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Crop and Pasture Science Crop and Pasture Science Society
Plant sciences, sustainable farming systems and food quality
RESEARCH ARTICLE

Physiological and biochemical analyses reveal drought tolerance in cool-season tall fescue (Festuca arundinacea) turf grass with the application of melatonin

Mohammad Nur Alam A B , Yanping Wang A and Zhulong Chan https://orcid.org/0000-0002-1933-6837 A C D
+ Author Affiliations
- Author Affiliations

A Key Laboratory of Horticultural Plant Biology, Ministry of Education, and Key Laboratory of Urban Agriculture in Central China, Ministry of Agriculture, College of Horticulture and Forestry Sciences, Huazhong Agricultural University, Wuhan, Hubei 430070, China.

B Agronomy Division, Bangladesh Wheat and Maize Research Institute, Nashipur, Dinajpur 5200, Bangladesh.

C College of Life Science and Technology, Hubei Engineering University, Xiaogan, Hubei 432000, China.

D Corresponding author. Email: zlchan@mail.hzau.edu.cn

Crop and Pasture Science 69(10) 1041-1049 https://doi.org/10.1071/CP18394
Submitted: 21 April 2018  Accepted: 29 August 2018   Published: 1 October 2018

Abstract

Tall fescue (Festuca arundinacea Schreb.) is a widely used, cool-season turf grass and is relatively sensitive to water stress. Melatonin has been reported to improve abiotic stress tolerance in many plants. In this study, we demonstrated that, although shoot height and fresh weight of tall fescue seedlings were significantly reduced by drought stress, they were increased by melatonin pre-treatment compared with control plants. Chemical analyses showed that tall fescue seedlings pre-treated with melatonin exhibited decreased levels of reactive oxygen species, electrolyte leakage and malondialdehyde, but higher levels of antioxidant enzyme activities (catalase, and peroxidase) and total chlorophyll content, compared with untreated seedlings. Leaf water loss was also partially mitigated and leaf water content increased by melatonin application, resulting in improved plant growth under drought stress. Moreover, root growth of tall fescue seedlings was promoted by melatonin under osmotic stress. The results show that drought tolerance was improved in cool-season tall fescue by application of exogenous melatonin. Therefore, melatonin may potentially be used as a protectant for plants against the deleterious effects of drought or water-deficit stress.

Additional keywords: hormone, oxidative stress, physiological metabolism.


References

Alam MN, Zhang L, Yang L, Islam MR, Liu Y, Luo H, Yang P, Wang Q, Chan Z (2018) Transcriptomic profiling of tall fescue in response to heat stress and improved thermotolerance by melatonin and 24-epibrassinolide. BMC Genomics 19, 224–237.
Transcriptomic profiling of tall fescue in response to heat stress and improved thermotolerance by melatonin and 24-epibrassinolide.Crossref | GoogleScholarGoogle Scholar |

Anjum SA, Wang L, Farooq M, Khan I, Xue L (2011) Methyl jasmonate induced alteration in lipid peroxidation, antioxidative defence system and yield in soybean under drought. Journal of Agronomy & Crop Science 197, 296–301.
Methyl jasmonate induced alteration in lipid peroxidation, antioxidative defence system and yield in soybean under drought.Crossref | GoogleScholarGoogle Scholar |

Antoniou C, Chatzimichail G, Xenofontos R, Pavlou JJ, Panagiotou E, Christou A, Fotopoulos V (2017) Melatonin systemically ameliorates drought stress-induced damage in Medicago sativa plants by modulating nitro-oxidative homeostasis and proline metabolism. Journal of Pineal Research 62, e12401
Melatonin systemically ameliorates drought stress-induced damage in Medicago sativa plants by modulating nitro-oxidative homeostasis and proline metabolism.Crossref | GoogleScholarGoogle Scholar |

Arnao MB, Hernandez-Ruiz J (2007) Melatonin promotes adventitious- and lateral root regeneration in etiolated hypocotyls of Lupinus albus L. Journal of Pineal Research 42, 147–152.
Melatonin promotes adventitious- and lateral root regeneration in etiolated hypocotyls of Lupinus albus L.Crossref | GoogleScholarGoogle Scholar |

