Arabidopsis phosphatidylglycerophosphate phosphatase 1 involved in phosphatidylglycerol biosynthesis and photosynthetic function
Summary Phosphatidylglycerol (PG) is an indispensable lipid constituent of photosynthetic membranes, whose function is essential in photosynthetic activity. In higher plants, the biological function of the last step of PG biosynthesis remains elusive because an enzyme catalyzing this reaction step,...
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| Veröffentlicht in: | The Plant journal : for cell and molecular biology 2016-12, Vol.88 (6), p.1022-1037 |
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| container_title | The Plant journal : for cell and molecular biology |
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| creator | Lin, Ying‐Chen Kobayashi, Koichi Hung, Chun‐Hsien Wada, Hajime Nakamura, Yuki |
| description | Summary
Phosphatidylglycerol (PG) is an indispensable lipid constituent of photosynthetic membranes, whose function is essential in photosynthetic activity. In higher plants, the biological function of the last step of PG biosynthesis remains elusive because an enzyme catalyzing this reaction step, namely phosphatidylglycerophosphate phosphatase (PGPP), has been a missing piece in the entire glycerolipid metabolic map. Here, we report the identification and characterization of AtPGPP1 encoding a PGPP in Arabidopsis thaliana. Heterologous expression of AtPGPP1 in yeast Δgep4 complemented growth phenotype and PG‐producing activity, suggesting that AtPGPP1 encodes a functional PGPP. The GUS reporter assay showed that AtPGPP1 was preferentially expressed in hypocotyl, vasculatures, trichomes, guard cells, and stigmas. A subcellular localization study with GFP reporter indicated that AtPGPP1 is mainly localized at chloroplasts. A T‐DNA‐tagged knockout mutant of AtPGPP1, designated pgpp1‐1, showed pale green phenotype with reduced PG and chlorophyll contents but no defect in embryo development. In the pgpp1‐1 mutant, ultrastructure of plastids indicated defective development of chloroplasts and measurement of photosynthetic parameters showed impaired photosynthetic activity. These results suggest that AtPGPP1 is a primary plastidic PGPP required for PG biosynthesis and photosynthetic function in Arabidopsis.
Significance Statement
Phosphatidylglycerol (PG) is an indispensable lipid constituent of photosynthetic membranes. Here we identified the previously unknown phosphatidylglycerophosphate phosphatase that is required for the last step in PG biosynthesis. |
| doi_str_mv | 10.1111/tpj.13311 |
| format | Article |
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Phosphatidylglycerol (PG) is an indispensable lipid constituent of photosynthetic membranes, whose function is essential in photosynthetic activity. In higher plants, the biological function of the last step of PG biosynthesis remains elusive because an enzyme catalyzing this reaction step, namely phosphatidylglycerophosphate phosphatase (PGPP), has been a missing piece in the entire glycerolipid metabolic map. Here, we report the identification and characterization of AtPGPP1 encoding a PGPP in Arabidopsis thaliana. Heterologous expression of AtPGPP1 in yeast Δgep4 complemented growth phenotype and PG‐producing activity, suggesting that AtPGPP1 encodes a functional PGPP. The GUS reporter assay showed that AtPGPP1 was preferentially expressed in hypocotyl, vasculatures, trichomes, guard cells, and stigmas. A subcellular localization study with GFP reporter indicated that AtPGPP1 is mainly localized at chloroplasts. A T‐DNA‐tagged knockout mutant of AtPGPP1, designated pgpp1‐1, showed pale green phenotype with reduced PG and chlorophyll contents but no defect in embryo development. In the pgpp1‐1 mutant, ultrastructure of plastids indicated defective development of chloroplasts and measurement of photosynthetic parameters showed impaired photosynthetic activity. These results suggest that AtPGPP1 is a primary plastidic PGPP required for PG biosynthesis and photosynthetic function in Arabidopsis.
