[en] Drought severely affects the yield of wheat (Triticum aestivum L.), which is mainly grown in arid and semi-arid regions. Melatonin plays an important role in various types of stress resistance in plants, including drought resistance. However, the molecular mechanism through which melatonin affects drought tolerance remains largely unknown. In this study, we revealed that melatonin (100 μM) significantly improved drought resistance during the maturation stage of Chinese Spring, Shi4185, and Hanxuan10 varieties, but not Chang6878. Further physiological, transcriptomic, and proteomic data analysis at the wheat seedling stage revealed that melatonin increased jasmonic acid (JA) content, upregulating the expression of JA genes (LOX1.5 and LOX2.1) and two transcription factors (HY5 and MYB86) under drought conditions. It also upregulated genes related to lignin biosynthesis (4CL2, P5CS1, and CCR2) as well as starch and sucrose metabolism (PME53 and SUS4). Additionally, melatonin alleviated photosynthetic and cell membrane damage caused by drought stress through maintaining low levels of hydrogen peroxide. The current results elucidate melatonin-regulated pathways in wheat and provide evidence for using melatonin as a potential biostimulant to improve wheat drought resistance under field conditions in the future.
Disciplines :
Agriculture & agronomy
Author, co-author :
Luo, Mingzhao ; Université de Liège - ULiège > TERRA Research Centre
Wang, Daoping; State Key Laboratory of Crop Gene Resources and Breeding, Institute of Crop Sciences, Chinese Academy of Agricultural Sciences (CAAS), Beijing, 100081, China
Delaplace, Pierre ; Université de Liège - ULiège > TERRA Research Centre > Plant Sciences
Pan, Yinghong; State Key Laboratory of Crop Gene Resources and Breeding, Institute of Crop Sciences, Chinese Academy of Agricultural Sciences (CAAS), Beijing, 100081, China
Zhou, Yongbin; State Key Laboratory of Crop Gene Resources and Breeding, Institute of Crop Sciences, Chinese Academy of Agricultural Sciences (CAAS), Beijing, 100081, China
Tang, Wensi; State Key Laboratory of Crop Gene Resources and Breeding, Institute of Crop Sciences, Chinese Academy of Agricultural Sciences (CAAS), Beijing, 100081, China
Chen, Kai; State Key Laboratory of Crop Gene Resources and Breeding, Institute of Crop Sciences, Chinese Academy of Agricultural Sciences (CAAS), Beijing, 100081, China
Chen, Jun; State Key Laboratory of Crop Gene Resources and Breeding, Institute of Crop Sciences, Chinese Academy of Agricultural Sciences (CAAS), Beijing, 100081, China
Xu, Zhaoshi; State Key Laboratory of Crop Gene Resources and Breeding, Institute of Crop Sciences, Chinese Academy of Agricultural Sciences (CAAS), Beijing, 100081, China
Ma, Youzhi; State Key Laboratory of Crop Gene Resources and Breeding, Institute of Crop Sciences, Chinese Academy of Agricultural Sciences (CAAS), Beijing, 100081, China. Electronic address: mayouzhi@caas.cn
Chen, Ming; State Key Laboratory of Crop Gene Resources and Breeding, Institute of Crop Sciences, Chinese Academy of Agricultural Sciences (CAAS), Beijing, 100081, China. Electronic address: chenming02@caas.cn
Language :
English
Title :
Melatonin enhances drought tolerance by affecting jasmonic acid and lignin biosynthesis in wheat (Triticum aestivum L.).
The authors are grateful to Prof. Pierre Delaplace, University of Liege, for revising this manuscript. This work was supported by the Agricultural Science and Technology Innovation and China Scholarship Council (Contract No. 202003250115 ). We would like to thank Editage ( www.editage.cn ) for English language editing.
Ali, M.S., Baek, K.H., Jasmonic acid signaling pathway in response to abiotic stresses in plants. Int. J. Mol. Sci., 21, 2020, 621, 10.3390/IJMS21020621.
Anders, S., Huber, W., Differential expression analysis for sequence count data. Genome Biol., 11, 2010, R106, 10.1186/GB-2010-11-10-R106.
