Melatonin-induced brassinosteroid biosynthesis enhances seed size, senescence tolerance, and salt stress susceptibility in transgenic rice plants overexpressing an archaeal serotonin N-acetyltransferase
Melatonin increases BR biosynthesis
Keywords:
Archaea, brassinosteroid, lamina angle, melatonin, serotonin N-acetyltransferase (SNAT), transgenic rice
Abstract
Serotonin N-acetyltransferase (SNAT) is the penultimate enzyme catalyzing serotonin into N-acetylserotonin in the melatonin biosynthetic pathway. Recently, an archaeal SNAT from Thermoplasma volcanium (TvSNAT) was cloned and rice lines with its ectopic overexpression (TvSNAT-OE) exhibited higher melatonin levels and generated larger seeds than those of the wild type (WT). In this study, we hypothesized that the increased seed size in TvSNAT-OE rice line might be linked to enhanced brassinosteroid (BR) synthesis since melatonin level is positively associated with BR production. In rice seedlings, roots were shorter and the lamina angle was larger in TvSNAT-OE lines than those in the WT. Also, the second leaves of seedlings were longer in the TvSNAT-OE lines than that in the WT, supporting BR elevation in the TvSNAT-OE lines. In parallel with these phenotypic features, BR levels were higher in the TvSNAT-OE lines than that in the WT. Increased BR levels were associated with enhanced expression of DWARF4 and BZR1, the key genes for BR biosynthesis and signaling, in the TvSNAT-OE lines compared with the WT. Consequently, the TvSNAT-OE lines showed delayed senescence, but were more susceptible to salt stress than the WT due to enhanced BR levels.
References
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40. Byeon Y, Lee HY, Lee K, Park S, Back K (2014) Cellular localization and kinetics of the rice melatonin biosynthetic enzymes SNAT and ASMT. J. Pineal Res. 56: 107-114.
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42. Jiang H, Zhang A, Liu X, Chen J (2022) Grain size associated genes and the molecular regulatory mechanism in rice. Int. J. Mol. Sci. 23: 3169.
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51. Yamamuro C, Ihara Y, Wu X, Noguchi T, Fujioka S, Takatsuto S, Ashikari M, Kitano H, Matsuoka M (2000) Loss of function of a rice brassinosteroid insensitive1 homolog prevents internode elongation and bending of the lamina joint. Plant Cell 12: 1591-1605.
52. Huang P, Zhao J, Hong J, Zhu B, Xia S, Zhu E, Han P, Zhang K (2023) Cytokinins regulate rice lamina joint development and leaf angle. Plant Physiol. 191: 56-69.
53. Hwang OJ, Back K (2022) Exogenous gibberellin treatment enhances melatonin synthesis for melatonin-enriched rice production. Biomolecules 12: 198.
54. Zou X, Shao J, Wang Q, Chen P, Zhu Y, Yin C (2018) Supraoptimal cytokinin content inhibits rice seminal root growth by reducing root meristem size and cell length via increased ethylene content. Int. J. Mol. Sci. 19: 4051.
55. Liu Y, Zhang M, Meng Z, Wang B, Chen M (2020) Research progress on the roles of cytokinin in plant response to stress. Int. J. Mol. Sci. 21: 6574.
56. Joshi R, Sahoo KK, Tripathi AK, Kumar R, Gupta BK, Pareek A, Singlapareek SL (2018) Knockdown of an inflorescence meristem-specific cytokinin oxidase-OsCKX2 in rice reduces yield penalty under salinity stress condition. Plant Cell Environ. 41: 936-946.
57. Vankova R, Gaudinova A, Dobrev PI, Malbeck J, Haisel D, Motyka V (2010) Comparison of salinity and drought stress effects on abscisic acid metabolites activity of cytokinin oxidase/dehydrogenase and chlorophyll levels in radish and tobacco. Ecol. Quest. 14: 99-100.
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59. Gomes MMA, Pinheiro DT, Bressan-Smith R, Campostrini E (2018) Exogenous brassinosteroid application delays senescence and promotes hyponasty in Carica papaya L. leaves. Theor. Exp. Plant Physiol. 30: 193–201.
