Auxin driven indoleamine biosynthesis and the role of tryptophan as an inductive signal in Hypericum perforatum (L.)

Autoři: Lauren A. E. Erland aff001;  Praveen Saxena aff001
Působiště autorů: Department of Plant Agriculture, Gosling Research Institute for Plant Preservation, University of Guelph, Guelph, Ontario, Canada aff001
Vyšlo v časopise: PLoS ONE 14(10)
Kategorie: Research Article
doi: 10.1371/journal.pone.0223878


In the 60 years since Skoog and Miller first reported the chemical redirection of plant growth the underlying biochemical mechanisms are still poorly understood, with one challenge being the capacity for applied growth regulators to act indirectly or be metabolized to active phytohormones. We hypothesized that tryptophan is metabolized to auxin, melatonin or serotonin inducing organogenesis in St. John’s wort (Hypericum perforatum L.). Root explants from two germplasm lines of St. John’s wort with altered melatonin metabolism and wildtype were incubated with auxin or tryptophan for 24, 48 or 72 h to induce regeneration. In wildtype, tryptophan had little effect on the indoleamine pathway, and was found to promote primary growth, suggesting excess tryptophan moved quickly through various secondary metabolite pathways and protein synthesis. In lines 4 and 112 tryptophan was associated with modified morphogenesis, indoleamine and auxin levels. Incubation with tryptophan increased shoot organogenesis while incubation with auxin led to root regeneration. The established paradigm of thought views tryptophan primarily as a precursor for auxin and indoleamines, among other metabolites, and mediation of auxin action by the indoleamines as a one-way interaction. We propose that these processes run in both directions with auxin modifying indoleamine biosynthesis and the melatonin:serotonin balance contributing to its effects on plant morphogenesis, and that tryptophan also functions as an inductive signal to mediate diverse phytochemical and morphogenetic pathways.

Klíčová slova:

Auxins – Biosynthesis – Morphogenesis – Organogenesis – Plant growth and development – Serotonin – Tryptophan – Melatonin


1. Maeda H, Dudareva N. The shikimate pathway and aromatic amino acid biosynthesis in plants. Annu Rev Plant Biol. 2012;63: 73–105. doi: 10.1146/annurev-arplant-042811-105439 22554242

2. Murch SJ, Krishnaraj S, Saxena PK. Tryptophan is a precursor for melatonin and serotonin biosynthesis in in vitro regenerated St. John’s wort (Hypericum perforatum L. cv. Anthos) plants. Plant Cell Rep. 2000;19: 698–704. doi: 10.1007/s002990000206 30754808

3. Woodward AW, Bartel B. Auxin: regulation, action, and interaction. Ann Bot. 2005;95: 707–735. doi: 10.1093/aob/mci083 15749753

4. Sherwin JE, Purves WK. Tryptophan as an auxin precursor in cucumber seedlings. Plant Physiol. 1969;44: 1303–1309. doi: 10.1104/pp.44.9.1303 5379108

5. O’Connor SE, Maresh JJ. Chemistry and biology of monoterpene indole alkaloid biosynthesis. Nat Prod Rep. 2006;23: 532–547. doi: 10.1039/b512615k 16874388

6. Kokubo Y, Nishizaka M, Ube N, Yabuta Y, Tebayashi S-I, Ueno K, et al. Distribution of the tryptophan pathway-derived defensive secondary metabolites gramine and benzoxazinones in Poaceae. Biosci Biotechnol Biochem. 2016;81: 431–440. doi: 10.1080/09168451.2016.1256758 27854190

7. Stotz HU, Brown PD, Tokuhisa J. Glucosinolate biosynthesis from amino acids. Amino acids in higher plants. Wallingford: CABI; 2015. pp. 436–447. doi: 10.1079/9781780642635.0436

8. Dubouzet JG, Matsuda F, Ishihara A, Miyagawa H, Wakasa K. Production of indole alkaloids by metabolic engineering of the tryptophan pathway in rice. Plant Biotechnology J. 2013;11: 1103–1111. doi: 10.1111/pbi.12105 23980801

