Phytochelatin-mediated metal detoxification pathway is crucial for an organomercurial phenylmercury tolerance in Arabidopsis
Key message An organomercurial phenylmercury activates AtPCS1, an enzyme known for detoxification of inorganic metal(loid) ions in Arabidopsis and the induced metal-chelating peptides phytochelatins are essential for detoxification of phenylmercury. Small thiol-rich peptides phytochelatins (PCs) and...
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| Veröffentlicht in: | Plant molecular biology 2022-07, Vol.109 (4-5), p.563-577 |
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| creator | Uraguchi, Shimpei Ohshiro, Yuka Otsuka, Yuto Wada, Emiko Naruse, Fumii Sugaya, Kakeru Nagai, Kenichiro Wongkaew, Arunee Nakamura, Ryosuke Takanezawa, Yasukazu Clemens, Stephan Ohkama-Ohtsu, Naoko Kiyono, Masako |
| description | Key message
An organomercurial phenylmercury activates AtPCS1, an enzyme known for detoxification of inorganic metal(loid) ions in Arabidopsis and the induced metal-chelating peptides phytochelatins are essential for detoxification of phenylmercury.
Small thiol-rich peptides phytochelatins (PCs) and their synthases (PCSs) are crucial for plants to mitigate the stress derived from various metal(loid) ions in their inorganic form including inorganic mercury [Hg(II)]. However, the possible roles of the PC/PCS system in organic mercury detoxification in plants remain elusive. We found that an organomercury phenylmercury (PheHg) induced PC synthesis in
Arabidopsis thaliana
plants as Hg(II), whereas methylmercury did not. The analyses of AtPCS1 mutant plants and in vitro assays using the AtPCS1-recombinant protein demonstrated that AtPCS1, the major PCS in
A. thaliana
, was responsible for the PheHg-responsive PC synthesis. AtPCS1 mutants
cad1-3
and
cad1-6
, and the double mutant of PC-metal(loid) complex transporters AtABCC1 and AtABCC2 showed enhanced sensitivity to PheHg as well as to Hg(II). The hypersensitivity of
cad1-3
to PheHg stress was complemented by the own-promoter-driven expression of AtPCS1-GFP. The confocal microscopy of the complementation lines showed that the AtPCS1-GFP was preferentially expressed in epidermal cells of the mature and elongation zones, and the outer-most layer of the lateral root cap cells in the meristematic zone. Moreover, in vitro PC-metal binding assay demonstrated that binding affinity between PC and PheHg was comparable to Hg(II). However, plant ionomic profiles, as well as root morphology under PheHg and Hg(II) stress, were divergent. These results suggest that PheHg phytotoxicity is different from Hg(II), but AtPCS1-mediated PC synthesis, complex formation, and vacuolar sequestration by AtABCC1 and AtABCC2 are similarly functional for both PheHg and Hg(II) detoxification in root surficial cell types. |
| doi_str_mv | 10.1007/s11103-021-01221-0 |
| format | Article |
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An organomercurial phenylmercury activates AtPCS1, an enzyme known for detoxification of inorganic metal(loid) ions in Arabidopsis and the induced metal-chelating peptides phytochelatins are essential for detoxification of phenylmercury.