Arnao, M.B., Hernández-Ruiz, J., Melatonin as a regulatory hub of plant hormone levels and action in stress situations. Plant Biol. 23 (2021), 7–19, 10.1111/PLB.13202.
Arnao, M.B., Hernández-Ruiz, J., Melatonin in flowering, fruit set and fruit ripening. Plant Reprod. 33 (2020), 77–87, 10.1007/S00497-020-00388-8.
Arnon, D.I., Copper enzymes in isolated chloroplasts. Polyphenoloxidase in beta vulgaris. Plant Physiol. 24 (1949), 1–15, 10.1104/pp.24.1.1.
Back, K., Melatonin metabolism, signaling and possible roles in plants. Plant J. 105 (2021), 376–391, 10.1111/TPJ.14915.
Chung, M.H., Deng, T.S., Effects of circadian clock and light on melatonin concentration in Hypericum perforatum L. (St. John's Wort). Bot. Stud., 61, 2020, 23, 10.1186/s40529-020-00301-6.
Cui, G., Sun, F., Gao, X., Xie, K., Zhang, C., Liu, S., Xi, Y., Proteomic analysis of melatonin-mediated osmotic tolerance by improving energy metabolism and autophagy in wheat (Triticum aestivum L.). Planta 248 (2018), 69–87, 10.1007/S00425-018-2881-2/FIGURES/11.
Cui, G., Zhao, X., Liu, S., Sun, F., Zhang, C., Xi, Y., Beneficial effects of melatonin in overcoming drought stress in wheat seedlings. Plant Physiol. Biochem. 118 (2017), 138–149, 10.1016/j.plaphy.2017.06.014.
Ding, Z., Xu, X., Tanaka, H., Xu, D., Xiao, Y., Chu, L., Zhang, Y., Bian, Y., Xiao, J., HY5: a pivotal regulator of light-dependent development in higher plants. Front. Plant Sci., 12, 2022, 800989, 10.3389/fpls.2021.800989.
Dubbels, R., Reiter, R.J., Klenke, E., Goebel, A., Schnakenberg, E., Ehlers, C., Schiwara, H.W., Schloot, W., Melatonin in edible plants identified by radioimmunoassay and by high performance liquid chromatography‐mass spectrometry. J. Pineal Res. 18 (1995), 28–31, 10.1111/j.1600-079X.1995.tb00136.x.
Gomi, K., Jasmonic acid pathway in plants 2.0. international journal of molecular sciences. Int. J. Mol. Sci., 22, 2021, 3506, 10.3390/IJMS22073506.
Hattori, A., Migitaka, H., Iigo, M., Itoh, M., Yamamoto, K., Ohtani-Kaneko, R., Hara, M., Suzuki, T., Reiter, R.J., Identification of melatonin in plants and its effects on plasma melatonin levels and binding to melatonin receptors in vertebrates. Biochem. Mol. Biol. Int. 35 (1995), 627–634.
Hu, Z., Fu, Q., Zheng, J., Zhang, A., Wang, H., Transcriptomic and metabolomic analyses reveal that melatonin promotes melon root development under copper stress by inhibiting jasmonic acid biosynthesis. Hortic. Res., 7, 2020, 79, 10.1038/s41438-020-0293-5.
Khadka, K., Raizada, M.N., Navabi, A., Recent progress in germplasm evaluation and gene mapping to enable breeding of drought-tolerant wheat. Front. Plant Sci., 11, 2020, 1149, 10.3389/fpls.2020.01149.
Kim, D., Langmead, B., Salzberg, S.L., HISAT: a fast spliced aligner with low memory requirements. Nat. Methods 12 (2015), 357–360, 10.1038/NMETH.3317.
Lee, H.Y., Back, K., 2-hydroxymelatonin, rather than melatonin, is responsible for RBOH-dependent reactive oxygen species production leading to premature senescence in plants. Antioxidants, 10, 2021, 1728, 10.3390/ANTIOX10111728.
Lee, H.Y., Back, K., Melatonin regulates chloroplast protein quality control via a mitogen-activated protein kinase signaling pathway. Antioxidants, 10, 2021, 511, 10.3390/ANTIOX10040511.
