The molecular events underpinning cultivar differences in melatonin counteracting salt damage in Phaseolus vulgaris
Yiqiang Han A B , Yamei Gao A C , Ming Li D , Yanli Du D , Yuxian Zhang B D , Wenhui Zhang D and Jidao Du B D *A College of Life Science and Technology, Heilongjiang Bayi Agricultural University, Daqing 163319, Heilongjiang Province, P. R. China.
B National Coarse Cereals Engineering Research Center, Daqing 163319, Heilongjiang Province, P. R. China.
C Heilongjiang Provincial Key Laboratory of Environmental Microbiology and Recycling of Argo-Waste in the Cold Region, Heilongjiang Bayi Agricultural University, Daqing 163319, Heilongjiang Province, P. R. China.
D College of Agriculture, Heilongjiang Bayi Agricultural University, Daqing 163319, Heilongjiang Province, P. R. China.
Functional Plant Biology 49(2) 201-217 https://doi.org/10.1071/FP21126
Submitted: 27 April 2021 Accepted: 13 November 2021 Published: 7 December 2021
© 2022 The Author(s) (or their employer(s)). Published by CSIRO Publishing
Abstract
Melatonin (N-acetyl-5-methoxytryptamine) plays important roles in multiple stress responses, especially under salt stress. However, cultivar differences in melatonin mediated salt stress tolerance are unclear. Phaseolus vulgaris L. (common bean) cultivars Jiyin 1 (JY, salt-tolerant) and Xuliyabai (XL, salt-sensitive) were used in this study. Exogenous melatonin significantly improved root growth under salt stress in JY, but had little effect on XL. Physiology analysis showed significant differences in activities of antioxidant enzymes (superoxide, SOD; and catalase, CAT) and malondialdehyde content between JY and XL. Meanwhile, the change of ABA content in JY and XL root was opposite in salt plus melatonin treatment. Comparative root transcriptomes of JY and XL revealed 3505 and 668 differentially expressed genes (DEGs) regulated by salt stress and melatonin. The most enriched melatonin-responsive genes under salt stress are mainly involved in regulation of transcription, oxidation–reduction process, transcription factor activity, oxidoreductase activity. In addition, melatonin induced more obvious changes of DEGs in JY than that in XL under salt condition. Melatonin also significantly induced 41 DEGs only in JY, including signal transduction genes, transcription factors, ubiquitin protein ligases, ion homeostasis and osmotic adjustment genes etc. This study uncovered the molecular mechanism of cultivar difference of melatonin response under salt stress in common bean.
Keywords: ABA, antioxidant enzyme, cultivar difference, melatonin, Phaseolus vulgaris, root, salt stress, transcriptome.
References
Al Hassan M, Morosan M, López-Gresa MD, Prohens J, Vicente O, Boscaiu M (2016) Salinity-induced variation in biochemical markers provides insight into the mechanisms of salt tolerance in common (Phaseolus vulgaris) and runner (P. coccineus) beans. International Journal of Molecular Sciences 17, 1582| Salinity-induced variation in biochemical markers provides insight into the mechanisms of salt tolerance in common (Phaseolus vulgaris) and runner (P. coccineus) beans.Crossref | GoogleScholarGoogle Scholar |
Barragán V, Leidi EO, Andrés Z, Rubio L, De Luca A, Fernández JA, Cubero B, Pardo JM (2012) Ion exchangers NHX1 and NHX2 mediate active potassium uptake into vacuoles to regulate cell turgor and stomatal function in Arabidopsis. The Plant Cell 24, 1127–1142.
| Ion exchangers NHX1 and NHX2 mediate active potassium uptake into vacuoles to regulate cell turgor and stomatal function in Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 22438021PubMed |
Bawa G, Feng L, Shi J, Chen G, Cheng Y, Luo J, Wu W, Ngoke B, Cheng P, Tang Z, Pu T, Liu J, Liu W, Yong T, Du J, Yang W, Wang X (2020) Evidence that melatonin promotes soybean seedlings growth from low-temperature stress by mediating plant mineral elements and genes involved in the antioxidant pathway. Functional Plant Biology 47, 815–824.
