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


CONCLUSIONS
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.
Keurentjes
Joost J B
JJ
Laboratory of Genetics, Wageningen University, Arboretumlaan, NL-6703 BD Wageningen, The Netherlands. joost.keurentjes@wur.nl
Sulpice
Ronan
R
Gibon
Yves
Y
Steinhauser
Marie-Caroline
MC
Fu
Jingyuan
J
Koornneef
Maarten
M
Stitt
Mark
M
Vreugdenhil
Dick
D
D017360:Arabidopsis / Q000201:enzymology / Q000235:genetics / Q000378:metabolism*; D029681:Arabidopsis Proteins / Q000235:genetics*; D050260:Carbohydrate Metabolism / Q000235:genetics*; D002874:Chromosome Mapping; D004843:Epistasis, Genetic; D014644:Genetic Variation; D008126:Lod Score; D025341:Principal Component Analysis; D040641:Quantitative Trait Loci; D012333:RNA, Messenger / Q000378:metabolism
D029681:Arabidopsis Proteins; D012333:RNA, Messenger