Methyl jasmonate mediates melatonin-induced cold tolerance of grafted watermelon plants

Hao Li , Yanliang Guo , Zhixiang Lan , Kai Xu , Jingjing Chang , Golam Jalal Ahammed , Jianxiang Ma , Chunhua Wei , Xian Zhang

Horticulture Research ›› 2021, Vol. 8 ›› Issue (1) : 57

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Horticulture Research ›› 2021, Vol. 8 ›› Issue (1) :57 DOI: 10.1038/s41438-021-00496-0
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Methyl jasmonate mediates melatonin-induced cold tolerance of grafted watermelon plants
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Abstract

Root–shoot communication has a critical role in plant adaptation to environmental stress. Grafting is widely applied to enhance the abiotic stress tolerance of many horticultural crop species; however, the signal transduction mechanism involved in this tolerance remains unknown. Here, we show that pumpkin- or figleaf gourd rootstock-enhanced cold tolerance of watermelon shoots is accompanied by increases in the accumulation of melatonin, methyl jasmonate (MeJA), and hydrogen peroxide (H2O2). Increased melatonin levels in leaves were associated with both increased melatonin in rootstocks and MeJA-induced melatonin biosynthesis in leaves of plants under cold stress. Exogenous melatonin increased the accumulation of MeJA and H2O2 and enhanced cold tolerance, while inhibition of melatonin accumulation attenuated rootstock-induced MeJA and H2O2 accumulation and cold tolerance. MeJA application induced H2O2 accumulation and cold tolerance, but inhibition of JA biosynthesis abolished rootstock- or melatonin- induced H2O2 accumulation and cold tolerance. Additionally, inhibition of H2O2 production attenuated MeJA-induced tolerance to cold stress. Taken together, our results suggest that melatonin is involved in grafting-induced cold tolerance by inducing the accumulation of MeJA and H2O2. MeJA subsequently increases melatonin accumulation, forming a self-amplifying feedback loop that leads to increased H2O2 accumulation and cold tolerance. This study reveals a novel regulatory mechanism of rootstock-induced cold tolerance.

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Hao Li, Yanliang Guo, Zhixiang Lan, Kai Xu, Jingjing Chang, Golam Jalal Ahammed, Jianxiang Ma, Chunhua Wei, Xian Zhang. Methyl jasmonate mediates melatonin-induced cold tolerance of grafted watermelon plants. Horticulture Research, 2021, 8 (1) : 57 DOI:10.1038/s41438-021-00496-0

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References

[1]

Rahman, A. Auxin: a regulator of cold stress response. Physiol. Plant. 147, 28-35 (2013).

[2]

Guo, X. Y., Liu, D. F. & Chong, K. Cold signaling in plants: Insights into mechanisms and regulation. J. Int. Plant Biol. 60, 745-756 (2018).

[3]

Wilkinson, S. & Davies, W. J. Drought, ozone, ABA and ethylene: new insights from cell to plant to community. Plant Cell Environ. 33, 510-525 (2010).

[4]

Zhou, Y. H. et al. Chill-induced decrease in capacity of RuBP carboxylation and associated H2O2 accumulation in cucumber leaves are alleviated by grafting onto figleaf gourd . Ann. Bot. 100, 839-848 (2007).

[5]

Li, H. et al. Hydrogen peroxide mediates abscisic acid-induced HSP70 accumulation and heat tolerance in grafted cucumber plants. Plant Cell Environ. 37, 2768-2780 (2014).

[6]

Calvo, J. R., González-Yanes, C. & Maldonado, M. D. The role of melatonin in the cells of the innate immunity: a review. J. Pineal Res. 55, 103-120 (2013).

[7]

Dubbels, R. et al. Melatonin in edible plants identified by radioimmunoassay and by high performance liquid chromatography-mass spectrometry. J. Pineal Res. 18, 28-31 (1995).

[8]

Hattori, A. et al. 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 (1995).

[9]

Arnao, M. B. & Hernández-Ruiz, J. Melatonin: plant growth regulator and/or biostimulator during stress? Trends Plant Sci. 19, 789-797 (2014).