Significance Statement
Phosphatidylglycerol (PG) is an indispensable lipid constituent of photosynthetic membranes. Here we identified the previously unknown phosphatidylglycerophosphate phosphatase that is required for the last step in PG biosynthesis.</description><identifier>ISSN: 0960-7412</identifier><identifier>EISSN: 1365-313X</identifier><identifier>DOI: 10.1111/tpj.13311</identifier><identifier>PMID: 27541283</identifier><language>eng</language><publisher>England: Blackwell Publishing Ltd</publisher><subject>Arabidopsis ; Arabidopsis - enzymology ; Arabidopsis - genetics ; Arabidopsis - metabolism ; Arabidopsis Proteins - genetics ; Arabidopsis Proteins - metabolism ; Arabidopsis thaliana ; Biosynthesis ; Chlorophyll ; chloroplast ; Chloroplasts ; Chloroplasts - genetics ; Chloroplasts - metabolism ; Deoxyribonucleic acid ; DNA ; DNA, Bacterial - metabolism ; Embryos ; Gene Expression Regulation, Plant - genetics ; glycerolipid ; Guard cells ; lipid phosphate phosphatase ; Lipids ; Localization ; Membranes ; Phenotypes ; Phosphatase ; Phosphatidylglycerol ; Phosphatidylglycerols - biosynthesis ; Phosphatidylglycerols - metabolism ; phosphatidylglycerophosphate phosphatase ; Phosphoric Monoester Hydrolases - genetics ; Phosphoric Monoester Hydrolases - metabolism ; Photosynthesis ; Photosynthesis - genetics ; Photosynthesis - physiology ; Plants (botany) ; Plastids ; Stigmas (botany) ; Trichomes ; Ultrastructure ; Yeast ; Yeasts</subject><ispartof>The Plant journal : for cell and molecular biology, 2016-12, Vol.88 (6), p.1022-1037</ispartof><rights>2016 The Authors The Plant Journal © 2016 John Wiley & Sons Ltd</rights><rights>2016 The Authors The Plant Journal © 2016 John Wiley & Sons Ltd.</rights><rights>Copyright © 2016 John Wiley & Sons Ltd and the Society for Experimental Biology</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c5151-c37af101e68f41eaca5c056c975c8232b7cdebe5eb1d935b8b5883b74392735c3</citedby><cites>FETCH-LOGICAL-c5151-c37af101e68f41eaca5c056c975c8232b7cdebe5eb1d935b8b5883b74392735c3</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://onlinelibrary.wiley.com/doi/pdf/10.1111%2Ftpj.13311$$EPDF$$P50$$Gwiley$$H</linktopdf><linktohtml>$$Uhttps://onlinelibrary.wiley.com/doi/full/10.1111%2Ftpj.13311$$EHTML$$P50$$Gwiley$$H</linktohtml><link.rule.ids>314,776,780,1411,1427,27901,27902,45550,45551,46384,46808</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/27541283$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Lin, Ying‐Chen</creatorcontrib><creatorcontrib>Kobayashi, Koichi</creatorcontrib><creatorcontrib>Hung, Chun‐Hsien</creatorcontrib><creatorcontrib>Wada, Hajime</creatorcontrib><creatorcontrib>Nakamura, Yuki</creatorcontrib><title>Arabidopsis phosphatidylglycerophosphate phosphatase 1 involved in phosphatidylglycerol biosynthesis and photosynthetic function</title><title>The Plant journal : for cell and molecular biology</title><addtitle>Plant J</addtitle><description>Summary
Phosphatidylglycerol (PG) is an indispensable lipid constituent of photosynthetic membranes, whose function is essential in photosynthetic activity. In higher plants, the biological function of the last step of PG biosynthesis remains elusive because an enzyme catalyzing this reaction step, namely phosphatidylglycerophosphate phosphatase (PGPP), has been a missing piece in the entire glycerolipid metabolic map. Here, we report the identification and characterization of AtPGPP1 encoding a PGPP in Arabidopsis thaliana. Heterologous expression of AtPGPP1 in yeast Δgep4 complemented growth phenotype and PG‐producing activity, suggesting that AtPGPP1 encodes a functional PGPP. The GUS reporter assay showed that AtPGPP1 was preferentially expressed in hypocotyl, vasculatures, trichomes, guard cells, and stigmas. A subcellular localization study with GFP reporter indicated that AtPGPP1 is mainly localized at chloroplasts. A T‐DNA‐tagged knockout mutant of AtPGPP1, designated pgpp1‐1, showed pale green phenotype with reduced PG and chlorophyll contents but no defect in embryo development. In the pgpp1‐1 mutant, ultrastructure of plastids indicated defective development of chloroplasts and measurement of photosynthetic parameters showed impaired photosynthetic activity. These results suggest that AtPGPP1 is a primary plastidic PGPP required for PG biosynthesis and photosynthetic function in Arabidopsis.
