Abstract
Abscisic acid (ABA) is an important phytohormone that regulates seed germination, dormancy, and plant responses to stresses such as salt, drought, and cold. Melatonin regulates ABA biosynthesis and catabolism during seed germination under various types of stress; however, the transcriptional regulation of ABA signaling genes by melatonin during cucumber seed germination under low temperature (LT, 15 °C) stress is poorly understood. Here we report that melatonin promoted seed germination under LT stress by decreasing ABA content and increasing the gibberellic acid (GA)/ABA ratio (gibberellic acid, GA). We also examined the expression levels of the ABA receptors PYR/PYL/RCAR (PYL), as well as the negative regulator protein phosphatase type 2C (PP2C) and positive regulator subfamily 2 of SNF1-related kinase (SnRK2) by real-time PCR. The expression of most tested genes increased during seed germination, showing an opposite trend to ABA level. The transcript levels of CsPYL1, CsPYL2, CsPYL3, CsPYL8, and CsPYL10 in 10 μM melatonin-pretreated seeds were significantly increased after 6 h of imbibition as a result of feedback regulation caused by the lack of ABA, and CsPP2C3, CsPP2C5, and CsSnRK2.1 exhibited higher expression levels than CK (control) treatment. The expression of most tested genes changed markedly in the initial water uptake phase (12 h after imbibition), suggesting that this period is critical for the regulation of ABA signaling during seed germination. We speculate that melatonin reduces ABA content, preventing CsPYL (CsPYL1/2/3/8/10) binding to CsPP2C and thereby enhancing the activity of CsPP2C (CsPP2C3/5) and blocking CsSnRK2.1 activation. Phosphorylation of the downstream factors ABA-responsive element-binding factor (ABF)/ABA-responsive element-binding protein (AREB) by CsSnRK2.1 is thus abolished, leading to seed germination under LT stress.
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References
Arnao MB, Hernandez-Ruiz J (2015) Functions of melatonin in plants: a review. J Pineal Res 59(2):133–150. https://doi.org/10.1111/jpi.12253
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(3):238–245. https://doi.org/10.1111/jpi.12115
Balabusta M, Szafranska K, Posmyk MM (2016) Exogenous melatonin improves antioxidant defensein cucumber seeds (Cucumis sativus L.) germinated under chilling stress. Front Plant Sci. https://doi.org/10.3389/fpls.2016.00575
Chen L, Lu B, Liu L, Duan W, Jiang D, Li J, Zhang K, Sun H, Zhang Y, Li C, Bai Z (2021) Melatonin promotes seed germination under salt stress by regulating ABA and GA3 in cotton (Gossypium Hirsutum L.). Plant Physiol Biochem 162:506–516. https://doi.org/10.1016/j.plaphy.2021.03.029
Chinnusamy V, Zhu J, Zhu J-K (2007) Cold stress regulation of gene expression in plants. Trends Plant Sci 12(10):444–451. https://doi.org/10.1016/j.tplants.2007.07.002
Cutler SR, Rodriguez PL, Finkelstein RR, Abrams SR (2010) Abscisic acid: emergence of a core signaling network. Annu Rev Plant Biol 61:651–679. https://doi.org/10.1146/annurev-arplant-042809-112122
Del Egido LL, Navarro-Miro D, Martinez-Heredia V, Toorop PE, Iannetta PPM (2017) A spectrophotometric assay for robust viability testing of seed batches using 2,3,5-triphenyl tetrazolium chloride: using Hordeum vulgare L. as a model. Front Plant Sci. https://doi.org/10.3389/fpls.2017.00747
Ding F, Liu B, Zhang S (2017) Exogenous melatonin ameliorates cold-induced damage in tomato plants. Sci Hortic 219:264–271. https://doi.org/10.1016/j.scienta.2017.03.029
