Activity Regulation by Heteromerization of Arabidopsis Allene Oxide Cyclase Family Members

. 2016 Jan 06 ; 5 (1) : . [epub] 20160106

Status PubMed-not-MEDLINE Jazyk angličtina Země Švýcarsko Médium electronic

Typ dokumentu časopisecké články

Perzistentní odkaz   https://www.medvik.cz/link/pmid27135223

Jasmonates (JAs) are lipid-derived signals in plant stress responses and development. A crucial step in JA biosynthesis is catalyzed by allene oxide cyclase (AOC). Four genes encoding functional AOCs (AOC1, AOC2, AOC3 and AOC4) have been characterized for Arabidopsis thaliana in terms of organ- and tissue-specific expression, mutant phenotypes, promoter activities and initial in vivo protein interaction studies suggesting functional redundancy and diversification, including first hints at enzyme activity control by protein-protein interaction. Here, these analyses were extended by detailed analysis of recombinant proteins produced in Escherichia coli. Treatment of purified AOC2 with SDS at different temperatures, chemical cross-linking experiments and protein structure analysis by molecular modelling approaches were performed. Several salt bridges between monomers and a hydrophobic core within the AOC2 trimer were identified and functionally proven by site-directed mutagenesis. The data obtained showed that AOC2 acts as a trimer. Finally, AOC activity was determined in heteromers formed by pairwise combinations of the four AOC isoforms. The highest activities were found for heteromers containing AOC4 + AOC1 and AOC4 + AOC2, respectively. All data are in line with an enzyme activity control of all four AOCs by heteromerization, thereby supporting a putative fine-tuning in JA formation by various regulatory principles.

Zobrazit více v PubMed

Wasternack C., Hause B. Jasmonates: Biosynthesis, perception, signal transduction and action in plant stress response, growth and development. An update to the 2007 review in Annals of Botany. Ann. Bot. 2013;111:1021–1058. doi: 10.1093/aob/mct067. PubMed DOI PMC

Chung H.S., Koo A.J.K., Gao X., Jayanty S., Thines B., Jones A.D., Howe G.A. Regulation and function of Arabidopsis JASMONATE ZIM-domain genes in response to wounding and herbivory. Plant Physiol. 2008;146:952–964. doi: 10.1104/pp.107.115691. PubMed DOI PMC

Laudert D., Schaller F., Weiler E. Transgenic Nicotiana tabacum and Arabidopsis thaliana plants overexpressing allene oxide synthase. Planta. 2000;211:163–165. doi: 10.1007/s004250000316. PubMed DOI

Stenzel I., Hause B., Maucher H., Pitzschke A., Miersch O., Ziegler J., Ryan C., Wasternack C. Allene oxide cyclase dependence of the wound response and vascular bundle-specific generation of jasmonates in tomato - amplification in wound signaling. Plant J. 2003;33:577–589. doi: 10.1046/j.1365-313X.2003.01647.x. PubMed DOI

Hause B., Stenzel I., Miersch O., Maucher H., Kramell R., Ziegler J., Wasternack C. Tissue-specific oxylipin signature of tomato flowers: Allene oxide cyclase is highly expressed in distinct flower organs and vascular bundles. Plant J. 2000;24:113–126. doi: 10.1046/j.1365-313x.2000.00861.x. PubMed DOI

Chauvin A., Caldelari D., Wolfender J.-L., Farmer E.E. Four 13-lipoxygenases contribute to rapid jasmonate synthesis in wounded Arabidopsis thaliana leaves: a role for lipoxygenase 6 in responses to long-distance wound signals. New Phytol. 2013;197:566–575. doi: 10.1111/nph.12029. PubMed DOI

Gasperini D., Chételat A., Acosta I.F., Goossens J., Pauwels L., Goossens A., Dreos R., Alfonso E., Farmer E.E. Multilayered organization of jasmonate signalling in the regulation of root growth. PLoS Genetics. 2015;11:3. doi: 10.1371/journal.pgen.1005300. PubMed DOI PMC

Breithaupt C., Kurzbauer R., Lilie H., Schaller A., Strassner J., Huber R., Macheroux P., Clausen T. Crystal structure of 12-oxophytodienoate reductase 3 from tomato: Self-inhibition by dimerization. Proc. Natl. Acad. Sci. USA. 2006;103:14337–14342. doi: 10.1073/pnas.0606603103. PubMed DOI PMC

Stenzel I., Otto M., Delker C., Kirmse N., Schmidt D., Miersch O., Hause B., Wasternack C. ALLENE OXIDE CYCLASE (AOC) gene family members of Arabidopsis thaliana: tissue- and organ-specific promoter activities and in vivo heteromerization. J. Exper. Bot. 2012;63:6125–6138. doi: 10.1093/jxb/ers261. PubMed DOI PMC

Miersch O., Wasternack C. Octadecanoid and jasmonate signaling in tomato (Lycopersicon esculentum Mill.) leaves: Endogenous jasmonates do not induce jasmonate biosynthesis. Biol. Chem. 2000;381:715–722. doi: 10.1515/BC.2000.092. PubMed DOI

Scholz S.S., Reichelt M., Boland W., Mithöfer A. Additional evidence against jasmonate-induced jasmonate induction hypothesis. Plant Sci. 2015;239:9–14. doi: 10.1016/j.plantsci.2015.06.024. PubMed DOI

Hofmann E., Zerbe P., Schaller F. The crystal structure of Arabidopsis thaliana allene oxide cyclase: Insights into the oxylipin cyclization reaction. Plant Cell. 2006;18:3201–3217. doi: 10.1105/tpc.106.043984. PubMed DOI PMC

