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New Phytol. 2022 Feb;233(3):1220-1237. doi: 10.1111/nph.17845. Epub 2021 Dec 03.

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

The New phytologist

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

Affiliations

  1. Department of Plant and Environmental Sciences, Weizmann Institute of Science, Rehovot, 7610001, Israel.
  2. Gilat Research Center, Agricultural Research Organization (ARO), Rural delivery Negev, 85280, Israel.
  3. Department of Botany, Savitribai Phule Pune University, Ganeshkhind, Pune, 411007, India.
  4. Department of Molecular Genetics, Leibniz Institute of Plant Genetics and Crop Plant Research, Gatersleben, Germany.
  5. Department of Biology I, Ludwig-Maximilians-University of Munich, Munich, Germany.
  6. Department of Vegetable Research, ARO-Volcani Center, Bet Dagan, 50250, Israel.
  7. Institute of Plant Sciences and Genetics in Agriculture, The Robert H. Smith Faculty of Agriculture, Food and Environment, The Hebrew University of Jerusalem, Rehovot, 76100, Israel.
  8. Plant Molecular Biology Unit, Division of Biochemical Sciences, Council of Scientific and Industrial Research-National Chemical Laboratory, Pune, 411008, India.
  9. Green Life Sciences Research Cluster, Swammerdam Institute for Life Sciences, University of Amsterdam, Science Park 904, Amsterdam, 1098 XH, the Netherlands.

PMID: 34758118 DOI: 10.1111/nph.17845

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.

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

Keywords: defence; gibberellin (GA); growth; jasmonate (JA); steroidal glycoalkaloids (SGAs); tomato; α-tomatine

