Abstract
Plant melatonin appears to be a multiregulatory molecule with multiple functions similar to those observed in animals. It induces growth in stems and stimulates root generation. It is also able to delay senescence by protecting photosynthetic systems and related processes. One of the most studied actions of melatonin is its effect on biotic and abiotic stresses in the plant, such as that produced by drought, extreme temperatures, chemical pollution, UV radiation, etc. Recent data have demonstrated its role as a modulator of gene expression in plants. In this review, we compare studies which show that melatonin behaves in a similar way to auxin, and present data that relate the physiological responses produced by melatonin with the action of auxin, such as promoting/inhibiting growth activity and rooting capacity. In addition, for the first time, the data presented demonstrate the possible involvement of melatonin in the tropic response of roots. The possible role of melatonin as a plant regulator and its relationship with auxin action and the signaling molecule nitric oxide is presented and discussed in a hypothetical model.
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References
Aloni R (2004) The induction of vascular tissues by auxin. In: Davies PJ (ed) Plant hormones. Biosynthesis, signal transduction, action. Kluwer Acad. Pub., Dordrecht, pp 471–492
Arnao MB, Hernández-Ruiz J (2006) The physiological function of melatonin in plants. Plant Sign Behav 1:89–95
Arnao MB, Hernández-Ruiz J (2007) Melatonin promotes adventitious- and lateral root regeneration in etiolated hypocotyls of Lupinus albus L. J Pineal Res 42:147–152
Arnao MB, Hernández-Ruiz J (2014) Melatonin: plant growth regulator and/or biostimulator during stress? Trends Plant Sci 19:789–797
Arnao MB, Hernández-Ruiz J (2015) Functions of melatonin in plants: a review. J Pineal Res 59:133–150
Bajwa VS, Shukla MR, Sherif SM, Murch SJ, Saxena PK (2014) Role of melatonin in alleviating cold stress in Arabidopsis thaliana. J Pineal Res 56:238–245
Chen Y, Kao C (2012) Calcium is involved in nitric oxide- and auxin-induced lateral root formation in rice. Protoplasma 249:187–195
Chen Q, Qi WB, Reiter RJ, Wei W, Wang BM (2009) Exogenously applied melatonin stimulates root growth and raises endogenous IAA in roots of etiolated seedling of Brassica juncea. J Plant Physiol 166:324–328
Cholodny N (1924) Über die hormonale wirkung der organspitze bei der geotropischen krümmung. Ber Dt Bot Ges 42:356–362
Correa-Aragunde N, Graziano M, Lamattina L (2004) Nitric oxide plays a central role in determining lateral root development in tomato. Planta 218:900–905
Correa-Aragunde N, Cejudo F, Lamattina L (2015a) Nitric oxide is required for the auxin-induced activation of NADPH-dependent thioredoxin reductase and protein denitrosylation during root growth responses in Arabidopsis. Ann Bot 116:695–702
Correa-Aragunde N, Foresi N, Lamattina L (2015b) Nitric oxide is a ubiquitous signal for maintaining redox balance in plant cells: regulation of ascorbate peroxidase as a case study. J Exp Bot 66:2913–2921
Di D, Zhang C, Guo G (2015) Involvement of secondary messengers and small organic molecules in auxin perception and signaling. Plant Cell Rep 34:895–904
Dubbels R, Reiter RJ, Klenke E, Goebel A, Schnakenberg E, Ehlers C, Schiwara HW, Schloot W (1995) Melatonin in edible plants identified by radioimmunoassay and by HPLC-MS. J Pineal Res 18:28–31