9. Berlin J, Rügenhagen C, Dietze P, Fecker LF, Goddijn OJM, Hoge JHC. Increased production of serotonin by suspension and root cultures of Peganum harmala transformed with a tryptophan decarboxylase cDNA clone from Catharanthus roseus. Transgenic Res. 1993;2: 336–344. doi: 10.1007/BF01976175

10. Chowdhury CN, Tyagi AK, Maheshwari N, Maheshwari SC. Effect of L-proline and L-tryptophan on somatic embryogenesis and plantlet regeneration of rice (Oryza sativa L. cv. Pusa 169). Plant Cell Tiss Organ Cult. 1993;32: 357–361.

11. Talaat IM, Bekheta MA, Mahgoub MH. Physiological response of periwinkle plants (Catharanthus roseus L.) to rryptophan and putrescine. Int J Agricult Biol. 2008;7: 210–213.

12. Stowe BB. Occurrence and Metabolism of Simple Indoles in Plants. Fortschritte der Chemie Organischer Naturstoffe / Progress in the Chemistry of Organic Natural Products / Progrès dans la Chimie des Substances Organiques Naturelles. Vienna: Springer Vienna; 1959. pp. 248–297. doi: 10.1007/978-3-7091-8052-5_5

13. Lund HA. The biosynthesis of indoleacetic acid in the styles and ovaries of tobacco preliminary to the setting of fruit. Plant Physiol. 1956;31: 334–339. doi: 10.1104/pp.31.5.334 16654895

14. Nitsch JP. Free auxins and free tryptophane in the strawberry. Plant Physiol. 1955;30: 33–39. doi: 10.1104/pp.30.1.33 16654724

15. Nitsch JP, Wetmore RH. The microdetermination of “free” L-tryptophane in the seedling of Lupinus albus. Science. 1952;116: 256–257. doi: 10.1126/science.116.3010.256 17742553

16. Murch SJ, Alan AR, Cao J, Saxena PK. Melatonin and serotonin in flowers and fruits of Datura metel L. J Pineal Res. 2009;47: 277–283. doi: 10.1111/j.1600-079X.2009.00711.x 19732299

17. Murch SJ, Hall BA, Le CH, Saxena PK. Changes in the levels of indoleamine phytochemicals during véraison and ripening of wine grapes. J Pineal Res. 2010;49: 95–100. doi: 10.1111/j.1600-079X.2010.00774.x 20536685

18. Okazaki M, Ezura H. Profiling of melatonin in the model tomato (Solanum lycopersicum L.) cultivar Micro-Tom. J Pineal Res. 2009;46: 338–343. doi: 10.1111/j.1600-079X.2009.00668.x 19317796

19. Hernández-Ruiz J, Arnao MB. Distribution of melatonin in different zones of lupin and barley plants at different ages in the presence and absence of light. J Agric Food Chem. 2008;56: 10567–10573. doi: 10.1021/jf8022063 18975965

20. Manchester LC, Tan DX, Reiter RJ, Park W, Monis K. High levels of melatonin in the seeds of edible plants: possible function in germ tissue protection. Life Sci. 2000;67: 3023–3029. doi: 10.1016/s0024-3205(00)00896-1 11125839

21. Erland LAE, Murch SJ, Reiter RJ, Saxena PK. A new balancing act: The many roles of melatonin and serotonin in plant growth and development. Plant Signal Behav. 2015;10: e1096469–15. doi: 10.1080/15592324.2015.1096469 26418957

22. Reiter R, Tan D-X, Zhou Z, Cruz M, Fuentes-Broto L, Galano A. Phytomelatonin: Assisting plants to aurvive and thrive. Molecules. 2015;20: 7396–7437. doi: 10.3390/molecules20047396 25911967

23. Erland LAE, Saxena PK. Melatonin in morphogenesis. In Vitro Cell Dev Biol—Plant. 2018;54: 3–24.

24. Erland LAE, Yasunaga A, Li ITS, Murch SJ, Saxena PK. Direct visualization of location and uptake of applied melatonin and serotonin in living tissues and their redistribution in plants in response to thermal stress. J Pineal Res. 2019;66: e12527. doi: 10.1111/jpi.12527 30267543