| Evidence that melatonin promotes soybean seedlings growth from low-temperature stress by mediating plant mineral elements and genes involved in the antioxidant pathway.Crossref | GoogleScholarGoogle Scholar | 32553087PubMed |
Chen YE, Mao JJ, Sun LQ, Huang B, Ding CB, Gu Y, Liao JQ, Hu C, Zhang ZW, Yuan S, Yuan M (2018) Exogenous melatonin enhances salt stress tolerance in maize seedlings by improving antioxidant and photosynthetic capacity. Physiologia Plantarum 164, 349–363.
| Exogenous melatonin enhances salt stress tolerance in maize seedlings by improving antioxidant and photosynthetic capacity.Crossref | GoogleScholarGoogle Scholar | 29633289PubMed |
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 Physiology and Biochemistry 162, 506–516.
| Melatonin promotes seed germination under salt stress by regulating ABA and GA3 in cotton (Gossypium hirsutum L.).Crossref | GoogleScholarGoogle Scholar | 33773227PubMed |
Chinnusamy V, Jagendorf A, Zhu JK (2005) Understanding and improving salt tolerance in plants. Crop Science 45, 437–448.
| Understanding and improving salt tolerance in plants.Crossref | GoogleScholarGoogle Scholar |
Corso M, Doccula FG, Melo JRFD, Costa A, Verbruggen N (2018) Endoplasmic reticulum-localized CCX2 is required for osmotolerance by regulating ER and cytosolic Ca2+ dynamics in Arabidopsis. Proceedings of the National Academy of the Sciences of the United States of America 115, 3966–3971.
| Endoplasmic reticulum-localized CCX2 is required for osmotolerance by regulating ER and cytosolic Ca2+ dynamics in Arabidopsis.Crossref | GoogleScholarGoogle Scholar |
ElSayed A, Rafudeen M, Gomaa A, Hasanuzzaman M (2021) Exogenous melatonin enhances the reactive oxygen species metabolism, antioxidant defense-related gene expression, and photosynthetic capacity of Phaseolus vulgaris L. to confer salt stress tolerance. Physiologia Plantarum 173, 1369–1381.
| Exogenous melatonin enhances the reactive oxygen species metabolism, antioxidant defense-related gene expression, and photosynthetic capacity of Phaseolus vulgaris L. to confer salt stress tolerance.Crossref | GoogleScholarGoogle Scholar | 33619766PubMed |
Fornes O, Castro-Mondragon JA, Khan A, van der Lee R, Zhang X, Richmond PA, Modi BP, Correard S, Gheorghe M, Baranašić D, Santana-Garcia W, Tan G, Chèneby J, Ballester B, Parcy F, Sandelin A, Lenhard B, Wasserman WW, Mathelier A (2020) JASPAR 2020: update of the open-access database of transcription factor binding profiles. Nucleic Acids Research 48, D87–D92.
| JASPAR 2020: update of the open-access database of transcription factor binding profiles.Crossref | GoogleScholarGoogle Scholar | 31701148PubMed |
Gao W, Feng Z, Bai Q, He J, Wang Y (2019) Melatonin-mediated regulation of growth and antioxidant capacity in salt-tolerant naked oat under salt stress. International Journal of Molecular Sciences 20, 1176
| Melatonin-mediated regulation of growth and antioxidant capacity in salt-tolerant naked oat under salt stress.Crossref | GoogleScholarGoogle Scholar |
Goodstein DM, Shu S, Howson R, Neupane R, Hayes RD, Fazo J, Mitros T, Dirks W, Hellsten U, Putnam N, Rokhsar DS (2012) Phytozome: a comparative platform for green plant genomics. Nucleic Acids Research 40, D1178–D1186.
| Phytozome: a comparative platform for green plant genomics.Crossref | GoogleScholarGoogle Scholar | 22110026PubMed |
Gou J, Strauss SH, Tsai CJ, Fang K, Chen Y, Jiang X, Busov VB (2010) Gibberellins regulate lateral root formation in Populus through interactions with auxin and other hormones. The Plant Cell 22, 623–639.
