Functional Plant Biology Functional Plant Biology Society
Plant function and evolutionary biology
RESEARCH ARTICLE

Melatonin alleviates aluminium toxicity through modulating antioxidative enzymes and enhancing organic acid anion exudation in soybean

Jiarong Zhang A , Bingjie Zeng A , Yawen Mao A , Xiangying Kong A C , Xinxun Wang E , Ye Yang A , Jie Zhang D , Jin Xu B , Zed Rengel E and Qi Chen A F
+ Author Affiliations
- Author Affiliations

A Faculty of Life Science and Technology, Kunming University of Science and Technology, Jingming South Road, Kunming, 650500, China.

B Xishuangbanna Tropical Botanical Garden, Chinese Academy of Sciences, Menglun, Mengla, Yunnan, 666303, China.

C Faculty of Architecture and City Planning, Kunming University of Science and Technology, Jingming South Road, Kunming, 650500, China.

D Biotechnology and Germplasm Resource Institute, Yunnan Academy of Agricultural Sciences, Yunnan Province Key Laboratory of Agricultural Biotechnology, Kunming 650223, China.

E UWA School of Agriculture and Environment, Faculty of Science, The University of Western Australia, 35 Stirling Highway, Perth WA 6009, Australia.

F Corresponding author. Email: chenq0321@163.com

Functional Plant Biology 44(10) 961-968 https://doi.org/10.1071/FP17003
Submitted: 3 January 2017  Accepted: 27 May 2017   Published: 23 June 2017

Abstract

Aluminium (Al) toxicity is a major chemical constraint limiting plant growth and production on acidic soils. Melatonin (N-acetyl-5-methoxytryptamine) is a ubiquitous molecule that plays crucial roles in plant growth and stress tolerance. However, there is no knowledge regarding whether melatonin is involved in plant responses to Al stress. Here, we show that optimal concentrations of melatonin could effectively ameliorate Al-induced phytotoxicity in soybean (Glycine max L.). The concentration of melatonin in roots was significantly increased by the 50 μM Al treatment. Such an increase in endogenous melatonin coincided with the upregulation of the gene encoding acetyltransferase NSI-like (nuclear shuttle protein-interacting) in soybean roots. Supplementation with low concentrations of melatonin (0.1 and 1 μM) conferred Al resistance as evident in partial alleviation of root growth inhibition and decreased H2O2 production: in contrast, high concentrations of melatonin (100 and 200 μM) had an opposite effect and even decreased root growth in Al-exposed seedlings. Mitigation of Al stress by the 1 μM melatonin root treatment was associated with enhanced activities of the antioxidant enzymes and increased exudation of malate and citrate. In conclusion, melatonin might play a critical role in soybean resistance to Al toxicity.

Additional keywords: Al toxicity, citrate, Glycine max, H2O2, malate, melatonin synthesis.


References

Aebi H (1984) Catalase in vitro. Methods in Enzymology 105, 121–126.
Catalase in vitro.CrossRef | 1:CAS:528:DyaL2cXltVKis7s%3D&md5=a0bf6214b75895f2b7bd71bb3e0c4088CAS |

Arnao MB, Hernandez-Ruiz J (2009) Chemical stress by different agents affects the melatonin content of barley roots. Journal of Pineal Research 46, 295–299.
Chemical stress by different agents affects the melatonin content of barley roots.CrossRef | 1:CAS:528:DC%2BD1MXktVWiurk%3D&md5=3f8e0e082c70d6c23afb035c192bc010CAS |

Arnao MB, Hernandez-Ruiz J (2015) Functions of melatonin in plants: a review. Journal of Pineal Research 59, 133–150.
Functions of melatonin in plants: a review.CrossRef | 1:CAS:528:DC%2BC2MXhtVGmtbjE&md5=03ff30e984761e3c182473a7b5bb72eeCAS |