25. Reiter RJ, Mayo JC, Tan D-X, Sainz RM, Alatorre-Jimenez M, Qin L. Melatonin as an antioxidant: under promises but over delivers. J Pineal Res. 2016;61: 253–278. doi: 10.1111/jpi.12360 27500468

26. Bajwa VS, Shukla MR, Sherif SM, Murch SJ, Saxena PK. Identification and characterization of serotonin as an anti-browning compound of apple and pear. Postharvest Biol Technol. 2015;110: 183–189. doi: 10.1016/j.postharvbio.2015.08.018

27. Erland LAE, Shukla MR, Singh AS, Murch SJ, Saxena PK. Melatonin and serotonin: mediators in the symphony of plant morphogenesis. J Pineal Res. 2019;64: e12452. doi: 10.1111/jpi.12452 29149453

28. Murch SJ, Campbell SSB, Saxena PK. The role of serotonin and melatonin in plant morphogenesis: Regulation of auxin-induced root organogenesis in in vitro-cultured explants of st. John’s Wort (Hypericum perforatum L.). In Vitro Cell Dev Biol—Plant. Springer-Verlag; 2001;37: 786–793. doi: 10.1007/s11627-001-0130-y

29. Ramakrishna A, Giridhar P, Ravishankar GA. Indoleamines and calcium channels influence morphogenesis in in vitro cultures of Mimosa pudica L. Plant Signal Behav. Landes Bioscience; 2009;4: 1136–1141.

30. Ramakrishna A, Giridhar P, Jobin M, Paulose CS, Ravishankar GA. Indoleamines and calcium enhance somatic embryogenesis in Coffea canephora P ex Fr. Plant Cell Tiss Organ Cult. Springer Netherlands; 2011;108: 267–278. doi: 10.1007/s11240-011-0039-z

31. Pelagio-Flores R, Muñoz Parra E, Ortíz-Castro R, López-Bucio J. Melatonin regulates Arabidopsis root system architecture likely acting independently of auxin signaling. J Pineal Res. 2012;53: 279–288. doi: 10.1111/j.1600-079X.2012.00996.x 22507071

32. Pelagio-Flores R, Ortíz-Castro R, Méndez-Bravo A, Macías-Rodríguez L, López-Bucio J. Serotonin, a tryptophan-derived signal conserved in plants and animals, regulates root system architecture probably acting as a natural auxin inhibitor in Arabidopsis thaliana. Plant Cell Physiol. 2011;52: 490–508. doi: 10.1093/pcp/pcr006 21252298

33. Wen D, Gong B, Sun S, Liu S, Wang X, Wei M, et al. Promoting roles of melatonin in adventitious root development of Solanum lycopersicum L. by regulating auxin and nitric oxide signaling. Front Plant Sci. 2016;7: 787–11.

34. Pelagio-Flores R, Ruiz-Herrera LF, López-Bucio J. Serotonin modulates Arabidopsis root growth via changes in reactive oxygen species and jasmonic acid-ethylene signaling. Physiol Plant. 2016;158: 92–105. doi: 10.1111/ppl.12429 26864878

35. Sliwiak J, Dauter Z, Jaskolski M. Crystal Structure of Hyp-1, a Hypericum perforatum PR-10 Protein, in complex with melatonin. Front Plant Sci. 2016;7: 668. doi: 10.3389/fpls.2016.00668 27242869

36. Sliwiak J, Sikorski M, Jaskolski M. PR-10 proteins as potential mediators of melatonin-cytokinin cross-talk in plants: crystallographic studies of LlPR-10.2B isoform from yellow lupine. FEBS J. 2018;48: 251–16. doi: 10.1111/febs.14455 29630775

37. Li C, Tan D-X, Liang D, Chang C, Jia D, Ma F. Melatonin mediates the regulation of ABA metabolism, free-radical scavenging, and stomatal behaviour in two Malus species under drought stress. J Exp Bot. 2015;66: 669–680. doi: 10.1093/jxb/eru476 25481689

