Please wait a minute...
Journal of Integrative Agriculture  2023, Vol. 22 Issue (8): 2397-2411    DOI: 10.1016/j.jia.2023.07.005
Horticulture Advanced Online Publication | Current Issue | Archive | Adv Search |
Physiological and transcriptome analyses provide new insights into the mechanism mediating the enhanced tolerance of melatonin-treated rhododendron plants to heat stress
XU Yan-xia1, 2#, ZHANG Jing1, WAN Zi-yun1, HUANG Shan-xia1, DI Hao-chen1, HE Ying1, JIN Song-heng1#

1 Jiyang College, Zhejiang A&F University, Zhuji 311800, P.R.China

2 Zhejiang Provincial Key Laboratory of Forest Aromatic Plants-based Healthcare Functions, Zhejiang A&F University, Hangzhou 311300, P.R.China

Download:  PDF in ScienceDirect  
Export:  BibTeX | EndNote (RIS)      

杜鹃花是杜鹃花属的总称,是具有很高的观赏和经济价值的著名木本植物。热胁迫是影响杜鹃花生长的主要环境因子。褪黑素近年来被报道可以缓解非生物胁迫对植物的影响。然而,褪黑素在杜鹃花中的作用尚不清楚。本研究探讨了褪黑素对热胁迫下杜鹃花的影响及其潜在机制。叶绿素荧光结果表明,喷施200 µmol L-1褪黑素对杜鹃花抵抗热胁迫效果最佳。为了阐明褪黑素如何限制高温的不利影响,本研究分别在25、35和40°C处理下分析了杜鹃花叶片中褪黑素含量、光合参数、Rubisco酶活性和ATP含量。结果表明,与对照相比,外源喷施褪黑素提高了杜鹃花叶片中褪黑素含量、热应激下的电子传递速率、光系统II和I活性、Rubisco酶活性和ATP含量。转录组分析结果表明,许多热胁迫下的差异表达基因富集在光合作用途径,这些基因中的大部分均在热处理后下调表达,且在无褪黑素处理的植株中下调幅度大于外源喷施褪黑素处理的植株。本研究鉴定出RhPGR5ARhATPBRhLHCB3RhRbsA作为关键基因。综合以上结果,我们推测褪黑素通过调控包括RhRbsA在内的特定基因的表达,促进光合电子传递,提高卡尔文循环酶活性,增加ATP的产生,由此提高了热应激下的光合效率和CO2同化能力。因此,施用外源褪黑素可提高杜鹃花对热胁迫的耐受性。


Rhododendron is a well-known genus consisting of commercially valuable ornamental woody plant species.  Heat stress is a major environmental factor that affects rhododendron growth.  Melatonin was recently reported to alleviate the effects of abiotic stress on plants.  However, the role of melatonin in rhododendron plants is unknown.  In this study, the effect of melatonin on rhododendron plants exposed to heat stress and the potential underlying mechanism were investigated.  Analyses of morphological characteristics and chlorophyll a fluorescence indicated 200 µmol L–1 was the optimal melatonin concentration for protecting rhododendron plants from heat stress.  To elucidate how melatonin limits the adverse effects of high temperatures, melatonin contents, photosynthetic indices, Rubisco activity, and adenosine triphosphate (ATP) contents were analyzed at 25, 35, and 40°C, respectively.  Compared with the control, exogenous application of melatonin improved the melatonin contents, electron transport rate, photosystem II and I activities, Rubisco activity, and ATP contents under heat stress.  The transcriptome analysis revealed many of the heat-induced differentially expressed genes were associated with the photosynthetic pathway; the expression of most of these genes was down-regulated by heat stress more in the melatonin-free plants than in the melatonin-treated plants.  We identified RhPGR5A, RhATPB, RhLHCB3, and RhRbsA as key genes.  Thus, we speculate that melatonin promotes photosynthetic electron transport, improves Calvin cycle enzyme activities, and increases ATP production.  These changes lead to increased photosynthetic efficiency and CO2 assimilation under heat stress conditions via the regulated expression of specific genes, including RhRbsA.  Therefore, the application of exogenous melatonin may increase the tolerance of rhododendron to heat stress.

Keywords:  ornamental woody        high temperature        stress        melatonin        photosynthesis  
Received: 09 February 2023   Accepted: 01 June 2023

This work was financially supported by the Shaoxing "Hometown of Celebrities" Talent Program (RC2022B05), Talent Startup Program of Jiyang College of Zhejiang Agriculture and Forestry University (RQ2020B15) and the Scientific Research Training Program of Jiyang College of Zhejiang Agriculture and Forestry University (JYKC2227).

