The mechanisms underlying melatonin improved soybean seedling growth at different nitrogen levels
Huamei Wang
A , Chunyuan Ren A , Liang Cao A , Xijun Jin A , Mengxue Wang A , Mingcong Zhang A , Qiang Zhao A , He Li A , Yuxian Zhang A B * and Gaobo Yu A *
+ Author Affiliations
- Author Affiliations
A College of Agronomy, Heilongjiang Bayi Agricultural University, Daqing 163319, China.
B National Coarse Cereals Engineering Research Center, Daqing 163000, China.
Functional Plant Biology 48(12) 1225-1240 https://doi.org/10.1071/FP21154
Submitted: 3 March 2021 Accepted: 25 August 2021 Published: 11 October 2021
© 2021 The Author(s) (or their employer(s)). Published by CSIRO Publishing. This is an open access article distributed under the Creative Commons Attribution-NonCommercial-NoDerivatives 4.0 International License (CC BY-NC-ND)
Abstract
To investigate the function of melatonin (MT) on nitrogen uptake and metabolism in soybean, six groups of treatments, with and without 100 μM melatonin were conducted at low, normal, and high nitrogen levels (1.5, 7.5, and 15 mM, respectively). The related indexes of nitrogen metabolism and the antioxidant system of seedlings were measured and analysed. Results indicated that MT could enhance the level of nitrogen metabolism by upregulating the coding genes of enzymes related to nitrogen metabolism and increasing total nitrogen content, especially under low nitrogen levels. Under high nitrogen conditions, the addition of MT not only accelerated ammonium assimilation and utilisation by enhancing the activity of glutamine synthetase involved in ammonium assimilation, but also reduced the extent of membrane lipid peroxidation to alleviate the degree of damage by improving the activity of antioxidant enzymes. In addition, MT enhanced soybean growth with positive effects in morphological changes at different nitrogen levels, including significantly increased stem diameter, total leaf area, and root nodule number, and biomass accumulation. Finally, biomass accumulation increased under low, normal, and high nitrogen levels by 9.80%, 14.06%, and 11.44%, respectively. The results suggested that MT could enhance the soybean tolerance to low and excessive N treatments.
Keywords: crop physiology, legumes, melanin, nitrogen inappropriate, nitrogen metabolism, nitrogen nutrition, nitrogen regulation, soybean.
References
Arnao MB, Hernández-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 | 29069281PubMed |
Arnao MB, Hernández-Ruiz J (2019) Melatonin: a new plant hormone and/or a plant master regulator? Trends in Plant Science 24, 38–48.
| Melatonin: a new plant hormone and/or a plant master regulator?Crossref | GoogleScholarGoogle Scholar | 30446305PubMed |
Arora D, Bhatla SC (2017) Melatonin and nitric oxide regulate sunflower seedling growth under salt stress accompanying differential expression of Cu/Zn SOD and Mn SOD. Free Radical Biology and Medicine 106, 315–328.
| Melatonin and nitric oxide regulate sunflower seedling growth under salt stress accompanying differential expression of Cu/Zn SOD and Mn SOD.Crossref | GoogleScholarGoogle Scholar | 28254544PubMed |
Arun M, Radhakrishnan R, Ai TN, Naing AH, Lee IJ, Kim CK (2016) Nitrogenous compounds enhance the growth of petunia and reprogram biochemical changes against the adverse effect of salinity. The Journal of Horticultural Science and Biotechnology 91, 562–572.
| Nitrogenous compounds enhance the growth of petunia and reprogram biochemical changes against the adverse effect of salinity.Crossref | GoogleScholarGoogle Scholar |
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
| 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 |
Bergersen FJ (1958) The bacterial component of soybean root nodules; changes in respiratory activity, cell dry weight and nucleic acid content with increasing nodule age. Journal of General Microbiology 19, 312–323.
