Differential roles of melatonin in plant‐host resistance and pathogen suppression in cucurbits

Mandal, Mihir Kumar; Suren, Haktan; Ward, Brian; Boroujerdi, Arezue; Kousik, Chandrasekar

doi:10.1111/jpi.12505

Title: Differential roles of melatonin in plant‐host resistance and pathogen suppression in cucurbits

Journal Article · Wed Jun 06 00:00:00 EDT 2018 · Journal of Pineal Research

DOI:https://doi.org/10.1111/jpi.12505· OSTI ID:1440803

Mandal, Mihir Kumar ^[1]; Suren, Haktan ^[2]; Ward, Brian ^[3]; Boroujerdi, Arezue ^[4]; Kousik, Chandrasekar ^[5]

USDA ARS, U.S. Vegetable Laboratory Charleston SC USA, ORISE Participant sponsored by the U.S. Vegetable Laboratory USDA, ARS Charleston SC USA
Department of Forest Resources and Environmental Conservation Virginia Tech Blacksburg VA USA
Clemson University, CREC Charleston SC USA
Department of Chemistry Claflin University Orangeburg SC USA
USDA ARS, U.S. Vegetable Laboratory Charleston SC USA

Abstract Since the 1950s, research on the animal neurohormone, melatonin, has focused on its multiregulatory effect on patients suffering from insomnia, cancer, and Alzheimer’s disease. In plants, melatonin plays major role in plant growth and development, and is inducible in response to diverse biotic and abiotic stresses. However, studies on the direct role of melatonin in disease suppression and as a signaling molecule in host‐pathogen defense mechanism are lacking. This study provides insight on the predicted biosynthetic pathway of melatonin in watermelon ( Citrullus lanatus ), and how application of melatonin, an environmental‐friendly immune inducer, can boost plant immunity and suppress pathogen growth where fungicide resistance and lack of genetic resistance are major problems. We evaluated the effect of spray‐applied melatonin and also transformed watermelon plants with the melatonin biosynthetic gene SNAT (serotonin N‐acetyltransferase) to determine the role of melatonin in plant defense. Increased melatonin levels in plants were found to boost resistance against the foliar pathogen Podosphaera xanthii (powdery mildew), and the soil‐borne oomycete Phytophthora capsici in watermelon and other cucurbits. Further, transcriptomic data on melatonin‐sprayed (1 mmol/L) watermelon leaves suggest that melatonin alters the expression of genes involved in both PAMP ‐mediated (pathogen‐associated molecular pattern) and ETI ‐mediated (effector‐triggered immunity) defenses. Twenty‐seven upregulated genes were associated with constitutive defense as well as initial priming of the melatonin‐induced plant resistance response. Our results indicate that developing strategies to increase melatonin levels in specialty crops such as watermelon can lead to resistance against diverse filamentous pathogens.

View Accepted Manuscript (Publisher)

Cite

Export

Save

Sponsoring Organization:: USDOE

OSTI ID:: 1440803

Journal Information:: Journal of Pineal Research, Journal Name: Journal of Pineal Research Vol. 65 Journal Issue: 3; ISSN 0742-3098

Publisher:: Wiley-BlackwellCopyright Statement

Country of Publication:: United States

Language:: English

Citation Metrics:

Cited by: 75 works

Citation information provided by
Web of Science

References (81)