Small thiol-rich peptides phytochelatins (PCs) and their synthases (PCSs) are crucial for plants to mitigate the stress derived from various metal(loid) ions in their inorganic form including inorganic mercury [Hg(II)]. However, the possible roles of the PC/PCS system in organic mercury detoxification in plants remain elusive. We found that an organomercury phenylmercury (PheHg) induced PC synthesis in
Arabidopsis thaliana
plants as Hg(II), whereas methylmercury did not. The analyses of AtPCS1 mutant plants and in vitro assays using the AtPCS1-recombinant protein demonstrated that AtPCS1, the major PCS in
A. thaliana
, was responsible for the PheHg-responsive PC synthesis. AtPCS1 mutants
cad1-3
and
cad1-6
, and the double mutant of PC-metal(loid) complex transporters AtABCC1 and AtABCC2 showed enhanced sensitivity to PheHg as well as to Hg(II). The hypersensitivity of
cad1-3
to PheHg stress was complemented by the own-promoter-driven expression of AtPCS1-GFP. The confocal microscopy of the complementation lines showed that the AtPCS1-GFP was preferentially expressed in epidermal cells of the mature and elongation zones, and the outer-most layer of the lateral root cap cells in the meristematic zone. Moreover, in vitro PC-metal binding assay demonstrated that binding affinity between PC and PheHg was comparable to Hg(II). However, plant ionomic profiles, as well as root morphology under PheHg and Hg(II) stress, were divergent. These results suggest that PheHg phytotoxicity is different from Hg(II), but AtPCS1-mediated PC synthesis, complex formation, and vacuolar sequestration by AtABCC1 and AtABCC2 are similarly functional for both PheHg and Hg(II) detoxification in root surficial cell types.</description><identifier>ISSN: 0167-4412</identifier><identifier>EISSN: 1573-5028</identifier><identifier>DOI: 10.1007/s11103-021-01221-0</identifier><identifier>PMID: 34837578</identifier><language>eng</language><publisher>Dordrecht: Springer Netherlands</publisher><subject>Analysis ; Arabidopsis ; Arabidopsis thaliana ; Biochemistry ; Biomedical and Life Sciences ; Confocal microscopy ; Detoxification ; Dimethylmercury ; Enzymes ; Hypersensitivity ; Ions ; Life Sciences ; Mercury ; Metallothionein ; Metals ; Methylmercury ; Molecular Biology of Chemical Defenses ; Mutants ; Peptides ; Phenylmercury ; Phytochelatins ; Phytotoxicity ; Plant Pathology ; Plant Sciences ; Recombinant proteins ; Thiols</subject><ispartof>Plant molecular biology, 2022-07, Vol.109 (4-5), p.563-577</ispartof><rights>The Author(s), under exclusive licence to Springer Nature B.V. 2021</rights><rights>2021. The Author(s), under exclusive licence to Springer Nature B.V.</rights><rights>COPYRIGHT 2022 Springer</rights><rights>The Author(s), under exclusive licence to Springer Nature B.V. 2021.</rights><lds50>peer_reviewed</lds50><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c480t-84b009b7a9ac9388b7e473fd01dfe7ea7b4f0743143cb59fd8352a953f73f47c3</citedby><cites>FETCH-LOGICAL-c480t-84b009b7a9ac9388b7e473fd01dfe7ea7b4f0743143cb59fd8352a953f73f47c3</cites><orcidid>0000-0003-1724-8435 ; 0000-0001-6150-5481</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://link.springer.com/content/pdf/10.1007/s11103-021-01221-0$$EPDF$$P50$$Gspringer$$H</linktopdf><linktohtml>$$Uhttps://link.springer.com/10.1007/s11103-021-01221-0$$EHTML$$P50$$Gspringer$$H</linktohtml><link.rule.ids>314,776,780,27901,27902,41464,42533,51294</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/34837578$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Uraguchi, Shimpei</creatorcontrib><creatorcontrib>Ohshiro, Yuka</creatorcontrib><creatorcontrib>Otsuka, Yuto</creatorcontrib><creatorcontrib>Wada, Emiko</creatorcontrib><creatorcontrib>Naruse, Fumii</creatorcontrib><creatorcontrib>Sugaya, Kakeru</creatorcontrib><creatorcontrib>Nagai, Kenichiro</creatorcontrib><creatorcontrib>Wongkaew, Arunee</creatorcontrib><creatorcontrib>Nakamura, Ryosuke</creatorcontrib><creatorcontrib>Takanezawa, Yasukazu</creatorcontrib><creatorcontrib>Clemens, Stephan</creatorcontrib><creatorcontrib>Ohkama-Ohtsu, Naoko</creatorcontrib><creatorcontrib>Kiyono, Masako</creatorcontrib><title>Phytochelatin-mediated metal detoxification pathway is crucial for an organomercurial phenylmercury tolerance in Arabidopsis</title><title>Plant molecular biology</title><addtitle>Plant Mol Biol</addtitle><addtitle>Plant Mol Biol</addtitle><description>Key message
An organomercurial phenylmercury activates AtPCS1, an enzyme known for detoxification of inorganic metal(loid) ions in Arabidopsis and the induced metal-chelating peptides phytochelatins are essential for detoxification of phenylmercury.
