Melatonin Deficiency Confers Tolerance to Multiple Abiotic Stresses in Rice via Decreased Brassinosteroid Levels
Abstract
:1. Introduction
2. Results
2.1. Phenotypes of snat2 and SNAT2 OE Rice Seedlings
2.2. Grain Phenotypes and Yield Performance
2.3. Altered GA Sensitivity in snat2 Rice
2.4. Enhanced Tolerance to Cadmium Stress in Melatonin-Deficient snat2 Rice
2.5. Melatonin-Deficient snat2 Rice Plants Exhibit Resistance to Salt, Cold, and Heat Stress
2.6. Enhanced Tolerance to Salt and Heat Stress in Other Types of Melatonin-Deficient Rice
3. Discussion
4. Materials and Methods
4.1. Plant Materials
4.2. Plant Growth Conditions
4.3. Semi-Quantitative Reverse Transcription–Polymerase Chain Reaction (RT-PCR) Analysis
4.4. Hormone Treatment
4.5. Melatonin Quantification
4.6. Germination Assay
4.7. Salt, Cold, Heat, and Cadmium Stress Tolerance Assays
4.8. Determination of Chlorophyll and Malondialdehyde (MDA) Contents
4.9. Quantification of Bioactive BRs and GA
4.10. Statistical Analysis
Author Contributions
Funding
Conflicts of Interest
References
- 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. 1995, 18, 28–31. [Google Scholar] [CrossRef] [PubMed]
- 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. 1995, 35, 627–634. [Google Scholar] [PubMed]
- Debnath, B.; Islam, W.; Li, M.; Sun, Y.; Lu, X.; Mitra, S.; Hussain, M.; Liu, S.; Qiu, D. Melatonin mediates enhancement of stress tolerance in plants. Int. J Mol. Sci. 2019, 20, 1040. [Google Scholar] [CrossRef] [PubMed]
- Wang, Y.; Reiter, R.J.; Chan, Z. Phytomelatonin: A universal abiotic stress regulator. J. Exp. Bot. 2018, 69, 963–974. [Google Scholar] [CrossRef] [PubMed]
- Reiter, R.J.; Tan, D.X.; Sharma, R. Historical perspective and evaluation of the mechanisms by which melatonin mediates seasonal reproduction in mammals. Melatonin Res. 2018, 1, 59–77. [Google Scholar] [CrossRef]
- Tan, D.X.; Reiter, R.J. Mitochondria: The birth place, battle ground and the site of melatonin metabolism in cells. Melatonin Res. 2019, 2, 44–66. [Google Scholar] [CrossRef]
- Manchester, L.C.; Tan, D.X.; Reiter, R.J.; Park, W.; Monis, K.; Qi, W. High levels of melatonin in the seeds of edible plants: Possible function in germ cell protection. Life Sci. 2000, 67, 3023–3029. [Google Scholar] [CrossRef]
- Kolář, J.; Johnson, C.H.; Macháčková, I. Exogenously applied melatonin (N-acetyl-5-methoxytryptamine) affects flowering of the short-day plant Chenopodium rubrum. Physiol. Plant. 2003, 118, 605–612. [Google Scholar] [CrossRef]
- Lei, X.Y.; Zhu, R.Y.; Zhang, G.Y.; Dai, Y.R. Attenuation of cold-induced apoptosis by exogenous melatonin in carrot suspension cells: The possible involvement of polyamines. J. Pineal Res. 2004, 36, 126–131. [Google Scholar] [CrossRef]
- Posmyk, M.M.; Balabusta, M.; Wieczorek, M.; Sliwinska, E.; Janas, K.M. Melatonin applied to cucumber (Cucumis sativus L.) seeds improves germination during chilling stress. J. Pineal Res. 2009, 46, 214–223. [Google Scholar] [CrossRef]
- Hernández-Ruiz, J.; Cano, A.; Arnao, M.B. Melatonin: A growth-stimulating compound present in lupin tissues. Planta 2004, 220, 140–144. [Google Scholar] [CrossRef]
