Abstract
Soil salinity has negative effects on crop growth and production, and melatonin (MT) plays an important role in regulating plant salt stress. However, it is not clear whether exogenous melatonin mitigates the negative effect on citrus plants subjected to salt stress. This study aimed to explore the response of exogenous melatonin (0, 50, 100, 150 µmol/L) on plant growth, root hormone levels and the photosynthetic system of trifoliate orange (Citrus (Poncirus) trifoliata L.) seedlings exposed to 0 or 150 mmol/L NaCl for 4 weeks. The 150 mmol/L NaCl treatment significantly increased root zeatin riboside, gibberellin and brassinolide levels, while dramatically reducing plant growth, root auxin levels, leaf photosynthesis and fluorescence indexes of seedlings. However, melatonin treatment partially ameliorated reductions in plant height and dry matter accumulation caused by salt stress. Melatonin (100 µmol/L) appears to interact with IAA but not the other hormones studied. Furthermore, the effects of NaCl stress on the net photosynthetic rate, stomatal conductance, maximum photochemical efficiency, PSII effective photon yield, photochemical quenching and other indicators of seedlings leaves were also partially alleviated and the damage of NaCl stress was also reduced when seedlings were treated with melatonin. This suggests that 100 µmol/L melatonin may be an effective treatment.
Similar content being viewed by others
References
Bajguz A, Piotrowska-Niczyporuk A (2014) Brassinosteroids implicated in growth and stress responses. In: Tran LS, Pal S (eds) Phytohormones: A Window to Metabolism, Signaling and Biotechnological Applications. Springer, New York, NY, pp 163–190
Baker NR (2008) Chlorophyll Fluorescence: A Probe of Photosynthesis In Vivo. Ann Rev Plant Bio 59:89–113
Byeon Y, Back K (2014) An increase in melatonin in transgenic rice causes pleiotropic phenotypes,including enhanced seedling growth,delayed flowering,and low grain yield. J Pineal Res 56:408–414
Centritto M, Loreto F, Chartzoulakis K (2003) The use of low [CO2] to estimate diffusional and non-diffusional limitations of photosynthetic capacity of salt‐stressed olive saplings. Plant Cell Environ 26:585–594
Chen ZP, Gu Q, Yu XL, Huang L, Xu S, Wang R, Shen W, Shen W (2018) Hydrogen peroxide acts downstream of melatonin to induce lateral root formation. Ann Bot 121:1127–1136
Colebrook EH, Thomas SG, Phillips AL, Hedden P (2014) The role of gibberellin signalling in plant responses to abiotic stress. J Exp Biol 217:67–75
Demming AB, Adams WW (1996) The role of the xanthophyll cycle carotenoids in the protection of photosynthesis. Trends Plant Sci 1:21–26
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 high performance liquid chromatography-mass spectrometry. J Pineal Res 18:28–31
Ennahli S, Earl HJ (2005) Physiological limitations to photosynthetic carbon assimilation in cotton under water stress. Crop Sci 45:2374–2382
Fan W, Li W, Zhang X (2021) Photosynthetic Physiological Characteristics of Tetracentron sinense Oliv in Different DBH Classes and the Factors Restricting Regeneration. J Plant Growth Regul 6:1–10
Farzad P, Mohammad N, Moghadam H, Hossein Z, Alahmadi MJ (2007) Effects of drought stress on chlorophyll fluorescence parameters, chlorophyll content and grain yield of wheat cultivars. J Biol Sci 7:841–847
Gao W, Feng Z, Bai Q, He J, Wang Y (2019) Melatonin-Mediated Regulation of Growth and Antioxidant Capacity in Salt-Tolerant Naked Oat under Salt Stress. Int J Mol Sci 20:1176
Han B, Chen GX, Gao ZP, Wei XD, Xie KB, Yang XS (2010) The changes of PSII chlorophyll fluorescence dynamic characteristic during leaf senescence of ginkgo. Acta Horticulturae Sinica 37(2):171–178 (in Chinese with English abstract)