Stenzel I., Hause B., Miersch O., Kurz T., Maucher H., Weichert H., Ziegler J., Feussner I., Wasternack C. Jasmonate biosynthesis and the allene oxide cyclase family of Arabidopsis thaliana. Plant Mol. Biol. 2003;51:895–911. doi: 10.1023/A:1023049319723. PubMed DOI

Sinz A. Chemical cross-linking and FTICR mass spectrometry for protein structure characterization. Anal. Bional. Chem. 2005;381:44–47. doi: 10.1007/s00216-004-2824-6. PubMed DOI

Ziegler J., Stenzel I., Hause B., Maucher H., Hamberg M., Grimm R., Ganal M., Wasternack C. Molecular cloning of allene oxide cyclase: The enzyme establishing the stereochemistry of octadecanoids and jasmonates. J. Biol. Chem. 2000;275:19132–19138. doi: 10.1074/jbc.M002133200. PubMed DOI

Levin E.J., Kondrashov D.A., Wesenberg G.E., Phillips G.N. Ensemble refinement of protein crystal structures: validation and application. Structure. 2007;15:1040–1052. doi: 10.1016/j.str.2007.06.019. PubMed DOI PMC

Hofmann E., Pollmann S. Molecular mechanism of enzymatic allene oxide cyclization in plants. Plant Physiol. Biochem. 2008;46:302–308. doi: 10.1016/j.plaphy.2007.12.007. PubMed DOI

Neumann P., Brodhun F., Sauer K., Herrfurth C., Hamberg M., Brinkmann J., Scholz J., Dickmanns A., Feussner I., Ficner R. Crystal structures of Physcomitrella patens AOC1 and AOC2: Insights into the enzyme mechanism and differences in substrate specificity. Plant Physiol. 2012;160:1251–1266. doi: 10.1104/pp.112.205138. PubMed DOI PMC

Schaller F., Zerbe P., Reinbothe S., Reinbothe C., Hofmann E., Pollmann S. The allene oxide cyclase family of Arabidopsis thaliana—localization and cyclization. FEBS J. 2008;275:2428–2441. doi: 10.1111/j.1742-4658.2008.06388.x. PubMed DOI

Gasperini D., Chauvin A., Acosta I.F., Kurenda A., Stolz S., Chételat A., Wolfender J.-L., Farmer E.E. Axial and radial oxylipin transport. Plant Physiol. 2015;169:2244–2254. doi: 10.1104/pp.15.01104. PubMed DOI PMC

Browse J. The power of mutants for investigating jasmonate biosynthesis and signaling. Phytochemistry. 2009;70:1539–1546. doi: 10.1016/j.phytochem.2009.08.004. PubMed DOI

Maucher H., Hause B., Feussner I., Ziegler J., Wasternack C. Allene oxide synthases of barley (Hordeum vulgare cv. Salome): Tissue specific regulation in seedling development. Plant J. 2000;21:199–213. doi: 10.1046/j.1365-313x.2000.00669.x. PubMed DOI

MacKerell J.A.D., Banavali N., Foloppe N. Development and current status of the CHARMM force field for nucleic acids. Biopolymers. 2001;56:257–265. doi: 10.1002/1097-0282(2000)56:4<257::AID-BIP10029>3.0.CO;2-W. PubMed DOI

Wojciechowski M., Lesyng B. Generalized born model: Analysis, refinement, and applications to proteins. J. Phys. Chem. B. 2004;108:18368–18376. doi: 10.1021/jp046748b. DOI

Kumar S., Nussinov R. Close-range electrostatic interactions in proteins. ChemBioChem. 2002;3:604–617. doi: 10.1002/1439-7633(20020703)3:7<604::AID-CBIC604>3.0.CO;2-X. PubMed DOI

Laemmli U.K. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature. 1970;227:680–685. doi: 10.1038/227680a0. PubMed DOI

Ziegler J., Hamberg M., Miersch O., Parthier B. Purification and characterization of allene oxide cyclase from dry corn seeds. Plant Physiol. 1997;114:565–573. PubMed PMC

Lischweski S., Muchow A., Guthörl D., Hause B. Jasmonates act positively in adventitious root formation in petunia cuttings. BMC Plant Biol. 2015;15:3. doi: 10.1186/s12870-015-0615-1. PubMed DOI PMC

Ziegler J., Wasternack C., Hamberg M. On the specificity of allene oxide cyclase. Lipids. 1999;34:1005–1015. doi: 10.1007/s11745-999-0451-z. PubMed DOI

Tsuchisaka A., Theologis A. Unique and overlapping expression patterns among the Arabidopsis 1-amino-cyclopropane-1-carboxylate synthase gene family members. Plant Physiol. 2004;136:2982–3000. doi: 10.1104/pp.104.049999. PubMed DOI PMC

Tsuchisaka A., Theologis A. Heterodimeric interactions among the 1-amino-cyclopropane-1-carboxylate synthase polypeptides encoded by the Arabidopsis gene family. Proc. Natl. Acad. Sci. USA. 2004;101:2275–2280. doi: 10.1073/pnas.0308515101. PubMed DOI PMC

Wasternack C. Jasmonates: An update on biosynthesis, signal transduction and action in plant stress response, growth and development. Ann. Bot. 2007;100:681–697. doi: 10.1093/aob/mcm079. PubMed DOI PMC

Schaller A., Stintzi A. Enzymes in jasmonate biosynthesis—Structure, function, regulation. Phytochemistry. 2009;70:1532–1538. doi: 10.1016/j.phytochem.2009.07.032. PubMed DOI

Najít záznam

Citační ukazatele

Nahrávání dat ...

Možnosti archivace

Nahrávání dat ...