Arora D, Bhatla SC (2017) Melatonin and nitric oxide regulate sunflower seedling growth under salt stress accompanying differential expression of Cu/Zn SOD and Mn SOD. Free Radical Biology & Medicine 106, 315–328.
Melatonin and nitric oxide regulate sunflower seedling growth under salt stress accompanying differential expression of Cu/Zn SOD and Mn SOD.CrossRef | 1:CAS:528:DC%2BC2sXjs1yisLY%3D&md5=45db4c77fcb67a9347a8c8f40c6b4480CAS |

Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Analytical Biochemistry 72, 248–254.
A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding.CrossRef | 1:CAS:528:DyaE28XksVehtrY%3D&md5=2821bcfbf01a16b0f1b14eb3a73c5812CAS |

Byeon Y, Lee HJ, Lee HY, Back K (2016) Cloning and functional characterization of the Arabidopsis N-acetylserotonin O-methyltransferase responsible for melatonin synthesis. Journal of Pineal Research 60, 65–73.
Cloning and functional characterization of the Arabidopsis N-acetylserotonin O-methyltransferase responsible for melatonin synthesis.CrossRef | 1:CAS:528:DC%2BC2MXhvVChtbzO&md5=e5b6dfca6b379691b0b6b6c6a6278509CAS |

Chen Q, Qi WB, Reiter RJ, Wei W, Wang BM (2009) Exogenously applied melatonin stimulates root growth and raises endogenous indoleacetic acid in roots of etiolated seedlings of Brassica juncea. Journal of Plant Physiology 166, 324–328.
Exogenously applied melatonin stimulates root growth and raises endogenous indoleacetic acid in roots of etiolated seedlings of Brassica juncea.CrossRef | 1:CAS:528:DC%2BD1MXitV2lu7w%3D&md5=3862760d5ee6471aa3dea9f8af76e441CAS |

Chen Q, Zhang X, Wang S, Wang Q, Wang G, Nian H, Li K, Yu Y, Chen L (2011) Transcriptional and physiological changes of alfalfa in response to aluminium stress. Journal of Agricultural Science 149, 737–751.
Transcriptional and physiological changes of alfalfa in response to aluminium stress.CrossRef | 1:CAS:528:DC%2BC3MXhtlKrsbjK&md5=1cf522975b13081f88e1f7d27777d8f9CAS |

Chen Q, Wu K, Zhang Y, Xuan-Huyen P, Li K, Yu Y, Chen L (2012) Physiological and molecular responses of broad bean (Vicia faba L.) to aluminum stress. Acta Physiologiae Plantarum 34, 2251–2263.
Physiological and molecular responses of broad bean (Vicia faba L.) to aluminum stress.CrossRef | 1:CAS:528:DC%2BC3sXpvFaqtLw%3D&md5=48056ede91702dc65c39cf492833aa16CAS |

Chen Q, Kan Q, Wang P, Yu W, Yu Y, Zhao Y, Li K, Chen L (2015) Phosphorylation and interaction with the 14-3-3 protein of the plasma membrane H+-ATPase are involved in the regulation of magnesium-mediated increases in aluminum-induced citrate exudation in broad bean (Vicia faba. L). Plant & Cell Physiology 56, 1144–1153.
Phosphorylation and interaction with the 14-3-3 protein of the plasma membrane H+-ATPase are involved in the regulation of magnesium-mediated increases in aluminum-induced citrate exudation in broad bean (Vicia faba. L).CrossRef | 1:CAS:528:DC%2BC28XhtlWhsLvE&md5=15867e623ee3cb336e7deafcf1661fccCAS |

Darkó É, Ambrusa H, Stefanovits-Bányaib É, Fodorc J, Bakosa F, Barnabása B (2004) Aluminium toxicity, Al tolerance and oxidative stress in an Al-sensitive wheat genotype and in Al-tolerant lines developed by in vitro microspore selection. Plant Science 166, 583–591.
Aluminium toxicity, Al tolerance and oxidative stress in an Al-sensitive wheat genotype and in Al-tolerant lines developed by in vitro microspore selection.CrossRef |