Harizanova A, Koleva-Valkova L (2019) Effect of silicon on photosynthetic rate and the chlorophyll fluorescence parameters at hydroponically grown cucumber plants under salinity stress. J Cent Eur Agric 20:953–960
Havaux M, Strasser RJ, Greppin H (1991) A theoretical and experimental analysis of the qP and qn coefficients of chlorophyll fluorescence quenching and their relation to photochemical and nonphotochemical events. Photosynth Res 27:41–55
He C, Yan J, Shen G, Fu L, Holaday AS, Auld D, Zhang H (2005a) Expression of an Arabidopsis vacuolar sodium/proton antiporter gene in cotton improves photosynthetic performance under salt conditions and increases fiber yield in the field. Plant Cell Physiol 46:1848–1854
He C, Yan JQ, Shen GX, Fu LH, Holaday AS, Auld D, Blumwald E, Zhang H (2005b) Expression of an Arabidopsis vacuolar sodium/proton antiporter gene in cotton improves photosynthetic performance under salt conditions and increases fiber yield in the field. Plant Cell Physiol 46:1848–1854
He JD, Li JL, Wu QS (2019) Effects of Rhizoglomus intraradices on plant growth and root endogenous hormones of trifoliate orange under salt stress. J Anim Plant Sci-PAK 29(1):245–250
Iqbal M, Ashraf M (2007) Seed treatment with auxins modulates growth and ion partitioning in salt-stressed wheat plants. Bot Gaz 49(7):1003–1015
Janas KM, Posmyk MM (2013) Melatonin, an underestimated natural substance with great potential for agricultural application. Acta Physiol Plant 35:3285–3292
Javid MG, Sorooshzadeh A, Moradi F, Sanavy SAMM, Allahdadi I (2011) The role of phytohormones in alleviating salt stress in crop plants. Aust J Crop Sci 32:726–734
Jiang CQ, Cui QR, Feng K, Xu D, Li C, Zheng Q (2016) Melatonin improves antioxidant capacity and ion homeostasis and enhances salt tolerance in maize seedlings. Acta Physiol Plant 38:82
Kaya C, Ashraf M, Dı̇kilitas M, Tuna AL (2013) Alleviation of salt stress-induced adverse effects on maize plants by exogenous application of indoleacetic acid (IAA) and inorganic nutrients - a field trial. Aust J Crop Sci 7:249–254
Kojima M, Sakakibara H (2012) Highly sensitive high-throughput profiling of six phytohormones using MS-probe modification and liquid chromatography-tandem mass spectrometry. Methods Mol Biol 918:151–164
Kostopoulou Z, Therios I, Roumeliotis E, Kanellis AK, Molassiotis A (2014) Melatonin combined with ascorbic acid provides salt adaptation in Citrus aurantium L. seedlings. Plant Physiol Bioch 86:155–165
Li H, Chang JJ, Chen HJ, Wang ZY, Gu XR, Wei CH, Zhang Y, Ma JX, Yang JQ, Zhang X (2017) Exogenous melatonin confers salt stress tolerance to Watermelon by improving photosynthesis and redox homeostasis. Front Plant Sci 8:295
Li J, Liu J, Zhu T, Zhao C, Li L, Chen M (2019) The role of melatonin in salt stress responses. Int J Mol Sci 20:1735
Liang D, Gao F, Ni ZY, Lin L (2018) Melatonin improves heat tolerance in kiwifruit seedlings through promoting antioxidant enzymatic activity and glutathione S-transferase transcription. Molecules 23:584
Liu CY, Wang P, Zhang DJ, Zou YN, Kuca K, Wu QS (2018) Mycorrhiza-induced change in root hair growth is associated with IAA accumulation and expression of EXPs in trifoliate orange under two P levels. Sci Horti 234:227–235
Liu J, Guo C, Chen ZL, He JD, Zou YN (2016) Mycorrhizal inoculation modulates root morphology and root phytohormone responses in trifoliate orange under drought stress. Emir J Food Agric 28:251–256
Lu C, Jiang G, Wang B, Kuang T (2003) Photosystem ii photochemistry and photosynthetic pigment composition in salt-adapted halophyte artimisia anethifolia grown under outdoor conditions. J Plant Physiol 160(4):403–408
