Abstract
BackgroundIsoprenoids are the most ancient and essential class of metabolites produced in all organisms, either via mevalonate (MVA)-and/or methylerythritol phosphate (MEP)-pathways. The MEP-pathway is present in all plastid-bearing organisms and most eubacteria. However, no comprehensive study reveals the origination and evolutionary characteristics of MEP-pathway genes in eukaryotes.ResultsHere, detailed bioinformatics analyses of the MEP-pathway provide an in-depth understanding the evolutionary history of this indispensable biochemical route, and offer a basis for the co-existence of the cytosolic MVA- and plastidial MEP-pathway in plants given the established exchange of the end products between the two isoprenoid-biosynthesis pathways. Here, phylogenetic analyses establish the contributions of both cyanobacteria and Chlamydiae sequences to the plant’s MEP-pathway genes. Moreover, Phylogenetic and inter-species syntenic block analyses demonstrate that six of the seven MEP-pathway genes have predominantly remained as single-copy in land plants in spite of multiple whole-genome duplication events (WGDs). Substitution rate and domain studies display the evolutionary conservation of these genes, reinforced by their high expression levels. Distinct phenotypic variation among plants with reduced expression levels of individual MEP-pathway genes confirm the indispensable function of each nuclear-encoded plastid-targeted MEP-pathway enzyme in plant growth and development.ConclusionCollectively, these findings reveal the polyphyletic origin and restrict conservation of MEP-pathway genes, and reinforce the potential function of the individual enzymes beyond production of the isoprenoids intermediates.
Highlights
Isoprenoids are the most ancient and essential class of metabolites produced in all organisms, either via mevalonate (MVA)-and/or methylerythritol phosphate (MEP)-pathways
MEP-pathway genes in plastid-bearing eukaryotes are derived from different bacteria lineages To gain insight into the evolution of the MEP-pathway genes, we constructed phylogenetic trees for individual genes by using protein sequences of a wide range of species from eukaryotes, cyanobacteria, PVC (Planctomycetes, Verrucomicrobia and Chlamydiae) group bacteria, and other non-cyanobacteria and non-PVC group bacteria
These analyses reveal the multiple origins of MEP-pathway genes in plastid-bearing eukaryotes (Figs. 2 a-f, 3 and S1-S7)
Summary
Isoprenoids are the most ancient and essential class of metabolites produced in all organisms, either via mevalonate (MVA)-and/or methylerythritol phosphate (MEP)-pathways. Isoprenoid-derived compounds in free-living organisms range from hormones, lipids, pigments, vitamins, electron transport chain and defense compounds, and as such of industrial interests for drugs, agrochemicals, rubber and fragrances [2]. Despite their diversity, isoprenoids are derived from two universal five-carbon precursors, isopentenyl diphosphate (IPP) and its isomer dimethylallyl diphosphate (DMAPP) [3]. These precursors are synthesized either by mevalonate (MVA)-pathway [4] and/or by the alternative route methyl erythritol phosphate (MEP)pathway [5]. Plastid-bearing eukaryotes are unique as they have retained both pathways compartmentalized in the cytosol (MVA) and
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