Small thiol-rich peptides phytochelatins (PCs) and their synthases (PCSs) are crucial for plants to mitigate the stress derived from various metal(loid) ions in their inorganic form including inorganic mercury [Hg(II)]. However, the possible roles of the PC/PCS system in organic mercury detoxification in plants remain elusive. We found that an organomercury phenylmercury (PheHg) induced PC synthesis in
Arabidopsis thaliana
plants as Hg(II), whereas methylmercury did not. The analyses of AtPCS1 mutant plants and in vitro assays using the AtPCS1-recombinant protein demonstrated that AtPCS1, the major PCS in
A. thaliana
, was responsible for the PheHg-responsive PC synthesis. AtPCS1 mutants
cad1-3
and
cad1-6
, and the double mutant of PC-metal(loid) complex transporters AtABCC1 and AtABCC2 showed enhanced sensitivity to PheHg as well as to Hg(II). The hypersensitivity of
cad1-3
to PheHg stress was complemented by the own-promoter-driven expression of AtPCS1-GFP. The confocal microscopy of the complementation lines showed that the AtPCS1-GFP was preferentially expressed in epidermal cells of the mature and elongation zones, and the outer-most layer of the lateral root cap cells in the meristematic zone. Moreover, in vitro PC-metal binding assay demonstrated that binding affinity between PC and PheHg was comparable to Hg(II). However, plant ionomic profiles, as well as root morphology under PheHg and Hg(II) stress, were divergent. These results suggest that PheHg phytotoxicity is different from Hg(II), but AtPCS1-mediated PC synthesis, complex formation, and vacuolar sequestration by AtABCC1 and AtABCC2 are similarly functional for both PheHg and Hg(II) detoxification in root surficial cell types.</description><subject>Analysis</subject><subject>Arabidopsis</subject><subject>Arabidopsis thaliana</subject><subject>Biochemistry</subject><subject>Biomedical and Life Sciences</subject><subject>Confocal microscopy</subject><subject>Detoxification</subject><subject>Dimethylmercury</subject><subject>Enzymes</subject><subject>Hypersensitivity</subject><subject>Ions</subject><subject>Life Sciences</subject><subject>Mercury</subject><subject>Metallothionein</subject><subject>Metals</subject><subject>Methylmercury</subject><subject>Molecular Biology of Chemical Defenses</subject><subject>Mutants</subject><subject>Peptides</subject><subject>Phenylmercury</subject><subject>Phytochelatins</subject><subject>Phytotoxicity</subject><subject>Plant Pathology</subject><subject>Plant Sciences</subject><subject>Recombinant 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B.V</general><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>3V.</scope><scope>7TM</scope><scope>7X7</scope><scope>7XB</scope><scope>88A</scope><scope>88E</scope><scope>8AO</scope><scope>8FD</scope><scope>8FE</scope><scope>8FH</scope><scope>8FI</scope><scope>8FJ</scope><scope>8FK</scope><scope>8G5</scope><scope>ABUWG</scope><scope>AEUYN</scope><scope>AFKRA</scope><scope>AZQEC</scope><scope>BBNVY</scope><scope>BENPR</scope><scope>BHPHI</scope><scope>CCPQU</scope><scope>DWQXO</scope><scope>FR3</scope><scope>FYUFA</scope><scope>GHDGH</scope><scope>GNUQQ</scope><scope>GUQSH</scope><scope>HCIFZ</scope><scope>K9.</scope><scope>LK8</scope><scope>M0S</scope><scope>M1P</scope><scope>M2O</scope><scope>M7P</scope><scope>MBDVC</scope><scope>P64</scope><scope>PQEST</scope><scope>PQQKQ</scope><scope>PQUKI</scope><scope>Q9U</scope><scope>RC3</scope><orcidid>https://orcid.org/0000-0003-1724-8435</orcidid><orcidid>https://orcid.org/0000-0001-6150-5481</orcidid></search><sort><creationdate>20220701</creationdate><title>Phytochelatin-mediated metal detoxification pathway is crucial for an organomercurial phenylmercury tolerance in Arabidopsis</title><author>Uraguchi, Shimpei ; Ohshiro, Yuka ; Otsuka, Yuto ; Wada, Emiko ; Naruse, Fumii ; Sugaya, Kakeru ; Nagai, Kenichiro ; Wongkaew, Arunee ; Nakamura, Ryosuke ; Takanezawa, Yasukazu ; Clemens, Stephan ; Ohkama-Ohtsu, Naoko ; Kiyono, Masako</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c480t-84b009b7a9ac9388b7e473fd01dfe7ea7b4f0743143cb59fd8352a953f73f47c3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2022</creationdate><topic>Analysis</topic><topic>Arabidopsis</topic><topic>Arabidopsis thaliana</topic><topic>Biochemistry</topic><topic>Biomedical and Life Sciences</topic><topic>Confocal microscopy</topic><topic>Detoxification</topic><topic>Dimethylmercury</topic><topic>Enzymes</topic><topic>Hypersensitivity</topic><topic>Ions</topic><topic>Life Sciences</topic><topic>Mercury</topic><topic>Metallothionein</topic><topic>Metals</topic><topic>Methylmercury</topic><topic>Molecular Biology of Chemical Defenses</topic><topic>Mutants</topic><topic>Peptides</topic><topic>Phenylmercury</topic><topic>Phytochelatins</topic><topic>Phytotoxicity</topic><topic>Plant Pathology</topic><topic>Plant Sciences</topic><topic>Recombinant proteins</topic><topic>Thiols</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Uraguchi, Shimpei</creatorcontrib><creatorcontrib>Ohshiro, Yuka</creatorcontrib><creatorcontrib>Otsuka, Yuto</creatorcontrib><creatorcontrib>Wada, Emiko</creatorcontrib><creatorcontrib>Naruse, Fumii</creatorcontrib><creatorcontrib>Sugaya, Kakeru</creatorcontrib><creatorcontrib>Nagai, Kenichiro</creatorcontrib><creatorcontrib>Wongkaew, Arunee</creatorcontrib><creatorcontrib>Nakamura, Ryosuke</creatorcontrib><creatorcontrib>Takanezawa, Yasukazu</creatorcontrib><creatorcontrib>Clemens, Stephan</creatorcontrib><creatorcontrib>Ohkama-Ohtsu, Naoko</creatorcontrib><creatorcontrib>Kiyono, Masako</creatorcontrib><collection>PubMed</collection><collection>CrossRef</collection><collection>ProQuest Central (Corporate)</collection><collection>Nucleic Acids Abstracts</collection><collection>Health & Medical Collection</collection><collection>ProQuest Central (purchase pre-March 2016)</collection><collection>Biology Database (Alumni Edition)</collection><collection>Medical Database (Alumni Edition)</collection><collection>ProQuest Pharma Collection</collection><collection>Technology Research Database</collection><collection>ProQuest SciTech Collection</collection><collection>ProQuest Natural Science Collection</collection><collection>Hospital Premium Collection</collection><collection>Hospital Premium Collection (Alumni Edition)</collection><collection>ProQuest Central (Alumni) (purchase pre-March 2016)</collection><collection>Research Library (Alumni 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Edition)</collection><collection>Medical Database</collection><collection>Research Library</collection><collection>Biological Science Database</collection><collection>Research Library (Corporate)</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>ProQuest One Academic Eastern Edition (DO NOT USE)</collection><collection>ProQuest One Academic</collection><collection>ProQuest One Academic UKI Edition</collection><collection>ProQuest Central Basic</collection><collection>Genetics Abstracts</collection><jtitle>Plant molecular biology</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Uraguchi, Shimpei</au><au>Ohshiro, Yuka</au><au>Otsuka, Yuto</au><au>Wada, Emiko</au><au>Naruse, Fumii</au><au>Sugaya, Kakeru</au><au>Nagai, Kenichiro</au><au>Wongkaew, Arunee</au><au>Nakamura, Ryosuke</au><au>Takanezawa, Yasukazu</au><au>Clemens, Stephan</au><au>Ohkama-Ohtsu, Naoko</au><au>Kiyono, Masako</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Phytochelatin-mediated metal detoxification pathway is crucial for an organomercurial phenylmercury tolerance in Arabidopsis</atitle><jtitle>Plant molecular biology</jtitle><stitle>Plant Mol Biol</stitle><addtitle>Plant Mol Biol</addtitle><date>2022-07-01</date><risdate>2022</risdate><volume>109</volume><issue>4-5</issue><spage>563</spage><epage>577</epage><pages>563-577</pages><issn>0167-4412</issn><eissn>1573-5028</eissn><abstract>Key message
An organomercurial phenylmercury activates AtPCS1, an enzyme known for detoxification of inorganic metal(loid) ions in Arabidopsis and the induced metal-chelating peptides phytochelatins are essential for detoxification of phenylmercury.