About author:  #Correspondence XU Yan-xia, E-mail:; JIN Song-heng, E-mail:

Cite this article: 

XU Yan-xia, ZHANG Jing, WAN Zi-yun, HUANG Shan-xia, DI Hao-chen, HE Ying, JIN Song-heng. 2023. Physiological and transcriptome analyses provide new insights into the mechanism mediating the enhanced tolerance of melatonin-treated rhododendron plants to heat stress. Journal of Integrative Agriculture, 22(8): 2397-2411.

Ahammed G J, Xu W, Liu A, Chen S. 2018. COMT1 silencing aggravates heat stress-induced reduction in photosynthesis by decreasing chlorophyll content, photosystem II activity, and electron transport efficiency in tomato. Frontiers in Plant Science9, 998.

Alric J, Johnson X. 2017. Alternative electron transport pathways in photosynthesis: A confluence of regulation. Current Opinion in Plant Biology37, 78–86.

Arnao M B, Hernandez-Ruiz J. 2014. Melatonin: Plant growth regulator and/or biostimulator during stress? Trends in Plant Science19, 789–797.

Arnao M B, Hernández-Ruiz J. 2020. Melatonin in flowering, fruit set and fruit ripening. Plant Reproduction33, 77–87.

Arnao M B, Hernández-Ruiz J. 2021. Melatonin against environmental plant stressors: A review. Current Protein & Peptide Science22, 413–429.

Bose S K, Howlader P. 2020. Melatonin plays multifunctional role in horticultural crops against environmental stresses: A review. Environmental and Experimental Botany176, 104063.

Buttar Z A, Wu S N, Arnao M B, Wang C, Ullah I, Wang C. 2020. Melatonin suppressed the heat stress-induced damage in wheat seedlings by modulating the antioxidant machinery. Plants9, 809.

Caniato R, Filippini R, Piovan A, Puricelli L, Borsarini A, Cappelletti E M. 2003. Melatonin in plants. Advances in Experimental Medicine and Biology527, 593–597.

Chen S G, Yang J, Zhang M S, Strasser R J, Qiang S. 2016. Classification and characteristics of heat tolerance in Ageratina adenophora populations using fast chlorophyll a fluorescence rise O-J-I-P. Environmental and Experimental Botany122, 126–140.

Commisso M, Negri S, Gecchele E, Fazion E, Pontoriero C, Avesani L, Guzzo F. 2022. Indolamine accumulation and TDC/T5H expression profiles reveal the complex and dynamic regulation of serotonin biosynthesis in tomato (Solanum lycopersicum L.). Frontiers in Plant Science13, 975434.

Curien G, Flori S, Villanova V, Magneschi L, Giustini C, Forti G, Matringe M, Petroutsos D, Kuntz M, Finazzi G. 2016. The water to water cycles in microalgae. Plant and Cell Physiology57, 1354–1363.

DalCorso G, Pesaresi P, Masiero S, Aseeva E, Schünemann D, Finazzi G, Joliot P, Barbato R, Leister D. 2008. A complex containing PGRL1 and PGR5 is involved in the switch between linear and cyclic electron flow in ArabidopsisCell132, 273–285.

Damkjaer J T, Kereiche S, Johnson M P, Kovacs L, Kiss A Z, Boekema E J, Jansson S. 2009. The photosystem II light-harvesting protein Lhcb3 affects the macrostructure of photosystem II and the rate of state transitions in ArabidopsisThe Plant Cell21, 3245–3256.

Dastmalchi M. 2020. A role for melatonin in the defense of sweet oranges against citrus greening disease. Plant Physiology184, 1633–1634.

Geng X M, Yang Q Y, Yue Y, Ozaki Y. 2019. Effects of high temperature on photosynthesis, membrane lipid peroxidation and osmotic adjustment in four Rhododendron species. Journal of the Faculty of Agriculture Kyushu University64, 33–38.

Ilíková I, Ilík P, Opatíková M, Arshad R, Nosek L, Karlický V, Kučerová Z, Roudnický P, Pospíšil P, Lazár D, Bartoš J, Kouřil R. 2021. Towards spruce-type photosystem II: consequences of the loss of light-harvesting proteins LHCB3 and LHCB6 in Arabidopsis. Plant Physiology187, 2691–2715.