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63. Lee HY, Back K (2024) Melatonin-regulated chaperone binding protein plays a key role in cadmium stress tolerance in rice, revealed by the functional characterization of a novel serotonin N-acetyltransferase 3 (SNAT3) in rice. Int. J. Mol. Sci. 25: 5952.
64. Lee K, Back K (2024) Functional characterization of the ciliate Stylonychia lemnae serotonin N-acetyltransferase, a pivotal enzyme in melatonin biosynthesis and its overexpression leads to peroxidizing herbicide tolerance in rice. Antioxidants 13: 1177.
65. Erland LAE, Dumigan CR, Forsyth JA, Frolova L, Yasunaga AB, Pun W, Li ITS, Deyholos MK, Murch SJ (2022) Mammalian melatonin agonist pharmaceuticals stimulate rhomboid proteins in plants. Biomolecules 12: 882.
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2. Back K (2021) Melatonin metabolism, signaling and possible roles in plants. Plant J. 105: 376-391.
3. Lee K, Choi GH, Back K (2022) Functional characterization of serotonin N-acetyltransferase in archaeon Thermoplasma volcanium. Antioxidants 11: 596.
4. Reiter RJ, Tan DX, Sharma R (2018) Historical perspective and evaluation of the mechanisms by which melatonin mediates seasonal reproduction in mammals. Melatonin Res. 1: 59-77.
5. Lee HY, Back K (2021) Melatonin regulates chloroplast protein quality control via a mitogen-activated protein kinase signaling pathway. Antioxidants 10: 511.
6. Lee HY, Hwang OJ, Back K (2022) Phytomelatonin as a signaling molecule for protein quality control via chaperone, autophagy, and ubiquitin–proteasome systems in plants. J. Exp. Bot. 73: 5863-5873.
7. Zhao D, Wang H, Chen S, Yu D, Reiter RJ (2021) Phytomelatonin: an emerging regulator of plant biotic stress resistance. Trends Plant Sci. 26: 70-82.
8. Wang L, Tanveer M, Wang H, Arnao MB (2024) Melatonin as a key regulator in seed germination under abiotic stress. J. Pineal Res. 76: e12937.
9. Aghdam MS, Arnao MB (2024) Phytomelatonin: from intracellular signaling to global horticulture market. J. Pineal Res. 76: e12990.
10. García-Cánovas I, Giraldo-Acosta M, Cano A, Arnao MB, Hernández-Ruiz J (2024) Effect of melatonin on germination and seedling growth in aging seeds or under drought conditions. Seeds 3: 341-356.
11. Arnao MB, Cano A, Hernández-Ruiz J (2022) Phytomelatonin: an unexpected molecule with amazing performance in plants. J. Exp. Bot. 73: 5779-5800.
12. Aghdam MS, Mukherjee S, Flores FB, Arnao MB, Luo Z, Corpas FJ (2022) Functions of melatonin during postharvest of horticultural crops. Plant Cell Physiol. 63: 1764-1786.
13. Lee K, Hwang OJ, Back K (2020) Rice N-acetylserotonin deacetylase regulates melatonin levels in transgenic rice. Melatonin Res. 3: 32-42.
14. Klein DC (2007) Arylakylamine N-acetyltransferase: “the timezyme”. J. Biol. Chem. 282: 4233-4237.
15. Lee K, Choi GH, Back K (2021) Inhibition of rice serotonin N-acetyltransferase by MG149 decreased melatonin synthesis in rice seedlings. Biomolecules 11: 658.
16. Byeon Y, Park S, Lee HY, Kim YS, Back K (2014) Elevated production of melatonin in transgenic rice seeds expressing rice tryptophan decarboxylase. J. Pineal Res. 56: 275-282.
17. Byeon Y, Back K (2014) An increase in melatonin in transgenic rice causes pleiotropic phenotypes, including enhanced seedling growth, delayed flowering, and low grain yield. J. Pineal Res. 56: 408-414.
18. Lee K, Back K (2017) Overexpression of rice serotonin N-acetyltransferase 1 in transgenic rice plants confers resistance to cadmium and senescence and increases grain yield. J. Pineal Res. 62: e12392.
