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Published on October 1, 2008; 10.1104/pp.108.124784

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Received June 15, 2008
Accepted September 26, 2008

THE TRANSCRIPT AND METABOLITE NETWORKS EFFECTED BY THE TWO CLADES OF ARABIDOPSIS GLUCOSINOLATE BIOSYNTHESIS REGULATORS

Sergey Malitsky , Eyal Blum , Hadar Less , Ilya Venger , Moshe Elbaz , Shai Morin , Yuval Eshed , and Asaph Aharoni *

Department of Plant Sciences, Weizmann Institute of Science, P.O. Box 26, Rehovot 76100, Israel; Department of Entomology, Faculty of Agriculture, The Hebrew University of Jerusalem, Rehovot 76100, Israel

* Corresponding author; email: asaph.aharoni{at}weizmann.ac.il.

In this study, transcriptomics and metabolomics data was integrated in order to examine the regulation of glucosinolate (GS) biosynthesis in Arabidopsis and its interface with pathways of primary metabolism. Our genetic material for analyses were transgenic plants overexpressing members of two clades of genes (ATR1-like and MYB28-like) that regulate the aliphatic and indole GSs biosynthetic pathways (AGs and IGs, respectively). We show that activity of these regulators is not restricted to the metabolic space surrounding GSs biosynthesis but is tightly linked to more distal metabolic networks of primary metabolism. This suggests that with similarity to the regulators we have investigated here, other factors controlling pathways of secondary metabolism might also control core pathways of central metabolism. The relatively broad view of transcript and metabolites altered in transgenic plants overexpressing the different factors underlined novel links of GSs metabolism to additional metabolic pathways including those of jasmonic acid, folate, benzoic acid and various phenylpropanoids. It also revealed transcriptional and metabolic hubs in the "distal" network of metabolic pathways supplying precursors to GSs biosynthesis and that over expression of the ATR1-like clade genes has a much broader effect on metabolism of indolic compounds than described previously. While the reciprocal, negative cross talk between the methionine and tryptophan pathways that generate GSs in Arabidopsis has been suggested previously we now show that it is not restricted to AGs and IGs but includes additional metabolites, as for example the phytoalexin camalexin. Combining the profiling data of transgenic lines with gene expression correlation analysis allowed us to propose a model of how the balance in the metabolic network is maintained by the GSs biosynthesis regulators. It appears that ATR1/MYB34 is an important mediator between the two clade genes activity. While it is very similar to the ATR1-like clade members in terms of downstream gene targets, its expression is highly correlated with the one of the MYB28-like clade members. Finally, we used the unique transgenic plants obtained here to show that AGs are likely more potent deterrents of white fly as compared to IGs. The influence on insect behavior raises an important question for future investigation on the functional aspect of our initial finding that pointed to enriched expression of the MYB28-like clade genes in the abaxial domain of the Arabidopsis leaf.




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