| Gibberellins regulate lateral root formation in Populus through interactions with auxin and other hormones.Crossref | GoogleScholarGoogle Scholar | 20354195PubMed |
Graham PH, Vance CP (2003) Legumes: importance and constraints to greater use. Plant Physiology 131, 872–877.
| Legumes: importance and constraints to greater use.Crossref | GoogleScholarGoogle Scholar | 12644639PubMed |
Guzmán P (2012) The prolific ATL family of RING-H2 ubiquitin ligases. Plant Signaling and Behavior 7, 1014–1021.
| The prolific ATL family of RING-H2 ubiquitin ligases.Crossref | GoogleScholarGoogle Scholar | 22827943PubMed |
Han Y, Gao Y, Shi Y, Du J, Zheng D, Liu G (2017) Genome-wide transcriptome profiling reveals the mechanism of the effects of uniconazole on root development in Glycine Max. Journal of Plant Biology 60, 387–403.
| Genome-wide transcriptome profiling reveals the mechanism of the effects of uniconazole on root development in Glycine Max.Crossref | GoogleScholarGoogle Scholar |
Hiz MC, Canher B, Niron H, Turet M (2014) Transcriptome analysis of salt tolerant common bean (Phaseolus vulgaris L.) under saline conditions. PLoS ONE 9, e92598
| Transcriptome analysis of salt tolerant common bean (Phaseolus vulgaris L.) under saline conditions.Crossref | GoogleScholarGoogle Scholar | 24651267PubMed |
Holtan HE, Bandong S, Marion CM, Adam L, Tiwari S, Shen Y, Maloof JN, Maszle DR, Ohto M-A, Preuss S, Meister R, Petracek M, Repetti PP, Reuber TL, Ratcliffe OJ, Khanna R (2011) BBX32, an Arabidopsis B-Box protein, functions in light signaling by suppressing HY5-regulated gene expression and interacting with STH2/BBX21. Plant Physiology 156, 2109–2123.
| BBX32, an Arabidopsis B-Box protein, functions in light signaling by suppressing HY5-regulated gene expression and interacting with STH2/BBX21.Crossref | GoogleScholarGoogle Scholar | 21632973PubMed |
Islam F, Ali B, Wang J, Farooq MA, Gill RA, Ali S, Wang D, Zhou W (2016) Combined herbicide and saline stress differentially modulates hormonal regulation and antioxidant defense system in Oryza sativa cultivars. Plant Physiology and Biochemistry 107, 82–95.
| Combined herbicide and saline stress differentially modulates hormonal regulation and antioxidant defense system in Oryza sativa cultivars.Crossref | GoogleScholarGoogle Scholar | 27258572PubMed |
Islam F, Xie Y, Farooq MA, Wang J, Yang C, Gill RA, Zhu J, Zhou W (2017) Salinity reduces 2,4-D efficacy in Echinochloa crusgalli by affecting redox balance, nutrient acquisition, and hormonal regulation. Protoplasma 255, 785–802.
| Salinity reduces 2,4-D efficacy in Echinochloa crusgalli by affecting redox balance, nutrient acquisition, and hormonal regulation.Crossref | GoogleScholarGoogle Scholar | 29151143PubMed |
Jiang C, Cui Q, Feng K, Xu D, Li C, Zheng Q (2016) Melatonin improves antioxidant capacity and ion homeostasis and enhances salt tolerance in maize seedlings. Acta Physiologiae Plantarum 38, 82
| Melatonin improves antioxidant capacity and ion homeostasis and enhances salt tolerance in maize seedlings.Crossref | GoogleScholarGoogle Scholar |
Kim D, Pertea G, Trapnell C, Pimentel H, Kelley R, Salzberg SL (2013) TopHat2: accurate alignment of transcriptomes in the presence of insertions, deletions and gene fusions. Genome Biology 14, R36
| TopHat2: accurate alignment of transcriptomes in the presence of insertions, deletions and gene fusions.Crossref | GoogleScholarGoogle Scholar | 23618408PubMed |
Lescot M, Déhais P, Thijs G, Marchal K, Moreau Y, Van de Peer Y, Rouzé P, Rombauts S (2002) PlantCARE, a database of plant cis-acting regulatory elements and a portal to tools for in silico analysis of promoter sequences. Nucleic Acids Research 30, 325–327.