| The bacterial component of soybean root nodules; changes in respiratory activity, cell dry weight and nucleic acid content with increasing nodule age.Crossref | GoogleScholarGoogle Scholar | 13587897PubMed |
Bi YM, Wang RL, Zhu T, Rothstein SJ (2007) Global transcription profiling reveals differential responses to chronic nitrogen stress and putative nitrogen regulatory components in Arabidopsis. BMC Genomics 8, 281
| Global transcription profiling reveals differential responses to chronic nitrogen stress and putative nitrogen regulatory components in Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 17705847PubMed |
Byeon Y, Back K (2014) An increase in melatonin in transgenic rice causes pleiotropic phenotypes, including enhanced seedling growth, delayed flowering, and low grain yield. Journal of Pineal Research 56, 408–414.
| An increase in melatonin in transgenic rice causes pleiotropic phenotypes, including enhanced seedling growth, delayed flowering, and low grain yield.Crossref | GoogleScholarGoogle Scholar | 24571270PubMed |
Cafaro La Menza N, Monzon JP, Specht JE, Grassini P (2017) Is soybean yield limited by nitrogen supply? Field Crops Research 213, 204–212.
| Is soybean yield limited by nitrogen supply?Crossref | GoogleScholarGoogle Scholar |
Cao L, Jin XJ, Zhang YX (2019) Melatonin confers drought stress tolerance in soybean (Glycine max L.) by modulating photosynthesis, osmolytes, and reactive oxygen metabolism. Photosynthetica 57, 812–819.
| Melatonin confers drought stress tolerance in soybean (Glycine max L.) by modulating photosynthesis, osmolytes, and reactive oxygen metabolism.Crossref | GoogleScholarGoogle Scholar |
Cataldo DA, Maroon M, Schrader LE, Youngs VL (1975) Rapid colorimetric determination of nitrate in plant tissue by nitration of salicylic acid. Communications in Soil Science and Plant Analysis 6, 71–80.
| Rapid colorimetric determination of nitrate in plant tissue by nitration of salicylic acid.Crossref | GoogleScholarGoogle Scholar |
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 Q, Wu W, Zhao T, Tan W, Tian J, Liang C (2019) Complex gene regulation underlying mineral nutrient homeostasis in soybean root response to acidity stress. Genes 10, 402
| Complex gene regulation underlying mineral nutrient homeostasis in soybean root response to acidity stress.Crossref | GoogleScholarGoogle Scholar |
Chen J, Wang Z, Liu S, Zhang S, Ge C, Shen Q, Ma H, Zhang X, Dong H, Zhao X, Liu R, Pang C (2021) Nitrogen stress inhibits root growth by regulating cell wall and hormone changes in cotton (Gossypium hirsutum L.). Journal of Agronomy and Crop Science 1–18.
| Nitrogen stress inhibits root growth by regulating cell wall and hormone changes in cotton (Gossypium hirsutum L.).Crossref | GoogleScholarGoogle Scholar |
Cheng L, Yuan HY, Ren R, Zhao SQ, Han YP, Zhou QY, Ke DX, Wang YX, Wang L (2016) Genome-wide identification, classification, and expression analysis of amino acid transporter gene family in Glycine Max. Frontiers in Plant Science 7, 515
| Genome-wide identification, classification, and expression analysis of amino acid transporter gene family in Glycine Max.Crossref | GoogleScholarGoogle Scholar | 27148336PubMed |
Ciampitti IA, Salvagiotti F (2018) New insights into soybean biological nitrogen fixation. Agronomy Journal 110, 1185–1196.
| New insights into soybean biological nitrogen fixation.Crossref | GoogleScholarGoogle Scholar |
Creighton MT, Sanmartín M, Kataya ARA, Averkina IO, Heidari B, Nemie-Feyissa D, Sánchez-Serrano JJ, Lillo C (2017) Light regulation of nitrate reductase by catalytic subunits of protein phosphatase 2A. Planta 246, 701–710.
| Light regulation of nitrate reductase by catalytic subunits of protein phosphatase 2A.Crossref | GoogleScholarGoogle Scholar | 28656346PubMed |
Du Q, Zhou L, Chen P, Liu X, Song C, Yang F, Wang X, Liu W, Sun X, Du J, Liu J, Shu K, Yang W, Yong T (2020) Relay-intercropping soybean with maize maintains soil fertility and increases nitrogen recovery efficiency by reducing nitrogen input. The Crop Journal 8, 140–152.
