji, Shizuka</creator><creator>Fukuda, Mayu</creator><creator>Kinoshita, Satoru</creator><creator>Mitsuda, Nobutaka</creator><creator>Ferjani, Ali</creator><creator>Maeshima, Masayoshi</creator><general>American Society of Plant Biologists</general><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>4T-</scope><scope>7QO</scope><scope>7TM</scope><scope>8FD</scope><scope>FR3</scope><scope>K9.</scope><scope>P64</scope><scope>RC3</scope><scope>5PM</scope><orcidid>https://orcid.org/0000-0003-4687-5630</orcidid><orcidid>https://orcid.org/0000-0002-1611-5481</orcidid><orcidid>https://orcid.org/0000-0003-1157-3261</orcidid></search><sort><creationdate>20180501</creationdate><title>Vacuolar H+-Pyrophosphatase and Cytosolic Soluble Pyrophosphatases Cooperatively Regulate Pyrophosphate Levels in Arabidopsis thaliana</title><author>Segami, Shoji ; Tomoyama, Takaaki ; Sakamoto, Shingo ; Gunji, Shizuka ; Fukuda, Mayu ; Kinoshita, Satoru ; Mitsuda, Nobutaka ; Ferjani, Ali ; Maeshima, Masayoshi</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c500t-c11f1f77d1c5ff1cefa5c75c6ee600c1d594e46f63e41c08f3d9f72c7dbef4f83</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2018</creationdate><topic>Arabidopsis thaliana</topic><topic>Cell walls</topic><topic>Cellulose</topic><topic>Cytosol</topic><topic>Dwarfism</topic><topic>Homeostasis</topic><topic>Hydrogen</topic><topic>Inorganic pyrophosphatase</topic><topic>Isoenzymes</topic><topic>Metabolism</topic><topic>Mutants</topic><topic>Nuclei</topic><topic>Phenotypes</topic><topic>Pyrophosphatase</topic><topic>Starch</topic><topic>Yeast</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Segami, Shoji</creatorcontrib><creatorcontrib>Tomoyama, Takaaki</creatorcontrib><creatorcontrib>Sakamoto, Shingo</creatorcontrib><creatorcontrib>Gunji, Shizuka</creatorcontrib><creatorcontrib>Fukuda, Mayu</creatorcontrib><creatorcontrib>Kinoshita, Satoru</creatorcontrib><creatorcontrib>Mitsuda, Nobutaka</creatorcontrib><creatorcontrib>Ferjani, Ali</creatorcontrib><creatorcontrib>Maeshima, Masayoshi</creatorcontrib><collection>PubMed</collection><collection>CrossRef</collection><collection>Docstoc</collection><collection>Biotechnology Research Abstracts</collection><collection>Nucleic Acids Abstracts</collection><collection>Technology Research Database</collection><collection>Engineering Research Database</collection><collection>ProQuest Health &amp; Medical Complete (Alumni)</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>Genetics Abstracts</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>The Plant cell</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Segami, Shoji</au><au>Tomoyama, Takaaki</au><au>Sakamoto, Shingo</au><au>Gunji, Shizuka</au><au>Fukuda, Mayu</au><au>Kinoshita, Satoru</au><au>Mitsuda, Nobutaka</au><au>Ferjani, Ali</au><au>Maeshima, Masayoshi</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Vacuolar H+-Pyrophosphatase and Cytosolic Soluble Pyrophosphatases Cooperatively Regulate Pyrophosphate Levels in Arabidopsis thaliana</atitle><jtitle>The Plant cell</jtitle><addtitle>Plant Cell</addtitle><date>2018-05-01</date><risdate>2018</risdate><volume>30</volume><issue>5</issue><spage>1040</spage><epage>1061</epage><pages>1040-1061</pages><issn>1040-4651</issn><eissn>1532-298X</eissn><notes>www.plantcell.org/cgi/doi/10.1105/tpc.17.00911</notes><notes>The authors responsible for distribution of materials integral to the findings presented in this article in accordance with the policy described in the Instructions for Authors (www.plantcell.org) are: Shoji Segami (segami@agr.nagoya-u.ac.jp) and Masayoshi Maeshima (maeshima@agr.nagoya-u.ac.jp).