Cyclic 3-hydroxymelatonin exhibits diurnal rhythm and cyclic 3-hydroxymelatonin overproduction increases secondary tillers in rice by upregulating MOC1 expression
Diurnal rhythm of cyclic 3-hydroxymelatonin
Keywords:
cyclic 3-hydroxymelatonin; diurnal rhythm; M3H; melatonin; RNAi; tiller number; transgenic rice
Abstract
Cyclic 3-hydroxymelatonin (c3OHM) is a major metabolite of melatonin in plants produced by the enzymatic action of melatonin 3-hydroxylase (M3H). However, the function of c3OHM in plants is unclear. Here, we report that M3H mRNA and c3OHM levels display diurnal rhythms with peaks at night, but not in a circadian manner. This diurnal rhythmicity occurred predominantly in the late vegetative growth stage (8 weeks after germination), but was absent in the early vegetative growth stage. Transgenic rice plants overexpressing or underexpressing M3H were generated to investigate the physiological roles of diurnal production of c3OHM. The M3H-overexpression (OE) line exhibited higher M3H activity and c3OHM production than the wild-type, and vice versa for the M3H‑underexpression rice (RNAi). The seedling growth phenotype of the OE and RNAi lines was comparable to that of the wild-type but exhibited pleiotropic phenotypic defects at the reproductive stage, such as decreased height, biomass, grain yield, and fertility. Of note, the OE rice showed significantly increased numbers of secondary tillers and panicles. The increase in tiller number of the OE line was linked to increased expression of tiller-related genes, such as MOC1 and TB1, suggesting that the diurnal rhythm of c3OHM production is associated with the tiller number, a pivotal agronomic trait governing grain yield in rice.
References
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14. Liang D, Shen Y, Ni Z, Wang Q, Lei Z, Xu N, Deng Q, Lin L, Wang J, Lv X, Xia H (2018) Exogenous melatonin application delays senescence of kiwifruit leaves by regulating the antioxidant capacity and biosynthesis of flavonoids. Front. Plant Sci. 9: 426. doi: 10.3389/fpls.2018.00426.
15. Sun Q, Zhang N, Wang J, Cao Y, Li X, Zhang H, Zhang L, Tan DX, Guo YD (2016) A label-free differential proteomics analysis reveals the effect of melatonin on promoting fruit ripening and anthocyanin accumulation upon postharvest in tomato. J. Pineal Res. 61: 138-153. doi: 10.1111/jpi.12315.
16. Li H, Chang J, Zheng J, Dong Y, Liu Q, Yang X, Wei C, Zhang Y, Ma J, Zhang X (2017) Local melatonin application induces cold tolerance in distant organs of Citrullus lanatus L. via long distance transport. Sci. Rep. 7: 40858. doi: 10.1038/srep40858.
17. Zhao H, Ye L, Wang Y, Zhou X, Yang J, Wang J, Cao K, Zou Z (2016) Melatonin increases the chilling tolerance of chloroplast in cucumber seedlings by regulating photosynthetic electron flux and the ascorbate-glutathione cycle. Front. Plant Sci. 7: 1814. doi: 10.3389/fpls.2016.01814.
18. Shi H, Wei Y, He C (2016) Melatonin-induced CBF/DREB1s are essential for diurnal change of disease resistance and CCA1 expression in Arabidopsis. Plant Physiol. Biochem. 100: 150-153. doi: 10.1016/j.plaphy.2016.01.018.
19. Qian Y, Tan DX, Reiter RJ, Shi H (2015) Comparative metabolomics analysis highlights the involvement of sugars and glycerol in melatonin-mediated innate immunity against bacterial pathogen in Arabidopsis. Sci. Rep. 4: 15815. doi: 10.1038/srep15815.
20. 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. doi: 10.1111/jpi.12392.
21. Cai SY, Zhang Y, Xu YP, Qi ZY, Li MQ, Ahammed GJ, Xia XJ, Shi K, Zhou YH, Reiter RJ, Yu JQ, Zhou J (2017) HsfA1a upregulates melatonin biosynthesis to confer cadmium tolerance in tomato plants. J. Pineal Res. 62: e12387. doi: 10.1111/jpi.12387.
22. Lee HY, Back K (2018) Melatonin plays a pivotal role in conferring tolerance against endoplasmic reticulum stress via mitogen-activated protein kinases and bZIP60 in Arabidopsis thaliana. Melatonin Res. 1: 93-107. doi: 10.32974/mr11250006.
23. Wang Y, Reiter RJ, Chan Z (2018) Phytomelatonin: a universal abiotic stress regulator. J. Exp. Bot. 69: 963-974. doi: 10.1093/jxb/erx473.24.
24. Debnath B, Islam W, Li M, Sun Y, Lu X, Mitra S, Hussain M, Liu S, Qiu D (2019) Melatonin mediates enhancement of stress tolerance in plants. Int. J. Mol. Sci. 20: 1040. doi: org/10.3390/ijms20051040.
25. Ahammed GJ, Xu W, Liu A, Chen S (2018) COMT1 silencing aggravates heat stress-induced reduction in photosynthesis by decreasing chlorophyll content, photosystem II activity, and electron transport efficiency in tomato. Front. Plant Sci. 9: 998. doi: 10.3389/fpls.2018.00998.
26. Gong B, Yan Y, Wen D, Shi Q (2017) Hydrogen peroxide produced by NADPH oxidase: a novel downstream signaling pathway in melatonin-induced stress tolerance in Solanum lycopersicum. Physiol. Plant. 160: 396-409. doi: 10.1111/ppl.12581.
27. Chen Z, Xie Y, Gu Q, Zhao G, Zhang Y, Cui W, Xu S, Wang R, Shen W (2017) The AtrbohF-dependent regulation of ROS signaling is required for melatonin-induced salinity tolerance in Arabidopsis. Free Radic. Biol. Med. 108: 465-477. doi: 10.1016/j.freeradbiomed.2017.04.009.
28. Choi GH, Lee HY, Back K (2017) Chloroplast overexpression of rice caffeic acid O-methyltransferase increase melatonin production in chloroplasts via the 5-methoxytryptamine pathway in transgenic rice plants. J. Pineal Res. 63: e12412. doi: 10.1111/jpi.12412.
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31. Back K, Tan DX, Reiter RJ (2016) Melatonin biosynthesis in plants: Multiple pathways catalyze tryptophan to melatonin in the cytoplasm or chloroplasts. J. Pineal Res. 61: 426-437. doi: 10.1111/jpi.12364.
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Published
2019-08-31
How to Cite
[1]
Choi, G.-H. and Back, K. 2019. Cyclic 3-hydroxymelatonin exhibits diurnal rhythm and cyclic 3-hydroxymelatonin overproduction increases secondary tillers in rice by upregulating MOC1 expression. Melatonin Research. 2, 3 (Aug. 2019), 120-138. DOI:https://doi.org/https://doi.org/10.32794/11250034.
Section
Research Articles
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