Abstract
Cold stress disturbs numerous physiological and biochemical processes, restricting plant growth and productivity. In the current study, the protective role of exogenous serotonin in alleviating cold stress was investigated in rapeseed (Brassica napus L.) seedlings. The rapeseed seedlings were pretreated with different concentrations (0, 0.01, 0.02, 0.03, and 0.04 g L− 1) of serotonin solution and then were exposed to cold stress (4, 2, 0, and − 2 °C). The results indicated that the pretreatment of serotonin significantly increased the survival rate. Mainly, 0.03 g L− 1 of serotonin increased the survival rate by 75% compared to control conditions. The physiological and biochemical indexes and the expression of cold tolerance-related genes were analyzed in the seedlings pretreated with 0.03 g L− 1 of serotonin. The contents of proline (PRO), soluble sugar (SS), and soluble protein (SP); and the activities of antioxidant defense such as catalase (CAT), peroxidase (POD), and superoxide dismutase (SOD) were significantly increased by exogenous serotonin under cold stress. Supplemented serotonin significantly increased the expression of SOD, COR6.6, COR15, and CBFs genes under cold stress.Overall, our results indicate that the optimal concentration (0.03 g L− 1) of exogenous serotonin maintained the osmotic potential balance in cells under cold stress by increasing the content of osmotic regulatory substances (SS, SP, and PRO), improving the scavenging ability of reactive oxygen species (ROS), increasing the antioxidant enzyme activities (CAT, POD, and SOD) and the transcriptional level of cold stress-related genes, helping rapeseed seedlings to cope with the cold stress. Therefore, serotonin-induced regulatory interactions between physiological and biochemical processes and the elevated expression of stress-associated genes may be a beneficial technique for cold stress tolerance in plants.
Similar content being viewed by others
References
Agarwal PK, Agarwal P, Reddy M, Sopory SK (2006) Role of DREB transcription factors in abiotic and biotic stress tolerance in plants. Plant Cell Rep 25:1263–1274
Arnao MB, Hernández-Ruiz J (2014) Melatonin: plant growth regulator and/or biostimulator during stress? Trends Plant Sci 19:789–797
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
Cen HF, Wang TT, Liu HY, Tian DY, Zhang YW (2020) Melatonin application improves salt tolerance of alfalfa (Medicago sativa L.) by enhancing antioxidant capacity. Plants 9:220
Chinnusamy V, Zhu J, Zhu JK (2006) Gene regulation during cold acclimation in plants. Physiol Plant 126:52–61
Csaba G, Katalin Pál (1982) Effects of insulin, triiodothyronine, and serotonin on plant seed development. Protoplasma 110:20–22
Ding Y, Shi Y, Yang S (2019) Advances and challenges in uncovering cold tolerance regulatory mechanisms in plants. New Phytol 222:690–1704
Hasanuzzaman M, Bhuyan MB, Zulfiqar F, Raza A, Mohsin SM, Mahmud JA, Fujita M, Fotopoulos V (2020) Reactive oxygen species and antioxidant defense in plants under abiotic stress: revisiting the crucial role of a universal defense regulator. Antioxidants 9:681
Hodges DM, DeLong JM, Forney CF, Prange RK (1999) Improving the thiobarbituric acid-reactive-substances assay for estimating lipid peroxidation in plant tissues containing anthocyanin and other interfering compounds. Planta 207:604–611
Janero D (1990) Malondialdehyde and thiobarbituric acidreactivity as diagnostic indices of lipid peroxidation and peroxidative tissue injury. Free Radical Biol Med 9:515–540
Jia H, Hao L, Guo X, Liu S, Yan Y, Guo X (2016) A Raf-like MAPKKK gene, GhRaf19, negatively regulates tolerance to drought and salt and positively regulates resistance to cold stress by modulating reactive oxygen species in cotton. Plant Sci 252:267–281
Kaur H, Mukherjee S, Baluska F, Bhatla SC (2015) Regulatory roles of serotonin and melatonin in abiotic stress tolerance in plants. Plant Signal Behav 10:e1049788
Kodama H, Horiguchi GL, Nishiuchi T, Nishimura M, Iba K (1995) Fatty acid desaturation during chilling acclimation is one of the factors involved in conferring low-temperature tolerance to young tobacco leaves. Plant Physiol 107:1177–1185
Li D, Zhu Z, Sun DW (2018a) Effects of freezing on cell structure of fresh cellular food materials: A review. Trends Food Sci Technol 75:46–55
Li J, Zeng L, Cheng Y, Lu G, Fu G, Ma H, Li C (2018b) Exogenous melatonin alleviates damage from drought stress in Brassica napus L. (rapeseed) seedlings. Acta Physiol Plant 40:43
Li X, Wei JP, Scott ER, Liu JW, Guo S, Li Y, Zhang L, Han WY (2018c) Exogenous melatonin alleviates cold stress by promoting antioxidant defense and redox homeostasis in Camellia sinensis L. Molecules 23:165
Mervat SS, Ahmed B (2020) Alleviation of drought stress by melatonin foliar treatment on twoflax varieties under sandy soil. Physiol Mol Biol Plants 26:907–919
McCully ME, Canny MJ, Huang CX (2004) The management of extracellular ice by frosted, acclimated herbaceous petioles. Ann Bot 94:665–674
Miller G, Shulaev V, Mittler R (2008) Reactive oxygen signaling and abiotic stress. Physiol Plant 133:481–489
