Research

Integrative analyses of genetic variation in enzyme activities of primary carbohydrate metabolism reveal distinct modes of regulation in Arabidopsis thaliana

Joost JB Keurentjes^1,2,3 , Ronan Sulpice⁴ , Yves Gibon⁴ , Marie-Caroline Steinhauser⁴ , Jingyuan Fu⁵ , Maarten Koornneef^1,6 , Mark Stitt⁴ and Dick Vreugdenhil²

¹  Laboratory of Genetics, Wageningen University, Arboretumlaan, NL-6703 BD Wageningen, The Netherlands

²  Laboratory of Plant Physiology, Wageningen University, Arboretumlaan, NL-6703 BD Wageningen, The Netherlands

³  Centre for Biosystems Genomics, Droevendaalsesteeg, NL-6708 PB Wageningen, The Netherlands

⁴  Max Planck Institute for Molecular Plant Physiology, Am Mühlenberg, 14476 Potsdam-Golm, Germany

⁵  Groningen Bioinformatics Centre, Groningen Biomolecular Sciences and Biotechnology Institute, University of Groningen, Kerklaan, NL-9751 NN Haren, The Netherlands

⁶  Max Planck Institute for Plant Breeding Research, Carl-von-Linné-Weg 10, 50829, Cologne, Germany

author email corresponding author email

Genome Biology 2008, 9:R129doi:10.1186/gb-2008-9-8-r129

Published:	18 August 2008

Subject areas: Biochemistry and structural biology, Plant biology, Genetics

Abstract

Background

Plant primary carbohydrate metabolism is complex and flexible, and is regulated at many levels. Changes of transcript levels do not always lead to changes in enzyme activities, and these do not always affect metabolite levels and fluxes. To analyze interactions between these three levels of function, we have performed parallel genetic analyses of 15 enzyme activities involved in primary carbohydrate metabolism, transcript levels for their encoding structural genes, and a set of relevant metabolites. Quantitative analyses of each trait were performed in the Arabidopsis thaliana Ler × Cvi recombinant inbred line (RIL) population and subjected to correlation and quantitative trait locus (QTL) analysis.

Results

Traits affecting primary metabolism were often correlated, possibly due to developmental control affecting multiple genes, enzymes, or metabolites. Moreover, the activity QTLs of several enzymes co-localized with the expression QTLs (eQTLs) of their structural genes, or with metabolite accumulation QTLs of their substrates or products. In addition, many trait-specific QTLs were identified, revealing that there is also specific regulation of individual metabolic traits. Regulation of enzyme activities often occurred through multiple loci, involving both cis- and trans-acting transcriptional or post-transcriptional control of structural genes, as well as independently of the structural genes.

Conclusion

Future studies of the regulatory processes in primary carbohydrate metabolism will benefit from an integrative genetic analysis of gene transcription, enzyme activity, and metabolite content. The multiparallel QTL analyses of the various interconnected transducers of biological information flow, described here for the first time, can assist in determining the causes and consequences of genetic regulation at different levels of complex biological systems.