Small thiol-rich peptides phytochelatins (PCs) and their synthases (PCSs) are crucial for plants to mitigate the stress derived from various metal(loid) ions in their inorganic form including inorganic mercury [Hg(II)]. However, the possible roles of the PC/PCS system in organic mercury detoxification in plants remain elusive. We found that an organomercury phenylmercury (PheHg) induced PC synthesis in
Arabidopsis thaliana
plants as Hg(II), whereas methylmercury did not. The analyses of AtPCS1 mutant plants and in vitro assays using the AtPCS1-recombinant protein demonstrated that AtPCS1, the major PCS in
A. thaliana
, was responsible for the PheHg-responsive PC synthesis. AtPCS1 mutants
cad1-3
and
cad1-6
, and the double mutant of PC-metal(loid) complex transporters AtABCC1 and AtABCC2 showed enhanced sensitivity to PheHg as well as to Hg(II). The hypersensitivity of
cad1-3
to PheHg stress was complemented by the own-promoter-driven expression of AtPCS1-GFP. The confocal microscopy of the complementation lines showed that the AtPCS1-GFP was preferentially expressed in epidermal cells of the mature and elongation zones, and the outer-most layer of the lateral root cap cells in the meristematic zone. Moreover, in vitro PC-metal binding assay demonstrated that binding affinity between PC and PheHg was comparable to Hg(II). However, plant ionomic profiles, as well as root morphology under PheHg and Hg(II) stress, were divergent. These results suggest that PheHg phytotoxicity is different from Hg(II), but AtPCS1-mediated PC synthesis, complex formation, and vacuolar sequestration by AtABCC1 and AtABCC2 are similarly functional for both PheHg and Hg(II) detoxification in root surficial cell types.</abstract><cop>Dordrecht</cop><pub>Springer Netherlands</pub><pmid>34837578</pmid><doi>10.1007/s11103-021-01221-0</doi><tpages>15</tpages><orcidid>https://orcid.org/0000-0003-1724-8435</orcidid><orcidid>https://orcid.org/0000-0001-6150-5481</orcidid></addata></record> |
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| ispartof | Plant molecular biology, 2022-07, Vol.109 (4-5), p.563-577 |
| issn | 0167-4412 1573-5028 |
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| source | SpringerLink Journals - AutoHoldings |
| subjects | Analysis Arabidopsis Arabidopsis thaliana Biochemistry Biomedical and Life Sciences Confocal microscopy Detoxification Dimethylmercury Enzymes Hypersensitivity Ions Life Sciences Mercury Metallothionein Metals Methylmercury Molecular Biology of Chemical Defenses Mutants Peptides Phenylmercury Phytochelatins Phytotoxicity Plant Pathology Plant Sciences Recombinant proteins Thiols |
| title | Phytochelatin-mediated metal detoxification pathway is crucial for an organomercurial phenylmercury tolerance in Arabidopsis |
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