Genome-Wide Association Mapping Reveals That Specific and Pleiotropic Regulatory Mechanisms Fine-Tune Central Metabolism and Growth in Arabidopsis

• Published in: The Plant cell 2017-10, Vol.29 (10), p.2349-2373
• Main Authors: Fusari, Corina M., Kooke, Rik, Lauxmann, Martin A., Annunziata, Maria Grazia, Enke, Beatrice, Hoehne, Melanie, Krohn, Nicole, Becker, Frank F.M., Schlereth, Armin, Sulpice, Ronan, Stitt, Mark, Keurentjes, Joost J.B.
• Format: Article
• Language: English
• Subjects: Adenosine diphosphate; Biomass; Biometris (WU MAT); Chromosome 4; Cues; Enzymatic activity; Enzyme activity; Enzymes; EPS; Fumarase; Gene mapping; Genome-wide association studies; Genomes; Glucose; Groep Koornneef; Invertase; Kinases; Laboratorium voor Erfelijkheidsleer; Laboratory of Genetics; Large-Scale Biology; LARGE-SCALE BIOLOGY ARTICLE; Mapping; Mathematical and Statistical Methods - Biometris; Metabolism; Metabolites; Phosphoglucose isomerase; Protein kinase; Proteins; Quantitative trait loci; Regulatory mechanisms (biology); Resource availability; Tradeoffs; Transcription factors; Wiskundige en Statistische Methoden - Biometris
• ISSN: 1040-4651; 1532-298X
• DOI: 10.1105/tpc.17.00232

Central metabolism is a coordinated network that is regulated at multiple levels by resource availability and by environmental and developmental cues. Its genetic architecture has been investigated by mapping metabolite quantitative trait loci (QTL). A more direct approach is to identify enzyme activity QTL, which distinguishes between cis-QTL in structural genes encoding enzymes and regulatory trans-QTL. Using genome-wide association studies, we mapped QTL for 24 enzyme activities, nine metabolites, three structural components, and biomass in Arabidopsis thaliana. We detected strong cis-QTL for five enzyme activities. A cis-QTL for UDP-glucose pyrophosphorylase activity in the UGP1 promoter is maintained through balancing selection. Variation in acid invertase activity reflects multiple evolutionary events in the promoter and coding region of VACINV. cis-QTL were also detected for ADP-glucose pyrophosphorylase, fumarase, and phosphoglucose isomerase activity. We detected many trans-QTL, including transcription factors, E3 ligases, protein targeting components, and protein kinases, and validated some by knockout analysis. trans-QTL are more frequent but tend to have smaller individual effects than cis-QTL. We detected many colocalized QTL, including a multitrait QTL on chromosome 4 that affects six enzyme activities, three metabolites, protein, and biomass. These traits are coordinately modified by different ACCELERATED CELL DEATH6 alleles, revealing a trade-off between metabolism and defense against biotic stress.