Functional roles of melatonin in plants, and perspectives in nutritional and agricultural science Tan, D. -X.; Hardeland, R.; Manchester, L. C. Journal of Experimental Botany, Vol. 63, Issue 2 https://doi.org/10.1093/jxb/err256	journal	October 2011
The draft genome of watermelon (Citrullus lanatus) and resequencing of 20 diverse accessions Guo, Shaogui; Zhang, Jianguo; Sun, Honghe Nature Genetics, Vol. 45, Issue 1 https://doi.org/10.1038/ng.2470	journal	November 2012
Melatonin-induced CBF/DREB1s are essential for diurnal change of disease resistance and CCA1 expression in Arabidopsis Shi, Haitao; Wei, Yunxie; He, Chaozu Plant Physiology and Biochemistry, Vol. 100 https://doi.org/10.1016/j.plaphy.2016.01.018	journal	March 2016
The efficacy and safety of exogenous melatonin for primary sleep disorders a meta-analysis Buscemi, Nina; Vandermeer, Ben; Hooton, Nicola Journal of General Internal Medicine, Vol. 20, Issue 12 https://doi.org/10.1111/j.1525-1497.2005.0243.x	journal	December 2005
High-throughput functional annotation and data mining with the Blast2GO suite Gotz, S.; Garcia-Gomez, J. M.; Terol, J. Nucleic Acids Research, Vol. 36, Issue 10 https://doi.org/10.1093/nar/gkn176	journal	April 2008
Melatonin as a Potent and Inducible Endogenous Antioxidant: Synthesis and Metabolism Tan, Dun-Xian; Manchester, Lucien; Esteban-Zubero, Eduardo Molecules, Vol. 20, Issue 10 https://doi.org/10.3390/molecules201018886	journal	October 2015
Melatonin Attenuates Potato Late Blight by Disrupting Cell Growth, Stress Tolerance, Fungicide Susceptibility and Homeostasis of Gene Expression in Phytophthora infestans Zhang, Shumin; Zheng, Xianzhe; Reiter, Russel J. Frontiers in Plant Science, Vol. 8 https://doi.org/10.3389/fpls.2017.01993	journal	November 2017
Melatonin: Signaling mechanisms of a pleiotropic agent Hardeland, Rüdiger BioFactors, Vol. 35, Issue 2 https://doi.org/10.1002/biof.23	journal	March 2009
Fast and accurate short read alignment with Burrows-Wheeler transform Li, H.; Durbin, R. Bioinformatics, Vol. 25, Issue 14 https://doi.org/10.1093/bioinformatics/btp324	journal	May 2009
Phytoremediative Capacity of Plants Enriched with Melatonin Tan, Dun-Xian; Manchester, Lucien C.; Helton, Pat Plant Signaling & Behavior, Vol. 2, Issue 6 https://doi.org/10.4161/psb.2.6.4639	journal	November 2007
Activation of MKK9-MPK3/MPK6 enhances phosphate acquisition in Arabidopsis thaliana Lei, Lei; Li, Yuan; Wang, Qian New Phytologist, Vol. 203, Issue 4 https://doi.org/10.1111/nph.12872	journal	May 2014
Melatonin Reiter, Russel J.; Tan, Dun-Xian Annals of the New York Academy of Sciences, Vol. 957, Issue 1 https://doi.org/10.1111/j.1749-6632.2002.tb02938.x	journal	May 2002
Melatonin as a signal molecule triggering defense responses against pathogen attack in Arabidopsis and tobacco Lee, Hyoung Yool; Byeon, Yeong; Back, Kyoungwhan Journal of Pineal Research, Vol. 57, Issue 3 https://doi.org/10.1111/jpi.12165	journal	August 2014
Melatonin and its potential biological functions in the fruits of sweet cherry Zhao, Yu; Tan, Dun-Xian; Lei, Qiong Journal of Pineal Research, Vol. 55, Issue 1 https://doi.org/10.1111/jpi.12044	journal	March 2013
Pineal Melatonin: Cell Biology of Its Synthesis and of Its Physiological Interactions* Reiter, Russel J. Endocrine Reviews, Vol. 12, Issue 2 https://doi.org/10.1210/edrv-12-2-151	journal	May 1991