- Hernández-Ruiz, J.; Cano, A.; Arnao, M.B. Melatonin acts as a growth-stimulating compound in some monocot species. J. Pineal Res. 2005, 39, 137–142. [Google Scholar] [CrossRef] [PubMed]
- Li, J.; Liu, J.; Zhu, T.; Zhao, C.; Li, L.; Chen, M. The role of melatonin in salt stress responses. Int. J. Mol. Sci. 2019, 20, 1735. [Google Scholar] [CrossRef] [PubMed]
- Okazaki, M.; Higuchi, K.; Hahawa, Y.; Shiraiwa, Y.; Ezura, H. Cloning and characterization of a Chlamydomonas reinhardtii cDNA arylalkylamine N-acetyltransferase and its use in the genetic engineering of melatonin content in the Micro-Tom tomato. J. Pineal Res. 2009, 46, 373–382. [Google Scholar] [CrossRef] [PubMed]
- Wang, Y.; Ji, J.; Bu, H.; Zhao, Y.; Xu, Y.; Johnson, C.H.; Kolár, J. Genetic transformation of Nicotiana tabacum L. by Agrobacterium tumefaciens carrying genes in the melatonin biosynthesis pathway and the enhancement of antioxidative capability in transgenic plants. Chin. J. Biotechnol. 2009, 25, 1014–1021. [Google Scholar]
- Back, K.; Tan, D.X.; Reiter, R.J. Melatonin biosynthesis in plants: Multiple pathways catalyze tryptophan to melatonin in the cytoplasm or chloroplasts. J. Pineal Res. 2016, 61, 426–437. [Google Scholar] [CrossRef] [PubMed]
- Kang, K.; Kong, K.; Park, S.; Natsagdorj, U.; Kim, Y.S.; Back, K. Molecular cloning of a plant N-acetylserotonin methyltransferase and its expression characteristics in rice. J. Pineal Res. 2011, 50, 304–309. [Google Scholar] [CrossRef]
- Kang, K.; Lee, K.; Park, S.; Byeon, Y.; Back, K. Molecular cloning of rice serotonin N-acetyltransferase, the penultimate gene in plant melatonin biosynthesis. J. Pineal Res. 2013, 55, 7–13. [Google Scholar] [CrossRef]
- Byeon, Y.; Lee, H.Y.; Back, K. Cloning and characterization of the serotonin N-acetyltransferase-2 gene (SNAT2) in rice (Oryza sativa). J. Pineal Res. 2016, 61, 198–207. [Google Scholar] [CrossRef]
- Byeon, Y.; Lee, K.; Park, Y.I.; Park, S.; Back, K. Molecular cloning and functional analysis of serotonin N-acetyltransferase from the cyanobacterium Synechocystis sp. PCC 6803. J. Pineal Res. 2013, 55, 371–376. [Google Scholar]
- Hwang, O.J.; Back, K. Melatonin is involved in skotomorphogenesis by regulating brassinosteroid biosynthesis in plants. J. Pineal Res. 2018, 65, e12495. [Google Scholar] [CrossRef] [PubMed]
- Byeon, Y.; Back, K. 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. 2016, 60, 348–359. [Google Scholar] [PubMed]
- Lee, K.; Back, K. Melatonin-deficient rice plants show a common semidwarf phenotype either dependent or independent of brassinosteroid biosynthesis. J. Pineal Res. 2019, 66, e12537. [Google Scholar] [CrossRef] [PubMed]
- Zhao, D.; Yu, Y.; Shen, Y.; Liu, Q.; Zhao, Z.; Sharma, R.; Reiter, R.J. Melatonin synthesis and function: Evolutionary history in animals and plants. Front. Endocrinol. 2019, 10, 249. [Google Scholar] [CrossRef] [PubMed]
- Sharif, R.; Xie, C.; Zhang, H.; Arnao, M.B.; Ali, M.; Ali, Q.; Muhammad, I.; Shalmani, A.; Nawaz, M.A.; Chen, P.; et al. Melatonin and its effects on plant systems. Molecules 2018, 23, 2352. [Google Scholar] [CrossRef]
