Crystal Structures of Physcomitrella patens AOC1 and AOC2: Insights into the Enzyme Mechanism and Differences in Substrate Specificity1[W][OA]
In plants, oxylipins regulate developmental processes and defense responses. The first specific step in the biosynthesis of the cyclopentanone class of oxylipins is catalyzed by allene oxide cyclase ( AOC ) that forms cis(+)-12-oxo-phytodienoic acid. The moss Physcomitrella patens has two AOCs (PpAO...
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Veröffentlicht in: | Plant physiology (Bethesda) 2012-09, Vol.160 (3), p.1251-1266 |
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description | In plants, oxylipins regulate developmental processes and defense responses. The first specific step in the biosynthesis of the cyclopentanone class of oxylipins is catalyzed by allene oxide cyclase (
AOC
) that forms cis(+)-12-oxo-phytodienoic acid. The moss
Physcomitrella patens
has two
AOCs
(PpAOC1 and PpAOC2) with different substrate specificities for C
18
- and C
20
-derived substrates, respectively. To better understand
AOC
’s catalytic mechanism and to elucidate the structural properties that explain the differences in substrate specificity, we solved and analyzed the crystal structures of 36 monomers of both apo and ligand complexes of PpAOC1 and PpAOC2. From these data, we propose the following intermediates in
AOC
catalysis: (1) a resting state of the apo enzyme with a closed conformation, (2) a first shallow binding mode, followed by (3) a tight binding of the substrate accompanied by conformational changes in the binding pocket, and (4) initiation of the catalytic cycle by opening of the epoxide ring. As expected, the substrate dihydro analog cis-12,13
S
-epoxy-9
Z
,15
Z
-octadecadienoic acid did not cyclize in the presence of PpAOC1; however, when bound to the enzyme, it underwent isomerization into the corresponding trans-epoxide. By comparing complex structures of the C
18
substrate analog with in silico modeling of the C
20
substrate analog bound to the enzyme allowed us to identify three major molecular determinants responsible for the different substrate specificities (i.e. larger active site diameter, an elongated cavity of PpAOC2, and two nonidentical residues at the entrance of the active site). |
doi_str_mv | 10.1104/pp.112.205138 |
format | Article |
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AOC
) that forms cis(+)-12-oxo-phytodienoic acid. The moss
Physcomitrella patens
has two
AOCs
(PpAOC1 and PpAOC2) with different substrate specificities for C
18
- and C
20
-derived substrates, respectively. To better understand
AOC
’s catalytic mechanism and to elucidate the structural properties that explain the differences in substrate specificity, we solved and analyzed the crystal structures of 36 monomers of both apo and ligand complexes of PpAOC1 and PpAOC2. From these data, we propose the following intermediates in
AOC
catalysis: (1) a resting state of the apo enzyme with a closed conformation, (2) a first shallow binding mode, followed by (3) a tight binding of the substrate accompanied by conformational changes in the binding pocket, and (4) initiation of the catalytic cycle by opening of the epoxide ring. As expected, the substrate dihydro analog cis-12,13
S
-epoxy-9
Z
,15
Z
-octadecadienoic acid did not cyclize in the presence of PpAOC1; however, when bound to the enzyme, it underwent isomerization into the corresponding trans-epoxide. By comparing complex structures of the C
18
substrate analog with in silico modeling of the C
20
