A root‐associated purple acid phosphatase, SgPAP23, mediates extracellular phytate‐P utilization in Stylosanthes guianensis
As a major fraction of soil organic phosphorus (P), phytate‐P is unavailable to plants unless hydrolysed by phytase. However, it remains fragmentary that natural variation in root‐associated phytase activity and its underlying molecular mechanisms in plants. In this study, variations in root‐associa...
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| Veröffentlicht in: | Plant, cell and environment cell and environment, 2018-12, Vol.41 (12), p.2821-2834 |
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| creator | Liu, Pandao Cai, Zefei Chen, Zhijian Mo, Xiaohui Ding, Xipeng Liang, Cuiyue Liu, Guodao Tian, Jiang |
| description | As a major fraction of soil organic phosphorus (P), phytate‐P is unavailable to plants unless hydrolysed by phytase. However, it remains fragmentary that natural variation in root‐associated phytase activity and its underlying molecular mechanisms in plants. In this study, variations in root‐associated phytase activity were observed among 39 stylo genotypes. Subsequently, a root‐associated purple acid phosphatase (PAP) with phytase activity, SgPAP23, was found to be a primary contributor to the superior extracellular phytate‐P utilization in stylo.
As a major component of soil organic phosphorus (P), phytate‐P is unavailable to plants unless hydrolysed by phytase to release inorganic phosphate. However, knowledge on natural variation in root‐associated phytase activity and its underlying molecular mechanisms in plants remains fragmentary. In this study, variations in root internal and associated phytase activity were observed among 39 genotypes of Stylosanthes guianensis (Stylo), which is well adapted to acid soils. Furthermore, TPRC2001‐1, the genotype with the highest root‐associated phytase activity, was more capable of utilizing extracellular phytate‐P than Fine‐stem, the genotype with the lowest root‐associated phytase activity. After protein liquid chromatography–tandem mass spectrometry analysis, a purple acid phosphatase (PAP), SgPAP23, was identified and cloned from TPRC2001‐1. SgPAP23 exhibited high activity against phytate‐P and was mainly localized on the plasma membrane. Furthermore, SgPAP23 overexpression resulted in significant increases of root‐associated phytase activity and thus facilitated extracellular phytate‐P utilization in both bean (Phaseolus vulgaris) hairy roots and Arabidopsis thaliana. The results herein support the conclusion that SgPAP23 is a primary contributor to the superior extracellular phytate‐P utilization in stylo and thus is used to develop cultivars with efficient extracellular phytate‐P utilization. |
| doi_str_mv | 10.1111/pce.13412 |
| format | Article |
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As a major component of soil organic phosphorus (P), phytate‐P is unavailable to plants unless hydrolysed by phytase to release inorganic phosphate. However, knowledge on natural variation in root‐associated phytase activity and its underlying molecular mechanisms in plants remains fragmentary. In this study, variations in root internal and associated phytase activity were observed among 39 genotypes of Stylosanthes guianensis (Stylo), which is well adapted to acid soils. Furthermore, TPRC2001‐1, the genotype with the highest root‐associated phytase activity, was more capable of utilizing extracellular phytate‐P than Fine‐stem, the genotype with the lowest root‐associated phytase activity. After protein liquid chromatography–tandem mass spectrometry analysis, a purple acid phosphatase (PAP), SgPAP23, was identified and cloned from TPRC2001‐1. SgPAP23 exhibited high activity against phytate‐P and was mainly localized on the plasma membrane. Furthermore, SgPAP23 overexpression resulted in significant increases of root‐associated phytase activity and thus facilitated extracellular phytate‐P utilization in both bean (Phaseolus vulgaris) hairy roots and Arabidopsis thaliana. The results herein support the conclusion that SgPAP23 is a primary contributor to the superior extracellular phytate‐P utilization in stylo and thus is used to develop cultivars with efficient extracellular phytate‐P utilization.