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Pathways to defense metabolites and evading fruit bitterness in genus Solanum evolved through 2-oxoglutarate-dependent dioxygenases

Author

Listed:
  • Pablo D. Cárdenas

    (Weizmann Institute of Science
    The Hebrew University of Jerusalem
    University of Copenhagen)

  • Prashant D. Sonawane

    (Weizmann Institute of Science)

  • Uwe Heinig

    (Weizmann Institute of Science)

  • Adam Jozwiak

    (Weizmann Institute of Science)

  • Sayantan Panda

    (Weizmann Institute of Science)

  • Bekele Abebie

    (Agricultural Research Organization, Volcani Center)

  • Yana Kazachkova

    (Weizmann Institute of Science)

  • Margarita Pliner

    (Weizmann Institute of Science)

  • Tamar Unger

    (Weizmann Institute of Science)

  • Dalia Wolf

    (Agricultural Research Organization, Volcani Center)

  • Itai Ofner

    (The Hebrew University of Jerusalem)

  • Ester Vilaprinyo

    (University of Lleida-IRBLleida)

  • Sagit Meir

    (Weizmann Institute of Science)

  • Olga Davydov

    (Weizmann Institute of Science)

  • Amit Gal-on

    (Agricultural Research Organization, Volcani Center)

  • Saul Burdman

    (The Hebrew University of Jerusalem)

  • Ashok Giri

    (Council of Scientific and Industrial Research-National Chemical Laboratory)

  • Dani Zamir

    (The Hebrew University of Jerusalem)

  • Tali Scherf

    (Weizmann Institute of Science)

  • Jedrzej Szymanski

    (Leibniz Institute of Plant Genetics and Crop Plant Research, OT Gatersleben)

  • Ilana Rogachev

    (Weizmann Institute of Science)

  • Asaph Aharoni

    (Weizmann Institute of Science)

Abstract

The genus Solanum comprises three food crops (potato, tomato, and eggplant), which are consumed on daily basis worldwide and also producers of notorious anti-nutritional steroidal glycoalkaloids (SGAs). Hydroxylated SGAs (i.e. leptinines) serve as precursors for leptines that act as defenses against Colorado Potato Beetle (Leptinotarsa decemlineata Say), an important pest of potato worldwide. However, SGA hydroxylating enzymes remain unknown. Here, we discover that 2-OXOGLUTARATE-DEPENDENT-DIOXYGENASE (2-ODD) enzymes catalyze SGA-hydroxylation across various Solanum species. In contrast to cultivated potato, Solanum chacoense, a widespread wild potato species, has evolved a 2-ODD enzyme leading to the formation of leptinines. Furthermore, we find a related 2-ODD in tomato that catalyzes the hydroxylation of the bitter α-tomatine to hydroxytomatine, the first committed step in the chemical shift towards downstream ripening-associated non-bitter SGAs (e.g. esculeoside A). This 2-ODD enzyme prevents bitterness in ripe tomato fruit consumed today which otherwise would remain unpleasant in taste and more toxic.

Suggested Citation

  • Pablo D. Cárdenas & Prashant D. Sonawane & Uwe Heinig & Adam Jozwiak & Sayantan Panda & Bekele Abebie & Yana Kazachkova & Margarita Pliner & Tamar Unger & Dalia Wolf & Itai Ofner & Ester Vilaprinyo & , 2019. "Pathways to defense metabolites and evading fruit bitterness in genus Solanum evolved through 2-oxoglutarate-dependent dioxygenases," Nature Communications, Nature, vol. 10(1), pages 1-13, December.
    • Handle: RePEc:nat:natcom:v:10:y:2019:i:1:d:10.1038_s41467-019-13211-4
    DOI: 10.1038/s41467-019-13211-4
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    Cited by:

    1. Feng Bai & Peng Shu & Heng Deng & Yi Wu & Yao Chen & Mengbo Wu & Tao Ma & Yang Zhang & Julien Pirrello & Zhengguo Li & Yiguo Hong & Mondher Bouzayen & Mingchun Liu, 2024. "A distal enhancer guides the negative selection of toxic glycoalkaloids during tomato domestication," Nature Communications, Nature, vol. 15(1), pages 1-13, December.

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