| Relay-intercropping soybean with maize maintains soil fertility and increases nitrogen recovery efficiency by reducing nitrogen input.Crossref | GoogleScholarGoogle Scholar |
Duan W, Wang Q, Zhang H, Xie B, Li A, Hou F, Dong S, Wang B, Qin Z, Zhang L (2018) Comparative study on carbon–nitrogen metabolism and endogenous hormone contents in normal and overgrown sweetpotato. South African Journal of Botany 115, 199–207.
| Comparative study on carbon–nitrogen metabolism and endogenous hormone contents in normal and overgrown sweetpotato.Crossref | GoogleScholarGoogle Scholar |
Erdal S (2019) Melatonin promotes plant growth by maintaining integration and coordination between carbon and nitrogen metabolisms. Plant Cell Reports 38, 1001–1012.
| Melatonin promotes plant growth by maintaining integration and coordination between carbon and nitrogen metabolisms.Crossref | GoogleScholarGoogle Scholar | 31069499PubMed |
Erland LAE, Saxena PK (2018) Melatonin in plant morphogenesis. In Vitro Cellular & Developmental Biology-Plant 54, 3–24.
| Melatonin in plant morphogenesis.Crossref | GoogleScholarGoogle Scholar |
Fan J, Xie Y, Zhang Z, Chen L (2018) Melatonin: a multifunctional factor in plants. International Journal of Molecular Sciences 19, 1528
| Melatonin: a multifunctional factor in plants.Crossref | GoogleScholarGoogle Scholar |
Gavili E, Moosavi AA, Zahedifar M (2019) Integrated effects of cattle manure-derived biochar and soil moisture conditions on soil chemical characteristics and soybean yield. Archives of Agronomy and Soil Science 65, 1758–1774.
| Integrated effects of cattle manure-derived biochar and soil moisture conditions on soil chemical characteristics and soybean yield.Crossref | GoogleScholarGoogle Scholar |
Giehl RFH, Laginha AM, Duan F, Rentsch D, Yuan L, von Wirén N (2017) A critical role of AMT2;1 in root-to-shoot translocation of ammonium in Arabidopsis. Molecular Plant 10, 1449–1460.
| A critical role of AMT2;1 in root-to-shoot translocation of ammonium in Arabidopsis.Crossref | GoogleScholarGoogle Scholar | 29032248PubMed |
Gong B, Yan Y, Wen D, Shi Q (2017) Hydrogen peroxide produced by NADPH oxidase: a novel downstream signaling pathway in melatonin-induced stress tolerance in Solanum lycopersicum. Physiologia Plantarum 160, 396–409.
| Hydrogen peroxide produced by NADPH oxidase: a novel downstream signaling pathway in melatonin-induced stress tolerance in Solanum lycopersicum.Crossref | GoogleScholarGoogle Scholar | 28464254PubMed |
Grassini P, Specht JE, Tollenaar M, Ciampitti I, Cassman KG (2014) High-yield maize-soybean cropping systems in the US Corn Belt. In ‘Crop physiology’, 2nd edn. pp. 17–41. (Academic Press: Cambridge, MA, USA)
Gu R, Duan F, An X, Zhang F, von Wirén N, Yuan L (2013) Characterization of AMT-mediated high-affinity ammonium uptake in roots of maize (Zea mays L.). Plant and Cell Physiology 54, 1515–1524.
| Characterization of AMT-mediated high-affinity ammonium uptake in roots of maize (Zea mays L.).Crossref | GoogleScholarGoogle Scholar | 23832511PubMed |
Guan M, de Bang TC, Pedersen C, Schjoerring JK (2016) Cytosolic glutamine synthetase Gln1;2 is the main isozyme contributing to GS1 activity and can be up-regulated to relieve ammonium toxicity. Plant Physiology 171, 1921–1933.