Hasan M, 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. Front Plant Sci 6:601
Hattori A, Migitaka H, Iigo M, Yamamoto K, Ohtani-Kaneko R, Hara M, Suzuki T, Reiter RJ (1995) Identification of melatonin in plants and its effects on plasma melatonin levels and binding to melatonin receptors in vertebrates. Biochem Mol Biol Int 35:627–634
Hernández IG, Gomez FJV, Cerutti S, Arana MV, Silva MF (2015) Melatonin in Arabidopsis thaliana acts as plant growth regulator at low concentrations and preserves seed viability at high concentrations. Plant Physiol Biochem 94:191–196
Hernández-Ruiz J, Arnao MB (2008a) Distribution of melatonin in different zones of lupin and barley plants at different ages in the presence and absence of light. J Agr Food Chem 56:10567–10573
Hernández-Ruiz J, Arnao MB (2008b) Melatonin stimulates the expansion of etiolated lupin cotyledons. Plant Growth Regul 55:29–34
Hernández-Ruiz J, Cano A, Arnao MB (2004) Melatonin: growth-stimulating compound present in lupin tissues. Planta 220:140–144
Hernández-Ruiz J, Cano A, Arnao MB (2005) Melatonin acts as a growth-stimulating compound in some monocot species. J Pineal Res 39:137–142
Hu X, Neill S, Tang Z, Cai W (2005) Nitric oxide mediates gravitropic bending in soybean roots. Plant Physiol 137:663–670
Hussain A, Mun BG, Imran QM, Lee SU, Adamu TA, Shahid M, Kim KM, Yun BW (2016) Nitric oxide mediated transcriptome profiling reveals activation of multiple regulatory pathways in Arabidopsis thaliana. Front Plant Sci 7:975
Ishikawa H, Evans ML (1992) Induction of curvature in maize roots by calcium or by thigmostimulation: role of the postmitotic isodiametric growth zone. Plant Physiol 100:762–768
Kim M, Seo H, Park C, Park WJ (2016) Examination of the auxin hypothesis of phytomelatonin action in classical auxin assay systems in maize. J Plant Physiol 190:67–71
Kögl F, Haagen-Smit AJ (1933) Über die chemie des wuchsstoffs. Proc Kon Akad V Wetensch Amsterdam 32:1411–1416
Kögl F, Haagen-Smit AJ, Erxleben H (1933) Studien über das vorkommen von auxinen im menschlichen und im tierischen organismus. Hoppe-Seyler’s Z Physiol Chem 220:137–161
Koyama FC, Carvalho TLG, Alves E, da Silva HB, de Azevedo MF, Hemerly AS, Garcia CRS (2013) The structurally related auxin and melatonin tryptophan-derivatives and their roles in Arabidopsis thaliana and in the human malaria parasite Plasmodium falciparum. J Euk Microbiol 60:646–651
Li C, Liang B, Chang C, Wei Z, Zhou S, Ma F (2016) Exogenous melatonin improved potassium content in Malus under different stress conditions. J Pineal Res 61:218–229
Lombardo M, Graziano M, Polacco J, Lamattina L (2006) Nitric oxide functions as a positive regulator of root hair development. Plant Sign Behav 1:28–33
Lüthen H (2015) What we can learn from old auxinology. J Plant Growth Regul 34:702–707
Mukherjee S, David A, Yadav S, Baluska F, Bhatla SC (2014) Salt stress-induced seedling growth inhibition coincides with differential distribution of serotonin and melatonin in sunflower seedling roots and cotyledons. Physiol Plantarum 152:714–728
Nawaz MA, Huang Y, Bie Z, Ahmad W, Reiter RJ, Niu M, Hameed S (2016) Melatonin: current status and future perspectives in plant science. Front Plant Sci 6:1230
Okazaki M, Higuchi K, Aouini A, Ezura H (2010) Lowering intercellular melatonin levels by transgenic analysis of indoleamine 2,3-dioxygenase from rice in tomato plants. J Pineal Res 49:239–247