Arnao MB, Hernandez-Ruiz J (2018) Melatonin and its relationship to plant hormones. Annals of Botany 121, 195–207.
Melatonin and its relationship to plant hormones.Crossref | GoogleScholarGoogle Scholar |

Ayala A, Muñoz MF, Argüelles S (2014) Lipid peroxidation: Production, metabolism, and signaling mechanisms of malondialdehyde and 4-hydroxy-2-nonenal. Oxidative Medicine and Cellular Longevity 2014, 360438
Lipid peroxidation: Production, metabolism, and signaling mechanisms of malondialdehyde and 4-hydroxy-2-nonenal.Crossref | GoogleScholarGoogle Scholar |

Barrera G (2012) Oxidative stress and lipid peroxidation products in cancer progression and therapy. International Scholarly Research Network Oncology 2012, 137289

Bi A, Fan J, Hu Z, Wang G, Amombo E, Fu J, Hu T (2016) Differential acclimation of enzymatic antioxidant metabolism and photosystem II photochemistry in tall fescue under drought and heat and the combined stresses. Frontiers of Plant Science 7, 453
Differential acclimation of enzymatic antioxidant metabolism and photosystem II photochemistry in tall fescue under drought and heat and the combined stresses.Crossref | GoogleScholarGoogle Scholar |

Bistgani ZE, Siadat SA, Bakhshandeh A, Pirbalouti AG, Hashemi M (2017) Interactive effects of drought stress and chitosan application on physiological characteristics and essential oil yield of Thymus daenensis Celak. The Crop Journal 5, 407–415.
Interactive effects of drought stress and chitosan application on physiological characteristics and essential oil yield of Thymus daenensis Celak.Crossref | GoogleScholarGoogle Scholar |

Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein dye binding. Analytical Biochemistry 72, 248–254.
A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein dye binding.Crossref | GoogleScholarGoogle Scholar |

Cheeseman J (2016) Food security in the face of salinity, drought, climate change, and population growth. In ‘Halophytes for food security in dry lands’. (Eds M Khan, M Ozturk, B Gul, MZ Ahmed) pp. 111–123. (Academic Press: San Diego, CA, USA)

Cramer GR, Urano K, Delrot S, Pezzotti M, Shinozaki K (2011) Effects of abiotic stress on plants: a systems biology perspective. BMC Plant Biology 11, 163–176.
Effects of abiotic stress on plants: a systems biology perspective.Crossref | GoogleScholarGoogle Scholar |

Davey MW, Stals E, Panis B, Keulemans J, Swennen RL (2005) High-throughput determination of malondialdehyde in plant tissues. Annals of Biochemistry 347, 201–207.
High-throughput determination of malondialdehyde in plant tissues.Crossref | GoogleScholarGoogle Scholar |

Devlin R (1975) ‘Plant physiology.’ (D. Van Nostrand Company: New York)

Du HM, Wang ZL, Huang BR (2009) Differential responses of warm-season and cool-season turfgrass species to heat stress associated with antioxidant enzyme activity. Journal of the American Society for Horticultural Science 134, 417–422.

El-Beltagi HS, Mohamed HI (2013) Reactive oxygen species, lipid peroxidation and antioxidative defense mechanism. Notulae Botanicae Horti Agrobotanici Cluj-Napoca 41, 44–57.
Reactive oxygen species, lipid peroxidation and antioxidative defense mechanism.Crossref | GoogleScholarGoogle Scholar |

Fan J, Chen K, Amombo E, Hu Z, Chen L, Fu J (2015) Physiological and molecular mechanism of nitric oxide (NO) involved in bermudagrass response to cold stress. PLoS One 10, e0132991
Physiological and molecular mechanism of nitric oxide (NO) involved in bermudagrass response to cold stress.Crossref | GoogleScholarGoogle Scholar |

Galano A, Tan D-X, Reiter RJ (2011) Melatonin as a natural ally against oxidative stress: a physicochemical examination. Journal of Pineal Research 51, 1–16.
Melatonin as a natural ally against oxidative stress: a physicochemical examination.Crossref | GoogleScholarGoogle Scholar |