References

  1. Abbasi BH, Stiles AR, Saxena PK, Liu CZ. 2012. Gibberellic acid increases secondary metabolite production in Echinacea purpurea hairy roots. Applied Biochemistry and Biotechnology 168: 2057-2066. - PubMed
  2. Abdelkareem A, Thagun C, Nakayasu M, Mizutani M, Hashimoto T, Shoji T. 2017. Jasmonate-induced biosynthesis of steroidal glycoalkaloids depends on COI1 proteins in tomato. Biochemical and Biophysical Research Communications 489: 206-210. - PubMed
  3. Balcke GU, Bennewitz S, Bergau N, Athmer B, Henning A, Majovsky P, Jiménez-Gómez JM, Hoehenwarter W, Tissier A. 2017. Multi-omics of tomato glandular trichomes reveals distinct features of central carbon metabolism supporting high productivity of specialized metabolites. Plant Cell 29: 960-983. - PubMed
  4. Bednarek P, Osbourn A. 2009. Plant-microbe interactions: chemical diversity in plant defense. Science 324: 746-748. - PubMed
  5. Cai J, Qin G, Chen T, Tian S. 2018. The mode of action of remorin1 in regulating fruit ripening at transcriptional and post-transcriptional levels. New Phytologist 219: 1406-1420. - PubMed
  6. Campos ML, Yoshida Y, Major IT, de Oliveira Ferreira D, Weraduwage SM, Froehlich JE, Johnson BF, Kramer DM, Jander G, Sharkey TD et al. 2016. Rewiring of jasmonate and phytochrome B signalling uncouples plant growth-defense tradeoffs. Nature Communications 7: 1-10. - PubMed
  7. Cárdenas PD, Sonawane PD, Heinig U, Jozwiak A, Panda S, Abebie B, Kazachkova Y, Pliner M, Unger T, Wolf D et al. 2019. Pathways to defense metabolites and evading fruit bitterness in genus Solanum evolved through 2-oxoglutarate-dependent dioxygenases. Nature Communications 10: 1-13. - PubMed
  8. Cárdenas PD, Sonawane PD, Pollier J, Vanden Bossche R, Dewangan V, Weithorn E, Tal L, Meir S, Rogachev I, Malitsky S et al. 2016. GAME9 regulates the biosynthesis of steroidal alkaloids and upstream isoprenoids in the plant mevalonate pathway. Nature Communications 7: 1-16. - PubMed
  9. Chen S, Wang X, Zhang L, Lin S, Liu D, Wang Q, Cai S, El-Tanbouly R, Gan L, Wu H et al. 2016. Identification and characterization of tomato gibberellin 2-oxidases (GA2oxs) and effects of fruit-specific SlGA2ox1 overexpression on fruit and seed growth and development. Horticulture Research 3: 1-9. - PubMed
  10. Chen X, Wang DD, Fang X, Chen XY, Mao YB. 2019. Plant specialized metabolism regulated by jasmonate signaling. Plant and Cell Physiology 60: 2638-2647. - PubMed
  11. Chini A, Ben-Romdhane W, Hassairi A, Aboul-Soud MAM. 2017. Identification of TIFY/JAZ family genes in Solanum lycopersicum and their regulation in response to abiotic stresses. PLoS ONE 12: e0177381. - PubMed
  12. Chini A, Fonseca S, Fernández G, Adie B, Chico JM, Lorenzo O, García-Casado G, López-Vidriero I, Lozano FM, Ponce MR et al. 2007. The JAZ family of repressors is the missing link in jasmonate signalling. Nature 448: 666-671. - PubMed
  13. Davière JM, Achard P. 2016. A pivotal role of DELLAs in regulating multiple hormone signals. Molecular Plant 9: 10-20. - PubMed
  14. Du M, Zhao J, Tzeng DTW, Liu Y, Deng L, Yang T, Zhai Q, Wu F, Huang Z, Zhou M et al. 2017. MYC2 orchestrates a hierarchical transcriptional cascade that regulates jasmonate-mediated plant immunity in tomato. Plant Cell 29: 1883-1906. - PubMed
  15. Flors V, Leyva MDLO, Vicedo B, Finiti I, Real MD, García-Agustín P, Bennett AB, González-Bosch C. 2007. Absence of the endo-β-1,4-glucanases Cel1 and Cel2 reduces susceptibility to Botrytis cinerea in tomato. The Plant Journal 52: 1027-1040. - PubMed
  16. Fonseca S, Chini A, Hamberg M, Adie B, Porzel A, Kramell R, Miersch O, Wasternack C, Solano R. 2009. (+)-7-iso-Jasmonoyl-L-isoleucine is the endogenous bioactive jasmonate. Nature Chemical Biology 5: 344-350. - PubMed
