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A New Mechanism of Metabolic Synthesis of Tomatine

A New Mechanism of Metabolic Synthesis of Tomatine

Steroid alkaloids (SA) and their glycosylated forms (steroidal glycoalkaloids, SGA) are a special class of metabolites widely present in Solanaceae plants, which have defensive effects on plant pathogens and herbivores. So far, nearly a hundred SAs have been detected in tomato, among which α-tomatine is the most important SGA in the leaves, flower buds and fruits of Solanaceae plants. During tomato ripening, toxic alkaloids and their glycosylated products undergo hydroxylation, oxidation, and transamination reactions by a series of glycoalkaloid metabolism (GAME) genes, and are finally transformed into non-toxic esculeoside A. This metabolic pathway has been reported, but the mechanism of regulation of SGA biosynthesis is less studied.

Recently, the team of Shouchuang Wang from Hainan University published a research paper entitled "SlERF.H6 mediates the orchestration of ethylene and gibberellin signaling that suppresses bitter-SGAs biosynthesis in tomato" on New Phytologist. This study used forward genetics and  genome-wide association study (GWAS) to discover an AP2/ERF transcription factor SlERF.H6, and analyzed its key role in regulating the crosstalk signal between ethylene and gibberellin to regulate SGA biosynthesis. This study not only provides a new idea for analyzing the regulation mechanism of SGA, but also lays a foundation for people to use a variety of techniques to cultivate excellent tomato varieties.

In this study, steroidal alkaloids in 349 tomato materials were detected, and an AP2/ERF transcription factor SlERF.H6 was located by metabolite genome wide association study (mGWAS). In order to verify whether the gene regulates the biosynthesis of SGA, the transgenic material constructed with this gene was used to detect the changes in the content of SGA metabolites, and it was found that the content of bitter SGA decreased in the SlERF.H6-OE material. The content of nonbitter esculeoside A increased, while the opposite result was found in SlERF.H6-ko material. The corresponding GAMEs genes in the SGA synthesis pathway also showed the same changes, indicating that SlERF.H6 participates in the biosynthesis of SGA in tomato and negatively regulates the synthesis of bitter SGA, promoting the production of nonbitter SGA.

The researchers further found that the SGA metabolic pathway is regulated by the plant hormones ethylene and gibberellin, and that SlERF.H6, as a transcription factor, can inhibit the expression of the gibberellin oxidase SlGA2ox12 gene. SlGA2ox12 can catalyze the conversion of gibberellin precursors (GA12 and GA53) to non-biologically active gibberellins (GA110 and GA97), so the overexpression of SlERF.H6 leads to an increase in the level of gibberellin precursors in tomato, which eventually leads to a decrease in the content of SGA.

Recent studies have shown that ethylene signaling can activate the expression of SlGA2ox, resulting in decreased bioactive GA content. In this study, it was found that ACC treatment of ethylene precursor weakened the regulatory effect of SlERF.H6 on GAMEs genes. The detection of metabolites found that under ACC treatment, the SGA content in SlERF.H6-OE material was not significantly different from that of wild type. Based on the above results, SlERF.H6 mediates the interaction between ethylene and gibberellin signaling to regulate the accumulation of SGAs in tomato.

 

Reference:

Hao, Y.C., et al. SlERF.H6 mediates the orchestration of ethylene and gibberellin signaling that suppresses bitter-SGA biosynthesis in tomato. New Phytol (2023). https://doi.org/10.1111/nph.19048

 

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