| Cytosolic glutamine synthetase Gln1;2 is the main isozyme contributing to GS1 activity and can be up-regulated to relieve ammonium toxicity.Crossref | GoogleScholarGoogle Scholar | 27231101PubMed |
Hageman RH, Reed AJ (1980) Nitrate reductase from higher plants. Methods in Enzymology 69, 270–280.
| Nitrate reductase from higher plants.Crossref | GoogleScholarGoogle Scholar |
Hao Q, Yang Y, Shan Z, Chen H, Zhang C, Chen L, Yuan S, Zhang X, Chen S, Yang Z, Qiu D, Zhou X (2021) Genome-wide investigation and expression profiling under abiotic stresses of a soybean unknown function (DUF21) and cystathionine-β-synthase (CBS) domain-containing protein family. Biochemical Genetics 59, 83–113.
| Genome-wide investigation and expression profiling under abiotic stresses of a soybean unknown function (DUF21) and cystathionine-β-synthase (CBS) domain-containing protein family.Crossref | GoogleScholarGoogle Scholar | 32778975PubMed |
Hao QN, Zhou XA, Sha AH, Wang C, Zhou R, Chen SL (2011) Identification of genes associated with nitrogen-use efficiency by genome-wide transcriptional analysis of two soybean genotypes. BMC Genomics 12, 525
| Identification of genes associated with nitrogen-use efficiency by genome-wide transcriptional analysis of two soybean genotypes.Crossref | GoogleScholarGoogle Scholar | 22029603PubMed |
Harper JE (1974) Soil and symbiotic nitrogen requirements for optimum soybean production. Crop Science 14, 255–260.
| Soil and symbiotic nitrogen requirements for optimum soybean production.Crossref | GoogleScholarGoogle Scholar |
Hernández-Ruiz J, Antonio C, Arnao MB (2004) Melatonin: a growth-stimulating compound present in lupin tissues. Planta 220, 140–144.
| Melatonin: a growth-stimulating compound present in lupin tissues.Crossref | GoogleScholarGoogle Scholar | 15232696PubMed |
Hu W, Tie W, Ou W, Yan Y, Kong H, Zuo J, Ding X, Ding Z, Liu Y, Wu C, Guo Y, Shi H, Li K, Guo A (2018) Crosstalk between calcium and melatonin affects postharvest physiological deterioration and quality loss in cassava. Postharvest Biology and Technology 140, 42–49.
| Crosstalk between calcium and melatonin affects postharvest physiological deterioration and quality loss in cassava.Crossref | GoogleScholarGoogle Scholar |
Kong L, Xie Y, Hu L, Si J, Wang Z (2017) Excessive nitrogen application dampens antioxidant capacity and grain filling in wheat as revealed by metabolic and physiological analyses. Scientific Reports 7, 43363
| Excessive nitrogen application dampens antioxidant capacity and grain filling in wheat as revealed by metabolic and physiological analyses.Crossref | GoogleScholarGoogle Scholar | 28233811PubMed |
Kushwaha HR, Singh AK, Sopory SK, Singla-Pareek SL, Pareek A (2009) Genome wide expression analysis of CBS domain containing proteins in Arabidopsis thaliana (L.) Heynh and Oryza sativa L. reveals their developmental and stress regulation. BMC Genomics 10, 200
| Genome wide expression analysis of CBS domain containing proteins in Arabidopsis thaliana (L.) Heynh and Oryza sativa L. reveals their developmental and stress regulation.Crossref | GoogleScholarGoogle Scholar | 19400948PubMed |
Lawlor DW (2002) Carbon and nitrogen assimilation in relation to yield: mechanisms are the key to understanding production systems. Journal of Experimental Botany 53, 773–787.
| Carbon and nitrogen assimilation in relation to yield: mechanisms are the key to understanding production systems.Crossref | GoogleScholarGoogle Scholar | 11912221PubMed |
Li C, Liang B, Chang C, Wei Z, Zhou S, Ma F (2016) Exogenous melatonin improved potassium content in Malus under different stress conditions. Journal of Pineal Research 61, 218–229.