</description><identifier>ISSN: 0140-7791</identifier><identifier>EISSN: 1365-3040</identifier><identifier>DOI: 10.1111/pce.13412</identifier><identifier>PMID: 30066375</identifier><language>eng</language><publisher>United States: Wiley Subscription Services, Inc</publisher><subject>6-Phytase - metabolism ; Acid phosphatase ; Acid Phosphatase - metabolism ; acid phosphatase activity ; Acidic soils ; Arabidopsis ; Chromatography, Liquid ; Cloning, Molecular ; Cultivars ; Fabaceae - enzymology ; Fabaceae - metabolism ; Genotypes ; Hairy root ; Liquid chromatography ; Mass spectrometry ; Mass spectroscopy ; Molecular modelling ; Organic phosphorus ; Organic soils ; Phaseolus vulgaris ; Phosphatase ; Phosphorus ; phosphorus deficiency ; Phytase ; phytate‐P ; Phytic Acid - metabolism ; Plant Proteins - metabolism ; Plant Roots - enzymology ; Plant Roots - metabolism ; Plants, Genetically Modified ; Proteins ; Purple acid phosphatase ; Real-Time Polymerase Chain Reaction ; Stylosanthes ; Stylosanthes guianensis ; Tandem Mass Spectrometry ; Utilization</subject><ispartof>Plant, cell and environment, 2018-12, Vol.41 (12), p.2821-2834</ispartof><rights>2018 John Wiley & Sons Ltd</rights><rights>2018 John Wiley & Sons Ltd.</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c3882-e9a8e37c68fafa9dc4dbd29c70bc2b84cb21e031f9000b6b3829b7779e0a6c4a3</citedby><cites>FETCH-LOGICAL-c3882-e9a8e37c68fafa9dc4dbd29c70bc2b84cb21e031f9000b6b3829b7779e0a6c4a3</cites><orcidid>0000-0002-1104-7803</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://onlinelibrary.wiley.com/doi/pdf/10.1111%2Fpce.13412$$EPDF$$P50$$Gwiley$$H</linktopdf><linktohtml>$$Uhttps://onlinelibrary.wiley.com/doi/full/10.1111%2Fpce.13412$$EHTML$$P50$$Gwiley$$H</linktohtml><link.rule.ids>314,776,780,1411,1427,27903,27904,45553,45554,46387,46811</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/30066375$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Liu, Pandao</creatorcontrib><creatorcontrib>Cai, Zefei</creatorcontrib><creatorcontrib>Chen, Zhijian</creatorcontrib><creatorcontrib>Mo, Xiaohui</creatorcontrib><creatorcontrib>Ding, Xipeng</creatorcontrib><creatorcontrib>Liang, Cuiyue</creatorcontrib><creatorcontrib>Liu, Guodao</creatorcontrib><creatorcontrib>Tian, Jiang</creatorcontrib><title>A root‐associated purple acid phosphatase, SgPAP23, mediates extracellular phytate‐P utilization in Stylosanthes guianensis</title><title>Plant, cell and environment</title><addtitle>Plant Cell Environ</addtitle><description>As a major fraction of soil organic phosphorus (P), phytate‐P is unavailable to plants unless hydrolysed by phytase. However, it remains fragmentary that natural variation in root‐associated phytase activity and its underlying molecular mechanisms in plants. In this study, variations in root‐associated phytase activity were observed among 39 stylo genotypes. Subsequently, a root‐associated purple acid phosphatase (PAP) with phytase activity, SgPAP23, was found to be a primary contributor to the superior extracellular phytate‐P utilization in stylo.
As a major component of soil organic phosphorus (P), phytate‐P is unavailable to plants unless hydrolysed by phytase to release inorganic phosphate. However, knowledge on natural variation in root‐associated phytase activity and its underlying molecular mechanisms in plants remains fragmentary. In this study, variations in root internal and associated phytase activity were observed among 39 genotypes of Stylosanthes guianensis (Stylo), which is well adapted to acid soils. Furthermore, TPRC2001‐1, the genotype with the highest root‐associated phytase activity, was more capable of utilizing extracellular phytate‐P than Fine‐stem, the genotype with the lowest root‐associated phytase activity. After protein liquid chromatography–tandem mass spectrometry analysis, a purple acid phosphatase (PAP), SgPAP23, was identified and cloned from TPRC2001‐1. SgPAP23 exhibited high activity against phytate‐P and was mainly localized on the plasma membrane. Furthermore, SgPAP23 overexpression resulted in significant increases of root‐associated phytase activity and thus facilitated extracellular phytate‐P utilization in both bean (Phaseolus vulgaris) hairy roots and Arabidopsis thaliana. The results herein support the conclusion that SgPAP23 is a primary contributor to the superior extracellular phytate‐P utilization in stylo and thus is used to develop cultivars with efficient extracellular phytate‐P utilization.