A glutathione S -transferase gene from Lilium regale Wilson confers transgenic tobacco resistance to Fusarium oxysporum Han, Qing; Chen, Rui; Yang, Ye Scientia Horticulturae, Vol. 198 https://doi.org/10.1016/j.scienta.2015.11.047	journal	January 2016
Melatonin regulates carbohydrate metabolism and defenses against Pseudomonas syringae pv. tomato DC3000 infection in Arabidopsis thaliana Zhao, Hongbo; Xu, Lingfei; Su, Tao Journal of Pineal Research, Vol. 59, Issue 1 https://doi.org/10.1111/jpi.12245	journal	June 2015
Identification of glutathione S-transferase genes responding to pathogen infestation in Populus tomentosa Liao, Weihua; Ji, Lexiang; Wang, Jia Functional & Integrative Genomics, Vol. 14, Issue 3 https://doi.org/10.1007/s10142-014-0379-y	journal	May 2014
Melatonin and its relationship to plant hormones Arnao, M. B.; Hernández-Ruiz, J. Annals of Botany, Vol. 121, Issue 2 https://doi.org/10.1093/aob/mcx114	journal	October 2017
Melatonin in Chinese medicinal herbs Chen, Guofang; Huo, Yushu; Tan, Dun-Xian Life Sciences, Vol. 73, Issue 1 https://doi.org/10.1016/S0024-3205(03)00252-2	journal	May 2003
Cloning and functional characterization of the Arabidopsis N -acetylserotonin O -methyltransferase responsible for melatonin synthesis Byeon, Yeong; Lee, Hye-Jung; Lee, Hyoung Yool Journal of Pineal Research, Vol. 60, Issue 1 https://doi.org/10.1111/jpi.12289	journal	November 2015
Melatonin induces nitric oxide and the potential mechanisms relate to innate immunity against bacterial pathogen infection in Arabidopsis Shi, Haitao; Chen, Yinhua; Tan, Dun-Xian Journal of Pineal Research, Vol. 59, Issue 1 https://doi.org/10.1111/jpi.12244	journal	May 2015
Phytophthora infestans RXLR Effector PexRD2 Interacts with Host MAPKKKε to Suppress Plant Immune Signaling King, Stuart R. F.; McLellan, Hazel; Boevink, Petra C. The Plant Cell, Vol. 26, Issue 3 https://doi.org/10.1105/tpc.113.120055	journal	March 2014
The efficacy and safety of melatonin in concurrent chemotherapy or radiotherapy for solid tumors: a meta-analysis of randomized controlled trials Wang, Ye-min; Jin, Bao-zhe; Ai, Fang Cancer Chemotherapy and Pharmacology, Vol. 69, Issue 5 https://doi.org/10.1007/s00280-012-1828-8	journal	January 2012
Chemical stress by different agents affects the melatonin content of barley roots Arnao, Marino B.; Hernández-Ruiz, Josefa Journal of Pineal Research, Vol. 46, Issue 3 https://doi.org/10.1111/j.1600-079X.2008.00660.x	journal	April 2009
Melatonin as an antioxidant and its semi-lunar rhythm in green macroalga Ulva sp. Tal, O.; Haim, A.; Harel, O. Journal of Experimental Botany, Vol. 62, Issue 6 https://doi.org/10.1093/jxb/erq378	journal	January 2011
Evaluation of Watermelon and Related Species for Resistance to Race 1W Powdery Mildew Davis, Angela R.; Levi, Amnon; Tetteh, Antonia Journal of the American Society for Horticultural Science, Vol. 132, Issue 6 https://doi.org/10.21273/JASHS.132.6.790	journal	November 2007
Effects of melatonin on oxidative stress, and resistance to bacterial, parasitic, and viral infections: A review Vielma, José Ramón; Bonilla, Ernesto; Chacín-Bonilla, Leonor Acta Tropica, Vol. 137 https://doi.org/10.1016/j.actatropica.2014.04.021	journal	September 2014
High-throughput tissue extraction protocol for NMR- and MS-based metabolomics Wu, Huifeng; Southam, Andrew D.; Hines, Adam Analytical Biochemistry, Vol. 372, Issue 2 https://doi.org/10.1016/j.ab.2007.10.002	journal	January 2008