substrate analog bound to the enzyme allowed us to identify three major molecular determinants responsible for the different substrate specificities (i.e. larger active site diameter, an elongated cavity of PpAOC2, and two nonidentical residues at the entrance of the active site).</description><identifier>ISSN: 0032-0889</identifier><identifier>EISSN: 1532-2548</identifier><identifier>DOI: 10.1104/pp.112.205138</identifier><identifier>PMID: 22987885</identifier><language>eng</language><publisher>American Society of Plant Biologists</publisher><subject>Biochemical Processes and Macromolecular Structures</subject><ispartof>Plant physiology (Bethesda), 2012-09, Vol.160 (3), p.1251-1266</ispartof><rights>2012 American Society of Plant Biologists. All Rights Reserved. 2012</rights><lds50>peer_reviewed</lds50><woscitedreferencessubscribed>false</woscitedreferencessubscribed></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><link.rule.ids>230,314,780,784,885,27924,27925</link.rule.ids></links><search><creatorcontrib>Neumann, Piotr</creatorcontrib><creatorcontrib>Brodhun, Florian</creatorcontrib><creatorcontrib>Sauer, Kristin</creatorcontrib><creatorcontrib>Herrfurth, Cornelia</creatorcontrib><creatorcontrib>Hamberg, Mats</creatorcontrib><creatorcontrib>Brinkmann, Jens</creatorcontrib><creatorcontrib>Scholz, Julia</creatorcontrib><creatorcontrib>Dickmanns, Achim</creatorcontrib><creatorcontrib>Feussner, Ivo</creatorcontrib><creatorcontrib>Ficner, Ralf</creatorcontrib><title>Crystal Structures of Physcomitrella patens AOC1 and AOC2: Insights into the Enzyme Mechanism and Differences in Substrate Specificity1[W][OA]</title><title>Plant physiology (Bethesda)</title><description>In plants, oxylipins regulate developmental processes and defense responses. The first specific step in the biosynthesis of the cyclopentanone class of oxylipins is catalyzed by allene oxide cyclase (
AOC
) that forms cis(+)-12-oxo-phytodienoic acid. The moss
Physcomitrella patens
has two
AOCs
(PpAOC1 and PpAOC2) with different substrate specificities for C
18
- and C
20
-derived substrates, respectively. To better understand
AOC
’s catalytic mechanism and to elucidate the structural properties that explain the differences in substrate specificity, we solved and analyzed the crystal structures of 36 monomers of both apo and ligand complexes of PpAOC1 and PpAOC2. From these data, we propose the following intermediates in
AOC
catalysis: (1) a resting state of the apo enzyme with a closed conformation, (2) a first shallow binding mode, followed by (3) a tight binding of the substrate accompanied by conformational changes in the binding pocket, and (4) initiation of the catalytic cycle by opening of the epoxide ring. As expected, the substrate dihydro analog cis-12,13
S
-epoxy-9
Z
,15
Z
-octadecadienoic acid did not cyclize in the presence of PpAOC1; however, when bound to the enzyme, it underwent isomerization into the corresponding trans-epoxide. By comparing complex structures of the C
18
substrate analog with in silico modeling of the C
20
substrate analog bound to the enzyme allowed us to identify three major molecular determinants responsible for the different substrate specificities (i.e. larger active site diameter, an elongated cavity of PpAOC2, and two nonidentical residues at the entrance of the active site).</description><subject>Biochemical Processes and Macromolecular Structures</subject><issn>0032-0889</issn><issn>1532-2548</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2012</creationdate><recordtype>article</recordtype><recordid>eNqljE9LwzAYh4MorlOP3t8vsJmkLaYehFEnepAJFTyMUbLs7Rpp05CkQv0QfmY78eJ5p-eB3x9CrhmdM0aTG2tH8jmnKYvFCYlYGvMZTxNxSiJKR6dCZBMy9f6DUspilpyTCeeZuBUijch37gYfZANFcL0KvUMPXQWv9eBV1-rgsGkkWBnQeFiscgbS7A7C7-DZeL2vgwdtQgehRliar6FFeEFVS6N9-1t-0FWFDo3CQxOKfuuDGw-hsKh0pZUOA1u_b9arxeaSnFWy8Xj1xwty_7h8y59mtt-2uFNoxmlTWqdb6Yayk7r8nxhdl_vus4yTjKaCx0cf_ADiKXOc</recordid><startdate>20120917</startdate><enddate>20120917</enddate><creator>Neumann, Piotr</creator><creator>Brodhun, Florian</creator><creator>Sauer, Kristin</creator><creator>Herrfurth, Cornelia</creator><creator>Hamberg, Mats</creator><creator>Brinkmann, Jens</creator><creator>Scholz, Julia</creator><creator>Dickmanns, Achim</creator><creator>Feussner, Ivo</creator><creator>Ficner, Ralf</creator><general>American Society of Plant Biologists</general><scope>5PM</scope></search><sort><creationdate>20120917</creationdate><title>Crystal Structures of Physcomitrella patens AOC1 and AOC2: Insights into the Enzyme Mechanism and Differences