Galano A, Tan D-X, Reiter RJ (2013) On the free radical scavenging activities of melatonin’s metabolites, AFMK and AMK. Journal of Pineal Research 54, 245–257.
On the free radical scavenging activities of melatonin’s metabolites, AFMK and AMK.Crossref | GoogleScholarGoogle Scholar |

Hasan MK, Ahammed GJ, Yin L, Xia X, Zhou Y, Yu J, Zhou J (2015) Melatonin mitigates cadmium phytotoxicity through modulation of phytochelatins biosynthesis, vacuolar sequestration, and antioxidant potential in Solanum lycopersicum L. Frontiers of Plant Science 6, 601
Melatonin mitigates cadmium phytotoxicity through modulation of phytochelatins biosynthesis, vacuolar sequestration, and antioxidant potential in Solanum lycopersicum L.Crossref | GoogleScholarGoogle Scholar |

Hassanpour H, Ali Khavari-Nejad R, Niknam V, Najafi F, Razavi K (2012) Effects of penconazole and water deficit stress on physiological and antioxidative responses in pennyroyal (Mentha pulegium L.). Acta Physiologiae Plantarum 34, 1537–1549.
Effects of penconazole and water deficit stress on physiological and antioxidative responses in pennyroyal (Mentha pulegium L.).Crossref | GoogleScholarGoogle Scholar |

Hattori A, Migitaka H, Ligo M (1995) Identification of melatonin in plants and its effects on plasma melatonin levels and binding to melatonin receptors in vertebrates. Biochemistry and Molecular Biology International 35, 627–634.

Hernández-Ruiz J, Arnao MB (2018) Relationship of melatonin and salicylic acid in biotic/abiotic plant stress responses. Agronomy 8, 33
Relationship of melatonin and salicylic acid in biotic/abiotic plant stress responses.Crossref | GoogleScholarGoogle Scholar |

Hu L, Wang Z, Huang B (2010) Diffusion limitations and metabolic factors associated with inhibition and recovery of photosynthesis from drought stress in a C3 perennial grass species. Physiologia Plantarum 139, 93–106.
Diffusion limitations and metabolic factors associated with inhibition and recovery of photosynthesis from drought stress in a C3 perennial grass species.Crossref | GoogleScholarGoogle Scholar |

Hu T, Liu S, Amombo E, Fu J (2015) Stress memory induced rearrangements of HSP transcription, photosystem II photochemistry and metabolism of tall fescue (Festuca arundinacea Schreb.) in response to high temperature stress. Frontiers of Plant Science 6, 403
Stress memory induced rearrangements of HSP transcription, photosystem II photochemistry and metabolism of tall fescue (Festuca arundinacea Schreb.) in response to high temperature stress.Crossref | GoogleScholarGoogle Scholar |

Hu Z, Fan J, Xie Y, Amombo E, Liu A, Gitau MM, Khaldun ABM, Chen L, Fu J (2016) Comparative photosynthetic and metabolic analyses reveal mechanism of improved cold stress tolerance in bermudagrass by exogenous melatonin. Plant Physiology and Biochemistry 100, 94–104.
Comparative photosynthetic and metabolic analyses reveal mechanism of improved cold stress tolerance in bermudagrass by exogenous melatonin.Crossref | GoogleScholarGoogle Scholar |

Jiang Y, Huang B (2002) Protein alterations in tall fescue in response to drought stress and abscisic acid. Crop Science 42, 202–207.
Protein alterations in tall fescue in response to drought stress and abscisic acid.Crossref | GoogleScholarGoogle Scholar |

Jin SH, Li XQ, Jia XL (2011) Genotypic differences in the responses of gas exchange, chlorophyll fluorescence, and antioxidant enzymes to aluminum stress in Festuca arundinacea. Russian Journal of Plant Physiology: a Comprehensive Russian Journal on Modern Phytophysiology 58, 560
Genotypic differences in the responses of gas exchange, chlorophyll fluorescence, and antioxidant enzymes to aluminum stress in Festuca arundinacea.Crossref | GoogleScholarGoogle Scholar |