[10]

Li, H. et al. Alkanes (C29 and C31)-mediated intracuticular wax accumulation contributes to melatonin- and ABA-induced drought tolerance in watermelon. J. Plant Growth Regul. https://doi.org/10.1007/s00344-020-10099-z (2020).

[11]

Sun, Y. D. et al. Melatonin treatment improves the shelf-life and postharvest quality of table grape (Vitis labrusca L. cv. ‘Fengzao’). J. Berry Res. https://doi.org/10.3233/JBR-200569 (2020).

[12]

Wei, J. et al. Phytomelatonin receptor PMTR1-mediated signaling regulates stomatal closure in Arabidopsis thaliana. J. Pineal Res. 65, e12500 (2018).

[13]

Arnao, M. B. & Hernández-Ruiz, J. Melatonin: a new plant hormone and/or a plant master regulator? Trends Plant Sci. 24, 38-48 (2018).

[14]

Bose, S. K. & Howlader, P. Melatonin plays multifunctional role in horticultural crops against environmental stresses: a review. Environ. Exp. Bot. 176, 104063 (2020).

[15]

Tan, D. X. et al. Novel rhythms of N1-acetyl-N2-formyl-5-methoxykynuramine and its precursor melatonin in water hyacinth: importance for phytoremediation. FASEB J. 21, 1724-1729 (2007).

[16]

Mukherjee, S. et al. 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 (2014).

[17]

Li, H. et al. Local melatonin application induces cold tolerance in distant organs of Citrullus lanatus L. via long distance transport. Sci. Rep. 8, 40858 (2017).

[18]

Huang, H. et al. Jasmonate action in plant growth and development. J. Exp. Bot. 68, 1349-1359 (2017).

[19]

Yu, X. X. et al. The roles of methyl jasmonate to stress in plants. Funct. Plant Biol. 46, 197-212 (2019).

[20]

Hu, Y. et al. Jasmonate regulates the INDUCER OF CBF EXPRESSION-C-REPEAT BINDING FACTOR/DRE BINDING FACTOR1 cascade and freezing tolerance in Arabidopsis. Plant Cell. 25, 2907-2924 (2013).

[21]

Wang, G. et al. Systemic root-shoot signaling drives jasmonate-based root defense against nematodes. Curr. Biol. 29, 3430-3438 (2019).

[22]

Schulze, A. et al. Wound-induced shoot-to-root relocation of JA-Ile precursors coordinates Arabidopsis growth. Mol. Plant. 12, 1383-1394 (2019).

[23]

Rivero, R. M. et al. Resistance to cold and heat stress: accumulation of phenolic compounds in tomato and watermelon plants. Plant Sci. 160, 315-321 (2001).

[24]

Liu, H. Y. et al. Study on relationship between physiological changes and chilling tolerance in grafted watermelon seedlings under low temperature stress. Agric. Sin. Chin. 36, 1325-1329 (2003).

[25]

Shi, X. F. et al. iTRAQ-based quantitative proteomics analysis of cold stress-induced mechanisms in grafted watermelon seedlings. J. Proteom. 192, 311-320 (2019).

[26]

Zhu, J. K. Abiotic stress signaling and responses in plants. Cell 167, 313-324 (2016).

[27]

Davis, A. R. et al. Cucurbit grafting. Crit. Rev. Plant Sci. 27, 50-74 (2008).

[28]

Wen, D. et al. Promoting roles of melatonin in adventitious root development of Solanum lycopersicum L. by regulating auxin and nitric oxide signaling. Front. Plant Sci. 7, 718 (2016).

[29]

Park, W. J. Melatonin as an endogenous plant regulatory signal: debates and perspectives. J. Plant Biol. 54, 143-149 (2011).

[30]

Rajendran, S. K. et al. Differential activation of sporamin expression in response to abiotic mechanical wounding and biotic herbivore attack in the sweet potato. BMC Plant Biol. 14, 112 (2014).

[31]

Xia, X. J. et al. Reactive oxygen species are involved in brassinosteroid-induced stress tolerance in cucumber. Plant Physiol. 150, 801-814 (2009).