Giannopolitis CN, Ries SK (1977) Superoxide dismutases: I. Occurrence in higher plants. Plant Physiology 59, 309–314.
Superoxide dismutases: I. Occurrence in higher plants.CrossRef | 1:CAS:528:DyaE2sXhtlKgtrs%3D&md5=6fb84ec18e9ef95b5943a146c9cbb149CAS |

Hardeland R (2016) Melatonin in plants-diversity of levels and multiplicity of functions. Frontiers in Plant Science 7, 198
Melatonin in plants-diversity of levels and multiplicity of functions.CrossRef |

Hasan MK, Ahammed GJ, Yin L, Shi K, Xia X, Zhou Y, Yu J, Zhou J (2015) Melatonin mitigates cadmium phytotoxicity through modulation of phytochelatins biosynthesis, vacuolar sequestration, and antioxidant potential in Solanum lycopersicum L. Frontiers in Plant Science 6, 601
Melatonin mitigates cadmium phytotoxicity through modulation of phytochelatins biosynthesis, vacuolar sequestration, and antioxidant potential in Solanum lycopersicum L.CrossRef |

Hernández-Ruiz J, Cano A, Arnao MB (2004) Melatonin: a growth-stimulating compound present in lupin tissues. Planta 220, 140–144.
Melatonin: a growth-stimulating compound present in lupin tissues.CrossRef |

Hernández-Ruiz J, Cano A, Arnao MB (2005) Melatonin acts as a growth-stimulating compound in some monocot species. Journal of Pineal Research 39, 137–142.
Melatonin acts as a growth-stimulating compound in some monocot species.CrossRef |

Kang K, Lee K, Park S, Byeon Y, Back K (2013) Molecular cloning of rice serotonin N-acetyltransferase, the penultimate gene in plant melatonin biosynthesis. Journal of Pineal Research 55, 7–13.
Molecular cloning of rice serotonin N-acetyltransferase, the penultimate gene in plant melatonin biosynthesis.CrossRef | 1:CAS:528:DC%2BC3sXhtFajs7jM&md5=0b45a94b1ef91d0a86b1572aab53eafeCAS |

Kaur H, Bhatla SC (2016) Melatonin and nitric oxide modulate glutathione content and glutathione reductase activity in sunflower seedling cotyledons accompanying salt stress. Nitric Oxide 59, 42–53.
Melatonin and nitric oxide modulate glutathione content and glutathione reductase activity in sunflower seedling cotyledons accompanying salt stress.CrossRef | 1:CAS:528:DC%2BC28Xht1ClurfF&md5=1b7d869566d341e48d7d5682b47fb51eCAS |

Kaur H, Mukherjee S, Baluska F, Bhatla SC (2015) Regulatory roles of serotonin and melatonin in abiotic stress tolerance in plants. Plant Signaling & Behavior 10, e1049788
Regulatory roles of serotonin and melatonin in abiotic stress tolerance in plants.CrossRef |

Kopittke PM (2016) Role of phytohormones in aluminium rhizotoxicity. Plant, Cell & Environment 39, 2319–2328.
Role of phytohormones in aluminium rhizotoxicity.CrossRef | 1:CAS:528:DC%2BC28XhsVCqtrvF&md5=adc8314864f4a51b0f1cd88a825e31deCAS |

Lee HY, Byeon Y, Lee K, Lee HJ, Back K (2014) Cloning of Arabidopsis serotonin N-acetyltransferase and its role with caffeic acid O-methyltransferase in the biosynthesis of melatonin in vitro despite their different subcellular localizations. Journal of Pineal Research 57, 418–426.
Cloning of Arabidopsis serotonin N-acetyltransferase and its role with caffeic acid O-methyltransferase in the biosynthesis of melatonin in vitro despite their different subcellular localizations.CrossRef | 1:CAS:528:DC%2BC2cXhslKgtbnL&md5=6b23d0867f78b839a08063479ba64680CAS |