Significance Statement
Phosphatidylglycerol (PG) is an indispensable lipid constituent of photosynthetic membranes. Here we identified the previously unknown phosphatidylglycerophosphate phosphatase that is required for the last step in PG biosynthesis.</description><subject>Arabidopsis</subject><subject>Arabidopsis - enzymology</subject><subject>Arabidopsis - genetics</subject><subject>Arabidopsis - metabolism</subject><subject>Arabidopsis Proteins - genetics</subject><subject>Arabidopsis Proteins - metabolism</subject><subject>Arabidopsis thaliana</subject><subject>Biosynthesis</subject><subject>Chlorophyll</subject><subject>chloroplast</subject><subject>Chloroplasts</subject><subject>Chloroplasts - genetics</subject><subject>Chloroplasts - metabolism</subject><subject>Deoxyribonucleic acid</subject><subject>DNA</subject><subject>DNA, Bacterial - metabolism</subject><subject>Embryos</subject><subject>Gene Expression Regulation, Plant - genetics</subject><subject>glycerolipid</subject><subject>Guard cells</subject><subject>lipid phosphate phosphatase</subject><subject>Lipids</subject><subject>Localization</subject><subject>Membranes</subject><subject>Phenotypes</subject><subject>Phosphatase</subject><subject>Phosphatidylglycerol</subject><subject>Phosphatidylglycerols - biosynthesis</subject><subject>Phosphatidylglycerols - metabolism</subject><subject>phosphatidylglycerophosphate phosphatase</subject><subject>Phosphoric Monoester Hydrolases - genetics</subject><subject>Phosphoric Monoester Hydrolases - metabolism</subject><subject>Photosynthesis</subject><subject>Photosynthesis - genetics</subject><subject>Photosynthesis - physiology</subject><subject>Plants (botany)</subject><subject>Plastids</subject><subject>Stigmas (botany)</subject><subject>Trichomes</subject><subject>Ultrastructure</subject><subject>Yeast</subject><subject>Yeasts</subject><issn>0960-7412</issn><issn>1365-313X</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2016</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNqNkc1O3DAUha2qqAyUBS9QReoGFgFfO_5bIkT_hEQXVGJn2Y7DeJSJQ5yAsuuj19MZWFQtqje2jj9_V9ZB6BjwGeR1PvarM6AU4A1aAOWspEDv3qIFVhyXogKyjw5SWmEMgvLqHdonguVU0gX6eTEYG-rYp5CKfhlTvzRjqOf2vp2dH-Jz5F8uTfIFFKF7jO2jr_Phb8_awoaY5m5c-o3YdPWGGnfRGFzRTJ0bQ-zeo73GtMkf7fZD9OPT1e3ll_L65vPXy4vr0jFgUDoqTAMYPJdNBd44wxxm3CnBnCSUWOFqbz3zFmpFmZWWSUmtqKgigjJHD9HJ1tsP8WHyadTrkJxvW9P5OCUNkimGMQf1HyitlBKSkIx-_ANdxWno8kc0IbwCIBzz16g8tsJKKl5l6nRLuSGmNPhG90NYm2HWgPWmZ5171r97zuyHnXGya1-_kM_FZuB8CzyF1s__Nunb79-2yl_wVbR0</recordid><startdate>201612</startdate><enddate>201612</enddate><creator>Lin, Ying‐Chen</creator><creator>Kobayashi, Koichi</creator><creator>Hung, Chun‐Hsien</creator><creator>Wada, Hajime</creator><creator>Nakamura, Yuki</creator><general>Blackwell Publishing 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>7QO</scope><scope>7QP</scope><scope>7QR</scope><scope>7TM</scope><scope>8FD</scope><scope>FR3</scope><scope>M7N</scope><scope>P64</scope><scope>RC3</scope><scope>7X8</scope></search><sort><creationdate>201612</creationdate><title>Arabidopsis phosphatidylglycerophosphate phosphatase 1 involved in phosphatidylglycerol