38. Shi H, Wei Y, Wang Q, Reiter RJ, He C. Melatonin mediates the stabilization of DELLA proteins to repress the floral transition in Arabidopsis. J Pineal Res. 2016;60: 373–379. doi: 10.1111/jpi.12320 26887824

39. Kang K, Kang S, Lee K, Park M, Back K. Enzymatic features of serotonin biosynthetic enzymes and serotonin biosynthesis in plants. Plant Signal Behav. 2008;3: 389–390. doi: 10.4161/psb.3.6.5401 19704574

40. Songstad DD, Kurz WGW, Nessler CL. Tyramine accumulation in Nicotiana tabacum transformed with a chimeric tryptophan decarboxylase gene. Phytochemistry. 1991;30: 3245–3246.

41. Songstad DD, De Luca V, Brisson N, Kurz WGW, Nessler CL. High levels of tryptamine accumulation in transgenic tobacco expressing tryptophan decarboxylase. Plant Physiol. 2008;94: 1410–1413.

42. Kang S, Kang K, Lee K, Back K. Characterization of tryptamine 5-hydroxylase and serotonin synthesis in rice plants. Plant Cell Rep. 2007;26: 2009–2015. doi: 10.1007/s00299-007-0405-9 17639402

43. Park S, Byeon Y, Lee HY, Kim Y-S, Ahn T, Back K. Cloning and characterization of a serotonin N-acetyltransferase from a gymnosperm, loblolly pine (Pinus taeda). J Pineal Res. 2014;57: 348–355. doi: 10.1111/jpi.12174 25208036

44. Park S, Byeon Y, Back K. Functional analyses of three ASMT gene family members in rice plants. J Pineal Res. 2013;55: 409–415. doi: 10.1111/jpi.12088 24033370

45. Back K, Tan D-X, Reiter RJ. Melatonin biosynthesis in plants: multiple pathways catalyze tryptophan to melatonin in the cytoplasm or chloroplasts. J Pineal Res. 2016;61: 426–437. doi: 10.1111/jpi.12364 27600803

46. Tan D-X, Hardeland R, Back K, Manchester LC, Alatorre-Jimenez MA, Reiter RJ. On the significance of an alternate pathway of melatonin synthesis via 5-methoxytryptamine: comparisons across species. J Pineal Res. 2016;61: 27–40. doi: 10.1111/jpi.12336 27112772

47. Byeon Y, Choi G-H, Lee HY, Back K. Melatonin biosynthesis requires N-acetylserotonin methyltransferase activity of caffeic acid O-methyltransferase in rice. J Exp Bot. 2015;66: 6917–6925. doi: 10.1093/jxb/erv396 26276868

48. Lee K, Lee HY, Back K. Rice histone deacetylase 10 and Arabidopsis histone deacetylase 14 genes encode N-acetylserotonin deacetylase, which catalyzes conversion of N-acetylserotonin into serotonin, a reverse reaction for melatonin biosynthesis in plants. J Pineal Res. 2018;64: e12460. doi: 10.1111/jpi.12460 29247559

49. Mano Y, Nemoto K. The pathway of auxin biosynthesis in plants. J Exp Bot. 2012;63: 2853–2872. doi: 10.1093/jxb/ers091 22447967


51. Murch SJ, Saxena PK. A melatonin-rich germplasm line of St John’s wort (Hypericum perforatum L.). J Pineal Res. 2006;41: 284–287. doi: 10.1111/j.1600-079X.2006.00367.x 16948791

52. Alan AR, Murch SJ, Saxena PK. Evaluation of ploidy variations in Hypericum perforatum L. (St. John’s wort) germplasm from seeds, in vitro germplasm collection, and regenerants from floral cultures. In Vitro Cell Dev Biol—Plant. 2015;51: 452–462. doi: 10.1007/s11627-015-9708-7

53. Murashige T, Skoog F. A revised medium for rapid growth and bioassays with tobacco tissue cultures. Physiol Plant. 1962;15: 473–497.

54. Erland LAE, Chattopadhyay A, Jones AMP, Saxena PK. Melatonin in plants and plant culture systems: variability, stability and efficient quantification. Front Plant Sci. 2016;7: 108.