Li C, Wang P, Wei Z, Liang D, Liu C, Yin L, Jia D, Fu M, Ma F (2012) The mitigation effects of exogenous melatonin on salinity-induced stress in Malus hupehensis. Journal of Pineal Research 53, 298–306.
The mitigation effects of exogenous melatonin on salinity-induced stress in Malus hupehensis.CrossRef | 1:CAS:528:DC%2BC38XhtlOjsLrN&md5=63f6a2c87708edcaf4912f94622f9c45CAS |

Liang C, Pineros MA, Tian J, Yao Z, Sun L, Liu J, Shaff J, Coluccio A, Kochian LV, Liao H (2013) Low pH, aluminum, and phosphorus coordinately regulate malate exudation through GmALMT1 to improve soybean adaptation to acid soils. Plant Physiology 161, 1347–1361.
Low pH, aluminum, and phosphorus coordinately regulate malate exudation through GmALMT1 to improve soybean adaptation to acid soils.CrossRef | 1:CAS:528:DC%2BC3sXmvFKrur0%3D&md5=f36f6b187f8c23b88246ec05f9b8955aCAS |

Ma JF, Zheng SJ, Matsumoto H, Hiradate S (1997) Detoxifying aluminium with buckwheat. Nature 390, 569–570.
Detoxifying aluminium with buckwheat.CrossRef |

Maehly AC, Chance B (1954) The assay of catalases and peroxidases. Methods of Biochemical Analysis 1, 357–424.

Marta B, Szafrańska K, Posmyk MM (2016) Exogenous melatonin improves antioxidant defense in cucumber seeds (Cucumis sativus L.) germinated under chilling stress. Frontiers in Plant Science 7, 575
Exogenous melatonin improves antioxidant defense in cucumber seeds (Cucumis sativus L.) germinated under chilling stress.CrossRef |

Mittler R (2002) Oxidative stress, antioxidants and stress tolerance. Trends in Plant Science 7, 405–410.
Oxidative stress, antioxidants and stress tolerance.CrossRef | 1:CAS:528:DC%2BD38XntVWnu7Y%3D&md5=f57d29645e044474f2197910ad0c0190CAS |

Mukherjee S, David A, Yadav S, Baluška F, Bhatla SC (2014) Salt stress-induced seedling growth inhibition coincides with differential distribution of serotonin and melatonin in sunflower seedling roots and cotyledons. Physiologia Plantarum 152, 714–728.
Salt stress-induced seedling growth inhibition coincides with differential distribution of serotonin and melatonin in sunflower seedling roots and cotyledons.CrossRef | 1:CAS:528:DC%2BC2cXitVamtLzJ&md5=81a26ab01f915b12afe0ccceb8a73c07CAS |

Nawaz MA, Huang Y, Bie Z, Ahmed W, Reiter RJ, Niu M, Hameed S (2015) Melatonin: current status and future perspectives in plant science. Frontiers in Plant Science 6, 1230

Nicoloso FT, Tabaldi LA, Cargnelutti D, Goncalves JF, Pereira LB, Castro GY, Maldaner J, Rauber R, Rossato LV, Bisognin DA, Schetinger MRC (2009) Lipid peroxidation is an early symptom triggered by aluminum, but not the primary cause of elongation inhibition in pea roots. Chemosphere 76, 1402–1409.

Pape C, Lüning K (2006) Quantification of melatonin in phototrophic organisms. Journal of Pineal Research 41, 157–165.
Quantification of melatonin in phototrophic organisms.CrossRef | 1:CAS:528:DC%2BD28Xpt1Sru7o%3D&md5=b14a03453f3ef455127313adb7a6201eCAS |

Posmyk MM, Kuran H, Marciniak K, Janas KM (2008) Pre-sowing seed treatment with melatonin protects red cabbage seedlings against toxic copper ion concentrations. Journal of Pineal Research 45, 24–31.
Pre-sowing seed treatment with melatonin protects red cabbage seedlings against toxic copper ion concentrations.CrossRef | 1:CAS:528:DC%2BD1cXpvVOnsLo%3D&md5=ff371c506f6f84ae0114df26b2f25b77CAS |

