The GORKY glycoalkaloid transporter is indispensable for preventing tomato bitterness

Kazachkova, Yana; Zemach, Itay; Panda, Sayantan; Bocobza, Samuel; Vainer, Andrii; Rogachev, Ilana; Dong, Yonghui; Ben‐Dor, Shifra; Veres, Dorottya; Kanstrup, Christa; Lambertz, Sophie Konstanze; Crocoll, Christoph; Hu, Yangjie; Shani, Eilon; Michaeli, Simon; Nour-Eldin, Hussam Hassan; Zamir, Dani; Aharoni, Asaph

doi:10.1038/s41477-021-00865-6

Cited by 62 publications

(53 citation statements)

References 74 publications

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“…GORKY, a number of peptide transporter family (NPF), has been recently reported to export α-tomatine and its derivatives to the cytosol from the vacuole, thereby facilitating the conversion of the entire α-tomatine pool to non-bitter forms. 193 Insights into such processes would be of great assistance to improve the tomato quality and to increase the efficiency and success of SGA metabolic engineering strategies. 3 (3) The relationship between epigenetics and bioactive secondary metabolites has been well established in many plants.…”

Section: Future Prospectivementioning

confidence: 99%

Solanum steroidal glycoalkaloids: structural diversity, biological activities, and biosynthesis

Zhao

Chen

et al. 2021

Nat. Prod. Rep.

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Section: Future Prospectivementioning

confidence: 99%

Solanum steroidal glycoalkaloids: structural diversity, biological activities, and biosynthesis

Zhao

Chen

et al. 2021

Nat. Prod. Rep.

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“…Samples of leaf protein extract were subjected to tryptic digestion (50 µg of total protein), using a modified Filter-Aided Sample Preparation protocol (FASP) (Kazachkova et al, 2021). Peptides were acidified with trifluoroacetic acid, dried in a Speedvac concentrator and analysed using nano-UPLC (Waters, Milford, MA, USA), coupled to a nano-ESI emitter (10 µM tip; New Objective, Cambridge, MA, USA) and to a quadrupole Orbitrap mass spectrometer (Q Exactive Plus; Thermo Scientific, Bremen, Germany) as described in Szymanski et al (2017).…”

Section: Proteomics Analysismentioning

confidence: 99%

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

et al. 2021

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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.

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“…Recently, Kazachkova et al . (2021) reported the discovery of the ‘GORKY’ glycoalkaloid transporter exporting α ‐tomatine and other SGAs from the vacuole to the cytosol. Several bitter flavour tomato accessions contain a deletion in GORKY that results in accumulation of the bitter α ‐tomatine and its downstream derivatives (e.g.…”

Section: Resultsmentioning

confidence: 99%

“…EA05978) accumulated high levels of α ‐tomatine, hydroxytomatine and acetoxytomatine as reported for other bitter accessions. Yet, EA05978 did not show any detectable levels of acetoxy‐hydroxytomatine (the predicted GAME40 reaction product) and esculeoside A (Kazachkova et al ., 2021). Next, we analysed the GAME40 expression in ripe fruits of the Micro Tom (MT), ‘Sweet cherry’ and EA05978 cultivars.…”

Section: Resultsmentioning

confidence: 99%

“…7d). This accession accumulated high levels of α ‐tomatine, hydroxytomatine and acetoxytomatine but not any detectable levels of acetoxy‐hydroxytomatine and esculeoside A (Kazachkova et al ., 2021). GAME40 activity shown here in the esculeoside A biosynthetic pathway links chemical shift in SGA metabolism with ethylene‐associated tomato fruit ripening.…”

Section: Discussionmentioning

confidence: 99%

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2‐oxoglutarate‐dependent dioxygenases drive expansion of steroidal alkaloid structural diversity in the genus Solanum

et al. 2022

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Summary Solanum steroidal glycoalkaloids (SGAs) are renowned defence metabolites exhibiting spectacular structural diversity. Genes and enzymes generating the SGA precursor pathway, SGA scaffold and glycosylated forms have been largely identified. Yet, the majority of downstream metabolic steps creating the vast repertoire of SGAs remain untapped. Here, we discovered that members of the 2‐OXOGLUTARATE‐DEPENDENT DIOXYGENASE (2‐ODD) family play a prominent role in SGA metabolism, carrying out three distinct backbone‐modifying oxidative steps in addition to the three formerly reported pathway reactions. The GLYCOALKALOID METABOLISM34 (GAME34) enzyme catalyses the conversion of core SGAs to habrochaitosides in wild tomato S. habrochaites. Cultivated tomato plants overexpressing GAME34 ectopically accumulate habrochaitosides. These habrochaitoside enriched plants extracts potently inhibit Puccinia spp. spore germination, a significant Solanaceae crops fungal pathogen. Another 2‐ODD enzyme, GAME33, acts as a desaturase (via hydroxylation and E/F ring rearrangement) forming unique, yet unreported SGAs. Conversion of bitter α‐tomatine to ripe fruit, nonbitter SGAs (e.g. esculeoside A) requires two hydroxylations; while the known GAME31 2‐ODD enzyme catalyses hydroxytomatine formation, we find that GAME40 catalyses the penultimate step in the pathway and generates acetoxy‐hydroxytomatine towards esculeosides accumulation. Our results highlight the significant contribution of 2‐ODD enzymes to the remarkable structural diversity found in plant steroidal specialized metabolism.

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The GORKY glycoalkaloid transporter is indispensable for preventing tomato bitterness

Cited by 62 publications

References 74 publications

Solanum steroidal glycoalkaloids: structural diversity, biological activities, and biosynthesis

Solanum steroidal glycoalkaloids: structural diversity, biological activities, and biosynthesis

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

2‐oxoglutarate‐dependent dioxygenases drive expansion of steroidal alkaloid structural diversity in the genus Solanum

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