- Jaillais, Y.; Vert, G. Brassinosteroids, gibberellins and light-mediated signaling are the three-way controls of plant sprouting. Nat. Cell Biol. 2012, 14, 788–790. [Google Scholar] [CrossRef]
- Saini, S.; Sharma, I.; Pati, P.K. Versatile roles of brassinosteroid in plants in the context of its homoeostasis, signaling and crosstalks. Front. Plant Sci. 2015, 6, 950. [Google Scholar] [CrossRef] [Green Version]
- Vardhini, B.V.; Anuradha, S.; Sujatha, E.; Rao, S.S.R. Role of brassinosteroids in alleviating various abiotic and biotic stresses—a review. Plant Stress 2010, 4, 55–61. [Google Scholar]
- Kim, S.Y.; Kim, B.H.; Lim, C.J.; Lim, C.O.; Nam, K.H. Constitutive activation of stress-inducible genes in a brassinosteroid-insensitive 1 (bri1) mutant results in higher tolerance to cold. Physiol. Plant. 2010, 138, 191–204. [Google Scholar] [CrossRef]
- Chung, Y.; Kwon, S.I.; Choe, S. Antagonistic regulation of Arabidopsis growth by brassinosteroids and abiotic stresses. Mol. Cells 2014, 37, 795–803. [Google Scholar] [CrossRef]
- Northey, J.G.B.; Liang, S.; Jamshed, M.; Deb, S.; Foo, E.; Reid, J.B.; McCourt, P.; Samuel, M.A. Farnesylation mediates brassinosteroid biosynthesis to regulate abscisic acid responses. Nat. Plants 2016, 2, 16114. [Google Scholar] [CrossRef] [PubMed]
- Lee, K.; Back, K. Overexpression of rice serotonin N-acetyltransferase 1 in transgenic rice plants confers resistance to cadmium and senescence and increases grain yield. J. Pineal Res. 2017, 62, e12392. [Google Scholar] [CrossRef] [PubMed]
- Je, B.I.; Piao, H.L.; Park, S.J.; Park, S.H.; Kim, C.M.; Xuan, Y.H.; Park, S.H.; Huang, J.; Choi, Y.D.; An, G.; et al. RAV-like1 maintains brassinosteroid homeostasis via the coordinated activation of BRI1 and biosynthetic genes in rice. Plant Cell 2010, 22, 1777–1791. [Google Scholar] [CrossRef] [PubMed]
- Hong, Z.; Ueguchi-Tanaka, M.; Umemura, K.; Uozu, S.; Fujioka, S.; Takatsuto, S.; Yoshida, S.; Ashikari, M.; Kitano, H.; Matsuoka, M. A rice brassinosteroid-deficient mutant, ebisu dwarf (d2), is caused by a loss of function of a new member of cytochrome P450. Plant Cell 2003, 15, 2900–2910. [Google Scholar] [CrossRef] [PubMed]
- Tanabe, S.; Ashikari, M.; Fujioka, S.; Takatsuto, S.; Yoshida, S.; Yano, M.; Yoshimura, A.; Kitano, H.; Matsuoka, M.; Fujisawa, Y.; et al. A novel cytochrome P450 is implicated in brassinosteroid biosynthesis via the characterization of a rice dwarf mutant, dwarf11, with reduced seed length. Plant Cell 2005, 17, 776–790. [Google Scholar] [CrossRef]
- Morinaka, Y.; Sakamoto, T.; Inukai, Y.; Agetsuma, M.; Kitano, H.; Ashikari, M.; Matsuoka, M. Morphological alteration caused by brassinosteroid insensitivity increases the biomass and grain production in rice. Plant Physiol. 2006, 141, 924–931. [Google Scholar] [CrossRef]
- Sakamoto, T.; Morinaka, Y.; Ohnishi, T.; Sunohara, H.; Fujioka, S.; Ueguchi-Tanaka, M.; Mizutani, M.; Sakata, K.; Takatsuto, S.; Yoshida, S.; et al. Erect leaves caused by brassinosteroid deficiency increase biomass production and grain yield in rice. Nat. Biotechnol. 2005, 24, 105–109. [Google Scholar] [CrossRef]