| PlantCARE, a database of plant cis-acting regulatory elements and a portal to tools for in silico analysis of promoter sequences.Crossref | GoogleScholarGoogle Scholar | 11752327PubMed |
Li C, Wang P, Wei Z, Liang D, Liu C, Yin L, Jia D, Fu M, Ma F (2012) The mitigation effects of exogenous melatonin on salinity-induced stress in Malus hupehensis. Journal of Pineal Research 53, 298–306.
| The mitigation effects of exogenous melatonin on salinity-induced stress in Malus hupehensis.Crossref | GoogleScholarGoogle Scholar | 22507106PubMed |
Li H, Chang J, Chen H, Wang Z, Gu X, Wei C, Zhang Y, Ma J, Yang J, Zhang X (2017a) Exogenous melatonin confers salt stress tolerance to watermelon by improving photosynthesis and redox homeostasis. Frontiers in Plant Science 8, 295
| Exogenous melatonin confers salt stress tolerance to watermelon by improving photosynthesis and redox homeostasis.Crossref | GoogleScholarGoogle Scholar | 28298921PubMed |
Li X, Yu B, Cui Y, Yin Y (2017b) Melatonin application confers enhanced salt tolerance by regulating Na+ and Cl− accumulation in rice. Plant Growth Regulation 83, 441–454.
| Melatonin application confers enhanced salt tolerance by regulating Na+ and Cl− accumulation in rice.Crossref | GoogleScholarGoogle Scholar |
Li J, Zhao C, Zhang M, Yuan F, Chen M (2019) Exogenous melatonin improves seed germination in Limonium bicolor under salt stress. Plant Signaling and Behavior 14, 1659705
| Exogenous melatonin improves seed germination in Limonium bicolor under salt stress.Crossref | GoogleScholarGoogle Scholar | 31460852PubMed |
Liang L, Flury S, Kalck V, Hohn B, Molinier J (2006) CENTRIN2 interacts with the Arabidopsis homolog of the human XPC Protein (AtRAD4) and contributes to efficient synthesis-dependent repair of bulky DNA Lesions. Plant Molecular Biology 61, 345–356.
| CENTRIN2 interacts with the Arabidopsis homolog of the human XPC Protein (AtRAD4) and contributes to efficient synthesis-dependent repair of bulky DNA Lesions.Crossref | GoogleScholarGoogle Scholar | 16786311PubMed |
Liang C, Zheng G, Li W, Wang Y, Hu B, Wang H, Wu H, Qian Y, Zhu XG, Tan DX, Chen SY, Chu C (2015) Melatonin delays leaf senescence and enhances salt stress tolerance in rice. Journal of Pineal Research 59, 91–101.