Mahmud S, Sharmin S, Chowdhury BLD, Hossain MA, Bhuiyan MJH (2016) Mitigation of salt stress in rice plant at germination stage by using methyl jasmonate. Asian J Med Biol Res 2:74–81
Meng JF, Xu TF, Wang ZZ, Fang YL, Xi ZM, Zhang ZW (2015) The ameliorative effects of exogenous melatonin on grape cuttings under water-deficient stress: antioxidant metabolites, leaf anatomy, and chloroplast morphology. J Pineal Res 57:200–212
Mimuro M, Akimoto S, Yamazaki I, Miyashita H, Miyachi S (1999) Fluorescence properties of chlorophyll d-dominating prokaryotic alga, acaryochloris marina: studies using time-resolved fluorescence spectroscopy on intact cells. Biochim Biophys Acta 1412:37–46
Park S, Back K (2012) Melatonin promotes seminal root elongation and root growth in transgenic rice after germination. J Pineal Res 53:385–389
Pazurkiewicz-kocot K, Kita A, Haduch A (2011) The effect of kinetin on the chlorophyll pigments content in leaves of Zea mays L. seedlings and accumulation of some metal ions. Inżynieria i Ochrona Środowiska 14:397–409
Schreiber U, Bilger W, Hormann H, Neubauer C (1998) Chlorophyll fluorescence as a diagnostic tool: basics and some aspects of practical relevance. Cambridge University Press, Cambridge, pp 320–336
Shibata S, Satou F, Kimura H, Oyabu T (2012) The relationship between chlorophyll fluorescence parameter (Fv/Fm) and frequency component of plant bioelectric potential in spraying chemical herbicides. IEEJ Trans Sens Micromachines 132:154–158
Sowmyalakshmi S, Han L, Pierre D, Smith DL (2015) Computed tomography scanning can monitor the effects of soil medium on root system development: an example of salt stress in corn. Front Plant Sci 6:256
Stassinos PM, Rossi M, Borromeo I, Capo C, Forni C (2021) Amelioration of salt stress tolerance in rapeseed (Brassica napus) cultivars by seed inoculation with Arthrobacter globiformis. Plant Biosyst 5:1–12
Sun S, Wen D, Yang W, Meng Q, Gong B (2020) Overexpression of caffeic acid O-methyltransferase 1 (COMT1) increases melatonin level and salt stress tolerance in tomato plant. J Plant Growth Regul 39(3):1–15
Tan DX, Hardeland R, Manchester LC, Ahmet K, Ma S, Sergio RC, Reiter RJ (2012) Functional roles of melatonin in plants, and perspectives in nutritional and agricultural science. J Exp Bot 63(2):577–597
Tan DX, Manchester LC, Reiter RJ, Qi WB, Karbownik M, Calvo JR (2000) Significance of melatonin in antioxidative defense system: Reactions and products. Biol Signal Recept 9:137–159
Tietz S, Hall CC, Cruz JA, Kramer DM (2017) NPQ(T): a chlorophyll fluorescence parameter for rapid estimation and imaging of non-photochemical quenching of excitons in photosystem‐II‐associated antenna complexes. Plant Cell Environ 40(8):1243–1255
Tiryaki I, Keles H (2012) Reversal of the inhibitory effect oflight and high temperature on germination of Phacelia tanacetifolia seeds by melatonin. J Pineal Res 52(3):332–339
Wang LY, Liu JL, Wang WX, Sun Y (2016) Exogenous melatonin improves growth and photosynthetic capacity of cucumber under salinity-induced stress. Photosynthetica 54:19–27
Wang X, Zhang D, Qi Q, Tong S, An Y, Lu X, Liu Y (2019) The restoration feasibility of degraded carex tussock in soda-salinization area in arid region. Ecol Indic 98:131–136
Wei W, Li QT, Chu YN, Reiter RJ, Yu XM, Zhu DH, Zhang WK, Ma B, Lin Q, Zhang JS (2015) Melatonin enhances plant growth and abiotic stress tolerance in soybean plants. J Exp Bot 3:695–707
Wu QS, Zou YN (2009) Arbuscular mycorrhizal symbiosis improves growth and root nutrient status of citrus subjected to salt stress. Sci Asia 35:388–391