Melatonin and the theories of aging: a critical appraisal of melatonin's role in antiaging mechanisms Hardeland, Rüdiger Journal of Pineal Research, Vol. 55, Issue 4 https://doi.org/10.1111/jpi.12090	journal	September 2013
Resistance to Phytophthora Fruit Rot of Watermelon Caused by Phytophthora capsici in U.S. Plant Introductions Kousik, Chandrasekar S.; Ikerd, Jennifer L.; Wechter, Patrick HortScience, Vol. 47, Issue 12 https://doi.org/10.21273/HORTSCI.47.12.1682	journal	December 2012
Growth conditions determine different melatonin levels in Lupinus albus L Arnao, Marino B.; Hernández-Ruiz, Josefa Journal of Pineal Research, Vol. 55, Issue 2 https://doi.org/10.1111/jpi.12055	journal	April 2013
Functions of melatonin in plants: a review Arnao, Marino B.; Hernández-Ruiz, Josefa Journal of Pineal Research, Vol. 59, Issue 2 https://doi.org/10.1111/jpi.12253	journal	June 2015
Melatonin for Sleep Disorders and Cognition in Dementia: A Meta-Analysis of Randomized Controlled Trials Xu, Jing; Wang, Li-Ling; Dammer, Eric B. American Journal of Alzheimer's Disease & Other Dementiasr, Vol. 30, Issue 5 https://doi.org/10.1177/1533317514568005	journal	January 2015
Melatonin, the circadian multioscillator system and health: the need for detailed analyses of peripheral melatonin signaling: Melatonin and peripheral oscillators Hardeland, Rüdiger; Madrid, Juan Antonio; Tan, Dun-Xian Journal of Pineal Research, Vol. 52, Issue 2 https://doi.org/10.1111/j.1600-079X.2011.00934.x	journal	October 2011
Arabidopsis Transcriptome Analysis Reveals Key Roles of Melatonin in Plant Defense Systems Weeda, Sarah; Zhang, Na; Zhao, Xiaolei PLoS ONE, Vol. 9, Issue 3 https://doi.org/10.1371/journal.pone.0093462	journal	March 2014
The mammalian pineal gland: known facts, unknown facets Maronde, Erik; Stehle, Jörg H. Trends in Endocrinology & Metabolism, Vol. 18, Issue 4 https://doi.org/10.1016/j.tem.2007.03.001	journal	May 2007
Phytomelatonin: Assisting Plants to Survive and Thrive Reiter, Russel; Tan, Dun-Xian; Zhou, Zhou Molecules, Vol. 20, Issue 4 https://doi.org/10.3390/molecules20047396	journal	April 2015
Arabidopsis serotonin N -acetyltransferase knockout mutant plants exhibit decreased melatonin and salicylic acid levels resulting in susceptibility to an avirulent pathogen Lee, Hyoung Yool; Byeon, Yeong; Tan, Dun-Xian Journal of Pineal Research, Vol. 58, Issue 3 https://doi.org/10.1111/jpi.12214	journal	February 2015
Melatonin is required for H ₂ O ₂ - and NO-mediated defense signaling through MAPKKK3 and OXI1 in Arabidopsis thaliana Lee, Hyoung Yool; Back, Kyoungwhan Journal of Pineal Research, Vol. 62, Issue 2 https://doi.org/10.1111/jpi.12379	journal	December 2016
Melatonin in higher plants: occurrence and possible functions Kolář, Jan; Macháčková, Ivana Journal of Pineal Research, Vol. 39, Issue 4 https://doi.org/10.1111/j.1600-079X.2005.00276.x	journal	November 2005
Efficient CRISPR/Cas9-based gene knockout in watermelon Tian, Shouwei; Jiang, Linjian; Gao, Qiang Plant Cell Reports, Vol. 36, Issue 3 https://doi.org/10.1007/s00299-016-2089-5	journal	December 2016
Cloning and characterization of the serotonin N -acetyltransferase-2 gene ( SNAT2 ) in rice ( Oryza sativa ) Byeon, Yeong; Lee, Hyoung Yool; Back, Kyoungwhan Journal of Pineal Research, Vol. 61, Issue 2 https://doi.org/10.1111/jpi.12339	journal	May 2016
The oomycete broad-host-range pathogen Phytophthora capsici: Phytophthora capsici Lamour, Kurt H.; Stam, Remco; Jupe, Julietta Molecular Plant Pathology, Vol. 13, Issue 4 https://doi.org/10.1111/j.1364-3703.2011.00754.x	journal	October 2011