| Exogenous melatonin improved potassium content in Malus under different stress conditions.Crossref | GoogleScholarGoogle Scholar | 27145234PubMed |
Li M, Xu J, Wang X, Fu H, Zhao M, Wang H, Shi L (2018) Photosynthetic characteristics and metabolic analyses of two soybean genotypes revealed adaptive strategies to low-nitrogen stress. Journal of Plant Physiology 229, 132–141.
| Photosynthetic characteristics and metabolic analyses of two soybean genotypes revealed adaptive strategies to low-nitrogen stress.Crossref | GoogleScholarGoogle Scholar | 30081252PubMed |
Liang C, Li A, Yu H, Li W, Liang C, Guo S, Zhang R, Chu C (2017) Melatonin regulates root architecture by modulating auxin response in rice. Frontiers in Plant Science 8, 134
| Melatonin regulates root architecture by modulating auxin response in rice.Crossref | GoogleScholarGoogle Scholar | 28223997PubMed |
Lin CC, Kao CH (1996) Disturbed ammonium assimilation is associated with growth inhibition of roots in rice seedlings caused by NaCl. Plant Growth Regulation 18, 233–238.
| Disturbed ammonium assimilation is associated with growth inhibition of roots in rice seedlings caused by NaCl.Crossref | GoogleScholarGoogle Scholar |
Liu B, Shen W, Wei H, Smith H, Louws FJ, Steadman JR, Correll JC (2016a) Rhizoctonia communities in soybean fields and their relation with other microbes and nematode communities. European Journal of Plant Pathology 144, 671–686.
| Rhizoctonia communities in soybean fields and their relation with other microbes and nematode communities.Crossref | GoogleScholarGoogle Scholar |
Liu J, Zhang R, Sun Y, Liu Z, Jin W, Sun Y (2016b) The beneficial effects of exogenous melatonin on tomato fruit properties. Scientia Horticulturae 207, 14–20.
| The beneficial effects of exogenous melatonin on tomato fruit properties.Crossref | GoogleScholarGoogle Scholar |
Massange-Sánchez JA, Palmeros-Suárez PA, Espitia-Rangel E, Rodríguez-Arévalo I, Sánchez-Segura L, Martínez-Gallardo NA, Alatorre-Cobos F, Tiessen A, Délano-Frier JP (2016) Overexpression of grain Amaranth (Amaranthus hypochondriacus) AhERF or AhDOF transcription factors in Arabidopsis thaliana increases water-deficit and salt-stress tolerance, respectively, via contrasting stress-amelioration mechanisms. PLoS One 11, e0164280
| Overexpression of grain Amaranth (Amaranthus hypochondriacus) AhERF or AhDOF transcription factors in Arabidopsis thaliana increases water-deficit and salt-stress tolerance, respectively, via contrasting stress-amelioration mechanisms.Crossref | GoogleScholarGoogle Scholar | 27749893PubMed |
Mohamed IAA, Shalby N, El-Badri AMA, Saleem MH, Khan MN, Nawaz MA, Qin M, Agami RA, Kuai J, Wang B, Zhou G (2020) Stomata and xylem vessels traits improved by melatonin application contribute to enhancing salt tolerance and fatty acid composition of Brassica napus L. plants. Agronomy 10, 1186
| Stomata and xylem vessels traits improved by melatonin application contribute to enhancing salt tolerance and fatty acid composition of Brassica napus L. plants.Crossref | GoogleScholarGoogle Scholar |
Nakano Y, Asada K (1981) Hydrogen peroxide is scavenged by ascorbate-specific peroxidase in spinach chloroplasts. Plant and Cell Physiology 22, 867–880.
| Hydrogen peroxide is scavenged by ascorbate-specific peroxidase in spinach chloroplasts.Crossref | GoogleScholarGoogle Scholar |
Nawaz MA, Yang SH, Chung G (2018) Wild soybeans: an opportunistic resource for soybean improvement. In ‘Rediscovery of landraces as a resource for the future’. pp. 160–174. (IntechOpen Limited: London, UK)
Oliveira HC, Freschi L, Sodek L (2013) Nitrogen metabolism and translocation in soybean plants subjected to root oxygen deficiency. Plant Physiology and Biochemistry 66, 141–149.