Domingos P, Prado AM, Wong A, Gehring C, Feijo JA (2015) Nitric oxide: a multitasked signaling gas in plants. Mol Plant 8(4):506–520. https://doi.org/10.1016/j.molp.2014.12.010
Dong W, Lv H, Xia G, Wang M (2012) Does diacylglycerol serve as a signaling molecule in plants? Plant Signal Behav 7(4):472–475. https://doi.org/10.4161/psb.19644
Farooq M, Hussain M, Nawaz A, Lee D-J, Alghamdi SS, Siddique KHM (2017) Seed priming improves chilling tolerance in chickpea by modulating germination metabolism, trehalose accumulation and carbon assimilation. Plant Physiol Biochem 111:274–283. https://doi.org/10.1016/j.plaphy.2016.12.012
Fu J, Wu Y, Miao Y, Xu Y, Zhao E, Wang J, Sun H, Liu Q, Xue Y, Xu Y, Hu T (2017) Improved cold tolerance in Elymus nutans by exogenous application of melatonin may involve ABA-dependent and ABA-independent pathways. Sci Rep. https://doi.org/10.1038/srep39865
Giannopolitis CN, Ries SK (1977) Superoxide dismutases. 1. occurrence in higher-plants. Plant Physiol 59(2):309–314. https://doi.org/10.1104/pp.59.2.309
Huangfu L, Zhang Z, Zhou Y, Zhang E, Chen R, Fang H, Li P, Xu Y, Yao Y, Zhu M, Yin S, Xu C, Lu Y, Yang Z (2021) Integrated physiological, metabolomic and transcriptomic analyses provide insights into the roles of exogenous melatonin in promoting rice seed germination under salt stress. Plant Growth Regul 95(1):19–31. https://doi.org/10.1007/s10725-021-00721-9
International Seed Testing Association (2021) Full Issue. International rules for seed testing 2022(1):i-19-8. https://doi.org/10.15258/istarules.2021.F
Isner JC, Maathuis FJM (2018) cGMP signalling in plants: from enigma to main stream. Funct Plant Biol 45(2):93–101. https://doi.org/10.1071/fp16337
Jahan MS, Shu S, Wang Y, Hasan MM, El-Yazied AA, Alabdallah NM, Hajjar D, Altaf MA, Sun J, Guo S (2021) Melatonin pretreatment confers heat tolerance and repression of heat-induced senescence in tomato through the modulation of ABA- and GA-mediated pathways. Front Plant Sci. https://doi.org/10.3389/fpls.2021.650955
Jain M, Nagar P, Goel P, Singh AK, Kumari S, Mustafiz A (2018) Second messengers: central regulators in plant abiotic stress response. In: Zargar S, Zargar M (eds) Abiotic stress-mediated sensing and signaling in plants: an omics perspective. Springer, Singapore
Kato M, Shimizu S (1987) Chlorophyll metabolism in higher-plants. 7. chlorophyll degradation in senescing tobacco-leaves—phenolic-dependent peroxidative degradation. Can J Bot 65(4):729–735. https://doi.org/10.1139/b87-097
Kolodziejczyk I, Dzitko K, Szewczyk R, Posmyk MM (2016) Exogenous melatonin improves corn (Zea mays L.) embryo proteome in seeds subjected to chilling stress. J Plant Physiol 193:47–56. https://doi.org/10.1016/j.jplph.2016.01.012
Korkmaz A, Karaca A, Kocacinar F, Cuci Y (2017) The effects of seed treatment with melatonin on germination and emergence performance of pepper seeds under chilling stress. J Agric Sci 23(2):167–176
Kushiro T, Okamoto M, Nakabayashi K, Yamagishi K, Kitamura S, Asami T, Hirai N, Koshiba T, Kamiya Y, Nambara E (2004) The Arabidopsis cytochrome P450CYP707A encodes ABA 8’-hydroxylases: key enzymes in ABA catabolism. Embo J 23(7):1647–1656. https://doi.org/10.1038/sj.emboj.7600121
Li C, Tan DX, Liang D, Chang C, Jia D, Ma F (2015) Melatonin mediates the regulation of ABA metabolism, free-radical scavenging, and stomatal behaviour in two Malus species under drought stress. J Exp Bot 66(3):669–680. https://doi.org/10.1093/jxb/eru476