  17. Goetz S, Hellwege A, Stenzel I, Kutter C, Hauptmann V, Forner S, McCaig B, Hause G, Miersch O, Wasternack C et al. 2012. Role of cis-12-Oxo-phytodienoic acid in tomato embryo development. Plant Physiology 158: 1715-1727. - PubMed
  18. Hedden P. 2020. The current status of research on gibberellin biosynthesis. Plant and Cell Physiology 61: 1832-1849. - PubMed
  19. Heinrich M, Hettenhausen C, Lange T, Wünsche H, Fang J, Baldwin IT, Wu J. 2013. High levels of jasmonic acid antagonize the biosynthesis of gibberellins and inhibit the growth of Nicotiana attenuata stems. The Plant Journal 73: 591-606. - PubMed
  20. Hellens RP, Allan AC, Friel EN, Bolitho K, Grafton K, Templeton MD, Karunairetnam S, Gleave AP, Laing WA. 2005. Transient expression vectors for functional genomics, quantification of promoter activity and RNA silencing in plants. Plant Methods 1: 1-14. - PubMed
  21. Hong GJ, Xue XY, Mao YB, Wang LJ, Chen XY. 2012. Arabidopsis MYC2 interacts with DELLA proteins in regulating sesquiterpene synthase gene expression. Plant Cell 24: 2635-2648. - PubMed
  22. Hou X, Lee LYC, Xia K, Yan Y, Yu H. 2010. DELLAs modulate jasmonate signaling via competitive binding to JAZs. Developmental Cell 19: 884-894. - PubMed
  23. Howe GA, Major IT, Koo AJ. 2018. Modularity in jasmonate signaling for multistress resilience. Annual Review of Plant Biology 69: 387-415. - PubMed
  24. Iijima Y, Watanabe B, Sasaki R, Takenaka M, Ono H, Sakurai N, Umemoto N, Suzuki H, Shibata D, Aoki K. 2013. Steroidal glycoalkaloid profiling and structures of glycoalkaloids in wild tomato fruit. Phytochemistry 95: 145-157. - PubMed
  25. Illouz-Eliaz N, Ramon U, Shohat H, Blum S, Livne S, Mendelson D, Weiss D. 2019. Multiple gibberellin receptors contribute to phenotypic stability under changing environments. Plant Cell 31: 1506-1519. - PubMed
  26. Ishiga Y, Ishiga T, Uppalapati SR, Mysore KS. 2013. Jasmonate ZIM-Domain (JAZ) protein regulates host and nonhost pathogen-induced cell death in tomato and Nicotiana benthamiana. PLoS ONE 8: e75728. - PubMed
  27. Itkin M, Heinig U, Tzfadia O, Bhide AJ, Shinde B, Cardenas PD, Bocobza SE, Unger T, Malitsky S, Finkers R et al. 2013. Biosynthesis of antinutritional alkaloids in Solanaceous crops is mediated by clustered genes. Science 341: 175-179. - PubMed
  28. Itkin M, Rogachev I, Alkan N, Rosenberg T, Malitsky S, Masini L, Meir S, Iijima Y, Aoki K, de Vos R et al. 2011. GLYCOALKALOID METABOLISM1 is required for steroidal alkaloid glycosylation and prevention of phytotoxicity in tomato. The Plant Cell 23: 4507-4525. - PubMed
  29. Kazachkova Y, Zemach I, Panda S, Bocobza S, Vainer A, Rogachev I, Dong Y, Ben-Dor S, Veres D, Kanstrup C et al. 2021. The GORKY glycoalkaloid transporter is indispensable for preventing tomato bitterness. Nature Plants 7: 468-480. - PubMed
  30. Kazan K, Manners JM. 2013. MYC2: the master in action. Molecular Plant 6: 686-703. - PubMed
  31. Kojima M, Kamada-Nobusada T, Komatsu H, Takei K, Kuroha T, Mizutani M, Ashikari M, Ueguchi-Tanaka M, Matsuoka M, Suzuki K et al. 2009. Highly sensitive and high-throughput analysis of plant hormones using MS-probe modification and liquid chromatographytandem mass spectrometry: an application for hormone profiling in Oryza sativa. Plant and Cell Physiology 50: 1201-1214. - PubMed
  32. Li J, Zingen-Sell I, Buchenauer H. 1996. Induction of resistance of cotton plants to Verticillium wilt and of tomato plants to Fusarium wilt by 3-aminobutyric acid and methyl jasmonate. Journal of Plant Diseases and Protection 103: 288-299. - PubMed
  33. Li L, Zhao Y, McCaig BC, Wingerd BA, Wang J, Whalon ME, Pichersky E, Howe GA. 2004. The tomato homolog of CORONATINE-INSENSITIVE 1 is required for the maternal control of seed maturation, jasmonate-signaled defense responses, and glandular trichome development. Plant Cell 16: 126-143. - PubMed
