The phosphorylated pathway of serine biosynthesis is crucial for indolic glucosinolate biosynthesis and plant growth promotion conferred by the root endophyte Colletotrichum tofieldiae

Abstract

Key message Phosphoglycerate 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. Abstract 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.

Comprehensive insight into an amino acid metabolic network in postharvest horticultural products: a review

“…Serine plays the main role in response to environmental stresses 54,55 . Transcriptomics and metabolomics results suggested that the key genes of tryptophan biosynthesis were co‐expressed with genes of the phosphorylated pathway of serine biosynthesis (PPSB), and the inhibition of PPSB caused a decrease in indole glucosinolates 56 . Therefore, serine metabolism is crucial for the synthesis of indole glucosinolates in plants.…”

“…54,55 Transcriptomics and metabolomics results suggested that the key genes of tryptophan biosynthesis were co-expressed with genes of the phosphorylated pathway of serine biosynthesis (PPSB), and the inhibition of PPSB caused a decrease in indole glucosinolates. 56 Therefore, serine metabolism is crucial for the synthesis of indole glucosinolates in plants. An increase in serine and threonine contents and a decrease in glycine content were found in postharvest grapes, citrus fruits and tomatoes, and exogenous melatonin and methyl jasmonate treatments promoted the accumulation of serine and threonine, thereby maintaining antioxidant ability and delaying the senescence of postharvest citrus and tomatoes.…”

Fungal endophytes of Brassicaceae: Molecular interactions and crop benefits

“…An important part of the genes regulated by PHR is known or predicted to mediate biosynthesis of defense-related IG (Castrillo et al, 2017). This fact, together with the need for an intact PEN2-myrosinasedependent IG pathway for the beneficial interaction with C. tofieldiae, points, again, to the relevance of these compounds in regulating Brassicaceae interactions with fungal endophytes (Hiruma et al, 2016;Frerigmann et al, 2020;Zimmermann et al, 2021).…”