Wu QS, Zou YN (2013) Mycorrhizal symbiosis alters root H+ effluxes and root system architecture of trifoliate orange seedlings under salt stress. J Anim Plant Sci-PAK 23:143–148
Wu QS, Zou YN, He XH (2010b) Contributions of arbuscular mycorrhizal fungi to growth, photosynthesis, root morphology and ionic balance of citrus seedlings under salt stress. Acta Physiol Plantarum 32:297–304
Wu QS, Zou YN, Liu W, Ye XF, Zai HF, Zhao LJ (2010a) Alleviation of salt stress in citrus seedlings inoculated with mycorrhiza: changes in leaf antioxidant defense systems. Plant Soil Environ 56:470–475
Ye J, Wang SW, Deng XP, Yin LN, Xiong BL, Wang XY (2016) Melatonin increased maize (Zea mays L.) seedling drought tolerance by alleviating drought-induced photosynthetic inhibition and oxidative damage. Acta Physiol Plantarum 38:48
Yu Z, Duan X, Luo L, Dai S, Ding Z, Xia G (2020) How plant hormones mediate salt stress responses. Trends Plant Sci 25(11):1117–1130
Zhang DJ, Liu CY, Yang YJ, Wu QS, Li YY (2019) Plant root hair growth in response to hormones. Not Bot Horti Agrobo 47:278–281
Zhang DJ, Xia RX, Cao X (2016) Ethylene modulates root hair development in trifoliate orange through auxin-signaling pathway. Sci Horti 213:252–259
Zhang DJ, Xia RX, Cao X, Shu B, Chen CL (2013) Root hair development of Poncirus trifoliata grown in different growth cultures and treated with 3-indolebutyric acid and ethephon. Sci Horti 160:389–397
Zhang DJ, Yang YJ, Liu CY, Zhang F, Hu W, Gong SB, Wu QS (2018) Auxin modulates root hair growth through its signaling pathway in citrus. Sci Horti 236:73–78
Zhang N, Jiang Q, Dian-Bo LI, Cai LT, Zhang HJ, Si WJ, Fan XF, Guo YD (2014) Effect of exogenous melatonin on germination of Pennisetum alopecuroides under NaCl stress. J China Agricultural Univ 19:54–60 (in Chinese with English abstract)
Zhang N, Zhao B, Zhang HJ, Weeda S, Yang C (2003) Melatonin promotes water-stress tolerance, lateral root formation, and seed germination in cucumber (Cucumis sativus L.). J Pineal Res 54:15–23
Zhang YC, Wang P, Wu QH, Zou YN, Bao Q, Wu QS (2017) Arbuscular mycorrhizas improve plant growth and soil structure in trifoliate orange under salt stress. Arch Agron Soil Sci 63:491–500
Zhou ZX, Li Z, Zhang Z, You L, Cui X (2021) Treatment of the saline-alkali soil with acidic corn stalk biochar and its effect on the sorghum yield in western songnen plain. Sci Total Environ 797:149190
Acknowledgements
This work was supported by the Young and Middle-aged Talent Project of Hubei Provincial Education Department (grant number Q20181304) and the National Natural Science Foundation of China (No. 32001984).
Author information
Authors and Affiliations
Corresponding author
Ethics declarations
Ethical Statements
In consideration of the publication, we hereby warrant and undertake: 1. This article is an original work and no portion of the study has been published or is under consideration for publication elsewhere. 2. None of the authors has any potential conflict of interest related to this manuscript. 3. All authors have contributed to the work, and they have agreed to submit the manuscript.
Additional information
Communicated by Paul Holford .
Publisher’s Note
Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.
Rights and permissions
About this article
Cite this article
Hu, Ch., Zheng, Y., Tong, Cl. et al. Effects of exogenous melatonin on plant growth, root hormones and photosynthetic characteristics of trifoliate orange subjected to salt stress. Plant Growth Regul 97, 551–558 (2022). https://doi.org/10.1007/s10725-022-00814-z
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10725-022-00814-z