| Melatonin delays leaf senescence and enhances salt stress tolerance in rice.Crossref | GoogleScholarGoogle Scholar | 25912474PubMed |
Long M, Shou J, Wang J, Hu W, Hannan F, Mwamba T, Farooq M, Zhou W, Islam F (2020) Ursolic acid limits salt-induced oxidative damage by interfering with nitric oxide production and oxidative defense machinery in rice. Frontiers in Plant Science 11, 697
| Ursolic acid limits salt-induced oxidative damage by interfering with nitric oxide production and oxidative defense machinery in rice.Crossref | GoogleScholarGoogle Scholar | 32670308PubMed |
Martinez V, Nieves-Cordones M, Lopez-Delacalle M, Rodenas R, Mestre T, Garcia-Sanchez F, Rubio F, Nortes P, Mittler R, Rivero R (2018) Tolerance to stress combination in tomato plants: new insights in the protective role of melatonin. Molecules 23, 535
| Tolerance to stress combination in tomato plants: new insights in the protective role of melatonin.Crossref | GoogleScholarGoogle Scholar |
Mukherjee S, David A, Yadav S, Baluška F, Bhatla SC (2014) Salt stress-induced seedling growth inhibition coincides with differential distribution of serotonin and melatonin in sunflower seedling roots and cotyledons. Physiologia Plantarum 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 | 24799301PubMed |
Munir S, Liu H, Xing Y, Hussain S, Ouyang B, Zhang Y, Li H, Ye Z (2016) Overexpression of calmodulin-like (ShCML44) stress-responsive gene from Solanum habrochaites enhances tolerance to multiple abiotic stresses. Scientific Reports 6, 31772
| Overexpression of calmodulin-like (ShCML44) stress-responsive gene from Solanum habrochaites enhances tolerance to multiple abiotic stresses.Crossref | GoogleScholarGoogle Scholar | 27546315PubMed |
Niron H, Barlas N, Salih B, Türet M (2021) Comparative transcriptome, metabolome, and ionome analysis of two contrasting common bean genotypes in saline conditions. Frontiers in Plant Science 12, 711806
| Comparative transcriptome, metabolome, and ionome analysis of two contrasting common bean genotypes in saline conditions.Crossref | GoogleScholarGoogle Scholar | 34267776PubMed |
Park S, Lee DE, Jang H, Byeon Y, Kim YS, Back K (2013) Melatonin rich transgenic rice plants exhibit resistance to herbicide-induced oxidative stress. Journal of Pineal Research 54, 258–263.
| Melatonin rich transgenic rice plants exhibit resistance to herbicide-induced oxidative stress.Crossref | GoogleScholarGoogle Scholar | 22856683PubMed |
Schmutz J, McClean PE, Mamidi S, Wu GA, Cannon SB, Grimwood J, et al. (2014) A reference genome for common bean and genome-wide analysis of dual domestications. Nature Genetics 46, 707–713.
| A reference genome for common bean and genome-wide analysis of dual domestications.Crossref | GoogleScholarGoogle Scholar | 24908249PubMed |
Shi H, Jiang C, Ye T, Tan DX, Reiter RJ, Zhang H, Liu R, Chan Z (2015) 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 | 25225478PubMed |
Shu K, Yang W (2017) E3 ubiquitin ligases: ubiquitous actors in plant development and abiotic stress responses. Plant and Cell Physiology 58, 1461
| E3 ubiquitin ligases: ubiquitous actors in plant development and abiotic stress responses.Crossref | GoogleScholarGoogle Scholar | 28541504PubMed |
Siddiqui MH, Alamri S, Al-Khaishany MY, Khan MN, Al-Amri A, Ali HM, Alaraidh IA, Alsahli AA (2019) Exogenous melatonin counteracts NaCl-induced damage by regulating the antioxidant system, proline and carbohydrates metabolism in tomato seedlings. International Journal of Molecular Sciences 20, 353
| Exogenous melatonin counteracts NaCl-induced damage by regulating the antioxidant system, proline and carbohydrates metabolism in tomato seedlings.Crossref | GoogleScholarGoogle Scholar |
Sliwiak J, Sikorski M, Jaskolski M (2018) PR-10 proteins as potential mediators of melatonin-cytokinin cross-talk in plants: crystal-lographic studies of LlPR-10.2B isoform from yellow lupine. The FEBS Journal 285, 1907–1922.
| PR-10 proteins as potential mediators of melatonin-cytokinin cross-talk in plants: crystal-lographic studies of LlPR-10.2B isoform from yellow lupine.Crossref | GoogleScholarGoogle Scholar | 29630775PubMed |
Sze H, Chanroj S (2018) Plant endomembrane dynamics: studies of K+/H+ antiporters provide insights on the effects of pH and ion homeostasis. Plant Physiology 177, 875–895.