</description><subject>6-Phytase - metabolism</subject><subject>Acid phosphatase</subject><subject>Acid Phosphatase - metabolism</subject><subject>acid phosphatase activity</subject><subject>Acidic soils</subject><subject>Arabidopsis</subject><subject>Chromatography, Liquid</subject><subject>Cloning, Molecular</subject><subject>Cultivars</subject><subject>Fabaceae - enzymology</subject><subject>Fabaceae - metabolism</subject><subject>Genotypes</subject><subject>Hairy root</subject><subject>Liquid chromatography</subject><subject>Mass spectrometry</subject><subject>Mass spectroscopy</subject><subject>Molecular modelling</subject><subject>Organic phosphorus</subject><subject>Organic soils</subject><subject>Phaseolus vulgaris</subject><subject>Phosphatase</subject><subject>Phosphorus</subject><subject>phosphorus deficiency</subject><subject>Phytase</subject><subject>phytate‐P</subject><subject>Phytic Acid - metabolism</subject><subject>Plant Proteins - metabolism</subject><subject>Plant Roots - enzymology</subject><subject>Plant Roots - metabolism</subject><subject>Plants, Genetically Modified</subject><subject>Proteins</subject><subject>Purple acid phosphatase</subject><subject>Real-Time Polymerase Chain Reaction</subject><subject>Stylosanthes</subject><subject>Stylosanthes guianensis</subject><subject>Tandem Mass Spectrometry</subject><subject>Utilization</subject><issn>0140-7791</issn><issn>1365-3040</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2018</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNp1kctqHDEQRUVIsCe2F_mBIMgmAbdHj34uh8GPgMEDY69FtVrtkelpdSQ1znhjf0K-MV_iGo-ThcHalChOXW7VJeQLZycc33TQ5oTLlIsPZMJlniWSpewjmTCesqQoKr5PPodwxxg2imqP7EvG8lwW2YQ8zqh3Lv59-gMhOG0hmoYOox86Q0Fb_K9cGFYQIZhjurxdzBZCHtO1abZooOZ39KBN140deIQ3EduotqBjtJ19gGhdT21Pl3HTuQB9XOHU7WihN32w4ZB8aqEL5ui1HpCbs9Pr-UVyeXX-cz67TLQsS5GYCkojC52XLbRQNTpt6kZUumC1FnWZ6lpwwyRvK1yyzmtZiqoucHXDINcpyAPyfac7ePdrNCGqtQ1b3-jDjUEJVvIsE0KmiH57g9650ffoTgkuM8Yl4zlSP3aU9i4Eb1o1eLsGv1GcqW0qClNRL6kg-_VVcazxcv_JfzEgMN0B97Yzm_eV1GJ-upN8BhLUmbA</recordid><startdate>201812</startdate><enddate>201812</enddate><creator>Liu, Pandao</creator><creator>Cai, Zefei</creator><creator>Chen, Zhijian</creator><creator>Mo, Xiaohui</creator><creator>Ding, Xipeng</creator><creator>Liang, Cuiyue</creator><creator>Liu, Guodao</creator><creator>Tian, Jiang</creator><general>Wiley Subscription Services, Inc</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>7QP</scope><scope>7ST</scope><scope>C1K</scope><scope>SOI</scope><scope>7X8</scope><orcidid>https://orcid.org/0000-0002-1104-7803</orcidid></search><sort><creationdate>201812</creationdate><title>A root‐associated purple acid phosphatase, SgPAP23, mediates extracellular phytate‐P utilization in Stylosanthes guianensis</title><author>Liu, Pandao ; Cai, Zefei ; Chen, Zhijian ; Mo, Xiaohui ; Ding, Xipeng ; Liang, Cuiyue ; Liu, Guodao ; Tian, Jiang</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c3882-e9a8e37c68fafa9dc4dbd29c70bc2b84cb21e031f9000b6b3829b7779e0a6c4a3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2018</creationdate><topic>6-Phytase - metabolism</topic><topic>Acid phosphatase</topic><topic>Acid Phosphatase - metabolism</topic><topic>acid phosphatase activity</topic><topic>Acidic soils</topic><topic>Arabidopsis</topic><topic>Chromatography, Liquid</topic><topic>Cloning, Molecular</topic><topic>Cultivars</topic><topic>Fabaceae - enzymology</topic><topic>Fabaceae - metabolism</topic><topic>Genotypes</topic><topic>Hairy root</topic><topic>Liquid chromatography</topic><topic>Mass spectrometry</topic><topic>Mass spectroscopy</topic><topic>Molecular modelling</topic><topic>Organic phosphorus</topic><topic>Organic soils</topic><topic>Phaseolus vulgaris</topic><topic>Phosphatase</topic><topic>Phosphorus</topic><topic>phosphorus deficiency</topic><topic>Phytase</topic><topic>phytate‐P</topic><topic>Phytic Acid - metabolism</topic><topic>Plant Proteins - metabolism</topic><topic>Plant Roots - enzymology</topic><topic>Plant Roots - metabolism</topic><topic>Plants, Genetically Modified</topic><topic>Proteins</topic><topic>Purple acid phosphatase</topic><topic>Real-Time Polymerase Chain Reaction</topic><topic>Stylosanthes</topic><topic>Stylosanthes guianensis</topic><topic>Tandem Mass