Jahan M S, Guo S R, Sun J, Shu S, Wang Y, El-Yazied A A, Alabdallah N M, Hikal M, Mohamed M H, Ibrahim M F M, Hasan M M. 2021. Melatonin-mediated photosynthetic performance of tomato seedlings under high-temperature stress. Plant Physiology and Biochemistry167, 309–320.

Jahan M S, Shu S, Wang Y, Chen Z, He M, Tao M, Sun J, Guo S. 2019. Melatonin alleviates heat-induced damage of tomato seedlings by balancing redox homeostasis and modulating polyamine and nitric oxide biosynthesis. BMC Plant Biology19, 414.

Li H, Guo Y, Lan Z, Zhang Z, Ahammed G J, Chang J, Zhang Y, Wei C, Zhang X. 2021. Melatonin antagonizes ABA action to promote seed germination by regulating Ca2+ efflux and H2O2 accumulation. Plant Science303, 110761.

Li N, Euring D J, Cha J Y, Lin Z, Lu M Z, Huang L J, Kim W Y. 2021. Plant hormone-mediated regulation of heat tolerance in response to global climate change. Frontiers in Plant Science11, 627969.

Li Z G, Xu Y, Bai L K, Zhang S Y, Wang Y. 2019. Melatonin enhances thermotolerance of maize seedlings (Zea mays L.) by modulating antioxidant defense, methylglyoxal detoxification, and osmoregulation systems. Protoplasma256, 471–490.

Liang D, Shen Y, Ni Z, Wang Q, Lei Z, Xu N, Deng Q, Lin L, Wang J, Lv X, Xia H. 2018. Exogenous melatonin application delays senescence of kiwifruit leaves by regulating the antioxidant capacity and biosynthesis of flavonoids. Frontiers in Plant Science9, 426.

Liu X Z, Huang B R. 2008. Photosynthetic acclimation to high temperatures associated with heat tolerance in creeping bentgrass. Journal of Plant Physiology165, 1947–1953.

Lv Y, Pan J, Wang H, Reiter R J, 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. Journal of Pineal Research70, e12736.

Munekage Y, Hojo M, Meurer J, Endo T, Tasaka M, Shikanai T. 2002. PGR5 is involved in cyclic electron flow around photosystem I and is essential for photoprotection in ArabidopsisCell110, 361–371.

Naohiko O, Hikaru S, Kazuo S, Kazuko Y S. 2017. Transcriptional regulatory network of plant heat stress response, Trends in Plant Science22, 53–65.

Nosaka Y, Nosaka A Y. 2017. Generation and detection of reactive oxygen species in photocatalysis. Chemical Reviews117, 11302–11336.

Pelagio-Flores R, Muñoz-Parra E, Ortiz-Castro R, López-Bucio J. 2012. Melatonin regulates Arabidopsis root system architecture likely acting independently of auxin signaling. Journal of Pineal Research, 53, 279–288.

Pietrzykowska M, Suorsa M, Semchonok D A, Tikkanen M, Boekema E J, Aro E M, Jansson S. 2014. The light-harvesting chlorophyll a/b binding proteins Lhcb1 and Lhcb2 play complementary roles during state transitions in ArabidopsisThe Plant Cell26, 3646–3660.

De Riek J, De Keyser E, Calsyn E, Eeckhaut T, Van Huylenbroeck J, Kobayashi N. 2018. Azalea. In: Van Huylenbroeck J. ed., Ornamental Crops. Springer, Cham. pp. 237–271.

De Ronde J A, Cress W A, Krüger G H J, Strasser R J, Van Staden J. 2004. Photosynthetic response of transgenic soybean plants, containing an Arabidopsis P5CR gene, during heat and drought stress. Journal of Plant Physiology161, 1211–1224.

Sharkey T D. 2005. Effects of moderate heat stress on photosynthesis: Importance of thylakoid reactions, rubisco deactivation, reactive oxygen species, and thermotolerance provided by isoprene. Plant Cell and Environment28, 269–277.

Shi H T, Tan D X, Reiter R J, Ye T T, Yang F, Chan Z L. 2015. Melatonin induces class A1 heat-shock factors (HSFA1s) and their possible involvement of thermotolerance in ArabidopsisJournal of Pineal Research58, 335–342.

Strasser R J, Tsimilli-Michael M, Qiang S, Goltsev V. 2010. Simultaneous in vivo recording of prompt and delayed fluorescence and 820-nm reflection changes during drying and after rehydration of the resurrection plant Haberlea rhodopensisBiochimica et Biophysica Acta1797, 1313–1326

Sun C, Liu L, Wang L, Li B, Jin C, Lin X J. 2021. Melatonin: A master regulator of plant development and stress responses. Journal of Integrative Plant Biology63, 126–145.