| Nitrogen metabolism and translocation in soybean plants subjected to root oxygen deficiency.Crossref | GoogleScholarGoogle Scholar | 23500717PubMed |
Park S, Back K (2012) Melatonin promotes seminal root elongation and root growth in transgenic rice after germination. Journal of Pineal Research 53, 385–389.
| Melatonin promotes seminal root elongation and root growth in transgenic rice after germination.Crossref | GoogleScholarGoogle Scholar | 22640001PubMed |
Pinto E, Fidalgo F, Teixeira J, Aguiar AA, Ferreira IMPLVO (2014) Influence of the temporal and spatial variation of nitrate reductase, glutamine synthetase and soil composition in the N species content in lettuce (Lactuca sativa. Plant Science 219–220, 35–41.
| Influence of the temporal and spatial variation of nitrate reductase, glutamine synthetase and soil composition in the N species content in lettuce (Lactuca sativa.Crossref | GoogleScholarGoogle Scholar | 24576762PubMed |
Purcell LC, Salmeron M, Ashlock L (2014) Soybean growth and development. In ‘Arkansas soybean production handbook. Vol. 197’. pp. 1–8. (University of Arkansas Division of Agriculture: Little Rock, AR, USA)
Qiao Y, Yin L, Wang B, Ke Q, Deng X, Wang S (2019) Melatonin promotes plant growth by increasing nitrogen uptake and assimilation under nitrogen deficient condition in winter wheat. Plant Physiology and Biochemistry 139, 342–349.
| Melatonin promotes plant growth by increasing nitrogen uptake and assimilation under nitrogen deficient condition in winter wheat.Crossref | GoogleScholarGoogle Scholar | 30952086PubMed |
Ray JD, Heatherly LG, Fritschi FB (2006) Influence of large amounts of nitrogen on nonirrigated and irrigated soybean. Crop Science 46, 52–60.
| Influence of large amounts of nitrogen on nonirrigated and irrigated soybean.Crossref | GoogleScholarGoogle Scholar |
Raza MA, Bin Khalid MH, Zhang X, Feng LY, Khan I, Hassan MJ, Ahmed M, Ansar M, Chen YK, Fan YF, Yang F, Yang W (2019) Effect of planting patterns on yield, nutrient accumulation and distribution in maize and soybean under relay intercropping systems. Scientific Reports 9, 4947
| Effect of planting patterns on yield, nutrient accumulation and distribution in maize and soybean under relay intercropping systems.Crossref | GoogleScholarGoogle Scholar | 30894625PubMed |
Shaha RK (2003) Role of light in the regulation of the nitrate reductase level in lentil (Lens esculenta L.). Pakistan Journal of Biological Sciences 6, 1802–1807.
| Role of light in the regulation of the nitrate reductase level in lentil (Lens esculenta L.).Crossref | GoogleScholarGoogle Scholar |
Sherrard JH, Dalling MJ (1979) In vitro stability of nitrate reductase from wheat leaves: I. Stability of highly purified enzyme and its component activities. Plant Physiology 63, 346–353.
| In vitro stability of nitrate reductase from wheat leaves: I. Stability of highly purified enzyme and its component activities.Crossref | GoogleScholarGoogle Scholar | 16660726PubMed |
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 |
Sinclair TR, de Wit CT (1975) Photosynthate and nitrogen requirements for seed production by various crops. Science 189, 565–567.
| Photosynthate and nitrogen requirements for seed production by various crops.Crossref | GoogleScholarGoogle Scholar | 17798304PubMed |
Singh KK, Saha S, Kadiravana RC, Mazumdar D, Rai V, Ghosh S (2020) Ammonium metabolism in Selaginella bryopteris in response to dehydration-rehydration and characterisation of desiccation tolerant, thermostable, cytosolic glutamine synthetase from plant. Functional Plant Biology 48, 257–267.