- Tong, H.; Xiao, Y.; Liu, D.; Gao, S.; Liu, L.; Yin, Y.; Jin, Y.; Qian, Q.; Chu, C. Brassinosteroid regulates cell elongation by modulating gibberellin metabolism in rice. Plant Cell 2014, 26, 4376–4393. [Google Scholar] [CrossRef]
- Hirano, K.; Yoshida, H.; Aya, K.; Kawamura, M.; Hayashi, M.; Hobo, T.; Sato-Izawa, K.; Kitano, H.; Ueguchi-Tanaka, M.; Matsuoka, M. SMALL ORGAN SIZE 1 and SMALL ORGAN SIZE 2/DWARF and LOW-TILLERING Form a complex to integrate auxin and brassinosteroid signaling in rice. Mol. Plant 2017, 10, 590–604. [Google Scholar] [CrossRef]
- Jung, H.; Lee, D.-K.; Choi, Y.D.; Kim, J.-K. OsIAA6, a member of the rice Aux/IAA gene family, is involved in drought tolerance and tiller outgrowth. Plant Sci. 2015, 236, 304–312. [Google Scholar]
- Gruszka, D.; Janeczko, A.; Dziurka, M.; Pociecha, E.; Okestkova, J.; Szarejko, I. Barley brassinosteroid mutants provide an insight into phytohormonal homeostasis in plant reaction to drought stress. Front. Plant Sci. 2016, 7, 1824. [Google Scholar] [CrossRef] [PubMed]
- Colebrook, E.H.; Thomas, S.G.; Phillips, A.L.; Hedden, P. The role of gibberellin signaling in plant responds to abiotic stress. J. Exp. Biol. 2014, 217, 67–75. [Google Scholar] [CrossRef] [PubMed]
- Reina, M.; Castañeda-Arriaga, R.; Perez-Gonzalez, A.; Guzman-Lopez, E.G.; Tan, D.X.; Reiter, R.J.; Galano, A. A computer-assisted systematic search for melatonin derivatives with high potential as antioxidants. Melatonin Res. 2018, 1, 27–58. [Google Scholar] [CrossRef]
- Li, C.; Wang, P.; Wei, Z.; Liang, D.; Liu, C.; Yin, L.; Jia, D.; Fu, M.; Ma, F. The mitigation effects of exogenous melatonin on salinity-induced stress in Malus hupehensis. J. Pineal Res. 2012, 53, 298–306. [Google Scholar] [CrossRef] [PubMed]
- Turk, H.; Erdal, S.; Genisel, M.; Atici, O.; Demir, Y.; Yanmis, D. The regulatory effect of melatonin on physiological, biochemical and molecular parameters in cold-stressed wheat seedlings. Plant Growth Regul. 2014, 74, 139–152. [Google Scholar] [CrossRef]
- Ullah, M.A.; Tungmunnithum, D.; Garros, L.; Drouet, S.; Hano, C.; Abbasi, B.H. Effect of ultraviolet-C radiation and melatonin stress on biosynthesis of antioxidant and antidiabetic metabolites produced in in vitro callus cultures of Lepidium sativum L. Int. J. Mol. Sci. 2019, 20, 1787. [Google Scholar] [CrossRef]
- Wang, P.; Sun, X.; Wang, N.; Tan, D.X.; Ma, F. Melatonin enhances the occurrence of autophagy induced by oxidative stress in Arabidopsis seedlings. J. Pineal Res. 2015, 58, 479–489. [Google Scholar] [CrossRef]
- Qi, Z.Y.; Wang, K.X.; Yan, M.Y.; Kanwar, M.K.; Li, D.Y.; Wijaya, L.; Alyemeni, M.N.; Ahmad, P.; Zhou, J. Melatonin alleviates high temperature-induced pollen abortion in Solanum lycopersicum. Molecules 2018, 23, 386. [Google Scholar] [CrossRef]
- Lee, H.Y.; Back, K. Melatonin plays a pivotal role in conferring tolerance against endoplasmic reticulum stress via mitogen-activated protein kinases and bZIP60 in Arabidopsis thaliana. Melatonin Res. 2018, 1, 93–107. [Google Scholar] [CrossRef]
- Kang, K.; Lee, K.; Park, S.; Kim, Y.S.; Back, K. Enhanced production of melatonin by ectopic overexpression of human serotonin N-acetyltransferase plays a role in cold resistance in transgenic rice seedlings. J. Pineal Res. 2010, 49, 176–182. [Google Scholar] [CrossRef]