Jin R, Wang Y, Liu R, Gou J, Chan Z (2016) Physiological and metabolic changes of purslane (Portulaca oleracea L.) in response to drought, heat, and combined stresses. Frontiers of Plant Science 6, 1123
Physiological and metabolic changes of purslane (Portulaca oleracea L.) in response to drought, heat, and combined stresses.Crossref | GoogleScholarGoogle Scholar |

Kirnak H, Kaya C, Tas I, Higgs D (2001) The influence of water deficit on vegetative growth, physiology, fruit yield and quality in eggplants. Bulgarian Journal of Plant Physiology 27, 34–46.

Lee HY, Byeon Y, Back K (2014) Melatonin as a signal molecule triggering defense responses against pathogen attack in Arabidopsis and tobacco. Journal of Pineal Research 57, 262–268.
Melatonin as a signal molecule triggering defense responses against pathogen attack in Arabidopsis and tobacco.Crossref | GoogleScholarGoogle Scholar |

Li X, Tan D-X, Jiang D, Liu F (2016b) Melatonin enhances cold tolerance in drought-primed wild-type and abscisic acid-deficient mutant barley. Journal of Pineal Research 61, 328–339.
Melatonin enhances cold tolerance in drought-primed wild-type and abscisic acid-deficient mutant barley.Crossref | GoogleScholarGoogle Scholar |

Li H, Hu T, Amombo E, Fu J (2017) Transcriptome profilings of two tall fescue (Festuca arundinacea) cultivars in response to lead (Pb) stress. BMC Genomics 18, 145
Transcriptome profilings of two tall fescue (Festuca arundinacea) cultivars in response to lead (Pb) stress.Crossref | GoogleScholarGoogle Scholar |

Lou Y, Zhao P, Wang D, Amombo E, Sun X, Wang H, Zhuge Y (2017) Germination, physiological responses and gene expression of tall fescue (Festuca arundinacea Schreb.) growing under Pb and Cd. PLoS One 12, e0169495
Germination, physiological responses and gene expression of tall fescue (Festuca arundinacea Schreb.) growing under Pb and Cd.Crossref | GoogleScholarGoogle Scholar |

Meng JF, Xu TF, Wang ZZ, Fang YL, Xi ZM, Zhang ZW (2014) The ameliorative effects of exogenous melatonin on grape cuttings under water-deficient stress: antioxidant metabolites, leaf anatomy, and chloroplast morphology. Journal of Pineal Research 57, 200–212.
The ameliorative effects of exogenous melatonin on grape cuttings under water-deficient stress: antioxidant metabolites, leaf anatomy, and chloroplast morphology.Crossref | GoogleScholarGoogle Scholar |

Moshelion M, Altman A (2015) Current challenges and future perspectives of plant and agricultural biotechnology. Trends in Biotechnology 33, 337–342.
Current challenges and future perspectives of plant and agricultural biotechnology.Crossref | GoogleScholarGoogle Scholar |

Mukherjee S, David A, Yadav S, Baluska F, Bhatla SC (2014) Salt stress-induced seedling growth inhibition coincides with differential distribution of serotonin and melatonin in sunflower seedling roots and cotyledons. Plant Physiology 152, 714–728.
Salt stress-induced seedling growth inhibition coincides with differential distribution of serotonin and melatonin in sunflower seedling roots and cotyledons.Crossref | GoogleScholarGoogle Scholar |

Murashige T, Skoog F (1962) A revised medium for rapid growth and bio-assays with tobacco tissue cultures. Physiologia Plantarum 15, 473–497.
A revised medium for rapid growth and bio-assays with tobacco tissue cultures.Crossref | GoogleScholarGoogle Scholar |

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.
Melatonin regulates Arabidopsis root system architecture likely acting independently of auxin signaling.Crossref | GoogleScholarGoogle Scholar |

Pinheiro C, Chaves MM (2011) Photosynthesis and drought: can we make metabolic connections from available data? Journal of Experimental Botany 62, 869–882.
Photosynthesis and drought: can we make metabolic connections from available data?Crossref | GoogleScholarGoogle Scholar |