Rengel Z (1992) Role of calcium in aluminium toxicity. New Phytologist 121, 499–513.
Role of calcium in aluminium toxicity.CrossRef | 1:CAS:528:DyaK38XmsVKlsLc%3D&md5=8fe293f4516e37d3c02f1c3c0dfb4502CAS |

Rengel Z, Zhang WH (2003) Role of dynamics of intracellular calcium in aluminium toxicity syndrome. New Phytologist 159, 295–314.
Role of dynamics of intracellular calcium in aluminium toxicity syndrome.CrossRef | 1:CAS:528:DC%2BD3sXmsl2rs7o%3D&md5=6b88c4ffedfcdda29a65bf02472372adCAS |

Richards KD, Schott EJ, Sharma YK, Davis KR, Gardner RC (1998) Aluminum induces oxidative stress genes in Arabidopsis thaliana. Plant Physiology 116, 409–418.
Aluminum induces oxidative stress genes in Arabidopsis thaliana.CrossRef | 1:CAS:528:DyaK1cXkslGitw%3D%3D&md5=397ce21e09d9dd38c75fd611aebf8d45CAS |

Ryan PR, Delhaize E, Randall PJ (1995) Characterisation of Al-stimulated efflux of malate from the apices of Al-tolerant wheat roots. Planta 196, 103–110.
Characterisation of Al-stimulated efflux of malate from the apices of Al-tolerant wheat roots.CrossRef | 1:CAS:528:DyaK2MXkvVemsLg%3D&md5=d1132ccb2f6722f05aced0dbc9f4d1b6CAS |

Sarropoulou V, Dimassi-Theriou K, Therios I, Koukourikou-Petridou M (2012) Melatonin enhances root regeneration, photosynthetic pigments, biomass, total carbohydrates and proline content in the cherry rootstock PHL-C (Prunus avium × Prunus cerasus). Plant Physiology and Biochemistry 61, 162–168.
Melatonin enhances root regeneration, photosynthetic pigments, biomass, total carbohydrates and proline content in the cherry rootstock PHL-C (Prunus avium × Prunus cerasus).CrossRef | 1:CAS:528:DC%2BC38XhslKru73F&md5=aa7c2844f3c160878061a59d533eec14CAS |

Silva IR, Smyth TJ, Raper CD, Carter TE, Rufty TW (2001) Differential aluminum tolerance in soybean: an evaluation of the role of organic acids. Physiologia Plantarum 112, 200–210.
Differential aluminum tolerance in soybean: an evaluation of the role of organic acids.CrossRef | 1:CAS:528:DC%2BD3MXktFeltrg%3D&md5=dd9db5adfae0ee6fc1735c3f2a2bc8cdCAS |

Tesfaye M, Temple SJ, Allan DL, Vance CP, Samac DA (2001) Overexpression of malate dehydrogenase in transgenic alfalfa enhances organic acid synthesis and confers tolerance to aluminum. Plant Physiology 127, 1836–1844.
Overexpression of malate dehydrogenase in transgenic alfalfa enhances organic acid synthesis and confers tolerance to aluminum.CrossRef | 1:CAS:528:DC%2BD38XjtVWksA%3D%3D&md5=66503f4ac11cacdb8d21458ae081872bCAS |

Tice KR, Parker DR, Demason DA (1992) Operationally defined apoplastic and symplastic aluminum fractions in root tips of aluminum-intoxicated wheat. Plant Physiology 100, 309–318.
Operationally defined apoplastic and symplastic aluminum fractions in root tips of aluminum-intoxicated wheat.CrossRef | 1:CAS:528:DyaK38Xmt1yjs7c%3D&md5=71214691423f2a83f39d475bfd4a343bCAS |

Wang YS, Yang ZM (2005) Nitric oxide reduces aluminum toxicity by preventing oxidative stress in the roots of Cassia tora L. Plant & Cell Physiology 46, 1915–1923.
Nitric oxide reduces aluminum toxicity by preventing oxidative stress in the roots of Cassia tora L.CrossRef | 1:CAS:528:DC%2BD28XhsVOitQ%3D%3D&md5=b2ffe5ec02941bc27bb67e9b58a8f806CAS |

Wang YS, Wang J, Yang ZM, Wang QY, Lu B, Li SQ, Lu YP, Wang SH, Sun X (2004) Salicylic acid modulates aluminum-induced oxidative stress in roots of Cassia tora. Journal of Integrative Plant Biology 46, 819–828.