- Zhang, L.J.; Jia, J.F.; Xu, Y.; Wang, Y.; Hao, J.G.; Li, T.K. Production of transgenic Nicotiana sylvestris plants expressing melatonin synthetase genes and their effect on UV-induced DNA damage. In Vitro Cell Dev. Biol. Plant 2012, 48, 275–283. [Google Scholar] [CrossRef]
- Park, S.; Lee, D.E.; Jang, H.; Byeon, Y.; Kim, Y.S.; Back, K. Melatonin-rich transgenic rice plants exhibit resistance to herbicide-induced oxidative stress. J. Pineal Res. 2013, 54, 258–263. [Google Scholar] [CrossRef] [PubMed]
- Wang, L.; Zhao, Y.; Reiter, R.J.; He, C.; Liu, G.; Lei, Q.; Zuo, B.; Zheng, X.D.; Li, Q.; Kong, J. Change in melatonin levels in transgenic ‘Micro-Tom’ tomato over-expressing ovine AANAT and ovine HIOMT genes. J. Pineal Res. 2014, 56, 134–142. [Google Scholar] [CrossRef] [PubMed]
- Zuo, B.; Zheng, X.; He, P.; Wang, L.; Lei, Q.; Feng, C.; Zhou, J.; Li, Q.; Han, Z.; Kong, J. Overexpression of MzASMT improves melatonin production and enhances drought tolerance in transgenic Arabidopsis thaliana plants. J. Pineal Res. 2014, 57, 408–417. [Google Scholar] [CrossRef] [PubMed]
- Yang, W.-J.; Du, Y.-T.; Zhou, Y.-B.; Chen, J.; Xu, Z.-S.; Ma, Y.-Z.; Chen, M.; Min, D.-H. Overexpression of TaCOMT improves melatonin production and enhances drought tolerance in transgenic Arabidopsis. Int. J. Mol. Sci. 2019, 20, 652. [Google Scholar] [CrossRef] [PubMed]
- Xu, W.; Cai, S.Y.; Zhang, Y.; Wang, Y.; Ahammed, G.J.; Xia, X.J.; Shi, K.; Zhou, Y.H.; Yu, J.Q.; Reiter, R.J.; et al. Melatonin enhances thermotolerance by promoting cellular protein protection in tomato plants. J. Pineal Res. 2016, 61, 457–469. [Google Scholar] [CrossRef]
- Zheng, X.; Tan, D.X.; Allan, A.C.; Zuo, B.; Zhao, Y.; Reiter, R.J.; Wang, L.; Wang, Z.; Guo, Y.; Zhou, J.; et al. Chloroplastic biosynthesis of melatonin and its involvement in protection of plants from salt stress. Sci. Rep. 2017, 7, 41236. [Google Scholar] [CrossRef]
- Li, M.Q.; Hasan, M.K.; Li, C.X.; Ahammed, G.J.; Xia, X.J.; Shi, K.; Zhou, Y.H.; Reiter, R.J.; Yu, J.Q.; Xu, M.X.; et al. Melatonin mediates selenium-induced tolerance to cadmium stress in tomato plants. J. Pineal Res. 2016, 61, 291–302. [Google Scholar] [CrossRef]
- Gu, Q.; Chen, Z.; Yu, X.; Cui, W.; Pan, J.; Zhao, G.; Xu, S.; Wang, R.; Shen, W. Melatonin confers plant tolerance against cadmium stress via the decrease of cadmium accumulation and reestablishment of microRNA-mediated redox homeostasis. Plant Sci. 2017, 261, 28–37. [Google Scholar] [CrossRef]
- Cai, S.Y.; Zhang, Y.; Xu, Y.P.; Qi, Z.Y.; Li, M.Q.; Ahammed, G.J.; Xia, X.J.; Shi, K.; Zhou, Y.H.; Reiter, R.J.; et al. HsfA1a upregulates melatonin biosynthesis to confer cadmium tolerance in tomato plants. J. Pineal Res. 2017, 62, e12387. [Google Scholar] [CrossRef]
- Choi, G.-H.; Lee, H.Y.; Back, K. 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. 2017, 63, e12412. [Google Scholar] [CrossRef] [PubMed]
- Lee, H.Y.; Back, K. Melatonin induction and its role in high light stress tolerance in Arabidopsis thaliana. J. Pineal Res. 2018, 65, e12504. [Google Scholar] [CrossRef] [PubMed]