Posmyk MM, Kuran H, Marciniak K, Janas KM (2008) Pre-sowing seed treatment with melatonin protects red cabbage seedlings against toxic copper ion concentrations. Journal of Pineal Research 45, 24–31.
Pre-sowing seed treatment with melatonin protects red cabbage seedlings against toxic copper ion concentrations.Crossref | GoogleScholarGoogle Scholar |

Pryor WA, Stanley JP (1975) Letter: A suggested mechanism for the production of malondialdehyde during the autoxidation of polyunsaturated fatty acids. Nonenzymatic production of prostaglandin endoperoxides during autoxidation. The Journal of Organic Chemistry 40, 3615–3617.
Letter: A suggested mechanism for the production of malondialdehyde during the autoxidation of polyunsaturated fatty acids. Nonenzymatic production of prostaglandin endoperoxides during autoxidation.Crossref | GoogleScholarGoogle Scholar |

Quan W, Liu X, Wang H, Chan Z (2016a) Comparative physiological and transcriptional analyses of two contrasting drought tolerant alfalfa varieties. Frontiers of Plant Science 6, 1256
Comparative physiological and transcriptional analyses of two contrasting drought tolerant alfalfa varieties.Crossref | GoogleScholarGoogle Scholar |

Quan W, Liu X, Wang H, Chan Z (2016b) Physiological and transcriptional responses of contrasting alfalfa (Medicago sativa L.) varieties to salt stress. Plant Cell, Tissue and Organ Culture 126, 105–115.
Physiological and transcriptional responses of contrasting alfalfa (Medicago sativa L.) varieties to salt stress.Crossref | GoogleScholarGoogle Scholar |

Raskin I (1992) Role of salicylic acid in plants. Annual Review of Plant Biology 43, 439–463.
Role of salicylic acid in plants.Crossref | GoogleScholarGoogle Scholar |

Reiter RJ, Tan D-X, Terron MP, Flores LJ, Czarnocki Z (2007) Melatonin and its metabolites: new findings regarding their production and their radical scavenging actions. Acta Biochimica Polonica 54, 1–9.

Reiter RJ, Tan D-X, Zhou Z, Cruz MHC, Fuentes-Broto L, Galano A (2015) Phytomelatonin: assisting plants to survive and thrive. Molecules 20, 7396–7437.
Phytomelatonin: assisting plants to survive and thrive.Crossref | GoogleScholarGoogle Scholar |

Shi H, Jiang C, Ye T, Tan D-X, Reiter RJ, Zhang H, Liu R, Chan Z (2015a) Comparative physiological, metabolomic, and transcriptomic analyses reveal mechanisms of improved abiotic stress resistance in bermudagrass [Cynodon dactylon (L). Pers.] by exogenous melatonin. Journal of Experimental Botany 66, 681–694.
Comparative physiological, metabolomic, and transcriptomic analyses reveal mechanisms of improved abiotic stress resistance in bermudagrass [Cynodon dactylon (L). Pers.] by exogenous melatonin.Crossref | GoogleScholarGoogle Scholar |

Shi H, Tan D-X, Reiter RJ, Ye T, Yang F, Chan Z (2015b) Melatonin induces class A1 heat-shock factors (HSFA1s) and their possible involvement of thermotolerance in Arabidopsis. Journal of Pineal Research 58, 335–342.
Melatonin induces class A1 heat-shock factors (HSFA1s) and their possible involvement of thermotolerance in Arabidopsis.Crossref | GoogleScholarGoogle Scholar |

Shi H, Wang X, Tan D-X, Reiter RJ, Chan Z (2015c) Comparative physiological and proteomic analyses reveal the actions of melatonin in the reduction of oxidative stress in bermudagrass (Cynodon dactylon (L). Pers.). Journal of Pineal Research 59, 120–131.
Comparative physiological and proteomic analyses reveal the actions of melatonin in the reduction of oxidative stress in bermudagrass (Cynodon dactylon (L). Pers.).Crossref | GoogleScholarGoogle Scholar |