Li X, Tan D-X, Jiang D, Liu F (2016) Melatonin enhances cold tolerance in drought-primed wild-type and abscisic acid-deficient mutant barley. J Pineal Res 61(3):328–339. https://doi.org/10.1111/jpi.12350
Li Z, Xu J, Gao Y, Wang C, Guo G, Luo Y, Huang Y, Hu W, Sheteiwy MS, Guan Y, Hu J (2017) The synergistic priming effect of exogenous salicylic acid and H2O2 on chilling tolerance enhancement during maize (Zea mays L.) seed germination. Front Plant Sci. https://doi.org/10.3389/fpls.2017.01153
Li J, Zhao C, Zhang M, Yuan F, Chen M (2019) Exogenous melatonin improves seed germination in Limonium bicolor under salt stress. Plant Signal Behav. https://doi.org/10.1080/15592324.2019.1659705
Li H, Guo Y, Lan Z, Xu K, Chang J, Ahammed GJ, Ma J, Wei C, Zhang X (2021a) Methyl jasmonate mediates melatonin-induced cold tolerance of grafted watermelon plants. Hortic Res 8:57. https://doi.org/10.1038/s41438-021-00496-0
Li H, Guo Y, Lan Z, Zhang Z, Ahammed GJ, Chang J, Zhang Y, Wei C, Zhang X (2021b) Melatonin antagonizes aba action to promote seed germination by regulating Ca2+ efflux and H2O2 accumulation. Plant Sci. https://doi.org/10.1016/j.plantsci.2020.110761
Liu L, Duan L, Zhang J, Zhang Z, Mi G, Ren H (2010) Cucumber (Cucumis sativus L.) over-expressing cold-induced transcriptome regulator ICE1 exhibits changed morphological characters and enhances chilling tolerance. Sci Hortic 124(1):29–33. https://doi.org/10.1016/j.scienta.2009.11.018
Lopez Del Egido L, Navarro-Miró D, Martinez-Heredia V, Toorop PE, Iannetta PPM (2017) A spectrophotometric assay for robust viability testing of seed batches using 2,3,5-triphenyl tetrazolium chloride: using Hordeum vulgare L. as a model. Front Plant Sci. https://doi.org/10.3389/fpls.2017.00747
Lv Y, Pan J, Wang H, Reiter RJ, Li X, Mou Z, Zhang J, Yao Z, Zhao D, Yu D (2021) Melatonin inhibits seed germination by crosstalk with abscisic acid, gibberellin, and auxin in Arabidopsis. J Pineal Res. https://doi.org/10.1111/jpi.12736
Ma Y, Szostkiewicz I, Korte A, Moes D, Yang Y, Christmann A, Grill E (2009) Regulators of PP2C phosphatase activity function as abscisic acid sensors. Science 324(5930):1064–1068. https://doi.org/10.1126/science.1172408
Manasa SL, Panigrahy M, Panigrahi KCS, Rout GR (2021) Overview of cold stress regulation in plants. Bot Rev. https://doi.org/10.1007/s12229-021-09267-x
Melcher K, Ng L-M, Zhou XE, Soon F-F, Xu Y, Suino-Powell KM, Park S-Y, Weiner JJ, Fujii H, Chinnusamy V, Kovach A, Li J, Wang Y, Li J, Peterson FC, Jensen DR, Yong E-L, Volkman BF, Cutler SR, Zhu J-K, Xu HE (2009) A gate-latch-lock mechanism for hormone signalling by abscisic acid receptors. Nature 462(7273):602–608. https://doi.org/10.1038/nature08613
Miyazono K-i, Miyakawa T, Sawano Y, Kubota K, Kang H-J, Asano A, Miyauchi Y, Takahashi M, Zhi Y, Fujita Y, Yoshida T, Kodaira K-S, Yamaguchi-Shinozaki K, Tanokura M (2009) Structural basis of abscisic acid signalling. Nature 462(7273):609–614. https://doi.org/10.1038/nature08583
Munnik T (2001) Phosphatidic acid: an emerging plant lipid second messenger. Trends Plant Sci 6(5):227–233. https://doi.org/10.1016/s1360-1385(01)01918-5
Nakano Y, Asada K (1981) Hydrogen-peroxide is scavenged by ascorbate-specific peroxidase in spinach-chloroplasts. Plant Cell Physiol 22(5):867–880. https://doi.org/10.1093/oxfordjournals.pcp.a076232
Nawaz MA, Huang Y, Bie Z, Reiter RJ, Niu M, Hameed S (2016) Melatonin: current status and future perspectives in plant science. Front Plant Sci 6:1230. https://doi.org/10.3389/fpls.2015.01230