- Chen, Z.; Xie, Y.; Gu, Q.; Zhao, G.; Zhang, Y.; Cui, W.; Xu, S.; Wang, R.; Shen, W. The AtrbohF-dependent regulation of ROS signaling is required for melatonin-induced salinity tolerance in Arabidopsis. Free Radic. Biol. Med. 2017, 108, 465–477. [Google Scholar] [CrossRef] [PubMed]
- 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. 2017, 62, e12379. [Google Scholar] [CrossRef]
- Sharma, I.; Kaur, N.; Pati, P.K. Brassinosteroids: A promising option in deciphering remedial strategies for abiotic stress tolerance in rice. Front. Plant Sci. 2017, 8, 2151. [Google Scholar] [CrossRef]
- Nakashita, H.; Yasuda, M.; Nitta, T.; Asami, T.; Fujioka, S.; Aria, Y.; Sekimata, K.; Takatsuto, S.; Yamaguchi, I.; Yoshida, S. Brassinosteroid functions in a broad range of disease resistance in tobacco and rice. Plant J. 2003, 33, 887–898. [Google Scholar] [CrossRef] [Green Version]
- Tian, H.; Lv, B.; Ding, T.; Bai, M.; Ding, Z. Auxin-BR interaction regulates plant growth and development. Front. Plant Sci. 2018, 8, 2256. [Google Scholar] [CrossRef]
- Wei, J.; Li, D.X.; Zhang, J.R.; Shan, C.; Rengel, Z.; Song, Z.B.; Chen, Q. Phytomelatonin receptor PMTR1-mediated signaling regulates stomatal closure in Arabidopsis thaliana. J. Pineal Res. 2018, 65, e12500. [Google Scholar] [CrossRef]
- Choi, G.-H.; Back, K. Suppression of melatonin 2-hydroxylase increases melatonin production leading to the enhanced abiotic stress tolerance against cadmium, senescence, salt, and tunicamycin in rice plants. Biomolecules 2019, 9, 589. [Google Scholar] [CrossRef]
- Lee, K.; Choi, G.H.; Back, K. Cadmium-induced melatonin synthesis in rice requires light, hydrogen peroxide, and nitric oxide: Key regulatory roles for tryptophan decarboxylase and caffeic acid O-methyltransferase. J. Pineal Res. 2017, 63, e12441. [Google Scholar] [CrossRef]
- Wang, S.; Liu, J.; Zhao, T.; Du, C.; Nie, S.; Zhang, Y.; Lv, S.; Huang, S.; Wang, X. Modification of threonine-1050 of SIBRI1 regulates BT signaling and increases fruit yield of tomato. BMC Plant Biol. 2019, 19, 256. [Google Scholar] [CrossRef] [PubMed]
© 2019 by the authors. Licensee MDPI, Basel, Switzerland. This article is an open access article distributed under the terms and conditions of the Creative Commons Attribution (CC BY) license (http://creativecommons.org/licenses/by/4.0/).
Share and Cite
Hwang, O.J.; Back, K. Melatonin Deficiency Confers Tolerance to Multiple Abiotic Stresses in Rice via Decreased Brassinosteroid Levels. Int. J. Mol. Sci. 2019, 20, 5173. https://0-doi-org.brum.beds.ac.uk/10.3390/ijms20205173
Hwang OJ, Back K. Melatonin Deficiency Confers Tolerance to Multiple Abiotic Stresses in Rice via Decreased Brassinosteroid Levels. International Journal of Molecular Sciences. 2019; 20(20):5173. https://0-doi-org.brum.beds.ac.uk/10.3390/ijms20205173
Chicago/Turabian StyleHwang, Ok Jin, and Kyoungwhan Back. 2019. "Melatonin Deficiency Confers Tolerance to Multiple Abiotic Stresses in Rice via Decreased Brassinosteroid Levels" International Journal of Molecular Sciences 20, no. 20: 5173. https://0-doi-org.brum.beds.ac.uk/10.3390/ijms20205173