19. Hwang OJ, Back K (2019) Melatonin deficiency confers tolerance to multiple abiotic stresses in rice via decreased brassinosteroid levels. Int. J. Mol. Sci. 20: 5173.
20. Huangfu L, Chen R, Lu Y, Zhang E, Miao J, Zuo Z, Zhao Y, Zhu M, Zhang Z, Li P, Xu Y, Yao Y, Liang G, Xu C, Zhou Y, Yang, Z (2022) OsCOMT, encoding a caffeic acid O-methyltransferase in melatonin biosynthesis, increases rice grain yield through dual regulation of leaf senescence and vascular development. Plant Biotechnol. J. 20: 1122-1139.
21. Lee K, Back K (2019) Melatonin-deficient rice plants show a common semidwarf phenotype either dependent or independent of brassinosteroid biosynthesis. J. Pineal Res. 66: e12537.
22. Hwang OJ, Back K (2022) Molecular regulation of antioxidant melatonin biosynthesis by brassinosteroid acting as an endogenous elicitor of melatonin induction in rice seedling. Antioxidants 11: 918.
23. Hwang OJ, Back K (2022) Functional characterization of arylalkylamine N-acetyltransferase, a pivotal gene in antioxidant melatonin biosynthesis from Chlamydomonas reinhardtii. Antioxidants 11: 1531.
24. Hwang OJ, Back K (2018) Melatonin is involved in skotomorphogenesis by regulating brassinosteroid biosynthesis in plants. J. Pineal Res. 65: e12495.
25. Wu C, Trieu A, Radhakrishnan P, Kwok SF, Harris S, Zhang K, Wang J, Wan J, Zhai H, Takatsuto S, Matsumoto S, Fujioka S, Feldmann KA, Pennell, RI (2008) Brassinosteroids regulate grain filling in rice. Plant Cell 20: 2130-2145.
26. Huang R, Jiang L, Zheng J, Wang T, Wang H, Huang Y, Hong Z (2013) Genetic bases of rice grain shape: so many genes, so little known. Trends Plant Sci. 18: 218-226.
27. Tong H, Xiao Y, Liu D, Gao S, Liu L, Yin Y, Jin Y, Qian Q, Chu C (2014) Brassinosteroid regulates cell elongation by modulating gibberellin metabolism in rice. Plant Cell 26: 4376-4393.
28. Krishna P (2003) Brassinosteroid-mediated stress responses. J. Plant Growth Regul. 22: 289-297.
29. Kim SY, Kim BH, Lim CJ, Lim CO, Nam KH (2010) Constitutive activation of stress-inducible genes in a brassinosteroid-insensitive 1 (bri1) mutant results in higher tolerance to cold. Physiol. Plant. 138: 191-204.
30. Sahni S, Prasad BD, Liu Q, Grbic V, Sharpe A, Singh SP, Krishna P (2016) Overexpression of the brassinosteroid biosynthetic gene DWF4 in Brassica napus simultaneously increases seed yield and stress tolerance. Sci. Rep. 6: 28298.
31. Yin W, Dong N, Niu M, Zhang X, Li L, Liu J, liu B, Tong H (2019) Brassinosteroid-regulated plant growth and development and gene expression in soybean. Crop J. 7: 411-418.
32. Li X, Yu B, Cui Y, Yin Y (2017) Melatonin application confers enhanced salt tolerance by regulating Na+ and Cl- accumulation in rice. Plant Growth Regul. 83: 441-454.
33. Yu Y, Ni Y, Qiao T, Ji X, Xu J, Li B, Sun Q (2022) Overexpression of VvASMT1 from grapevine enhances salt and osmotic stress tolerance in Nicotiana benthamiana. PLoS ONE 17: e0269028.
34. Janas KM, Posmyk MM (2013) Melatonin, an underestimated natural substance with great potential for agricultural application. Acta Physiol. Plant 35: 3285-3292.
35. Liu J, Ruimin Z, Yunkuo S, Zeyu L, Wen, J, Yan S (2016) The beneficial effects of exogenous melatonin on tomato fruit properties. Sci. Hortic. 207: 14-20.