  34. Livne S, Lor VS, Nir I, Eliaz N, Aharoni A, Olszewski NE, Eshed Y, Weiss D. 2015. Uncovering DELLA-independent gibberellin responses by characterizing new tomato procera mutants. Plant Cell 27: 1579-1594. - PubMed
  35. Loreti E, Povero G, Novi G, Solfanelli C, Alpi A, Perata P. 2008. Gibberellins, jasmonate and abscisic acid modulate the sucrose-induced expression of anthocyanin biosynthetic genes in Arabidopsis. New Phytologist 179: 1004-1016. - PubMed
  36. Machado RAR, Baldwin IT, Erb M. 2017. Herbivory-induced jasmonates constrain plant sugar accumulation and growth by antagonizing gibberellin signaling and not by promoting secondary metabolite production. New Phytologist 215: 803-812. - PubMed
  37. Major IT, Guo Q, Zhai J, Kapali G, Kramer DM, Howea GA. 2020. A phytochrome b-independent pathway restricts growth at high levels of jasmonate defense. Plant Physiology 183: 733-749. - PubMed
  38. Major IT, Yoshida Y, Campos ML, Kapali G, Xin XF, Sugimoto K, de Oliveira FD, He SY, Howe GA. 2017. Regulation of growth-defense balance by the JASMONATE ZIM-DOMAIN (JAZ)-MYC transcriptional module. New Phytologist 215: 1533-1547. - PubMed
  39. Masoud AN, Sciuchetti LA, Farnsworth NR, Blomster RN, Meer WA. 1968. Effect of gibberellic acid on the growth, alkaloid production, and VLB content of Catharanthus roseus. Journal of Pharmaceutical Sciences 57: 589-593. - PubMed
  40. Millard PS, Weber K, Kragelund BB, Burow M. 2019. Specificity of MYB interactions relies on motifs in ordered and disordered contexts. Nucleic Acids Research 47: 9592-9608. - PubMed
  41. Min D, Li F, Cui X, Zhou J, Li J, Ai W, Shu P, Zhang X, Li X, Meng D et al. 2020. SlMYC2 are required for methyl jasmonate-induced tomato fruit resistance to Botrytis cinerea. Food Chemistry 310: 125901. - PubMed
  42. Monte I, Ishida S, Zamarreño AM, Hamberg M, Franco-Zorrilla JM, García-Casado G, Gouhier-Darimont C, Reymond P, Takahashi K, García-Mina JM et al. 2018. Ligand-receptor co-evolution shaped the jasmonate pathway in land plants. Nature Chemical Biology 14: 480-488. - PubMed
  43. Navarro L, Bari R, Achard P, Lisón P, Nemri A, Harberd NP, Jones JD. 2008. DELLAs control plant immune responses by modulating the balance of jasmonic acid and salicylic acid signaling. Current Biology 18: 650-655. - PubMed
  44. Nir I, Shohat H, Panizel I, Olszewski N, Aharoni A, Weiss D. 2017. The tomato DELLA protein PROCERA acts in guard cells to promote stomatal closure. Plant Cell 29: 3186-3197. - PubMed
  45. Panda S, Kazachkova Y, Aharoni A. 2021. Catch-22 in specialized metabolism: balancing defense and growth. Journal of Experimental Botany 72: 6027-6041. - PubMed
  46. Paudel JR, Davidson C, Song J, Maxim I, Aharoni A, Tai HH. 2017. Pathogen and pest responses are altered due to RNAi-mediated knockdown of GLYCOALKALOID METABOLISM 4 in solanum tuberosum. Molecular Plant-Microbe Interactions 30: 876-885. - PubMed
  47. Schrager-Lavelle A, Gath NN, Devisetty UK, Carrera E, López-Díaz I, Blázquez MA, Maloof JN. 2019. The role of a class III gibberellin 2-oxidase in tomato internode elongation. The Plant Journal 97: 603-615. - PubMed
  48. Schweizer F, Fernández-Calvo P, Zander M, Diez-Diaz M, Fonseca S, Glauser G, Lewsey MG, Ecker JR, Solano R, Reymond P. 2013. Arabidopsis basic helix-loop-helix transcription factors MYC2, MYC3, andMYC4 regulate glucosinolate biosynthesis, insect performance, and feeding behavior. Plant Cell 25: 3117-3132. - PubMed
  49. Sonawane PD, Pollier J, Panda S, Szymanski J, Massalha H, Yona M, Unger T, Malitsky S, Arendt P, Pauwels L et al. 2016. Plant cholesterol biosynthetic pathway overlaps with phytosterol metabolism. Nature Plants 3: 1-13. - PubMed