Melatonin in plant organs Van Tassel, David L.; Roberts, Nicholas; Lewy, Alfred Journal of Pineal Research, Vol. 31, Issue 1 https://doi.org/10.1034/j.1600-079X.2001.310102.x	journal	August 2001
edgeR: a Bioconductor package for differential expression analysis of digital gene expression data Robinson, M. D.; McCarthy, D. J.; Smyth, G. K. Bioinformatics, Vol. 26, Issue 1 https://doi.org/10.1093/bioinformatics/btp616	journal	November 2009
The role of serotonin and melatonin in plant morphogenesis: Regulation of auxin-induced root organogenesis in in vitro-cultured explants of st. John's Wort (Hypericum perforatum L.) Murch, Susan J.; Campbell, Skye S. B.; Saxena, Praveen K. In Vitro Cellular & Developmental Biology - Plant, Vol. 37, Issue 6 https://doi.org/10.1007/s11627-001-0130-y	journal	November 2001
Outbreak of Cucurbit Powdery Mildew on Watermelon Fruit Caused by Podosphaera xanthii in Southwest Florida Kousik, C. S.; Donahoo, R. S.; Webster, C. G. Plant Disease, Vol. 95, Issue 12 https://doi.org/10.1094/PDIS-06-11-0521	journal	December 2011
Overexpression of MzASMT improves melatonin production and enhances drought tolerance in transgenic Arabidopsis thaliana plants Zuo, Bixiao; Zheng, Xiaodong; He, Pingli Journal of Pineal Research, Vol. 57, Issue 4 https://doi.org/10.1111/jpi.12180	journal	October 2014
Melatonin decreases delirium in elderly patients: A randomized, placebo-controlled trial Al-Aama, Tareef; Brymer, Christopher; Gutmanis, Iris International Journal of Geriatric Psychiatry, Vol. 26, Issue 7 https://doi.org/10.1002/gps.2582	journal	September 2010
Structure and functions of the GNAT superfamily of acetyltransferases Vetting, Matthew W.; S. de Carvalho, Luiz Pedro; Yu, Michael Archives of Biochemistry and Biophysics, Vol. 433, Issue 1 https://doi.org/10.1016/j.abb.2004.09.003	journal	January 2005
Identification of Resistance to Fusarium oxysporum f. sp. niveum Race 2 in Citrullus lanatus var. citroides Plant Introductions Wechter, W. Patrick; Kousik, Chandrasekar; McMillan, Melanie HortScience, Vol. 47, Issue 3 https://doi.org/10.21273/HORTSCI.47.3.334	journal	March 2012
Cellular localization and kinetics of the rice melatonin biosynthetic enzymes SNAT and ASMT Byeon, Yeong; Lee, Hyoung Yool; Lee, Kyungjin Journal of Pineal Research, Vol. 56, Issue 1 https://doi.org/10.1111/jpi.12103	journal	November 2013
Powdery Mildew Resistant Rootstocks that Impart Tolerance to Grafted Susceptible Watermelon Scion Seedlings Kousik, Chandrasekar S.; Mandal, Mihir; Hassell, Richard Plant Disease, Vol. 102, Issue 7 https://doi.org/10.1094/PDIS-09-17-1384-RE	journal	July 2018
Mitochondria and chloroplasts as the original sites of melatonin synthesis: a hypothesis related to melatonin's primary function and evolution in eukaryotes Tan, Dun-Xian; Manchester, Lucien C.; Liu, Xiaoyan Journal of Pineal Research, Vol. 54, Issue 2 https://doi.org/10.1111/jpi.12026	journal	November 2012
Regulation of basal and oxidative stress-triggered jasmonic acid-related gene expression by glutathione: Glutathione status and jasmonic acid Han, Yi; Mhamdi, Amna; Chaouch, Sejir Plant, Cell & Environment, Vol. 36, Issue 6 https://doi.org/10.1111/pce.12048	journal	January 2013
Melatonin in walnuts: Influence on levels of melatonin and total antioxidant capacity of blood Reiter, Russel J.; Manchester, L. C.; Tan, Dun-xian Nutrition, Vol. 21, Issue 9 https://doi.org/10.1016/j.nut.2005.02.005	journal	September 2005
