The ancient CYP716 family is a major contributor to the diversification of eudicot triterpenoid biosynthesis.
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ABSTRACT:
SUBMITTER: Miettinen K
PROVIDER: S-EPMC5303825 | biostudies-literature | 2017 Feb
REPOSITORIES: biostudies-literature
Publications
The ancient CYP716 family is a major contributor to the diversification of eudicot triterpenoid biosynthesis.
Miettinen Karel K Pollier Jacob J Buyst Dieter D Arendt Philipp P Csuk René R Sommerwerk Sven S Moses Tessa T Mertens Jan J Sonawane Prashant D PD Pauwels Laurens L Aharoni Asaph A Martins José J Nelson David R DR Goossens Alain A
Nature communications 20170206
Triterpenoids are widespread bioactive plant defence compounds with potential use as pharmaceuticals, pesticides and other high-value products. Enzymes belonging to the cytochrome P450 family have an essential role in creating the immense structural diversity of triterpenoids across the plant kingdom. However, for many triterpenoid oxidation reactions, the corresponding enzyme remains unknown. Here we characterize CYP716 enzymes from different medicinal plant species by heterologous expression i ...[more]
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Project description:Triterpenoids are a group of structurally diverse specialized metabolites that frequently show useful bioactivities. These chemicals are biosynthesized from the common precursor 2,3-oxidosqualene in plants. The carbon skeletons produced by oxidosqualene cyclase (OSC) are usually modified by cytochrome P450 monooxygenases (P450s) and UDP-dependent glycosyltransferases. These biosynthetic enzymes contribute to the structural diversification of plant triterpenoids. Until now, many P450 enzymes have been characterized as triterpenoid oxidases. Among them, the CYP716 family P450 enzymes, which have been isolated from a wide range of plant families, seem to contribute to the triterpenoid structural diversification. Many CYP716 family P450 enzymes have been characterized as the multifunctional triterpene C-28 oxidases, which oxidize α-amyrin and β-amyrin to the widely distributed triterpenoids ursolic and oleanolic acids, respectively. Tomato (Solanum lycopersicum) is one of the most important solanaceous crops in the world. However, little information is known regarding its triterpenoid biosynthesis. To understand the mechanism of triterpenoid biosynthesis in tomato, we focused on the function of CYP716 family enzymes as triterpenoid oxidases. We isolated all six CYP716 family genes from the Micro-Tom cultivar of tomato, and functionally characterized them in the heterologous yeast expression system. The in vivo enzymatic assays showed that CYP716A44 and CYP716A46 exhibited the ordinary C-28 oxidation activity against α-amyrin and β-amyrin to produce ursolic and oleanolic acids, respectively. Interestingly, one CYP716E subfamily enzyme, CYP716E26, exhibited the previously unreported C-6β hydroxylation activity against β-amyrin to produce a rare bioactive triterpenoid, daturadiol (olean-12-ene-3β,6β-diol). To determine the roles of the CYP716 family genes in tomato triterpenoid biosynthesis, we analyzed the gene expression and triterpenoid accumulation patterns in different plant tissues by performing the quantitative real-time polymerase chain reaction (qPCR) and gas chromatography-mass spectrometry (GC-MS) analyses, respectively. High levels of the CYP716A44 gene expression and the accumulation of C-28-oxidized triterpenoids, ursolic acid, and oleanolic acid were observed in the roots, indicating a significant contribution of the CYP716A44 gene in the triterpenoid biosynthesis in tomato. Thus, our study partially elucidated the mechanism of triterpenoid biosynthesis in tomato, and identified CYP716E26 as a novel C-6β hydroxylase for its subsequent use in the combinatorial biosynthesis of bioactive triterpenoids.
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Project description:Eudicots account for ~75% of living angiosperms, containing important food and energy crops. Recently, high-quality genome sequences of several eudicots including Aquilegia coerulea and Nelumbo nucifera have become available, providing an opportunity to investigate the early evolutionary characteristics of eudicots. We performed genomic hierarchical and event-related alignments to infer homology within and between representative species of eudicots. The results provide strong evidence for multiple independent polyploidization events during the early diversification of eudicots, three of which are likely to be allopolyploids: The core eudicot-common hexaploidy (ECH), Nelumbo-specific tetraploidy (NST), and Ranunculales-common tetraploidy (RCT). Using different genomes as references, we constructed genomic alignment to list the orthologous and paralogous genes produced by polyploidization and speciation. This could provide a fundamental framework for studying other eudicot genomes and gene(s) evolution. Further, we revealed significantly divergent evolutionary rates among these species. By performing evolutionary rate correction, we dated RCT to be ~118-134 million years ago (Mya), after Ranunculales diverged with core eudicots at ~123-139 Mya. Moreover, we characterized genomic fractionation resulting from gene loss and retention after polyploidizations. Notably, we revealed a high degree of divergence between subgenomes. In particular, synonymous nucleotide substitutions at synonymous sites (Ks) and phylogenomic analyses implied that A. coerulea might provide the subgenome(s) for the gamma-hexaploid hybridization.