Pagnussat G, Simontacchi M, Puntarulo S, Lamattina L (2002) Nitric oxide is required for root organogenesis. Plant Physiol 129:954–956
Pagnussat G, Lanteri M, Lombardo M, Lamattina L (2004) Nitric oxide mediates the indole acetic acid induction activation of a mitogen-activated protein kinase cascade involved in adventitious root development. Plant Physiol 135:179–286
Park S, Back K (2012) Melatonin promotes seminal root elongation and root growth in transgenic rice after germination. J Pineal Res 53:385–389
Pelagio-Flores R, Muñoz-Parra E, Ortiz-Castro R, Lopez-Bucio J (2012) Melatonin regulates Arabidopsis root system architecture likely acting independently of auxin signaling. J Pineal Res 53:279–288
Perrin R, Young LS, Murthy UMN, Harrison BR, Wang Y, Will JL, Masson PH (2005) Gravity signal transduction in primary roots. Ann Bot 96:737–743
Posmyk MM, Kuran H, Marciniak K, Janas KM (2008) Presowing seed treatment with melatonin protects red cabbage seedlings against toxic copper ion concentrations. J Pineal Res 45:24–31
Qian Y, Tan DX, Reiter RJ, Shi H (2015) Comparative metabolomic analysis highlights the involvement of sugars and glycerol in melatonin-mediated innate immunity against bacterial pathogen in Arabidopsis. Sci Rep 5:15815
Rademacher W (2015) Plant growth regulators: backgrounds and uses in plant production. J Plant Growth Regul 34:845–872
Reiter RJ, Tan DX, Zhou Z, Coelho-Cruz MH, Fuentes-Broto L, Galano A (2015) Phytomelatonin: assisting plants to survive and thrive. Molecules 20:7396–7437
Sarropoulou VN, Therios IN, Dimassi-Theriou KN (2012a) Melatonin promotes adventitious root regeneration in in vitro shoot tip explants of the commercial sweet cherry rootstocks CAB-6P (Prunus cerasus L.), Gisela 6 (P. cerasus x P. canescens), and MxM 60 (P. avium x P.mahaleb). J Pineal Res 52:38–46
Sarropoulou VN, Dimassi-Theriou KN, Therios IN, Koukourikou-Petridou M (2012b) Melatonin enhances root regeneration, photosynthetic pigments, biomass, total carbohydrates and proline content in the cherry rootstock PHL-C (Prunus avium x Prunus cerasus). Plant Physiol Biochem 61:162–168
Sarrou E, Therios IN, Dimassi-Theriou KN (2014) Melatonin and other factors that promote rooting and sprouting of shoot cuttings in Punica granatum cv. Wonderful. Turk J Bot 38:293–301
Shi HT, Li RJ, Cai W, Liu W, Wang CL, Lu YT (2012) Increasing nitric oxide content in Arabidopsis thaliana by expressing rat neuronal nitric oxide synthase resulted in enhanced stress tolerance. Plant Cell Physiol 53:344–357
Shi H, Chen Y, Tan DX, Reiter RJ, Chan Z, He C (2015a) Melatonin induces nitric oxide and the potential mechanisms relate to innate immunity against bacterial pathogen infection in Arabidopsis. J Pineal Res 59:102–108
Shi H, Jiang C, Ye T, Tan D, Reiter RJ, Zhang H, Liu R, Chan Z (2015b) Comparative physiological, metabolomic, and transcriptomic analyses reveal mechanisms of improved abiotic stress resistance in bermudagrass [Cynodon dactylon (L). Pers.] by exogenous melatonin. J Exp Bot 66:681–694
Shi H, Chen K, Wei Y, He C (2016) Fundamental issues of melatonin-mediated stress signaling in plants. Front Plant Sci 7:1124
Swarup R, Péret B (2012) AUX/LAX family of auxin influx carriers-an overview. Front Plant Sci 3:225