NMR-based metabolomic analysis of plants Kim, Hye Kyong; Choi, Young Hae; Verpoorte, Robert Nature Protocols, Vol. 5, Issue 3 https://doi.org/10.1038/nprot.2009.237	journal	February 2010
Generation of transgenic watermelon resistant to Zucchini yellow mosaic virus and Papaya ringspot virus type W Yu, Tsong-Ann; Chiang, Chu-Hui; Wu, Hui-Wen Plant Cell Reports, Vol. 30, Issue 3 https://doi.org/10.1007/s00299-010-0951-4	journal	November 2010
Phytophthora Fruit Rot-resistant Watermelon Germplasm Lines USVL489-PFR, USVL782-PFR, USVL203-PFR, and USVL020-PFR Kousik, Chandrasekar S.; Ling, Kai-Shu; Adkins, Scott HortScience, Vol. 49, Issue 1 https://doi.org/10.21273/HORTSCI.49.1.101	journal	January 2014
Melatonin: plant growth regulator and/or biostimulator during stress? Arnao, Marino B.; Hernández-Ruiz, Josefa Trends in Plant Science, Vol. 19, Issue 12 https://doi.org/10.1016/j.tplants.2014.07.006	journal	December 2014
Melatonin, Serotonin, and Tryptamine in Some Egyptian Food and Medicinal Plants Badria, Farid A. Journal of Medicinal Food, Vol. 5, Issue 3 https://doi.org/10.1089/10966200260398189	journal	September 2002
Melatonin: Occurrence and daily rhythm in Chenopodium rubrum Kolář, Jan; Macháčková, Ivana; Eder, Josef Phytochemistry, Vol. 44, Issue 8 https://doi.org/10.1016/S0031-9422(96)00568-7	journal	April 1997
Oleic Acid–Dependent Modulation of NITRIC OXIDE ASSOCIATED1 Protein Levels Regulates Nitric Oxide–Mediated Defense Signaling in Arabidopsis Mandal, Mihir Kumar; Chandra-Shekara, A. C.; Jeong, Rae-Dong The Plant Cell, Vol. 24, Issue 4 https://doi.org/10.1105/tpc.112.096768	journal	April 2012
Melatonin from different fruit sources, functional roles, and analytical methods Feng, Xiaoyuan; Wang, Meng; Zhao, Yanyun Trends in Food Science & Technology, Vol. 37, Issue 1 https://doi.org/10.1016/j.tifs.2014.02.001	journal	May 2014
14-3-3 Proteins and photoneuroendocrine transduction: role in controlling the daily rhythm in melatonin Klein, D. C.; Ganguly, S.; Coon, S. Biochemical Society Transactions, Vol. 30, Issue 4 https://doi.org/10.1042/bst0300365	journal	August 2002
Melatonin for Treatment and Prevention of Postoperative Delirium Hanania, Michael; Kitain, Eric Anesthesia & Analgesia, Vol. 94, Issue 2 https://doi.org/10.1097/00000539-200202000-00019	journal	January 2002
Induced Systemic Resistance against Botrytis cinerea by Bacillus cereus AR156 through a JA/ET- and NPR1-Dependent Signaling Pathway and Activates PAMP-Triggered Immunity in Arabidopsis Nie, Pingping; Li, Xia; Wang, Shune Frontiers in Plant Science, Vol. 8 https://doi.org/10.3389/fpls.2017.00238	journal	February 2017
A Rapid Method of Total Lipid Extraction and Purification Bligh, E. G.; Dyer, W. J. Canadian Journal of Biochemistry and Physiology, Vol. 37, Issue 1 https://doi.org/10.1139/y59-099	journal	January 1959
NMR Spectroscopy Identifies Metabolites Translocated from Powdery Mildew Resistant Rootstocks to Susceptible Watermelon Scions Mahmud, Iqbal; Kousik, Chandrasekar; Hassell, Richard Journal of Agricultural and Food Chemistry, Vol. 63, Issue 36 https://doi.org/10.1021/acs.jafc.5b02108	journal	September 2015
Melatonin in plants Posmyk, Małgorzata M.; Janas, Krystyna M. Acta Physiologiae Plantarum, Vol. 31, Issue 1 https://doi.org/10.1007/s11738-008-0213-z	journal	September 2008