Ng L-M, Soon F-F, Zhou XE, West GM, Kovach A, Suino-Powell KM, Chalmers MJ, Li J, Yong E-L, Zhu J-K, Griffin PR, Melcher K, Xu HE (2011) Structural basis for basal activity and autoactivation of abscisic acid (ABA) signaling SnRK2 kinases. Proc Natl Acad Sci USA 108(52):21259–21264. https://doi.org/10.1073/pnas.1118651109
Okamoto M, Kuwahara A, Seo M, Kushiro T, Asami T, Hirai N, Kamiya Y, Koshiba T, Nambara E (2006) CYP707A1 and CYP707A2, which encode abscisic acid 8’-hydroxylases, are indispensable for proper control of seed dormancy and germination in Arabidopsis. Plant Physiol 141(1):97–107. https://doi.org/10.1104/pp.106.079475
Pallavi S, Jha AB, Dubey RS, Pessarakli M (2012) Reactive oxygen species, oxidative damage, and antioxidative defense mechanism in plants under stressful conditions. J Botany. https://doi.org/10.1155/2012/217037
Park S-Y, Fung P, Nishimura N, Jensen DR, Fujii H, Zhao Y, Lumba S, Santiago J, Rodrigues A, Chow T-FF, Alfred SE, Bonetta D, Finkelstein R, Provart NJ, Desveaux D, Rodriguez PL, McCourt P, Zhu J-K, Schroeder JI, Volkman BF, Cutler SR (2009) Abscisic acid inhibits type 2C protein phosphatases via the PYR/PYL family of start proteins. Science 324(5930):1068–1071. https://doi.org/10.1126/science.1173041
Posmyk MM, Balabusta M, Wieczorek M, Sliwinska E, Janas KM (2009) Melatonin applied to cucumber (Cucumis sativus L.) seeds improves germination during chilling stress. J Pineal Res 46(2):214–223. https://doi.org/10.1111/j.1600-079X.2008.00652.x
Qin XQ, Zeevaart JAD (1999) The 9-cis-epoxycarotenoid cleavage reaction is the key regulatory step of abscisic acid biosynthesis in water-stressed bean. Proc Natl Acad Sci USA 96(26):15354–15361. https://doi.org/10.1073/pnas.96.26.15354
Qin XQ, Zeevaart JAD (2002) Overexpression of a 9-cis-epoxycarotenoid dioxygenase gene in Nicotiana plumbaginifolia increases abscisic acid and phaseic acid levels and enhances drought tolerance. Plant Physiol 128(2):544–551. https://doi.org/10.1104/pp.010663
Rodas-Junco BA, Racagni-Di-Palma GE, Canul-Chan M, Usorach J, Hernandez-Sotomayor SMT (2021) Link between lipid second messengers and osmotic stress in plants. Int J Mol Sci 22(5):2658. https://doi.org/10.3390/ijms22052658
Santiago J, Rodrigues A, Saez A, Rubio S, Antoni R, Dupeux F, Park SY, Marquez JA, Cutler SR, Rodriguez PL (2009) Modulation of drought resistance by the abscisic acid receptor PYL5 through inhibition of clade A PP2Cs. Plant J 60(4):575–588. https://doi.org/10.1111/j.1365-313X.2009.03981.x
Scebba F, Sebastiani L, Vitagliano C (2001) Activities of antioxidant enzymes during senescence of Prunus armeniaca leaves. Biol Plantarum 44(1):41–46. https://doi.org/10.1023/A:1017962102950
Soon FF, Ng LM, Zhou XE, West GM, Kovach A, Tan MHE, Suino-Powell KM, He Y, Xu Y, Chalmers MJ, Brunzelle JS, Zhang H, Yang H, Jiang H, Li J, Yong EL, Cutler S, Zhu JK, Griffin PR, Melcher K, Xu HE (2012) Molecular mimicry regulates ABA signaling by SnRK2 kinases and PP2C phosphatases. Science 335(6064):85–88. https://doi.org/10.1126/science.1215106
Steinhorst L, Kudla J (2014) Signaling in cells and organisms—calcium holds the line. Curr Opin Plant Biol 22:14–21. https://doi.org/10.1016/j.pbi.2014.08.003
Stevenson JM, Perera IY, Heilmann I, Persson S, Boss WF (2000) Inositol signaling and plant growth. Trends Plant Sci 5(8):357–357. https://doi.org/10.1016/s1360-1385(00)01739-8
Szafranska K, Szewczyk R, Janas KM (2014) Involvement of melatonin applied to Vigna radiata L. seeds in plant response to chilling stress. Cent Eur J Biol 9(11):1117–1126. https://doi.org/10.2478/s11535-014-0330-1