  50. Suza WP, Rowe ML, Hamberg M, Staswick PE. 2010. A tomato enzyme synthesizes (+)-7-iso-jasmonoyl-L-isoleucine in wounded leaves. Planta 231: 717-728. - PubMed
  51. Swinnen G, De Meyer M, Pollier J, Molina-Hidalgo FJ, Ceulemans E, De Clercq R, Bossche RV, Fernández-Calvo P, Ron M, Pauwels L et al. 2020. Constitutive steroidal glycoalkaloid biosynthesis in tomato is regulated by the clade IIIe basic helix-loop-helix transcription factors MYC1 and MYC2. bioRxiv. doi: 10.1101/2020.01.27.921833. - PubMed
  52. Szymanski J, Levin Y, Savidor A, Breitel D, Chappell-Maor L, Heinig U, Töpfer N, Aharoni A. 2017. Label-free deep shotgun proteomics reveals protein dynamics during tomato fruit tissues development. The Plant Journal 90: 396-417. - PubMed
  53. Thagun C, Imanishi S, Kudo T, Nakabayashi R, Ohyama K, Mori T, Kawamoto K, Nakamura Y, Katayama M, Nonaka S et al. 2016. Jasmonate-responsive ERF transcription factors regulate steroidal glycoalkaloid biosynthesis in tomato. Plant and Cell Physiology 57: 961-975. - PubMed
  54. Thines B, Katsir L, Melotto M, Niu Y, Mandaokar A, Liu G, Nomura K, He SY, Howe GA, Browse J. 2007. JAZ repressor proteins are targets of the SCFCOI1 complex during jasmonate signalling. Nature 448: 661-665. - PubMed
  55. Van Tuinen A, Peters AHLJ, Kendrick RE, Zeevaart JAD, Koornneef M. 1999. Characterisation of the procera mutant of tomato and the interaction of gibberellins with end-of-day far-red light treatments. Physiologia Plantarum 106: 121-128. - PubMed
  56. Vazquez-Vilar M, Bernabé-Orts JM, Fernandez-del-Carmen A, Ziarsolo P, Blanca J, Granell A, Orzaez D. 2016. A modular toolbox for gRNA-Cas9 genome engineering in plants based on the GoldenBraid standard. Plant Methods 12: 1-12. - PubMed
  57. Waller GR, Burström H. 1969. Diterpenoid alkaloids as plant growth inhibitors. Nature 222: 576-578. - PubMed
  58. Wasternack C, Hause B. 2013. Jasmonates: biosynthesis, perception, signal transduction and action in plant stress response, growth and development. An update to the 2007 review in Annals of Botany. Annals of Botany 111: 1021-1058. - PubMed
  59. Wasternack C, Strnad M. 2019. Jasmonates are signals in the biosynthesis of secondary metabolites - pathways, transcription factors and applied aspects - a brief review. New Biotechnology 48: 1-11. - PubMed
  60. Wild M, Davière JM, Cheminant S, Regnault T, Baumberger N, Heintz D, Baltz R, Genschik P, Achard P. 2012. The Arabidopsis DELLA RGA-LIKE3 is a direct target of MYC2 and modulates jasmonate signaling responses. Plant Cell 24: 3307-3319. - PubMed
  61. Xu J, Van Herwijnen ZO, Dräger DB, Sui C, Haring MA, Schuurink RC. 2018. SlMYC1 regulates type VI glandular trichome formation and terpene biosynthesis in tomato glandular cells. Plant Cell 30: 2988-3005. - PubMed
  62. Xu L, Liu F, Lechner E, Genschik P, Crosby WL, Ma H, Peng W, Huang D, Xie D. 2002. The SCFCOI1 ubiquitin-ligase complexes are required for jasmonate response in Arabidopsis. Plant Cell 14: 1919-1935. - PubMed
  63. Yamaguchi S. 2008. Gibberellin metabolism and its regulation. Annual Review of Plant Biology 59: 225-251. - PubMed
  64. Yang D-L, Yao J, Mei C-S, Tong X-H, Zeng L-J, Li Q, Xiao L-T, Sun T-P, Li J, Deng X-W et al. 2012. Plant hormone jasmonate prioritizes defense over growth by interfering with gibberellin signaling cascade. Proceedings of the National Academy of Sciences, USA 109: E1192-E1200. - PubMed
  65. Züst T, Agrawal AA. 2017. Trade-offs between plant growth and defense against insect herbivory: an emerging mechanistic synthesis. Annual Review of Plant Biology 68: 513-534. - PubMed

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