Spectrometry</topic><topic>Utilization</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Liu, Pandao</creatorcontrib><creatorcontrib>Cai, Zefei</creatorcontrib><creatorcontrib>Chen, Zhijian</creatorcontrib><creatorcontrib>Mo, Xiaohui</creatorcontrib><creatorcontrib>Ding, Xipeng</creatorcontrib><creatorcontrib>Liang, Cuiyue</creatorcontrib><creatorcontrib>Liu, Guodao</creatorcontrib><creatorcontrib>Tian, Jiang</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>Calcium & Calcified Tissue Abstracts</collection><collection>Environment Abstracts</collection><collection>Environmental Sciences and Pollution Management</collection><collection>Environment Abstracts</collection><collection>MEDLINE - Academic</collection><jtitle>Plant, cell and environment</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Liu, Pandao</au><au>Cai, Zefei</au><au>Chen, Zhijian</au><au>Mo, Xiaohui</au><au>Ding, Xipeng</au><au>Liang, Cuiyue</au><au>Liu, Guodao</au><au>Tian, Jiang</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>A root‐associated purple acid phosphatase, SgPAP23, mediates extracellular phytate‐P utilization in Stylosanthes guianensis</atitle><jtitle>Plant, cell and environment</jtitle><addtitle>Plant Cell Environ</addtitle><date>2018-12</date><risdate>2018</risdate><volume>41</volume><issue>12</issue><spage>2821</spage><epage>2834</epage><pages>2821-2834</pages><issn>0140-7791</issn><eissn>1365-3040</eissn><abstract>As a major fraction of soil organic phosphorus (P), phytate‐P is unavailable to plants unless hydrolysed by phytase. However, it remains fragmentary that natural variation in root‐associated phytase activity and its underlying molecular mechanisms in plants. In this study, variations in root‐associated phytase activity were observed among 39 stylo genotypes. Subsequently, a root‐associated purple acid phosphatase (PAP) with phytase activity, SgPAP23, was found to be a primary contributor to the superior extracellular phytate‐P utilization in stylo.
As a major component of soil organic phosphorus (P), phytate‐P is unavailable to plants unless hydrolysed by phytase to release inorganic phosphate. However, knowledge on natural variation in root‐associated phytase activity and its underlying molecular mechanisms in plants remains fragmentary. In this study, variations in root internal and associated phytase activity were observed among 39 genotypes of Stylosanthes guianensis (Stylo), which is well adapted to acid soils. Furthermore, TPRC2001‐1, the genotype with the highest root‐associated phytase activity, was more capable of utilizing extracellular phytate‐P than Fine‐stem, the genotype with the lowest root‐associated phytase activity. After protein liquid chromatography–tandem mass spectrometry analysis, a purple acid phosphatase (PAP), SgPAP23, was identified and cloned from TPRC2001‐1. SgPAP23 exhibited high activity against phytate‐P and was mainly localized on the plasma membrane. Furthermore, SgPAP23 overexpression resulted in significant increases of root‐associated phytase activity and thus facilitated extracellular phytate‐P utilization in both bean (Phaseolus vulgaris) hairy roots and Arabidopsis thaliana. The results herein support the conclusion that SgPAP23 is a primary contributor to the superior extracellular phytate‐P utilization in stylo and thus is used to develop cultivars with efficient extracellular phytate‐P utilization.</abstract><cop>United States</cop><pub>Wiley Subscription Services, Inc</pub><pmid>30066375</pmid><doi>10.1111/pce.13412</doi><tpages>14</tpages><orcidid>https://orcid.org/0000-0002-1104-7803</orcidid><oa>free_for_read</oa></addata></record> |
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| subjects | 6-Phytase - metabolism Acid phosphatase Acid Phosphatase - metabolism acid phosphatase activity Acidic soils Arabidopsis Chromatography, Liquid Cloning, Molecular Cultivars Fabaceae - enzymology Fabaceae - metabolism Genotypes Hairy root Liquid chromatography Mass spectrometry Mass spectroscopy Molecular modelling Organic phosphorus Organic soils Phaseolus vulgaris Phosphatase Phosphorus phosphorus deficiency Phytase phytate‐P Phytic Acid - metabolism Plant Proteins - metabolism Plant Roots - enzymology Plant Roots - metabolism Plants, Genetically Modified Proteins Purple acid phosphatase Real-Time Polymerase Chain Reaction Stylosanthes Stylosanthes guianensis Tandem Mass Spectrometry Utilization |
| title | A root‐associated purple acid phosphatase, SgPAP23, mediates extracellular phytate‐P utilization in Stylosanthes guianensis |
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