[32]

Hong, S. W., Lee, U. & Vierling, E. Arabidopsis hot mutants define multiple functions required for acclimation to high temperatures. Plant Physiol. 132, 757-767 (2003).

[33]

Okazaki, M. & Ezura, H. Profiling of melatonin in the model tomato (Solanum lycopersicum L.) cultivar Micro-Tom. J. Pineal Res. 46, 338-343 (2009).

[34]

Pan, X., Welti, R. & Wang, X. Quantitative analysis of major plant hormones in crude plant extracts by high-performance liquid chromatography-mass spectrometry. Nat. Protoc. 5, 986-992 (2010).

[35]

Bellincampi, D. et al. Extracellular H2O2 induced by oligogalacturonides is not involved in the inhibition of the auxin-regulated rolB gene expression in tobacco leaf explants . Plant Physiol. 122, 1379-1385 (2000).

[36]

Thordal-Christensen, H. et al. Subcellular localization of H2O2 in plants. H2O2 accumulation in papillae and hypersensitive response during the barley-powdery mildew interaction . Plant J. 11, 1187-1194 (1997).

[37]

Kong, Q. S. et al. Identification of suitable reference genes for gene expression normalization in qRT-PCR analysis in watermelon. PLoS ONE 9, e90612 (2014).

[38]

Livak, K. J. & Schmittgen, T. D. Analysis of relative gene expression data using real-time quantitative PCR and the 2−ΔΔCT method . Methods 25, 402-408 (2001).

[39]

Xu, J. H. et al. Comparative transcriptome profiling of chilling stress responsiveness in grafted watermelon seedlings. Plant Physiol. Biochem. 109, 561-570 (2016).

[40]

Liu, J. Y., Shi, Y. T. & Yang, S. H. Insights into the regulation of C-repeat binding factors in plant cold signaling. J. Int. Plant Biol. 60, 780-795 (2018).

[41]

Shi, H. et al. Melatonin induces the transcripts of CBF/DREB1s and their involvement in both abiotic and biotic stresses in Arabidopsis. J. Pineal Res. 59, 334-342 (2015).

[42]

Zhang, N. et al. Roles of melatonin in abiotic stress resistance in plants. J. Exp. Bot. 66, 647-656 (2015).

[43]

Kazan, K. Diverse roles of jasmonates and ethylene in abiotic stress tolerance. Trends Plant Sci. 20, 219-229 (2015).

[44]

Liu, C. X. et al. Melatonin induces disease resistance to Botrytis cinerea in tomato fruit by activating jasmonic acid signaling pathway. J. Agric. Food Chem. 67, 6116-6124 (2019).

[45]

Zhou, J. et al. H2O2 mediates the crosstalk of brassinosteroid and abscisic acid in tomato responses to heat and oxidative stresses . J. Exp. Bot. 65, 4371-4383 (2014).

[46]

Ahammed, G. J. et al. Tomato WRKY81 acts as a negative regulator for drought tolerance by modulating guard cell H2O2-mediated stomatal closure . Environ. Exp. Bot. 171, 103960 (2020).

[47]

Zhang, H. M. & Zhang, Y. Q. Melatonin: a well-documented antioxidant with conditional pro-oxidant actions. J. Pineal Res. 57, 131-146 (2014).

[48]

Gong, B. et al. Hydrogen peroxide produced by NADPH oxidase: a novel downstream signaling pathway in melatonin-induced stress tolerance in Solanum lycopersicum. Physiol. Plant. 160, 396-409 (2017).

[49]

Chen, Z. et al. Hydrogen peroxide acts downstream of melatonin to induce lateral root formation. Ann. Bot. 121, 1127-1136 (2018).

[50]

Suhita, D. et al. Cytoplasmic alkalization precedes reactive oxygen species production during methyl jasmonate-and abscisic acid-induced stomatal closure. Plant Physiol. 134, 1536-1545 (2004).

[51]

Nazir, F., Fariduddin, Q. & Khan, T. A. Hydrogen peroxide as a signalling molecule in plants and its crosstalk with other plant growth regulators under heavy metal stress. Chemosphere 252, 126486 (2020).

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