biosynthesis and photosynthetic function</title><author>Lin, Ying‐Chen ; Kobayashi, Koichi ; Hung, Chun‐Hsien ; Wada, Hajime ; Nakamura, Yuki</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c5151-c37af101e68f41eaca5c056c975c8232b7cdebe5eb1d935b8b5883b74392735c3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2016</creationdate><topic>Arabidopsis</topic><topic>Arabidopsis - enzymology</topic><topic>Arabidopsis - genetics</topic><topic>Arabidopsis - metabolism</topic><topic>Arabidopsis Proteins - genetics</topic><topic>Arabidopsis Proteins - metabolism</topic><topic>Arabidopsis thaliana</topic><topic>Biosynthesis</topic><topic>Chlorophyll</topic><topic>chloroplast</topic><topic>Chloroplasts</topic><topic>Chloroplasts - genetics</topic><topic>Chloroplasts - metabolism</topic><topic>Deoxyribonucleic acid</topic><topic>DNA</topic><topic>DNA, Bacterial - metabolism</topic><topic>Embryos</topic><topic>Gene Expression Regulation, Plant - genetics</topic><topic>glycerolipid</topic><topic>Guard cells</topic><topic>lipid phosphate phosphatase</topic><topic>Lipids</topic><topic>Localization</topic><topic>Membranes</topic><topic>Phenotypes</topic><topic>Phosphatase</topic><topic>Phosphatidylglycerol</topic><topic>Phosphatidylglycerols - biosynthesis</topic><topic>Phosphatidylglycerols - metabolism</topic><topic>phosphatidylglycerophosphate phosphatase</topic><topic>Phosphoric Monoester Hydrolases - genetics</topic><topic>Phosphoric Monoester Hydrolases - metabolism</topic><topic>Photosynthesis</topic><topic>Photosynthesis - genetics</topic><topic>Photosynthesis - physiology</topic><topic>Plants (botany)</topic><topic>Plastids</topic><topic>Stigmas (botany)</topic><topic>Trichomes</topic><topic>Ultrastructure</topic><topic>Yeast</topic><topic>Yeasts</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Lin, Ying‐Chen</creatorcontrib><creatorcontrib>Kobayashi, Koichi</creatorcontrib><creatorcontrib>Hung, Chun‐Hsien</creatorcontrib><creatorcontrib>Wada, Hajime</creatorcontrib><creatorcontrib>Nakamura, Yuki</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>Biotechnology Research Abstracts</collection><collection>Calcium & Calcified Tissue Abstracts</collection><collection>Chemoreception Abstracts</collection><collection>Nucleic Acids Abstracts</collection><collection>Technology Research Database</collection><collection>Engineering Research Database</collection><collection>Algology Mycology and Protozoology Abstracts (Microbiology C)</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>Genetics Abstracts</collection><collection>MEDLINE - Academic</collection><jtitle>The Plant journal : for cell and molecular biology</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Lin, Ying‐Chen</au><au>Kobayashi, Koichi</au><au>Hung, Chun‐Hsien</au><au>Wada, Hajime</au><au>Nakamura, Yuki</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Arabidopsis phosphatidylglycerophosphate phosphatase 1 involved in phosphatidylglycerol biosynthesis and photosynthetic function</atitle><jtitle>The Plant journal : for cell and molecular biology</jtitle><addtitle>Plant J</addtitle><date>2016-12</date><risdate>2016</risdate><volume>88</volume><issue>6</issue><spage>1022</spage><epage>1037</epage><pages>1022-1037</pages><issn>0960-7412</issn><eissn>1365-313X</eissn><abstract>Summary