Lee, H.Y., Back, K., Melatonin is required for H2O2- and NO-mediated defense signaling through MAPKKK3 and OXI1 in Arabidopsis thaliana. J. Pineal Res., 62, 2017, e12379, 10.1111/JPI.12379.
Lee, K., Back, K., Melatonin-deficient rice plants show a common semidwarf phenotype either dependent or independent of brassinosteroid biosynthesis. J. Pineal Res., 66, 2019, e12537, 10.1111/JPI.12537.
Lerner, A.B., Case, J.D., Takahashi, Y., Lee, T.H., Mori, W., Isolation of melatonin, the pineal gland factor that lightens melanocytes. J. Am. Chem. Soc., 80, 1958, 2587, 10.1021/ja01543a060.
Li, D., Batchelor, W.D., Zhang, D., Miao, H., Li, H., Song, S., Li, R., Analysis of melatonin regulation of germination and antioxidant metabolism in different wheat cultivars under polyethylene glycol stress. PLoS One, 15, 2020, e0237536, 10.1371/journal.pone.0237536.
Li, X., Tan, D.X., Jiang, D., Liu, F., Melatonin enhances cold tolerance in drought-primed wild-type and abscisic acid-deficient mutant barley. J. Pineal Res. 62 (2016), 328–339, 10.1111/jpi.12350.
Liu, C., Chen, L., Zhao, R., Li, R., Zhang, S., Yu, W., Sheng, J., Shen, L., Melatonin induces disease resistance to botrytis cinerea in tomato fruit by activating jasmonic acid signaling pathway. J. Agric. Food Chem. 67 (2019), 6116–6124, 10.1021/ACS.JAFC.9B00058.
Liu, G., Hu, Q., Zhang, X., Jiang, J., Zhang, Y., Zhang, Z., Melatonin biosynthesis and signal transduction in plants in response to environmental conditions. J. Exp. Bot. 73 (2022), 5818–5827, 10.1093/JXB/ERAC196.
Murch, S.J., Erland, L.A.E., A systematic review of melatonin in plants: an example of evolution of literature. Front. Plant Sci., 12, 2021, 683047, 10.3389/FPLS.2021.683047/FULL.
Qiu, Y., An, K., Sun, J., Chen, X., Gong, X., Ma, L., Wu, S., Jiang, S., Zhang, Z., Wang, Y., Investigating the effect of methyl jasmonate and melatonin on resistance of Malus crabapple ‘Hong Jiu’ to ozone stress. Environ. Sci. Pollut. Res. Int. 26 (2019), 27761–27768, 10.1007/s11356-019-05946-w.
Sanchez-Barcelo, E.J., Mediavilla, M.D., Vriend, J., Reiter, R.J., Constitutive photomorphogenesis protein 1 (COP1) and COP9 signalosome, evolutionarily conserved photomorphogenic proteins as possible targets of melatonin. J. Pineal Res. 1 (2016), 41–51, 10.1111/jpi.12340.
Shi, H., Tan, D.X., Reiter, R.J., Ye, T., Yang, F., Chan, Z., Melatonin induces class A1 heat-shock factors (HSFA1s) and their possible involvement of thermotolerance in Arabidopsis. J. Pineal Res. 58 (2015), 335–342, 10.1111/JPI.12219.
Su, X., Fan, X., Shao, R., Guo, J., Wang, Y., Yang, J., Yang, Q., Guo, L., Physiological and iTRAQ-based proteomic analyses reveal that melatonin alleviates oxidative damage in maize leaves exposed to drought stress. Plant Physiol. Biochem. 142 (2019), 263–274, 10.1016/J.PLAPHY.2019.07.012.
Sun, C., Liu, L., Wang, L., Li, B., Jin, C., Lin, X., Melatonin: a master regulator of plant development and stress responses. J. Integr. Plant Biol. 63 (2021), 126–145, 10.1111/JIPB.12993.
Sun, Q., Zhang, N., Wang, J., Cao, Y., Li, X., Zhang, H., Zhang, L., Tan, D.X., Guo, Y.D., 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., 2016, 138–153, 10.1111/jpi.12315.