Alzheimer’s disease: pathological mechanisms and the beneficial role of melatonin: Alzheimer’s disease and melatonin Rosales-Corral, Sergio A.; Acuña-Castroviejo, Dario; Coto-Montes, Ana Journal of Pineal Research, Vol. 52, Issue 2 https://doi.org/10.1111/j.1600-079X.2011.00937.x	journal	November 2011
Comparative metabolomic analysis highlights the involvement of sugars and glycerol in melatonin-mediated innate immunity against bacterial pathogen in Arabidopsis Qian, Yongqiang; Tan, Dun-Xian; Reiter, Russel J. Scientific Reports, Vol. 5, Issue 1 https://doi.org/10.1038/srep15815	journal	October 2015
ISOLATION OF MELATONIN, THE PINEAL GLAND FACTOR THAT LIGHTENS MELANOCYTES ¹ Lerner, Aaron B.; Case, James D.; Takahashi, Yoshiyata Journal of the American Chemical Society, Vol. 80, Issue 10 https://doi.org/10.1021/ja01543a060	journal	May 1958
The Physiological Function of Melatonin in Plants Arnao, Marino B.; Hernández-Ruiz, Josefa Plant Signaling & Behavior, Vol. 1, Issue 3 https://doi.org/10.4161/psb.1.3.2640	journal	May 2006
The Sequence Alignment/Map format and SAMtools Li, H.; Handsaker, B.; Wysoker, A. Bioinformatics, Vol. 25, Issue 16 https://doi.org/10.1093/bioinformatics/btp352	journal	June 2009
The HvNAC6 transcription factor: a positive regulator of penetration resistance in barley and Arabidopsis Jensen, Michael Krogh; Rung, Jesper Henrik; Gregersen, Per Langkjaer Plant Molecular Biology, Vol. 65, Issue 1-2 https://doi.org/10.1007/s11103-007-9204-5	journal	July 2007
Modulation of defense signal transduction by flagellin-induced WRKY41 transcription factor in Arabidopsis thaliana Higashi, Kuniaki; Ishiga, Yasuhiro; Inagaki, Yoshishige Molecular Genetics and Genomics, Vol. 279, Issue 3 https://doi.org/10.1007/s00438-007-0315-0	journal	January 2008
Evaluation of fungicides for prevention and management of powdery mildew on watermelon Keinath, Anthony P.; DuBose, Virginia B. Crop Protection, Vol. 23, Issue 1 https://doi.org/10.1016/S0261-2194(03)00165-0	journal	January 2004
The ameliorative effects of exogenous melatonin on grape cuttings under water-deficient stress: antioxidant metabolites, leaf anatomy, and chloroplast morphology Meng, Jiang-Fei; Xu, Teng-Fei; Wang, Zhi-Zhen Journal of Pineal Research, Vol. 57, Issue 2 https://doi.org/10.1111/jpi.12159	journal	July 2014
Exogenous melatonin improves Malus resistance to Marssonina apple blotch Yin, Lihua; Wang, Ping; Li, Mingjun Journal of Pineal Research, Vol. 54, Issue 4 https://doi.org/10.1111/jpi.12038	journal	January 2013

Similar Records

Capsicum annuum homeobox 1 (CaHB1) is a nuclear factor that has roles in plant development, salt tolerance, and pathogen defense

Journal Article · Fri Dec 06 00:00:00 EST 2013 · Biochemical and Biophysical Research Communications · OSTI ID:1440803

Oh, Sang-Keun; Yoon, Joonseon; Choi, Gyung Ja; +3 more

Antimicrobial mechanisms of g‐C ₃ N ₄ @ ZnO against oomycetes Phytophthora capsici: from its metabolism, membrane structures and growth

Journal Article · Sat Jan 20 00:00:00 EST 2024 · Pest Management Science · OSTI ID:1440803

Cai, Lin; Huang, Xunliang; Feng, Hui; +2 more

Copper ions suppress abscisic acid biosynthesis to enhance defence against Phytophthora infestans in potato

Journal Article · Wed Feb 19 00:00:00 EST 2020 · Molecular Plant Pathology · OSTI ID:1440803

Liu, Hai‐Feng; Xue, Xiao‐Jing; Yu, Yue; +6 more

Title: Differential roles of melatonin in plant‐host resistance and pathogen suppression in cucurbits

Citation Formats

References (81)

Similar Records

Related Subjects