Phosphatidylglycerol (PG) is an indispensable lipid constituent of photosynthetic membranes, whose function is essential in photosynthetic activity. In higher plants, the biological function of the last step of PG biosynthesis remains elusive because an enzyme catalyzing this reaction step, namely phosphatidylglycerophosphate phosphatase (PGPP), has been a missing piece in the entire glycerolipid metabolic map. Here, we report the identification and characterization of AtPGPP1 encoding a PGPP in Arabidopsis thaliana. Heterologous expression of AtPGPP1 in yeast Δgep4 complemented growth phenotype and PG‐producing activity, suggesting that AtPGPP1 encodes a functional PGPP. The GUS reporter assay showed that AtPGPP1 was preferentially expressed in hypocotyl, vasculatures, trichomes, guard cells, and stigmas. A subcellular localization study with GFP reporter indicated that AtPGPP1 is mainly localized at chloroplasts. A T‐DNA‐tagged knockout mutant of AtPGPP1, designated pgpp1‐1, showed pale green phenotype with reduced PG and chlorophyll contents but no defect in embryo development. In the pgpp1‐1 mutant, ultrastructure of plastids indicated defective development of chloroplasts and measurement of photosynthetic parameters showed impaired photosynthetic activity. These results suggest that AtPGPP1 is a primary plastidic PGPP required for PG biosynthesis and photosynthetic function in Arabidopsis.
Significance Statement
Phosphatidylglycerol (PG) is an indispensable lipid constituent of photosynthetic membranes. Here we identified the previously unknown phosphatidylglycerophosphate phosphatase that is required for the last step in PG biosynthesis.</abstract><cop>England</cop><pub>Blackwell Publishing Ltd</pub><pmid>27541283</pmid><doi>10.1111/tpj.13311</doi><tpages>16</tpages><oa>free_for_read</oa></addata></record> |
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| subjects | Arabidopsis Arabidopsis - enzymology Arabidopsis - genetics Arabidopsis - metabolism Arabidopsis Proteins - genetics Arabidopsis Proteins - metabolism Arabidopsis thaliana Biosynthesis Chlorophyll chloroplast Chloroplasts Chloroplasts - genetics Chloroplasts - metabolism Deoxyribonucleic acid DNA DNA, Bacterial - metabolism Embryos Gene Expression Regulation, Plant - genetics glycerolipid Guard cells lipid phosphate phosphatase Lipids Localization Membranes Phenotypes Phosphatase Phosphatidylglycerol Phosphatidylglycerols - biosynthesis Phosphatidylglycerols - metabolism phosphatidylglycerophosphate phosphatase Phosphoric Monoester Hydrolases - genetics Phosphoric Monoester Hydrolases - metabolism Photosynthesis Photosynthesis - genetics Photosynthesis - physiology Plants (botany) Plastids Stigmas (botany) Trichomes Ultrastructure Yeast Yeasts |
| title | Arabidopsis phosphatidylglycerophosphate phosphatase 1 involved in phosphatidylglycerol biosynthesis and photosynthetic function |
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