36. Ye J, Yang W, Li Y, Wang S, Yin L, Deng X (2020) Seed pre-soaking with melatonin improves wheat yield by delaying leaf senescence and promoting root development. Agronomy 10: 84.
37. Wang K, Xing Q, Ahammed GJ, Zhou J (2022) Functions and prospects of melatonin in plant growth, yield, and quality. J. Exp. Bot. 73: 5928-5946.
38. Byeon Y, Back K (2016) Low melatonin production by suppression of either serotonin N-acetyltransferase or N-acetylserotonin methyltransferase in rice causes seedling growth retardation with yield penalty, abiotic stress susceptibility, and enhanced coleoptile growth under anoxic conditions. J. Pineal Res. 60: 348-359.
39. Byeon Y, Lee HY, Back K (2015) Chloroplastic and cytoplasmic overexpression of sheep serotonin N-acetyltransferase in transgenic rice plants is associated with low melatonin production despite high enzyme activity. J. Pineal Res. 58: 461-469.
40. Byeon Y, Lee HY, Lee K, Park S, Back K (2014) Cellular localization and kinetics of the rice melatonin biosynthetic enzymes SNAT and ASMT. J. Pineal Res. 56: 107-114.
41. Vriet C, Russinova E, Reuzeau C (2012) Boosting crop yields with plant steroids. Plant Cell 24: 842-857.
42. Jiang H, Zhang A, Liu X, Chen J (2022) Grain size associated genes and the molecular regulatory mechanism in rice. Int. J. Mol. Sci. 23: 3169.
43. Lo SF, Cheng ML, Hsing YC, Chen YS, Lee KW, Hong YF, Hsiao Y, Hsiao AS, Chen PJ, Wong LI, Chen NC, Reuzeau C, Ho THD, Yu SM (2020) Rice Big Grain 1 promotes cell division to enhance organ development, stress tolerance and grain yield. Plant Biotechnol. J. 18: 1969-1983.
44. Yeh SY, Chen HW, Ng CY, Lin CY, Tseng TH, Li WH, Ku MSB (2015) Down-regulation of cytokinin oxidase 2 expression increases tiller number and improves rice yield. Rice 8: 36.
45. Shi CL, Dong NQ, Guo T, Ye WW, Shan JX, Lin HX (2020) A quantitative trait locus GW6 controls rice grain size and yield through the gibberellin pathway. Plant J. 103: 1174-1188.
46. Seo H, Kim SH, Lee BD, Lim JH, Lee SJ, An G, Paek NC (2020) The rice basic helix-loop-helix 79 (OsbHLH079) determines leaf angle and grain shape. Int. J. Mol. Sci. 21: 2090.
47. Choe S, Fujioka S, Noguchi T, Takatsuto S, Yoshida S, Feldmann KA (2001) Overexpression of DWARF4 in the brassinosteroid biosynthetic pathway results in increased vegetative growth and seed yield in Arabidopsis. Plant J. 26: 573-582.
48. Tanabe S, Ashikari M, Fujioka S, Takatsuto S, Yoshida S, Yano M, Yoshimura A, Kitano H, Matsuoka M, Fujisawa Y, Kato H (2005) A novel cytochrome P450 is implicated in brassinosteroid biosynthesis via the characterization of a rice dwarf mutant, dwarf11, with reduced seed length. Plant Cell 17: 776-790.
49. Hong Z, Ueguchi-Tanaka M, Umemura K, Uozu S, Fujioka S, Takatsuto S, Yoshida S, Ashikari M, Kitano H, Matsuoka M (2003) A rice brassinosteroid-deficient mutant, ebisu dwarf (d2), is caused by a loss of function of a new member of cytochrome P450. Plant Cell 15: 2900-2910.
50. Wang K, Li MQ, Chang YP, Zhang B, Zhao QZ, Zhao WL (2020) The basic helix-loop-helix transcription factor OsBLR1 regulates leaf angle in rice via brassinosteroid signaling. Plant Mol. Biol. 102: 589-602.
51. Yamamuro C, Ihara Y, Wu X, Noguchi T, Fujioka S, Takatsuto S, Ashikari M, Kitano H, Matsuoka M (2000) Loss of function of a rice brassinosteroid insensitive1 homolog prevents internode elongation and bending of the lamina joint. Plant Cell 12: 1591-1605.
