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

Sayantan Panda, Adam Jozwiak, Prashant D. Sonawane, Jedrzej Szymanski, Yana Kazachkova, Andrii Vainer, Himabindu Vasuki Kilambi, Efrat Almekias-Siegl, Varvara Dikaya, Samuel Bocobza, Hagai Shohat, Sagit Meir, Guy Wizler, Ashok P. Giri, Robert Schuurink, David Weiss, Hagai Yasuor, Avinash Kamble*, Asaph Aharoni*

*Corresponding author for this work

Research output: Contribution to journalArticlepeer-review

21 Scopus citations

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.

Original languageAmerican English
Pages (from-to)1220-1237
Number of pages18
JournalNew Phytologist
Volume233
Issue number3
DOIs
StatePublished - Feb 2022

Bibliographical note

Funding Information:
We are grateful to Bettina Hause and Chuanyou Li for providing the tomato and plants, respectively. We thank Marganit Levy and Dhruv Srivastava for providing . cultures. We are thankful to Constantine Garagounis for the constructive criticism of the manuscript. We thank the Adelis Foundation, Leona M. and Harry B. Helmsley Charitable Trust, Jeanne and Joseph Nissim Foundation for Life Sciences, Tom and Sondra Rykoff Family Foundation Research and the Raymond Burton Plant Genome Research Fund for supporting the AA laboratory activity. AA is the incumbent of the Peter J. Cohn Professorial Chair. The authors declare no competing financial interests. AOC‐RNAi MYC2‐RNAi B cinerea

Publisher Copyright:
© 2021 The Authors. New Phytologist © 2021 New Phytologist Foundation

© 2021 The Authors. New Phytologist © 2021 New Phytologist Foundation.

Keywords

  • Alkaloids/metabolism
  • Cyclopentanes/metabolism
  • Gene Expression Regulation, Plant
  • Gibberellins/metabolism
  • Lycopersicon esculentum/metabolism
  • Oxylipins/metabolism

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