| Ammonium metabolism in Selaginella bryopteris in response to dehydration-rehydration and characterisation of desiccation tolerant, thermostable, cytosolic glutamine synthetase from plant.Crossref | GoogleScholarGoogle Scholar |
Skopelitis DS, Paranychianakis NV, Paschalidis KA, Pliakonis ED, Delis ID, Yakoumakis DI, Kouvarakis A, Papadakis AK, Stephanou EG, Roubelakis-Angelakis KA (2006) Abiotic stress generates ROS that signal expression of anionic glutamate dehydrogenases to form glutamate for proline synthesis in tobacco and grapevine. The Plant Cell 18, 2767–2781.
| Abiotic stress generates ROS that signal expression of anionic glutamate dehydrogenases to form glutamate for proline synthesis in tobacco and grapevine.Crossref | GoogleScholarGoogle Scholar | 17041150PubMed |
Takahashi M, Nakayama N, Arihara J (2005) Plant nitrogen levels and photosynthesis in the supernodulating soybean (Glycine max L. Merr.) cultivar ‘Sakukei 4’. Plant Production Science 8, 412–418.
| Plant nitrogen levels and photosynthesis in the supernodulating soybean (Glycine max L. Merr.) cultivar ‘Sakukei 4’.Crossref | GoogleScholarGoogle Scholar |
Tamagno S, Balboa GR, Assefa Y, Kovács P, Casteel SN, Salvagiotti F, García FO, Stewart WM, Ciampitti IA (2017) Nutrient partitioning and stoichiometry in soybean: a synthesis-analysis. Field Crops Research 200, 18–27.
| Nutrient partitioning and stoichiometry in soybean: a synthesis-analysis.Crossref | GoogleScholarGoogle Scholar |
Timpo EE, Neyra CA (1983) Expression of nitrate and nitrite reductase activities under various forms of nitrogen nutrition in Phaseolus vulgaris L. Plant Physiology 72, 71–75.
| Expression of nitrate and nitrite reductase activities under various forms of nitrogen nutrition in Phaseolus vulgaris L.Crossref | GoogleScholarGoogle Scholar | 16662985PubMed |
Turk H, Erdal S (2015) Melatonin alleviates cold-induced oxidative damage in maize seedlings by up-regulating mineral elements and enhancing antioxidant activity. Journal of Plant Nutrition and Soil Science 178, 433–439.
| Melatonin alleviates cold-induced oxidative damage in maize seedlings by up-regulating mineral elements and enhancing antioxidant activity.Crossref | GoogleScholarGoogle Scholar |
Wang WX, Zhang RM, Sun Y, Liu JL (2016) Effect of exogenous melatonin on the antioxidant system of cucumber seedlings under nitrate stress. Acta Horticulturae Sinica 43, 695–703.
| Effect of exogenous melatonin on the antioxidant system of cucumber seedlings under nitrate stress.Crossref | GoogleScholarGoogle Scholar |
Wang X, Li D, Jiang J, Dong Z, Ma Y (2017) Soybean NAC gene family: sequence analysis and expression under low nitrogen supply. Biologia Plantarum 61, 473–482.
| Soybean NAC gene family: sequence analysis and expression under low nitrogen supply.Crossref | GoogleScholarGoogle Scholar |
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 |
Xia X, Ma C, Dong S, Xu Y, Gong Z (2017) Effects of nitrogen concentrations on nodulation and nitrogenase activity in dual root systems of soybean plants. Soil Science and Plant Nutrition (Tokyo) 63, 470–482.
| Effects of nitrogen concentrations on nodulation and nitrogenase activity in dual root systems of soybean plants.Crossref | GoogleScholarGoogle Scholar |
Xie M, Chung CYL, Li MW, Wong FL, Wang X, Liu A, Wang Z, Leung AKY, Wong TH, Tong SW, Xiao Z, Fan K, Ng MS, Qi X, Yang L, Deng T, He L, Chen L, Fu A, Ding Q, He J, Chung G, Isobe S, Tanabata T, Valliyodan B, Nguyen HT, Cannon SB, Foyer CH, Chan TF, Lam HM (2019) A reference-grade wild soybean genome. Nature Communications 10, 1216
| A reference-grade wild soybean genome.Crossref | GoogleScholarGoogle Scholar | 30872580PubMed |
Xu G, Fan X, Miller AJ (2012) Plant nitrogen assimilation and use efficiency. Annual Review of Plant Biology 63, 153–182.