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. Physiol Plant 152:714–728
Nawaz MA, Huang Y, Bie Z, Ahmed W, Reiter RJ, Niu M, Hameed S (2016) Melatonin: current status and future perspectives in plant science. Front Plant Sci 6:1230
Park S, Back K (2012) Melatonin promotes seminal root elongation and root growth in transgenic rice after germination. J Pineal Res 53:385–389
Pearce RS (2001) Plant freezing and damage. Ann Bot 87:417–424
Pelagio-Flores R, Ortíz-Castro R, Méndez-Bravo A, Macías-Rodríguez L, López-Bucio J (2011) Serotonin, a tryptophan-derived signal conserved in plants and animals, regulates root system architecture probably acting as a natural auxin inhibitor in Arabidopsis thaliana. Plant Cell Physiol 52:490–508
Radhakrishnan R, Lee IJ (2013) Ameliorative effects of spermine against osmotic stress through antioxidants and abscisic acid changes in soybean pods and seeds. Acta Physiol Plant 35:263–269
Raza A (2020) Eco-physiological and biochemical responses of rapeseed (Brassica napus L.) to abiotic Stresses: consequences and mitigation strategies. J Plant Growth Regul. https://doi.org/10.1007/s00344-020-10231-z
Raza A, Razzaq A, Mehmood SS, Zou X, Zhang X, Lv Y, Xu J (2019) Impact of climate change on crops adaptation and strategies to tackle its outcome: a review. Plants 8:34
Raza A, Ashraf F, Zou X, Zhang X, Tosif H (2020) Plant adaptation and tolerance to environmental stresses: mechanisms and perspectives. In: Plant ecophysiology and adaptation under climate change: mechanisms and perspectives I. Springer, Singapore, pp 117–145
Sharma A, Wang JF, Xu DB, Tao SC, Chong SL, Yan DL, Li Z, Yuan HW, Zheng BS (2020) Melatonin regulates the functional components of photosynthesis, antioxidant system, gene expression, and metabolic pathways to induce drought resistance in grafted Carya cathayensis plants. Sci Total Environ 713
Shi HT, Qian YQ, Tan DX, Russel JR, He CZ (2015) Melatonin induces the transcripts of CBF/DREB1s and their involvement in both abiotic and biotic stresses in Arabidopsis. J Pineal Res 59:334–342
Shi H, Chen K, Wei Y, He C (2016) Fundamental issues of melatonin-mediated stress signaling in plants. Front Plant Sci 7:1124
Strydhorst S, Hall L, Perrott L (2018) Plant growth regulators: What agronomists need to know. Crops Soils 51:22–26
Song FN, Yang CP, Liu XM, Li GB (2006) Effect of salt stress on activity of superoxide dismutase (SOD) in Ulmus Pumila L. J Forest Res 017:13–16
Soumya M (2018) Novel perspectives on the molecular crosstalk mechanisms of serotonin and melatonin in plants. Plant Physiol Biochem 132:33–45
Tian S, Li JQ, Zhang XK, Fu GP et al (2019) Effect of exogenous 5-hydroxytryptamine on rapessed (Brassica napus L.) seedling under drought stress. Chin J Oil Crops 41:192–198 (in Chinese)
Wang Y, Luo Z, Du R, Liu Y, Ying T, Mao L (2013) Effect of nitric oxide on antioxidative response and proline metabolism in banana during cold storage. J Agric Food Chem 61:8880–8887
Xin Z, Browse J (2000) Cold comfort farm: the acclimation of plants to freezing temperatures. Plant Cell Environ 23:893–902
Yan L, Cai J, Gao L, Huang B, Ma H, Liu Q, Dai X, Zhang X, Chen Y, Zou X (2018) Identification method and selection of cold tolerance in rapeseed (Brassica napus L.). Chinese J Oil Crop Sci 40:074–083 (in Chinese)
Yan L, Tariq S, Chen Y, Lü Y, Zhang X, Zou X (2019) Physiological and molecular responses to cold stress in rapeseed (Brassica napus L.). J Integr Agric 18:2742–2752
Yu Y, Lv Y, Shi YN, Li T, Chen YC, Zhao DK, Zhao ZW (2018) The role of phyto-melatonin and related metabolites in response to stress. Molecules 23:1887
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 Y, Yu H, Yang X, Li Q, Ling J, Wang H, Gu X, Huang S, Jiang W (2016) CsWRKY46, a WRKY transcription factor from cucumber, confers cold resistance in transgenic-plant by regulating a set of cold-stress responsive genes in an ABA-dependent manner. Plant Physiol Biochem 108:478–487
Funding
This work was supported by the National Key Research and Development Program (2017YFD0101700), Agricultural Science and Technology Innovation Program of CAAS, and the Hubei Agricultural Science and Technology Innovation Center.
Author information
Authors and Affiliations
Contributions
HH and LY performed the experiment and collected the data; HH, LY, and AR wrote and revised the manuscript; YZ helped in preparing the initial draft; AR, YL, and YC helped in the relevant literature; LZ and XD provided the reagents and materials; XZ designed and supervised the study.
Corresponding author
Ethics declarations
Conflict of interest
All authors declare that they have no conflict of interest.
Additional information
Communicated by: Luca Sebastiani.
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
He, H., Lei, Y., Yi, Z. et al. Study on the mechanism of exogenous serotonin improving cold tolerance of rapeseed (Brassica napus L.) seedlings. Plant Growth Regul 94, 161–170 (2021). https://doi.org/10.1007/s10725-021-00700-0
Received:
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s10725-021-00700-0