Wang LY, Liu JL, Wang WX, Sun Y (2016a) Exogenous melatonin improves growth and photosynthetic capacity of cucumber under salinity-induced stress. Photosynthetica 54, 19–27.
Exogenous melatonin improves growth and photosynthetic capacity of cucumber under salinity-induced stress.CrossRef | 1:CAS:528:DC%2BC2MXps1ehs7g%3D&md5=41c7eb582ed58670473fa92d7587201eCAS |

Wang P, Yu W, Zhang J, Rengel Z, Xu J, Han Q, Chen L, Li K, Yu Y, Chen Q (2016b) Auxin enhances aluminum-induced citrate exudation through upregulation of GmMATE and activation of the plasma membrane H+-ATPase in soybean roots. Annals of Botany 118, 933–940.
Auxin enhances aluminum-induced citrate exudation through upregulation of GmMATE and activation of the plasma membrane H+-ATPase in soybean roots.CrossRef |

Wang Q, An B, Wei Y, Reiter RJ, Shi H, Luo H, He C (2016c) Melatonin regulates root meristem by repressing auxin synthesis and polar auxin transport in Arabidopsis. Frontiers in Plant Science 7, 1882
Melatonin regulates root meristem by repressing auxin synthesis and polar auxin transport in Arabidopsis.CrossRef |

Wu K, Xiao S, Chen Q, Wang Q, Zhang Y, Li K, Yu Y, Chen L (2013) Changes in the activity and transcription of antioxidant enzymes in response to Al stress in black soybeans. Plant Molecular Biology Reporter 31, 141–150.
Changes in the activity and transcription of antioxidant enzymes in response to Al stress in black soybeans.CrossRef | 1:CAS:528:DC%2BC3sXnt12jtg%3D%3D&md5=97f387643c2667139f5f040f478c1d95CAS |

Yang ZM, Wang J, Wang SH, Xu LL (2003) Salicylic acid-induced aluminum tolerance by modulation of citrate efflux from roots of Cassia tora L. Planta 217, 168–174.

Yang ZM, Yang H, Wang J, Wang YS (2004) Aluminum regulation of citrate metabolism for Al-induced citrate efflux in the roots of Cassia tora L. Plant Science 166, 1589–1594.
Aluminum regulation of citrate metabolism for Al-induced citrate efflux in the roots of Cassia tora L.CrossRef | 1:CAS:528:DC%2BD2cXjt1Sjtr4%3D&md5=d75d037f83a86d86a2151a7a56a5f5b3CAS |

Yang JL, You JF, Li YY, Wu P, Zheng SJ (2007) Magnesium enhances aluminum-induced citrate secretion in rice bean roots (Vigna umbellata) by restoring plasma membrane H+-ATPase activity. Plant & Cell Physiology 48, 66–73.
Magnesium enhances aluminum-induced citrate secretion in rice bean roots (Vigna umbellata) by restoring plasma membrane H+-ATPase activity.CrossRef | 1:CAS:528:DC%2BD2sXisFCnu7c%3D&md5=a35a64e1e32838adbb9382bb99891f3cCAS |

Yi HL, Yi M, Li HH, Wu LH (2010) Aluminum induces chromosome aberrations, micronuclei, and cell cycle dysfunction in root cells of Vicia faba. Environmental Toxicology 25, 124–129.

Zhang N, Sun Q, Zhang H, Cao Y, Weeda S, Ren S, Guo YD (2015) Roles of melatonin in abiotic stress resistance in plants. Journal of Experimental Botany 66, 647–656.
Roles of melatonin in abiotic stress resistance in plants.CrossRef | 1:CAS:528:DC%2BC2MXitVWhsbvJ&md5=002f7ac6f848c91ff0a1fb79ca5a487aCAS |



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