| Plant endomembrane dynamics: studies of K+/H+ antiporters provide insights on the effects of pH and ion homeostasis.Crossref | GoogleScholarGoogle Scholar | 29691301PubMed |
Takahashi Y, Zhang J, Hsu PK, Ceciliato PHO, Zhang L, Dubeaux G, Munemasa S, Ge C, Zhao Y, Hauser F, Schroeder JI (2020) MAP3Kinase-dependent SnRK2-kinase activation is required for abscisic acid signal transduction and rapid osmotic stress response. Nature Communications 11, 12
| MAP3Kinase-dependent SnRK2-kinase activation is required for abscisic acid signal transduction and rapid osmotic stress response.Crossref | GoogleScholarGoogle Scholar | 31896774PubMed |
Tan DX, Rudiger H, Manchester LC, Ahmet K, Ma S, Rosales-Corral S, Reiter RJ (2012) Functional roles of melatonin in plants, and perspectives in nutritional and agricultural science. Journal of Experimental Botany 63, 577–597.
| Functional roles of melatonin in plants, and perspectives in nutritional and agricultural science.Crossref | GoogleScholarGoogle Scholar | 22016420PubMed |
Vlasova A, Capella-Gutiérrez S, Rendón-Anaya M, Hernández-Oñate M, Minoche AE, Erb I, Câmara F, Prieto-Barja P, Corvelo A, Sanseverino W, Westergaard G, Dohm JC, Pappas GJ, Saburido-Alvarez S, Kedra D, Gonzalez I, Cozzuto L, Gómez-Garrido J, Aguilar-Morón MA, Andreu N, Aguilar OM, Garcia-Mas J, Zehnsdorf M, Vázquez MP, Delgado-Salinas A, Delaye L, Lowy E, Mentaberry A, Vianello-Brondani RP, García JL, Alioto T, Sánchez F, Himmelbauer H, Santalla M, Notredame C, Gabaldón T, Herrera-Estrella A, Guigó R (2016) Genome and transcriptome analysis of the Mesoamerican common bean and the role of gene duplications in establishing tissue and temporal specialization of genes. Genome Biology 17, 32
| Genome and transcriptome analysis of the Mesoamerican common bean and the role of gene duplications in establishing tissue and temporal specialization of genes.Crossref | GoogleScholarGoogle Scholar | 26911872PubMed |
Walley JW, Coughlan S, Hudson ME, Covington MF, Kaspi R, Banu G, Harmer SL, Dehesh K (2007) Mechanical stress induces biotic and abiotic stress responses via a novel cis-element. PLoS Genetics 3, e172
| Mechanical stress induces biotic and abiotic stress responses via a novel cis-element.Crossref | GoogleScholarGoogle Scholar |
Wang LY, Liu JL, Wang WX, Sun Y (2016) Exogenous melatonin improves growth and photosynthetic capacity of cucumber under salinity-induced stress. Photosynthetica 54, 19–27.
| Exogenous melatonin improves growth and photosynthetic capacity of cucumber under salinity-induced stress.Crossref | GoogleScholarGoogle Scholar |
Weeda S, Zhang N, Zhao XL, Ndip G, Guo Y, Buck GA, Fu C, Ren S (2014) Arabidopsis transcriptome analysis reveals key roles of melatonin in plant defense systems. PLoS ONE 9, e93462
| Arabidopsis transcriptome analysis reveals key roles of melatonin in plant defense systems.Crossref | GoogleScholarGoogle Scholar | 24682084PubMed |
Wei W, Li QT, 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 | 25297548PubMed |
Xie Y, Mao Y, Lai D, Zhang W, Shen W (2012) H2 enhances Arabidopsis salt tolerance by manipulating ZAT10/12-mediated antioxidant defence and controlling sodium exclusion. PLoS ONE 7, e49800
| H2 enhances Arabidopsis salt tolerance by manipulating ZAT10/12-mediated antioxidant defence and controlling sodium exclusion.Crossref | GoogleScholarGoogle Scholar | 23185443PubMed |
Xu DB, Gao SQ, Ma YN, Wang XT, Feng L, Li LC, Xu ZS, Chen YF, Chen M, Ma YZ (2017) The G-protein β subunit AGB1 promotes hypocotyl elongation through inhibiting transcription activation function of BBX21 in Arabidopsis. Molecular Plant 10, 1206–1223.
