Abstract
Key messagePhosphoglycerate Dehydrogenase 1 of the phosphorylated pathway of serine biosynthesis, active in heterotrophic plastids, is required for the synthesis of serine to enable plant growth at high rates of indolic glucosinolate biosynthesis.Plants have evolved effective strategies to defend against various types of pathogens. The synthesis of a multitude of specialized metabolites represents one effective approach to keep plant attackers in check. The synthesis of those defense compounds is cost intensive and requires extensive interaction with primary metabolism. However, how primary metabolism is adjusted to fulfill the requirements of specialized metabolism is still not completely resolved. Here, we studied the role of the phosphorylated pathway of serine biosynthesis (PPSB) for the synthesis of glucosinolates, the main class of defensive compounds in the model plant Arabidopsis thaliana. We show that major genes of the PPSB are co-expressed with genes required for the synthesis of tryptophan, the unique precursor for the formation of indolic glucosinolates (IG). Transcriptional and metabolic characterization of loss-of-function and dominant mutants of ALTERED TRYPTOPHAN1-like transcription factors revealed demand driven activation of PPSB genes by major regulators of IG biosynthesis. Trans-activation of PPSB promoters by ATR1/MYB34 transcription factor in cultured root cells confirmed this finding. The content of IGs were significantly reduced in plants compromised in the PPSB and these plants showed higher sensitivity against treatment with 5-methyl-tryptophan, a characteristic behavior of mutants impaired in IG biosynthesis. We further found that serine produced by the PPSB is required to enable plant growth under conditions of high demand for IG. In addition, PPSB-deficient plants lack the growth promoting effect resulting from interaction with the beneficial root-colonizing fungus Colletotrichum tofieldiae.
Highlights
Plants produce thousands of different chemical structures classified as specialized metabolites, which are thought to function in facilitating the ecological interaction to optimizeSandraE
The analysis of publicly available expression data revealed that the genes of the phosphorylated pathway of serine biosynthesis (PPSB), namely PGDH1, PGDH2 and PSAT1 are strongly upregulated after infection of plants with pathogenic bacteria and fungi (Fig. 1a)
The paradigm about the function of glucosinolates in plant defense has been changed by the realization that, in addition to their function in herbivore defense, they play an essential role in controlling the invasion of various filamentous pathogens (Pastorczyk and Bednarek 2016)
Summary
Plants produce thousands of different chemical structures classified as specialized metabolites, which are thought to function in facilitating the ecological interaction to optimizeSandraE. In the “classical” pathway glucosinolates are stored in specialized cells (S-cells) and separated from the myrosinase, which is localized in so called myrosine cells This spatial separation of substrate and enzyme is required to prevent premature glucosinolate breakdown, which occurs only after disruption of the plant tissue by wounding or herbivore attack (Wittstock et al 2016). The degradation of indolic glucosinolates (IG) is catalyzed by the atypical myrosinase PEN2 and occurs within intact cells (Bednarek et al 2009) This pathway is part of the plant innate immune response and is required to control the entry of filamentous pathogens into the plant (Pastorczyk and Bednarek 2016). Mutants deficient in major components of this pathway are no longer able to establish a beneficial interaction with C.t. and the fungus behaves like a pathogen in these plants
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