in Substrate Specificity1[W][OA]</title><author>Neumann, Piotr ; Brodhun, Florian ; Sauer, Kristin ; Herrfurth, Cornelia ; Hamberg, Mats ; Brinkmann, Jens ; Scholz, Julia ; Dickmanns, Achim ; Feussner, Ivo ; Ficner, Ralf</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-pubmedcentral_primary_oai_pubmedcentral_nih_gov_34905823</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2012</creationdate><topic>Biochemical Processes and Macromolecular Structures</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Neumann, Piotr</creatorcontrib><creatorcontrib>Brodhun, Florian</creatorcontrib><creatorcontrib>Sauer, Kristin</creatorcontrib><creatorcontrib>Herrfurth, Cornelia</creatorcontrib><creatorcontrib>Hamberg, Mats</creatorcontrib><creatorcontrib>Brinkmann, Jens</creatorcontrib><creatorcontrib>Scholz, Julia</creatorcontrib><creatorcontrib>Dickmanns, Achim</creatorcontrib><creatorcontrib>Feussner, Ivo</creatorcontrib><creatorcontrib>Ficner, Ralf</creatorcontrib><collection>PubMed Central (Full Participant titles)</collection><jtitle>Plant physiology (Bethesda)</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Neumann, Piotr</au><au>Brodhun, Florian</au><au>Sauer, Kristin</au><au>Herrfurth, Cornelia</au><au>Hamberg, Mats</au><au>Brinkmann, Jens</au><au>Scholz, Julia</au><au>Dickmanns, Achim</au><au>Feussner, Ivo</au><au>Ficner, Ralf</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Crystal Structures of Physcomitrella patens AOC1 and AOC2: Insights into the Enzyme Mechanism and Differences in Substrate Specificity1[W][OA]</atitle><jtitle>Plant physiology (Bethesda)</jtitle><date>2012-09-17</date><risdate>2012</risdate><volume>160</volume><issue>3</issue><spage>1251</spage><epage>1266</epage><pages>1251-1266</pages><issn>0032-0889</issn><eissn>1532-2548</eissn><abstract>In plants, oxylipins regulate developmental processes and defense responses. The first specific step in the biosynthesis of the cyclopentanone class of oxylipins is catalyzed by allene oxide cyclase (
AOC
) that forms cis(+)-12-oxo-phytodienoic acid. The moss
Physcomitrella patens
has two
AOCs
(PpAOC1 and PpAOC2) with different substrate specificities for C
18
- and C
20
-derived substrates, respectively. To better understand
AOC
’s catalytic mechanism and to elucidate the structural properties that explain the differences in substrate specificity, we solved and analyzed the crystal structures of 36 monomers of both apo and ligand complexes of PpAOC1 and PpAOC2. From these data, we propose the following intermediates in
AOC
catalysis: (1) a resting state of the apo enzyme with a closed conformation, (2) a first shallow binding mode, followed by (3) a tight binding of the substrate accompanied by conformational changes in the binding pocket, and (4) initiation of the catalytic cycle by opening of the epoxide ring. As expected, the substrate dihydro analog cis-12,13
S
-epoxy-9
Z
,15
Z
-octadecadienoic acid did not cyclize in the presence of PpAOC1; however, when bound to the enzyme, it underwent isomerization into the corresponding trans-epoxide. By comparing complex structures of the C
18
substrate analog with in silico modeling of the C
20
substrate analog bound to the enzyme allowed us to identify three major molecular determinants responsible for the different substrate specificities (i.e. larger active site diameter, an elongated cavity of PpAOC2, and two nonidentical residues at the entrance of the active site).</abstract><pub>American Society of Plant Biologists</pub><pmid>22987885</pmid><doi>10.1104/pp.112.205138</doi></addata></record> |
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source | JSTOR Archive Collection A-Z Listing; Oxford University Press Journals All Titles (1996-Current); EZB-FREE-00999 freely available EZB journals |
subjects | Biochemical Processes and Macromolecular Structures |
title | Crystal Structures of Physcomitrella patens AOC1 and AOC2: Insights into the Enzyme Mechanism and Differences in Substrate Specificity1[W][OA] |
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