Distinct evolutionary strategies in the GGPPS family from plants.

Diana Coman,Stefan Zoller,Eva Vranovã¡,Wilhelm Gruissem,Adrian Altenhoff

doi:10.3389/fpls.2014.00230

Abstract

Multiple geranylgeranyl diphosphate synthases (GGPPS) for biosynthesis of geranylgeranyl diphosphate (GGPP) exist in plants. GGPP is produced in the isoprenoid pathway and is a central precursor for various primary and specialized plant metabolites. Therefore, its biosynthesis is an essential regulatory point in the isoprenoid pathway. We selected 119 GGPPSs from 48 species representing all major plant lineages, based on stringent homology criteria. After the diversification of land plants, the number of GGPPS paralogs per species increases. Already in the moss Physcomitrella patens, GGPPS appears to be encoded by multiple paralogous genes. In gymnosperms, neofunctionalization of GGPPS may have enabled optimized biosynthesis of primary and specialized metabolites. Notably, lineage-specific expansion of GGPPS occurred in land plants. As a representative species we focused here on Arabidopsis thaliana, which retained the highest number of GGPPS paralogs (twelve) among the 48 species we considered in this study. Our results show that the A. thaliana GGPPS gene family is an example of evolution involving neo- and subfunctionalization as well as pseudogenization. We propose subfunctionalization as one of the main mechanisms allowing the maintenance of multiple GGPPS paralogs in A. thaliana genome. Accordingly, the changes in the expression patterns of the GGPPS paralogs occurring after gene duplication led to developmental and/or condition specific functional evolution.

Highlights

Isoprenoids represent the largest group of biologically active specialized metabolites in plants
We have focused on the model plant A. thaliana whose nuclear genome retained 12 geranylgeranyl diphosphate synthases (GGPPS) (Lange and Ghassemian, 2003), the highest number of GGPPS paralogs in plants whose genomes have been sequenced to date
THE NUMBER OF GGPPS GENE PARALOGS INCREASES DURING THE EVOLUTION OF PLANT FUNCTIONAL COMPLEXITY We have investigated the phylogenetic relationships among GGPPSs from plants to infer evolutionary mechanisms leading to the formation and maintenance of multiple gene copies within the A. thaliana genome, which had retained the highest number of paralogs

Summary

Introduction

Isoprenoids represent the largest group of biologically active specialized metabolites in plants. Other isoprenoids have important roles in photosynthesis and respiration or as hormones (abscisic acid, brassinosteroids, cytokinins, gibberellic acid, strigolactones) in development and growth regulation (Bouvier et al, 2005; Liang, 2009; Vranová et al, 2012). In spite of their broad diversity of functions and structures, the biosynthesis of all isoprenoids in plants invariably requires two five-carbon (C5) building units: the isopentenyl diphosphate (IPP) and its isomer dimethylallyl diphosphate (DMAPP) (Liang et al, 2002; Hsieh et al, 2011; Vranová et al, 2013). Most of the essential plant isoprenoids are derived from the C15 and C20 allylic prenyl diphosphates farnesyl-PP (FPP)

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Conclusion