In Planta Recapitulation of Isoprene Synthase Evolution from Ocimene Synthases

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Titel: In Planta Recapitulation of Isoprene Synthase Evolution from Ocimene Synthases
Autoren: Urska Vrhovsek, Luca Cappellin, Jia Xu, Silvia Carlin, Enrico Barbaro, Francesco Loreto, Alberto Algarra Alarcon, Violeta Velikova, Claudio Varotto, Mingai Li
Weitere Verfasser: Li, M., Xu, J., Algarra Alarcon, A., Carlin, S., Barbaro, E., Cappellin, L., Velikova, V., Vrhovsek, U., Loreto, F., Varotto, C.
Quelle: Mol Biol Evol
Molecular Biology and Evolution
Verlagsinformationen: Oxford University Press (OUP), 2017.
Publikationsjahr: 2017
Schlagwörter: 0301 basic medicine, BIOCHEMICAL-CHARACTERIZATION, Short-chain terpene synthases parallel evolution, TERPENE SYNTHASES, Substrate specificity, Ocimene synthase, Arabidopsis, Evolution, Molecular, 03 medical and health sciences, Hemiterpenes, Pentanes, Isoprene synthase evolution, Site-directed mutagenesis, Active site size modulation, Butadienes, Amino Acid Sequence, SPECIFICITY, Discoveries, GENE-EXPRESSION, Plant Proteins, 0303 health sciences, Alkyl and Aryl Transferases, IDENTIFICATION, Sequence Homology, Amino Acid, Settore BIO/02 - BOTANICA SISTEMATICA, ENZYME PROMISCUITY, PERFORMANCE, 15. Life on land, ARABIDOPSIS, MODEL, Mutagenesis, Site-Directed, EMISSION
Beschreibung: Isoprene is the most abundant biogenic volatile hydrocarbon compound naturally emitted by plants and plays a major role in atmospheric chemistry. It has been proposed that isoprene synthases (IspS) may readily evolve from other terpene synthases, but this hypothesis has not been experimentally investigated. We isolated and functionally validated in Arabidopsis the first isoprene synthase gene, AdoIspS, from a monocotyledonous species (Arundo donax L., Poaceae). Phylogenetic reconstruction indicates that AdoIspS and dicots isoprene synthases most likely originated by parallel evolution from TPS-b monoterpene synthases. Site-directed mutagenesis demonstrated invivo the functional and evolutionary relevance of the residues considered diagnostic for IspS function. One of these positions was identified by saturating mutagenesis as a major determinant of substrate specificity in AdoIspS able to cause invivo a dramatic change in total volatile emission from hemi- to monoterpenes and supporting evolution of isoprene synthases from ocimene synthases. The mechanism responsible for IspS neofunctionalization by active site size modulation by a single amino acid mutation demonstrated in this study might be general, as the very same amino acidic position is implicated in the parallel evolution of different short-chain terpene synthases from both angiosperms and gymnosperms. Based on these results, we present a model reconciling in a unified conceptual framework the apparently contrasting patterns previously observed for isoprene synthase evolution in plants. These results indicate that parallel evolution may be driven by relatively simple biophysical constraints, and illustrate the intimate molecular evolutionary links between the structural and functional bases of traits with global relevance.
Publikationsart: Article
Other literature type
Dateibeschreibung: application/pdf
Sprache: English
ISSN: 1537-1719
0737-4038
DOI: 10.1093/molbev/msx178
Zugangs-URL: https://academic.oup.com/mbe/article-pdf/34/10/2583/24366702/msx178.pdf
https://pubmed.ncbi.nlm.nih.gov/28637270
http://hdl.handle.net/11588/796450
http://europepmc.org/articles/PMC5850473/
https://pubmed.ncbi.nlm.nih.gov/28637270/
https://www.ncbi.nlm.nih.gov/pubmed/28637270
https://academic.oup.com/mbe/article/34/10/2583/3869250
https://hdl.handle.net/11577/3289211
https://doi.org/10.1093/molbev/msx178
Rights: CC BY NC
Dokumentencode: edsair.doi.dedup.....8a63e632abff8797e39796ad2a0a92e8
Datenbank: OpenAIRE
Beschreibung
Abstract:Isoprene is the most abundant biogenic volatile hydrocarbon compound naturally emitted by plants and plays a major role in atmospheric chemistry. It has been proposed that isoprene synthases (IspS) may readily evolve from other terpene synthases, but this hypothesis has not been experimentally investigated. We isolated and functionally validated in Arabidopsis the first isoprene synthase gene, AdoIspS, from a monocotyledonous species (Arundo donax L., Poaceae). Phylogenetic reconstruction indicates that AdoIspS and dicots isoprene synthases most likely originated by parallel evolution from TPS-b monoterpene synthases. Site-directed mutagenesis demonstrated invivo the functional and evolutionary relevance of the residues considered diagnostic for IspS function. One of these positions was identified by saturating mutagenesis as a major determinant of substrate specificity in AdoIspS able to cause invivo a dramatic change in total volatile emission from hemi- to monoterpenes and supporting evolution of isoprene synthases from ocimene synthases. The mechanism responsible for IspS neofunctionalization by active site size modulation by a single amino acid mutation demonstrated in this study might be general, as the very same amino acidic position is implicated in the parallel evolution of different short-chain terpene synthases from both angiosperms and gymnosperms. Based on these results, we present a model reconciling in a unified conceptual framework the apparently contrasting patterns previously observed for isoprene synthase evolution in plants. These results indicate that parallel evolution may be driven by relatively simple biophysical constraints, and illustrate the intimate molecular evolutionary links between the structural and functional bases of traits with global relevance.
ISSN:15371719
07374038
DOI:10.1093/molbev/msx178