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Project description:Alkylresorcinols are members of an extensive family of bioactive compounds referred to as phenolic lipids, which occur primarily in plants, fungi, and bacteria. In plants, alkylresorcinols and their derivatives are thought to serve important roles as phytoanticipins and allelochemicals, although direct evidence for this is still somewhat lacking. Specialized type III polyketide synthases (referred to as 'alkylresorcinol synthases'), which catalyze the formation of 5-alkylresorcinols using fatty acyl-CoA starter units and malonyl-CoA extender units, have been characterized from several microbial species, however until very recently little has been known concerning their plant counterparts. Through the use of sorghum and rice EST and genomic data sets, significant inroads have now been made in this regard. Here we provide additional information concerning our recent report on the identification and characterization of alkylresorcinol synthases from Sorghum bicolor and Oryza sativa, as well as a brief consideration of the emergence of this intriguing subfamily of enzymes.
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Project description:BackgroundYeast and animal cells require six mini-chromosome maintenance proteins (Mcm2-7) for pre-replication complex formation, DNA replication initiation and DNA synthesis. These six individual MCM proteins form distinct heterogeneous subunits within a hexamer which is believed to form the replicative helicase and which associates with the essential but non-homologous Mcm10 protein during DNA replication. In contrast Archaea generally only possess one MCM homologue which forms a homohexameric MCM helicase. In some eukaryotes Mcm8 and Mcm9 paralogues also appear to be involved in DNA replication although their exact roles are unclear.ResultsWe used comparative genomics and phylogenetics to reconstruct the diversification of the eukaryotic Mcm2-9 gene family, demonstrating that Mcm2-9 were formed by seven gene duplication events before the last common ancestor of the eukaryotes. Mcm2-7 protein paralogues were present in all eukaryote genomes studied suggesting that no gene loss or functional replacements have been tolerated during the evolutionary diversification of eukaryotes. Mcm8 and 9 are widely distributed in eukaryotes and group together on the MCM phylogenetic tree to the exclusion of all other MCM paralogues suggesting co-ancestry. Mcm8 and Mcm9 are absent in some taxa, including Trichomonas and Giardia, and appear to have been secondarily lost in some fungi and some animals. The presence and absence of Mcm8 and 9 is concordant in all taxa sampled with the exception of Drosophila species. Mcm10 is present in most eukaryotes sampled but shows no concordant pattern of presence or absence with Mcm8 or 9.ConclusionA multifaceted and heterogeneous Mcm2-7 hexamer evolved during the early evolution of the eukaryote cell in parallel with numerous other acquisitions in cell complexity and prior to the diversification of extant eukaryotes. The conservation of all six paralogues throughout the eukaryotes suggests that each Mcm2-7 hexamer component has an exclusive functional role, either by a combination of unique lock and key interactions between MCM hexamer subunits and/or by a range of novel side interactions. Mcm8 and 9 evolved early in eukaryote cell evolution and their pattern of presence or absence suggests that they may have linked functions. Mcm8 is highly divergent in all Drosophila species and may not provide a good model for Mcm8 in other eukaryotes.
| S-EPMC2667178 | biostudies-literature
Project description:BackgroundMicroRNAs (miRNAs) play important roles in plant growth and development. MiRNAs and their targets have been widely studied in model plants, but limited knowledge is available concerning this small RNA population and their targets in sacred lotus (Nelumbo nucifera Gaertn.).ResultsIn this study, a total of 145 known miRNAs belonging to 47 families and 78 novel miRNAs were identified during seed germination using high-throughput small RNA sequencing. Furthermore, some miRNA families which have not yet been reported in monocot or eudicot species were detected in N. nucifera, indicating that these miRNAs was divergence from monocots and core eudicots during evolution. Using degradome sequencing, 2580 targets were detected for all the miRNAs. GO (Gene Ontology) and KEGG pathway analyses showed that many target genes enriched in "regulation of transcription" and involved in "carbohydrate", "amino acid and energy metabolism". Nine miRNAs and three corresponding targets of them were further validated by quantitative RT-PCR.ConclusionsThe results present here suggested that many miRNAs were involved in the regulation of seed germination of sacred lotus, providing a foundation for future studies of sacred lotus seed longevity. Comparative analysis of miRNAs from different plants also provided insight into the evolutionary gains and losses of miRNAs in plants.
| S-EPMC5002175 | biostudies-literature
Project description:BackgroundBecause of their known role as transcriptional regulators of key plant developmental processes, the diversification of MADS-box gene function is thought to be a major driving force in the developmental evolution of plants. Yet the function of some MADS-box gene subfamilies has remained elusive thus far. One such lineage, AGL6, has now been functionally characterized in three angiosperm species, but a phylogenetic framework for comparison of AGL6 gene function is currently missing.ResultsBased on phylogenetic analyses of newly isolated and EST-based sequences, we describe the duplication history of the AGL6 subfamily in angiosperms. Our analyses provide support for four ancient duplications in the evolution of the AGL6 lineage: one at the base of core eudicots resulting in euAGL6 and AGL6-like gene clades, one during basal angiosperm diversification and two in monocot evolution. To investigate whether the spatial domains in which AGL6 genes function have diverged after duplication, we use quantitative Real Time PCR. We show that the core eudicot AGL6-like clade acquired expression in vegetative tissues, while its paralog euAGL6 remains predominantly confined to reproductive tissues.ConclusionsThese and previous data lead us to propose that the AGL6 lineage in core eudicots, in addition to functions related to the expression in reproductive structures, may have acquired a function in developmental transitions of vegetative shoots.
| S-EPMC3095293 | biostudies-literature