Tan D X, Hardeland R, Manchester L C, Korkmaz A, Ma S, Rosales-Corral S, Reiter R J. 2012. Functional roles of melatonin in plants, and perspectives in nutritional and agricultural science. Journal of Experimental Botany63, 577–597.

Tan X L, Fan Z Q, Kuang J F, Lu W J, Reiter R J, Lakshmanan P, Su X G, Zhou J, Chen J Y, Shan W J, Pineal R. 2019. Melatonin delays leaf senescence of Chinese flowering cabbage by suppressing ABFs-mediated abscisic acid biosynthesis and chlorophyll degradation. Journal of Pineal Research67, e12570.

Tiwari R K, Lal M K, Kumar R, Mangal V, Altaf M A, Sharma S, Singh B, Kumar M. 2022. Insight into melatonin-mediated response and signaling in the regulation of plant defense under biotic stress. Plant Molecular Biology109, 385–399.

Tsunoda Y, Hano S, Imoto N, Shibuya T, Ikeda H, Amagaya K, Kato K, Shirakawa H, Aso H, Kanayama Y. 2021. Physiological roles of tryptophan decarboxylase revealed by overexpression of SlTDC1 in tomato. Scientia Horticulturae275,109672.

Wahid A, Gelani S, Ashraf M, Foolad M R. 2007. Heat tolerance in plants. An overview. Environmental and Experimental Botany61, 199–223.

Wang D, Chen Q Y, Chen W W, Guo Q G, Xia Y, Wang S M, Jing D L, Liang G L. 2021. Physiological and transcription analyses reveal the regulatory mechanism of melatonin in inducing drought resistance in loquat (Eriobotrya japonica Lindl.) seedlings. Environmental and Experimental Botany181, 104291.

Wang S Y, Shi X C, Wang R, Wang H L, Liu F, Laborda P. 2020. Melatonin in fruit production and postharvest preservation: A review. Food Chemistry320, 126642.

Wang X, Li Z, Liu B, Zhou H, Elmongy M S, Xia Y. 2020. Combined proteome and transcriptome analysis of heat-primed azalea reveals new insights into plant heat acclimation memory. Frontiers in Plant Science11, 1278.

Wang X Y, Liu Y, Li H X, Wang F, Xia P X, Li W, Zhang X C, Zhang N, Guo Y D. 2022. SlSNAT2, a chloroplast-localized acetyltransferase, is involved in Rubisco lysine acetylation and negatively regulates drought stress tolerance in tomato. Environmental and Experimental Botany201, 105003.

Wang X Y, Zhang H J , Xie Q, Liu Y, Lv H M, Bai R Y , Ma R, Li X D, Zhang X C , Guo Y D, Zhang N. 2020. SlSNAT interacts with HSP40, a molecular chaperone, to regulate melatonin biosynthesis and promote thermotolerance in tomato. Plant and Cell Physiology61, 909–921.

Xing X J, Ding Y R, Jin J Y, Song A P, Chen S M, Chen F D, Fang W M, Jiang J F. 2021. Physiological and transcripts analyses reveal the mechanism by which melatonin alleviates heat stress in chrysanthemum seedlings. Frontiers in Plant Science12, 673236.

Xu Y X, Lei Y S, Huang S X, Zhang J, Wan Z Y, Zhu X T, Jin S H. 2022. Combined de novo transcriptomic and physiological analyses reveal RyALS3-mediated aluminum tolerance in Rhododendron yunnanense Franch. Frontiers in Plant Science13, 951003.

Xu Y X, Xiao M Z, Liu Y, Fu J L, He Y, Jiang D A. 2017. The small auxin-up RNA OsSAUR45 affects auxin synthesis and transport in rice. Plant Molecular Biology94, 97–107.

Xu Y X, Zhang S N, Guo H P, Wang S K, Xu L G, Li C Y, Qian Q, Chen F, Geisler M, Qi Y H, Jiang D A. 2014. OsABCB14 functions in auxin transport and iron homeostasis in rice (Oryza sativa L.). Plant Journal79, 106–123.

Yang F S, Nie S, Liu H, Shi T L, Tian X C, Zhou S S, Bao Y T, Jia K H, Guo J F, Zhao W, An N, Zhang R G, Yun Q Z, Wang X Z, Mannapperuma C, Porth I, El-Kassaby Y A, Street N R, Wang X R, Yves V D P, et al. 2020. Chromosome-level genome assembly of a parent species of widely cultivated azaleas. Nature Communications11, 5269.