</notes><abstract>Inorganic pyrophosphate (PPi) is a phosphate donor and energy source. Many metabolic reactions that generate PPi are suppressed by high levels of PPi. Here, we investigated how proper levels of cytosolic PPi are maintained, focusing on soluble pyrophosphatases (AtPPa1 to AtPPa5; hereafter PPa1 to PPa5) and vacuolar H+-pyrophosphatase (H+-PPase, AtVHP1/FUGU5) in Arabidopsis thaliana. In planta, five PPa isozymes tagged with GFP were detected in the cytosol and nuclei. Immunochemical analyses revealed a high abundance of PPa1 and the absence of PPa3 in vegetative tissue. In addition, the heterologous expression of each PPa restored growth in a soluble PPase-defective yeast strain. Although the quadruple knockout mutant plant ppa1 ppa2 ppa4 ppa5 showed no obvious phenotypes, H+-PPase and PPa1 double mutants (fugu5 ppa1) exhibited significant phenotypes, including dwarfism, high PPi concentrations, ectopic starch accumulation, decreased cellulose and callose levels, and structural cell wall defects. Altered cell arrangements and weakened cell walls in the root tip were particularly evident in fugu5 ppa1 and were more severe than in fugu5. Our results indicate that H+-PPase is essential for maintaining adequate PPi levels and that the cytosolic PPa isozymes, particularly PPa1, prevent increases in PPi concentrations to toxic levels. We discuss fugu5 ppa1 phenotypes in relation to metabolic reactions and PPi homeostasis.</abstract><cop>United States</cop><pub>American Society of Plant Biologists</pub><pmid>29691313</pmid><doi>10.1105/tpc.17.00911</doi><tpages>22</tpages><orcidid>https://orcid.org/0000-0003-4687-5630</orcidid><orcidid>https://orcid.org/0000-0002-1611-5481</orcidid><orcidid>https://orcid.org/0000-0003-1157-3261</orcidid><oa>free_for_read</oa></addata></record>
fulltext fulltext
identifier ISSN: 1040-4651
ispartof The Plant cell, 2018-05, Vol.30 (5), p.1040-1061
issn 1040-4651
1532-298X
language eng
recordid cdi_pubmedcentral_primary_oai_pubmedcentral_nih_gov_6002195
source JSTOR Archival Journals and Primary Sources Collection; Oxford Journals - Connect here FIRST to enable access
subjects Arabidopsis thaliana
Cell walls
Cellulose
Cytosol
Dwarfism
Homeostasis
Hydrogen
Inorganic pyrophosphatase
Isoenzymes
Metabolism
Mutants
Nuclei
Phenotypes
Pyrophosphatase
Starch
Yeast
title Vacuolar H+-Pyrophosphatase and Cytosolic Soluble Pyrophosphatases Cooperatively Regulate Pyrophosphate Levels in Arabidopsis thaliana
url http://sfxeu10.hosted.exlibrisgroup.com/loughborough?ctx_ver=Z39.88-2004&ctx_enc=info:ofi/enc:UTF-8&ctx_tim=2024-09-21T08%3A17%3A27IST&url_ver=Z39.88-2004&url_ctx_fmt=infofi/fmt:kev:mtx:ctx&rfr_id=info:sid/primo.exlibrisgroup.com:primo3-Article-jstor_pubme&rft_val_fmt=info:ofi/fmt:kev:mtx:journal&rft.genre=article&rft.atitle=Vacuolar%20H+-Pyrophosphatase%20and%20Cytosolic%20Soluble%20Pyrophosphatases%20Cooperatively%20Regulate%20Pyrophosphate%20Levels%20in%20Arabidopsis%20thaliana&rft.jtitle=The%20Plant%20cell&rft.au=Segami,%20Shoji&rft.date=2018-05-01&rft.volume=30&rft.issue=5&rft.spage=1040&rft.epage=1061&rft.pages=1040-1061&rft.issn=1040-4651&rft.eissn=1532-298X&rft_id=info:doi/10.1105/tpc.17.00911&rft_dat=%3Cjstor_pubme%3E90022329%3C/jstor_pubme%3E%3Cgrp_id%3Ecdi_FETCH-LOGICAL-c500t-c11f1f77d1c5ff1cefa5c75c6ee600c1d594e46f63e41c08f3d9f72c7dbef4f83%3C/grp_id%3E%3Coa%3E%3C/oa%3E%3Curl%3E%3C/url%3E&rft_id=info:oai/&rft_pqid=2052517218&rft_id=info:pmid/29691313&rft_jstor_id=90022329&rfr_iscdi=true