Abstract
While R2R3 MYB transcription factors are a large gene family of transcription factors within plants, comprehensive functional data in planta are still scarce. A model for studying R2R3 MYB control of metabolic networks is the glucosinolates (GLSs), secondary metabolites that control plant resistance against insects and pathogens and carry cancer-preventive properties. Three related members of the R2R3 MYB transcription factor family within Arabidopsis (Arabidopsis thaliana), MYB28, MYB29, and MYB76, are the commonly defined regulators of aliphatic GLS biosynthesis. We utilized new genotypes and systems analysis techniques to test the existing regulatory model in which MYB28 is the dominant regulator, MYB29 plays a minor rheostat role, and MYB76 is largely uninvolved. We unequivocally show that MYB76 is not dependent on MYB28 and MYB29 for induction of aliphatic GLSs and that MYB76 plays a role in determining the spatial distribution of aliphatic GLSs within the leaf, pointing at a potential role of MYB76 in transport regulation. Transcriptional profiling of knockout mutants revealed that GLS metabolite levels are uncoupled from the level of transcript accumulation for aliphatic GLS biosynthetic genes. This uncoupling of chemotypes from biosynthetic transcripts suggests revising our view of the regulation of GLS metabolism from a simple linear transcription factor-promoter model to a more modular system in which transcription factors cause similar chemotypes via nonoverlapping regulatory patterns. Similar regulatory networks might exist in other secondary pathways.
Highlights
While R2R3 MYB transcription factors are a large gene family of transcription factors within plants, comprehensive functional data in planta are still scarce
An in planta model might regard all three proteins to act as direct biosynthetic transcriptional activators, with MYB28 as the major regulator of aliphatic GLSs followed by MYB29 and MYB76 having minor, accessory roles (Fig. 1B; Gigolashvili et al, 2009a)
We unequivocally demonstrate that MYB76 has a MYB28- and MYB29-independent role in Arabidopsis and that MYB76 has transcriptional effects on specific parts of the biosynthetic pathway
Summary
While R2R3 MYB transcription factors are a large gene family of transcription factors within plants, comprehensive functional data in planta are still scarce. T-DNA mutants in MYB29 and MYB76 are decreased in short-chained aliphatic GLSs (one to three cycles of chain elongation; Sonderby et al, 2007; Beekwilder et al, 2008; Gigolashvili et al, 2008), as are T-DNA mutants in MYB28 that, in addition, are almost devoid of long-chained aliphatic GLSs (four to six cycles of chain elongation; Hirai et al, 2007; Sonderby et al, 2007; Beekwilder et al, 2008) Based on these data, an in planta model might regard all three proteins to act as direct biosynthetic transcriptional activators, with MYB28 as the major regulator of aliphatic GLSs followed by MYB29 and MYB76 having minor, accessory roles (Fig. 1B; Gigolashvili et al, 2009a). There must be mechanisms by which relative amounts of individual GLSs can be adjusted beyond the link of MYB28 to long-chained aliphatic GLSs
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