| The G-protein β subunit AGB1 promotes hypocotyl elongation through inhibiting transcription activation function of BBX21 in Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 28827171PubMed |
Zhan H, Nie X, Zhang T, Li S, Wang X, Du X, Tong W, Song W (2019) Melatonin: a small molecule but important for salt stress tolerance in plants. International Journal of Molecular Sciences 20, 709
| Melatonin: a small molecule but important for salt stress tolerance in plants.Crossref | GoogleScholarGoogle Scholar |
Zhan Y, Wu T, Zhao X, Wang Z, Chen Y (2021) Comparative physiological and full-length transcriptome analyses reveal the molecular mechanism of melatonin-mediated salt tolerance in okra (Abelmoschus esculentus L.). BMC Plant Biology 21, 180
| Comparative physiological and full-length transcriptome analyses reveal the molecular mechanism of melatonin-mediated salt tolerance in okra (Abelmoschus esculentus L.).Crossref | GoogleScholarGoogle Scholar | 33858330PubMed |
Zhang HJ, Zhang N, Yang RC, Wang L, Sun QQ, Li DB, Cao YY, Weeda S, Zhao B, Ren S, Guo YD (2014) 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 | 25112973PubMed |
Zhang J, Zeng B, Mao Y, Kong X, Wang X, Yang Y, Zhang J, Xu J, Rengel Z, Chen Q (2017a) Melatonin alleviates aluminium toxicity through modulating antioxidative enzymes and enhancing organic acid anion exudation in soybean. Functional Plant Biology 44, 961–968.
| Melatonin alleviates aluminium toxicity through modulating antioxidative enzymes and enhancing organic acid anion exudation in soybean.Crossref | GoogleScholarGoogle Scholar | 32480624PubMed |
Zhang N, Zhang HJ, Sun QQ, Cao YY, Li X, Zhao B, Wu P, Guo YD (2017b) Proteomic analysis reveals a role of melatonin in promoting cucumber seed germination under high salinity by regulating energy production. Scientific Reports 7, 503
| Proteomic analysis reveals a role of melatonin in promoting cucumber seed germination under high salinity by regulating energy production.Crossref | GoogleScholarGoogle Scholar | 28356562PubMed |
Zhang M, He S, Zhan Y, Qin B, Jin X, Wang M, Zhang Y, Hu G, Teng Z, Wu Y (2019) Exogenous melatonin reduces the inhibitory effect of osmotic stress on photosynthesis in soybean. PLoS ONE 14, e0226542
| Exogenous melatonin reduces the inhibitory effect of osmotic stress on photosynthesis in soybean.Crossref | GoogleScholarGoogle Scholar | 31869357PubMed |
Zhang Q, Zhang WJ, Yin ZG, Li WJ, Zhao HH, Zhang S, Zhuang L, Wang YX, Zhang WH, Du JD (2020) Genome- and transcriptome-wide identification of c3hs in common bean (Phaseolus vulgaris l.) and structural and expression-based analyses of their functions during the sprout stage under salt-stress conditions. Frontiers in Genetics 11, 564607
| Genome- and transcriptome-wide identification of c3hs in common bean (Phaseolus vulgaris l.) and structural and expression-based analyses of their functions during the sprout stage under salt-stress conditions.Crossref | GoogleScholarGoogle Scholar | 33101386PubMed |
Zhao G, Zhao Y, Yu X, Kiprotich F, Han H, Guan R, Wang R, Shen W (2018) Nitric oxide is required for melatonin-enhanced tolerance against salinity stress in rapeseed (Brassica napus L.) seedlings. International Journal of Molecular science 19, 1912
| Nitric oxide is required for melatonin-enhanced tolerance against salinity stress in rapeseed (Brassica napus L.) seedlings.Crossref | GoogleScholarGoogle Scholar |