Tan, D.X., Manchester, L.C., Esteban-Zubero, E., Zhou, Z., Reiter, R.J., Melatonin as a potent and inducible endogenous antioxidant: synthesis and metabolism. Molecules 20 (2015), 18886–18906, 10.3390/molecules201018886.
Wang, Y., Zhang, X., Huang, G., Feng, F., Liu, X., Guo, R., Gu, F., Zhong, X., Mei, X., iTRAQ-based quantitative analysis of responsive proteins under PEG-induced drought stress in wheat leaves. Int. J. Mol. Sci., 20, 2019, 2621, 10.3390/IJMS20112621.
Wei, Y., Bai, Y., Cheng, X., Zhu, B., Reiter, R.J., Shi, H., The dual roles of melatonin biosynthesis enzymes in the coordination of melatonin biosynthesis and autophagy in cassava. J. Pineal Res. 69 (2020), 1–13, 10.1111/jpi.12652.
Wei, Y., Chang, Y., Zeng, H., Liu, G., He, C., Shi, H., RAV transcription factors are essential for disease resistance against cassava bacterial blight via activation of melatonin biosynthesis genes. J. Pineal Res. 64 (2018), 1–10, 10.1111/jpi.12454.
Wei, Y., Liu, G., Chang, Y., Lin, D., Reiter, R.J., He, C., Shi, H., Melatonin biosynthesis enzymes recruit WRKY transcription factors to regulate melatonin accumulation and transcriptional activity on W-box in cassava. J. Pineal Res. 65 (2018), 1–13, 10.1111/jpi.12487.
Xia, H., Ni, Z., Hu, R., Lin, L., Deng, H., Wang, J., Tang, Y., Sun, G., Wang, X., Li, H., Liao, M., Lv, X., Liang, D., Melatonin alleviates drought stress by a non‐ enzymatic and enzymatic antioxidative system in kiwifruit seedlings. Int. J. Mol. Sci., 21, 2020, 852, 10.3390/ijms21030852.
Xu, H., Wang, C., Shao, G., Wu, Shasha, Liu, P., Cao, P., Jiang, P., Wang, S., Zhu, H., Lin, X., Tauqeer, A., Lin, Y., Chen, W., Huang, W., Wen, Q., Chang, J., Zhong, F., Wu, Shuang, The reference genome and full-length transcriptome of pakchoi provide insights into cuticle formation and heat adaption. Hortic. Res., 9, 2022, 10.1093/HR/UHAC123 uhac123.
Yin, X., Bai, Y.-L., Gong, C., Song, W., Wu, Y., Ye, T., Feng, Y.-Q., The phytomelatonin receptor PMTR1 regulates seed development and germination by modulating abscisic acid homeostasis in Arabidopsis thaliana. J. Pineal Res., 72, 2022, e12797, 10.1111/JPI.12797.
Yu, R., Zuo, T., Diao, P., Fu, J., Fan, Y., Wang, Y., Zhao, Q., Ma, X., Lu, W., Li, A., Wang, R., Yan, F., Pu, L., Niu, Y., Wuriyanghan, H., Melatonin enhances seed germination and seedling growth of medicago sativa under salinity via a putative melatonin receptor MsPMTR1. Front. Plant Sci., 12, 2021, 1719, 10.3389/FPLS.2021.702875/BIBTEX.
Yu, Y., Lv, Y., Shi, Y., Li, T., Chen, Y., Zhao, D., Zhao, Z., The role of phyto-melatonin and related metabolites in response to stress. Molecules 23 (2018), 1–15, 10.3390/molecules23081887.
Zhang, L., Jiang, | Xiaochun, Liu, Q., Golam Ahammed, J., Lin, R., Wang, L., Shao, S., Yu, J., Zhou, Y., The HY5 and MYB15 transcription factors positively regulate cold tolerance in tomato via the CBF pathway. Plant Cell Environ., 43, 2020, 10.1111/pce.13868 2127–2126.
Zhang, S., Tang, S., Tang, C., Luo, M., Jia, G., Zhi, H., Diao, X., SiSTL2 is required for cell cycle, leaf organ development, chloroplast biogenesis, and has effects on C4 photosynthesis in Setaria italica (L.) P. Beauv. Front. Plant Sci., 9, 2018, 1103, 10.3389/fpls.2018.01103.