Swarup R, Kramer EM, Perry P, Knox K, Leyser HM, Haseloff J, Beemster GT, Bhalerao R, Bennett M (2005) Root gravitropism requires lateral root cap and epidermal cells for transport and response to a mobile auxin signal. Nat Cell Biol 7:1057–1065
Tukey HB, Went FW, Muir RM, van Overbeek J (1954) Nomenclature of chemical plant regulators: report by a committee of the American Society of Plant Physiologists. Plant Physiol 29:307–308
Wang L, Zhao Y, Reiter RJ, He C, Liu G, Lei Q, Zuo B, Zheng XD, Li Q, Kong J (2014) Changes in melatonin levels in transgenic Micro-Tom tomato overexpressing ovine AANAT and ovine HIOMT genes. J Pineal Res 56:134–142
Wang Q, An B, Wei Y, Reiter RJ, Shi H, Luo H, He C (2016) Melatonin regulates root meristem by repressing auxin synthesis and polar auxin transport in Arabidopsis. Front Plant Sci 7:1882
Weeda S, Zhang N, Zhao X, Ndip G, Guo YD, Buck G, Fu C, Ren S (2014) Arabidopsis transcriptome analysis reveals key roles of melatonin in plant defense systems. PLoS One 9:e93462
Wei W, Li Q, Chu Y-N, Reiter RJ, Yu XM, Zhu DH, Zhang WK, Ma B, Lin Q, Zhang JS, Chen SY (2015) Melatonin enhances plant growth and abiotic stress tolerance in soybean plants. J Exp Bot 66:695–707
Wei Y, Zeng H, Hu W, Chen L, He C, Shi H (2016) Comparative transcriptional profiling of melatonin synthesis and catabolic genes indicates the possible role of melatonin in developmental and stress responses in rice. Front Plant Sci 7:676
Wen D, Gong B, Sun S, Liu S, Wang X, Wei M, Yang F, Li Y, Shi Q (2016) Promoting roles of melatonin in adventitious root development of Solanum lycopersicum L. by regulating auxin and nitric oxide signaling. Front Plant Sci 7:718
Went FW (1928) Wuchsstoff und Wachstum. Rec Trav Bot Neerl 25:1–116
Zhang N, Zhao B, Zhang HJ, Weeda S, Yang C, Yang ZC, Ren S, Guo YD (2013) Melatonin promotes water-stress tolerance, lateral root formation, and seed germination in cucumber (Cucumis sativus L.). J Pineal Res 54:15–23
Zhang HJ, Zhang N, Yang RC, Wang L, Sun QQ, Li DB, Cao YY, Weeda S, Zhao B, Ren S, Guo YD (2014a) Melatonin promotes seed germination under high salinity by regulating antioxidant systems, ABA and GA4 interaction in cucumber (Cucumis sativus L.). J Pineal Res 57:269–279
Zhang N, Zhang HJ, Zhao B, Sun QQ, Cao YY, Li R, Wu XX, Weeda S, Li L, Ren S, Reiter RJ, Guo YD (2014b) The RNA-seq approach to discriminate gene expression profiles in response to melatonin on cucumber lateral root formation. J Pineal Res 56:39–50
Zhang N, Sun Q, Zhang H, Cao Y, Weeda S, Ren S, Guo YD (2015) Roles of melatonin in abiotic stress resistance in plants. J Exp Bot 66:647–656
Zhao H, Su T, Huo L, Wei H, Jiang Y, Xu L, Ma F (2015) Unveiling the mechanism of melatonin impacts on maize seedling growth: sugar metabolism as a case. J Pineal Res 59:255–266
Zuo B, Zheng X, He P, Wang L, Lei Q, Feng C, Zhou J, Li Q, Han Z, Kong J (2014) Overexpression of MzASMT improves melatonin production and enhances drought tolerance in transgenic Arabidopsis thaliana plants. J Pineal Res 57:408–417
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Communicated by A Gniazdowska-Piekarska.
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Arnao, M.B., Hernández-Ruiz, J. Growth activity, rooting capacity, and tropism: three auxinic precepts fulfilled by melatonin. Acta Physiol Plant 39, 127 (2017). https://doi.org/10.1007/s11738-017-2428-3
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DOI: https://doi.org/10.1007/s11738-017-2428-3