Tan WJ, Yang YC, Zhou Y, Huang LP, Xu L, Chen QF, Yu LJ, Xiao S (2018) Diacylglycerol acyltransferase and diacylglycerol kinase modulate triacylglycerol and phosphatidic acid production in the plant response to freezing stress. Plant Physiol 178(3):1424–1425. https://doi.org/10.1104/pp.18.01200
Thompson AJ, Jackson AC, Symonds RC, Mulholland BJ, Dadswell AR, Blake PS, Burbidge A, Taylor IB (2000) Ectopic expression of a tomato 9-cis-epoxycarotenoid dioxygenase gene causes over-production of abscisic acid. Plant J 23(3):363–374. https://doi.org/10.1046/j.1365-313x.2000.00789.x
Turk H, Erdal S, Genisel M, Atici O, Demir Y, Yanmis D (2014) The regulatory effect of melatonin on physiological, biochemical and molecular parameters in cold-stressed wheat seedlings. Plant Growth Regul 74(2):139–152. https://doi.org/10.1007/s10725-014-9905-0
Umezawa T, Nakashima K, Miyakawa T, Kuromori T, Tanokura M, Shinozaki K, Yamaguchi-Shinozaki K (2010) Molecular basis of the core regulatory network in ABA responses: sensing, signaling and transport. Plant Cell Physiol 51(11):1821–1839. https://doi.org/10.1093/pcp/pcq156
Yin P, Fan H, Hao Q, Yuan X, Wu D, Pang Y, Yan C, Li W, Wang J, Yan N (2009) Structural insights into the mechanism of abscisic acid signaling by PYL proteins. Nat Struct Mol Biol 16(12):1230–1236. https://doi.org/10.1038/nsmb.1730
Zhang N, Zhao B, Zhang H-J, Weeda S, Yang C, Yang Z-C, Ren S, Guo Y-D (2013) Melatonin promotes water-stress tolerance, lateral root formation, and seed germination in cucumber (Cucumis sativus L.). J Pineal Res 54(1):15–23. https://doi.org/10.1111/j.1600-079X.2012.01015.x
Zhang H-J, Zhang N, Yang R-C, Wang L, Sun Q-Q, Li D-B, Cao Y-Y, Weeda S, Zhao B, Ren S, Guo Y-D (2014) Melatonin promotes seed germination under high salinity by regulating antioxidant systems, ABA and GA(4) interaction in cucumber (Cucumis sativus L.). J Pineal Res 57(3):269–279. https://doi.org/10.1111/jpi.12167
Zhang J, Zhou MJ, Zhou H, Zhao DD, Gotor C, Romero LC, Shen J, Ge ZL, Zhang Z, Shen WB, Yuan XX, Xie YJ (2021) Hydrogen sulfide, a signaling molecule in plant stress responses. J Integr Plant Biol 63(1):146–160. https://doi.org/10.1111/jipb.13022
Zhao H, Zhang K, Zhou X, Xi L, Wang Y, Xu H, Pan T, Zou Z (2017) Melatonin alleviates chilling stress in cucumber seedlings by up-regulation of CsZat12 and modulation of polyamine and abscisic acid metabolism. Sci Rep. https://doi.org/10.1038/s41598-017-05267-3
Zheng S, Su M, Wang L, Zhang TG, Wang J, Xie HC, Wu XX, Ul Haq SI, Qiu QS (2021) Small signaling molecules in plant response to cold stress. J Plant Physiol 266:153534. https://doi.org/10.1016/j.jplph.2021.153534
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This research was supported by the National Natural Science Foundation of China (No. 31902022), the youth fund of BAAFS (QNJJ201915), the Science and Technology Innovation Capacity Project of BAAFS (KJCX20200212, KJCX20200113).
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HZ, YQ, and PW conceived and designed research. HZ, YJ, and XW conducted experiments, analyzed data, and wrote the manuscript. HZ, XX, and PW modified the paper.
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Zhang, H., Qiu, Y., Ji, Y. et al. Melatonin Promotes Seed Germination via Regulation of ABA Signaling Under Low Temperature Stress in Cucumber. J Plant Growth Regul 42, 2232–2245 (2023). https://doi.org/10.1007/s00344-022-10698-y
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DOI: https://doi.org/10.1007/s00344-022-10698-y