Steroidal alkaloids defence metabolism and plant growth are modulated by the joint action of gibberellin and jasmonate signalling

TLDR

Steroidal glycoalkaloids are constitutively produced defensive metabolites in Solanaceae, and while their biosynthetic genes are largely known, how gibberellin and jasmonate signaling coordinate their production remains unclear. The study aimed to elucidate how gibberellin and jasmonate pathways regulate SGA metabolism during the growth‑versus‑defence trade‑off in tomato. Researchers performed genetic and biochemical analyses of JA and GA pathway components and conducted in‑vitro experiments to uncover the hormonal crosstalk governing SGA biosynthesis. They found that diminished JA reduces SGA levels while reduced GA or its receptor increases SGA accumulation, with MYC1/2 transcription factors mediating the crosstalk by activating SGA biosynthetic and GA‑catabolic genes and regulating DELLA, thereby balancing defense costs with growth.

Abstract

Steroidal glycoalkaloids (SGAs) are protective metabolites constitutively produced by Solanaceae species. Genes and enzymes generating the vast structural diversity of SGAs have been largely identified. Yet, mechanisms of hormone pathways coordinating defence (jasmonate; JA) and growth (gibberellin; GA) controlling SGAs metabolism remain unclear. We used tomato to decipher the hormonal regulation of SGAs metabolism during growth vs defence tradeoff. This was performed by genetic and biochemical characterisation of different JA and GA pathways components, coupled with in vitro experiments to elucidate the crosstalk between these hormone pathways mediating SGAs metabolism. We discovered that reduced active JA results in decreased SGA production, while low levels of GA or its receptor led to elevated SGA accumulation. We showed that MYC1 and MYC2 transcription factors mediate the JA/GA crosstalk by transcriptional activation of SGA biosynthesis and GA catabolism genes. Furthermore, MYC1 and MYC2 transcriptionally regulate the GA signalling suppressor DELLA that by itself interferes in JA-mediated SGA control by modulating MYC activity through protein-protein interaction. Chemical and fungal pathogen treatments reinforced the concept of JA/GA crosstalk during SGA metabolism. These findings revealed the mechanism of JA/GA interplay in SGA biosynthesis to balance the cost of chemical defence with growth.