Stehle JH, Saade A, Rawashdeh O, Ackermann K, Jilg A, Sebestény T, Maronde E (2011) A survey of molecular details in the human pineal gland in the light of phylogeny, structure, function and chronobiological diseases. Journal of Pineal Research 51, 17–43.
A survey of molecular details in the human pineal gland in the light of phylogeny, structure, function and chronobiological diseases.Crossref | GoogleScholarGoogle Scholar |

Sun X, Wang P, Jia X, Huo L, Che R, Ma F (2018) Improvement of drought tolerance by overexpressing MdATG18a is mediated by modified antioxidant system and activated autophagy in transgenic apple. Plant Biotechnology Journal 16, 545–557.
Improvement of drought tolerance by overexpressing MdATG18a is mediated by modified antioxidant system and activated autophagy in transgenic apple.Crossref | GoogleScholarGoogle Scholar |

Tan D-X, Manchester LC, Reiter RJ, Plummer BF, Hardies LJ, Weintraub ST, et al (1998) A novel melatonin metabolite, cyclic 3-hydroxymelatonin: a biomarker of in vivo hydroxyl radical generation. Biochemical and Biophysical Research Communications 253, 614–620.
A novel melatonin metabolite, cyclic 3-hydroxymelatonin: a biomarker of in vivo hydroxyl radical generation.Crossref | GoogleScholarGoogle Scholar |

Tan D-X, Manchester LC, Reiter RJ, Plummer BF, Limson J, Weintraub ST, Qi W (2000) Melatonin directly scavenges hydrogen peroxide: a potentially new metabolic pathway of melatonin biotransformation. Free Radical Biology & Medicine 29, 1177–1185.
Melatonin directly scavenges hydrogen peroxide: a potentially new metabolic pathway of melatonin biotransformation.Crossref | GoogleScholarGoogle Scholar |

van der Weele CM, Spollen WG, Sharp RE, Baskin TI (2000) Growth of Arabidopsis thaliana seedlings under water deficit studied by control of water potential in nutrient-agar media. Journal of Experimental Botany 51, 1555–1562.
Growth of Arabidopsis thaliana seedlings under water deficit studied by control of water potential in nutrient-agar media.Crossref | GoogleScholarGoogle Scholar |

Venegas C, Garcia JA, Escames G, Ortiz F, López A, Doerrier C, García-Corzo L, López LC, Reiter RJ, Acuña-Castroviejoet D (2012) Extrapineal melatonin: analysis of its subcellular distribution and daily fluctuations. Journal of Pineal Research 52, 217–227.
Extrapineal melatonin: analysis of its subcellular distribution and daily fluctuations.Crossref | GoogleScholarGoogle Scholar |

Verslues PE, Bray EA (2004) LWR1 and LWR2 are required for osmoregulation and osmotic adjustment in Arabidopsis. Plant Physiology 136, 2831–2842.
LWR1 and LWR2 are required for osmoregulation and osmotic adjustment in Arabidopsis.Crossref | GoogleScholarGoogle Scholar |

Wang Z-Y, Hopkins A, Lawrence R, Bell J, Scott M (2004) Field evaluation and risk assessment of transgenic tall fescue (Festuca arundinacea) plants. In ‘Molecular breeding of forage and turf’. (Eds A Hopkins, ZY Wang, R Mian, M Sledge, RE Barker) pp. 367–79. (Springer: Dordrecht, The Netherlands)

Wang P, Sun X, Li C, Wei Z, Liang D, Ma F (2013) Long-term exogenous application of melatonin delays drought-induced leaf senescence in apple. Journal of Pineal Research 54, 292–302.
Long-term exogenous application of melatonin delays drought-induced leaf senescence in apple.Crossref | GoogleScholarGoogle Scholar |

Wang Y, Shen W, Chan Z, Wu Y (2015) Endogenous cytokinin overproduction modulates ROS homeostasis and decreases salt stress resistance in Arabidopsis thaliana. Frontiers of Plant Science 6, 1004
Endogenous cytokinin overproduction modulates ROS homeostasis and decreases salt stress resistance in Arabidopsis thaliana.Crossref | GoogleScholarGoogle Scholar |