52. Huang P, Zhao J, Hong J, Zhu B, Xia S, Zhu E, Han P, Zhang K (2023) Cytokinins regulate rice lamina joint development and leaf angle. Plant Physiol. 191: 56-69.
53. Hwang OJ, Back K (2022) Exogenous gibberellin treatment enhances melatonin synthesis for melatonin-enriched rice production. Biomolecules 12: 198.
54. Zou X, Shao J, Wang Q, Chen P, Zhu Y, Yin C (2018) Supraoptimal cytokinin content inhibits rice seminal root growth by reducing root meristem size and cell length via increased ethylene content. Int. J. Mol. Sci. 19: 4051.
55. Liu Y, Zhang M, Meng Z, Wang B, Chen M (2020) Research progress on the roles of cytokinin in plant response to stress. Int. J. Mol. Sci. 21: 6574.
56. Joshi R, Sahoo KK, Tripathi AK, Kumar R, Gupta BK, Pareek A, Singlapareek SL (2018) Knockdown of an inflorescence meristem-specific cytokinin oxidase-OsCKX2 in rice reduces yield penalty under salinity stress condition. Plant Cell Environ. 41: 936-946.
57. Vankova R, Gaudinova A, Dobrev PI, Malbeck J, Haisel D, Motyka V (2010) Comparison of salinity and drought stress effects on abscisic acid metabolites activity of cytokinin oxidase/dehydrogenase and chlorophyll levels in radish and tobacco. Ecol. Quest. 14: 99-100.
58. Vardhini BV, Anuradha S, Sujatha E, Rao SSR (2010) Role of brassinosteroids in alleviating various abiotic and biotic stressesa review. Plant Stress 4: 55-61.
59. Gomes MMA, Pinheiro DT, Bressan-Smith R, Campostrini E (2018) Exogenous brassinosteroid application delays senescence and promotes hyponasty in Carica papaya L. leaves. Theor. Exp. Plant Physiol. 30: 193–201.
60. Yang S, Zhao Y, Qin X, Ding C, Chen Y, Tang Z, Huang Y, Reiter RJ, Yuan S, Yuan M (2022) New insights into the role of melatonin in photosynthesis. J. Exp. Bot. 73: 5918-5927.
61. Lee K, Back K (2023) Human Naa50 shows serotonin N-acetyltransferase activity, and its overexpression enhances melatonin biosynthesis, resulting in osmotic stress tolerance in rice. Antioxidants 12: 319.
62. Lee K, Back K (2023) Escherichia coli RimI encodes serotonin N-acetyltransferase activity and its overexpression leads to enhanced growth and melatonin biosynthesis. Biomolecules 13: 908.
63. Lee HY, Back K (2024) Melatonin-regulated chaperone binding protein plays a key role in cadmium stress tolerance in rice, revealed by the functional characterization of a novel serotonin N-acetyltransferase 3 (SNAT3) in rice. Int. J. Mol. Sci. 25: 5952.
64. Lee K, Back K (2024) Functional characterization of the ciliate Stylonychia lemnae serotonin N-acetyltransferase, a pivotal enzyme in melatonin biosynthesis and its overexpression leads to peroxidizing herbicide tolerance in rice. Antioxidants 13: 1177.
65. Erland LAE, Dumigan CR, Forsyth JA, Frolova L, Yasunaga AB, Pun W, Li ITS, Deyholos MK, Murch SJ (2022) Mammalian melatonin agonist pharmaceuticals stimulate rhomboid proteins in plants. Biomolecules 12: 882.
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Published
2024-12-08
How to Cite
[1]
Lee, K. and Back, K. 2024. Melatonin-induced brassinosteroid biosynthesis enhances seed size, senescence tolerance, and salt stress susceptibility in transgenic rice plants overexpressing an archaeal serotonin N-acetyltransferase. Melatonin Research. 7, 3 (Dec. 2024), 249-259. DOI:https://doi.org/https://doi.org/10.32794/mr112500180.
Section
Research Articles
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