Zhao J G, Lu Z G, Wang L, Jin B. 2020. Plant responses to heat stress: Physiology, transcription, noncoding RNAs, and epigenetics. International Journal of Molecular Sciences22, 117.

[1] WU Han-yu, QIAO Mei-yu, ZHANG Wang-feng, WANG Ke-ru, LI Shao-kun, JIANG Chuang-dao. Systemic regulation of photosynthetic function in maize plants at graining stage under vertically heterogeneous light environment[J]. >Journal of Integrative Agriculture, 2022, 21(3): 666-676.
[2] WANG Yi-bo, HUANG Rui-dong, ZHOU Yu-fei. Effects of shading stress during the reproductive stages on photosynthetic physiology and yield characteristics of peanut (Arachis hypogaea Linn.)[J]. >Journal of Integrative Agriculture, 2021, 20(5): 1250-1265.
[3] Iram SHAFIQ, Sajad HUSSAIN, Muhammad Ali RAZA, Nasir IQBAL, Muhammad Ahsan ASGHAR, Ali RAZA, FAN Yuan-fang, Maryam MUMTAZ, Muhammad SHOAIB, Muhammad ANSAR, Abdul MANAF, YANG Wen-yu, YANG Feng. Crop photosynthetic response to light quality and light intensity[J]. >Journal of Integrative Agriculture, 2021, 20(1): 4-23.
[4] JIA Teng-jiao, LI Jing-jing, WANG Li-feng, CAO Yan-yong, MA Juan, WANG Hao, ZHANG Deng-feng, LI Hui-yong. Evaluation of drought tolerance in ZmVPP1-overexpressing transgenic inbred maize lines and their hybrids[J]. >Journal of Integrative Agriculture, 2020, 19(9): 2177-2187.
[5] YE Yu-xiu, WEN Zhang-rong, YANG Huan, LU Wei-ping, LU Da-lei. Effects of post-silking water deficit on the leaf photosynthesis and senescence of waxy maize[J]. >Journal of Integrative Agriculture, 2020, 19(9): 2216-2228.
[6] WANG Yi-fan, LIAO Yu-qiu, WANG Ya-peng, YANG Jiang-wei, ZHANG Ning, SI Huai-jun. Genome-wide identification and expression analysis of StPP2C gene family in response to multiple stresses in potato (Solanum tuberosum L.)[J]. >Journal of Integrative Agriculture, 2020, 19(6): 1609-1624.
[7] WEN Bing-xiao, Sajad Hussain, YANG Jia-yue, WANG Shan, ZHANG Yi, QIN Si-si, XU Mei, YANG Wen-yu, LIU Wei-guo. Rejuvenating soybean (Glycine max L.) growth and development through slight shading stress[J]. >Journal of Integrative Agriculture, 2020, 19(10): 2439-2450.
[8] ZHANG He, LI Yan1, MENG Ya-li, CAO Nan, LI Duan-sheng, ZHOU Zhi-guo, CHEN Bing-lin, DOU Fu-gen .
The effects of soil moisture and salinity as functions of groundwater depth on wheat growth and yield in coastal saline soils
[J]. >Journal of Integrative Agriculture, 2019, 18(11): 2472-2482.
[9] Hafiz Ghulam Muhu-Din Ahmed, Abdus Salam khan, LI Ming-ju, Sultan Habibullah Khan, Muhammad Kashif . Early selection of bread wheat genotypes using morphological and photosynthetic attributes conferring drought tolerance[J]. >Journal of Integrative Agriculture, 2019, 18(11): 2483-2491.
[10] ZHANG Yi, SHI Yu, GONG Hai-jun, ZHAO Hai-liang, LI Huan-li, HU Yan-hong, WANG Yi-chao. Beneficial effects of silicon on photosynthesis of tomato seedlings under water stress[J]. >Journal of Integrative Agriculture, 2018, 17(10): 2151-2159.
[11] ZHOU Yan, DIAO Ming, CUI Jin-xia, CHEN Xian-jun, WEN Ze-lin, ZHANG Jian-wei, LIU Hui-ying. Exogenous GSH protects tomatoes against salt stress by modulating photosystem II efficiency, absorbed light allocation and H2O2- scavenging system in chloroplasts[J]. >Journal of Integrative Agriculture, 2018, 17(10): 2257-2272.
No Suggested Reading articles found!