Wang Y, Reiter RJ, Chan Z (2018) Phytomelatonin: a universal abiotic stress regulator. Journal of Experimental Botany 69, 963–974.
Phytomelatonin: a universal abiotic stress regulator.Crossref | GoogleScholarGoogle Scholar |

Wei W, Li Q, Chu YN, Reiter RJ, Yu XM, Zhu DH, Zhang WK, Ma B, Lin Q, Zhang JS, Chen SY (2015) Melatonin enhances plant growth and abiotic stress tolerance in soybean plants. Journal of Experimental Botany 66, 695–707.
Melatonin enhances plant growth and abiotic stress tolerance in soybean plants.Crossref | GoogleScholarGoogle Scholar |

Wellburn A, Lichtenthaler H (1984) Formulae and program to determine total carotenoids and chlorophylls a and b of leaf extracts in different solvents. In ‘Advances in photosynthesis research’. (Ed. C Sybesma) pp. 9–12. (Springer: Dordrecht, The Netherlands)

Xu W, Cai S-Y, Zhang Y, Wang Y, Ahammed GJ, Xia X-J, Shi K, Zhou Y-H, Yu J-Q, Reiter RJ, Zhou J (2016) Melatonin enhances thermotolerance by promoting cellular protein protection in tomato plants. Journal of Pineal Research 61, 457–469.
Melatonin enhances thermotolerance by promoting cellular protein protection in tomato plants.Crossref | GoogleScholarGoogle Scholar |

Yadava P, Kaushal J, Gautam A, et al (2016) Physiological and biochemical effects of 24-epibrassinolide on heat-stress adaptation in maize (Zea mays L.). Nature and Science 8, 171–179.
Physiological and biochemical effects of 24-epibrassinolide on heat-stress adaptation in maize (Zea mays L.).Crossref | GoogleScholarGoogle Scholar |

Yang L, You J, Wang Y, et al (2017) Systematic analysis of the G-box Factor 14-3-3 gene family and functional characterization of GF14a in Brachypodium distachyon. Plant Physiology and Biochemistry 117, 1–11.
Systematic analysis of the G-box Factor 14-3-3 gene family and functional characterization of GF14a in Brachypodium distachyon.Crossref | GoogleScholarGoogle Scholar |

Ye T, Shi H, Wang Y, Chan Z (2015) Contrasting changes caused by drought and submergence stresses in bermudagrass (Cynodon dactylon). Frontiers of Plant Science 6, 951
Contrasting changes caused by drought and submergence stresses in bermudagrass (Cynodon dactylon).Crossref | GoogleScholarGoogle Scholar |

Yin M, Wang Y, Zhang L, Li J, Quan W, Yang L, Wang Q, Chan Z (2017) The Arabidopsis Cys2/His2 zinc finger transcription factor ZAT18 is a positive regulator of plant tolerance to drought stress. Journal of Experimental Botany 68, 2991–3005.

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.). Journal of Pineal Research 54, 15–23.
Melatonin promotes water stress tolerance, lateral root formation, and seed germination in cucumber (Cucumis sativus L.).Crossref | GoogleScholarGoogle Scholar |

Zhang N, Zhang H-J, Zhao B, Sun Q-Q, Cao Y-Y, Li R, Wu X-X, Weeda S, Li L, Ren S, Reiter RJ, Guo Y-D (2014a) The RNA-seq approach to discriminate gene expression profiles in response to melatonin on cucumber lateral root formation. Journal of Pineal Research 56, 39–50.
The RNA-seq approach to discriminate gene expression profiles in response to melatonin on cucumber lateral root formation.Crossref | GoogleScholarGoogle Scholar |

Zhang HJ, Zhang N, Yang RC, Wang L, Sun QQ, Li DB, Guo YD (2014b) Melatonin promotes seed germination under high salinity by regulating antioxidant systems, ABA and GA4 interaction in cucumber (Cucumis sativus L.). Journal of Pineal Research 57, 269–279.
Melatonin promotes seed germination under high salinity by regulating antioxidant systems, ABA and GA4 interaction in cucumber (Cucumis sativus L.).Crossref | GoogleScholarGoogle Scholar |