55. Erland LAE, Shukla MR, Glover WB, Saxena PK. A simple and efficient method for analysis of plant growth regulators: a new tool in the chest to combat recalcitrance in plant tissue culture. Plant Cell Tiss Organ Cult. 2017;131: 459–470. doi: 10.1007/s11240-017-1297-1

56. Enders TA, Strader LC. Auxin activity: Past, present, and future. Am J Bot. 2015;102: 180–196. doi: 10.3732/ajb.1400285 25667071

57. Skoog F, Miller CO. Chemical regulation of growth and organ formation in plant tissues cultured in vitro. Symp Soc Exp Biol. 1957;11: 118–130. 13486467

58. Murch SJ, Saxena PK. Role of indoleamines in regulation of morphogenesis in in vitro cultures of St. John’s wort (Hypericum perforatum L.). Acta Hortic. International Society for Horticultural Science—ISHS; 2004;629: 425–432. doi: 10.17660/ActaHortic.2004.629.56

59. Murch SJ, Saxena PK. Mammalian neurohormones: potential significance in reproductive physiology of St. John’s wort (Hypericum perforatum L.)? Naturwissenschaften. 2002;89: 555–560 12536277

60. Erland LAE, Turi CE, Saxena PK. Serotonin: An ancient molecule and an important regulator of plant processes. Biotechnol Adv. 2016;8: 1347–1361. doi: 10.1016/j.biotechadv.2016.10.002 27742596

61. Steward FC, Bidwell RGS. Nitrogen metabolism, respiration, and growth of cultured plant tissue: PART IV. THE IMPACT OF GROWTH ON PROTEIN METABOLISM AND RESPIRATION OF CARROT TISSUE EXPLANTS. GENERAL DISCUSSION OF RESULTS. J Exp Bot. 1958;9: 285–305.

62. Saremba BM, Tymm FJM, Baethke K, Rheault MR, Sherif SM, Saxena PK, et al. Plant signals during beetle (Scolytus multistriatus) feeding in American elm (Ulmus americana Planch). Plant Signal Behav. 2017;12: e1296997. doi: 10.1080/15592324.2017.1296997 28448744

63. Hernández IG, Gomez FJV, Cerutti S, Arana MV, Silva MF. Melatonin in Arabidopsis thaliana acts as plant growth regulator at low concentrations and preserves seed viability at high concentrations. Plant Physiol Biochem. 2015;94: 191–196. doi: 10.1016/j.plaphy.2015.06.011 26113158

64. Byeon Y, Lee HY, Lee K, Park S, Back K. Cellular localization and kinetics of the rice melatonin biosynthetic enzymes SNAT and ASMT. J Pineal Res. 2013;56: 107–114. doi: 10.1111/jpi.12103 24134674

65. Pelagio-Flores R, Muñoz Parra E, Ortíz-Castro R, López-Bucio J. Melatonin regulates Arabidopsis root system architecture likely acting independently of auxin signaling. J Pineal Res. 2012;53: 279–288. doi: 10.1111/j.1600-079X.2012.00996.x 22507071

66. Liang C, Li A, Yu H, Li W, Liang C, Guo S, et al. Melatonin regulates root architecture by modulating auxin response in rice. Front Plant Sci. 2017;8: 89–12.

67. Wang Q, An B, Wei Y, Reiter RJ, Shi H, Luo H, et al. Melatonin regulates root meristem by repressing auxin synthesis and polar auxin transport in Arabidopsis. Front Plant Sci. 2016;07: 1–11. doi: 10.3389/fpls.2016.01882 28018411

68. Wen D, Gong B, Sun S, Liu S, Wang X, Wei M, et al. Promoting roles of melatonin in adventitious root development of Solanum lycopersicum L. by regulating auxin and nitric oxide signaling. Front Plant Sci. 2016;7: 787–11.

69. Murch SJ, Saxena PK. Melatonin: A potential regulator of plant growth and development? In Vitro Cell Dev Biol—Plant. 2002;38: 531–536. doi: 10.1079/IVP2002333

Článek vyšel v časopise


2019 Číslo 10