| Plant nitrogen assimilation and use efficiency.Crossref | GoogleScholarGoogle Scholar | 22224450PubMed |
Yanagisawa S, Akiyama A, Kisaka H, Uchimiya H, Miwa T (2004) Metabolic engineering with Dof1 transcription factor in plants: improved nitrogen assimilation and growth under low-nitrogen conditions. Proceedings of the National Academy of Sciences of the United States of America 101, 7833–7838.
| Metabolic engineering with Dof1 transcription factor in plants: improved nitrogen assimilation and growth under low-nitrogen conditions.Crossref | GoogleScholarGoogle Scholar | 15136740PubMed |
Yong TW, Chen P, Dong Q, Du Q, Yang F, Wang XC, Liu WG, Yang WY (2018) Optimized nitrogen application methods to improve nitrogen use efficiency and nodule nitrogen fixation in a maize–soybean relay intercropping system. Journal of Integrative Agriculture 17, 664–676.
| Optimized nitrogen application methods to improve nitrogen use efficiency and nodule nitrogen fixation in a maize–soybean relay intercropping system.Crossref | GoogleScholarGoogle Scholar |
Zeng A, Chen P, Korth KL, Ping J, Thomas J, Wu C, Srivastava S, Pereira A, Hancock F, Brye K, Ma J (2019) RNA sequencing analysis of salt tolerance in soybean (Glycine max. Genomics 111, 629–635.
| RNA sequencing analysis of salt tolerance in soybean (Glycine max.Crossref | GoogleScholarGoogle Scholar | 29626511PubMed |
Zhang ZL, Zai WJ, Li XF (2016) ‘Plant physiology experimental guide’, 5th edn. pp. 139–141. (Higher Education Press: Beijing, China)
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
| Melatonin alleviates aluminium toxicity through modulating antioxidative enzymes and enhancing organic acid anion exudation in soybean.Crossref | GoogleScholarGoogle Scholar | 32480624PubMed |
Zhang R, Sun Y, Liu Z, Jin W, Sun Y (2017b) Effects of melatonin on seedling growth, mineral nutrition, and nitrogen metabolism in cucumber under nitrate stress. Journal of Pineal Research 62, e12403
| Effects of melatonin on seedling growth, mineral nutrition, and nitrogen metabolism in cucumber under nitrate stress.Crossref | GoogleScholarGoogle Scholar |
Zhang MH, Wang BY, Li S, Li K, Chen Y, He B, Sun DM (2018) Effect of uniconazole and rhizobium interaction on growth and nitrogen fixation in soybean. Soybean Science 37, 112––116.
| Effect of uniconazole and rhizobium interaction on growth and nitrogen fixation in soybean.Crossref | GoogleScholarGoogle Scholar |
Zhang M, He S, Qin B, Jin X, Wang M, Ren C, Cao L, Zhang Y (2020) Exogenous melatonin reduces the inhibitory effect of osmotic stress on antioxidant properties and cell ultrastructure at germination stage of soybean. PLoS One 15, e0243537
| Exogenous melatonin reduces the inhibitory effect of osmotic stress on antioxidant properties and cell ultrastructure at germination stage of soybean.Crossref | GoogleScholarGoogle Scholar | 33320882PubMed |
Zhou X, Yang T, Jiang Z, He Z, Zou Z (2019) Regulation of melatonin on chlorophyll fluorescence and nitrate accumulation in lettuce seedlings under excess nitrate stress. IOP conference series. Earth and Environmental Science 330, 42043
| Regulation of melatonin on chlorophyll fluorescence and nitrate accumulation in lettuce seedlings under excess nitrate stress.Crossref | GoogleScholarGoogle Scholar |
Zou JN, Yu Q, Jin XJ, Wang MY, Qin B, Ren CY, Wang MX, Zhang YX (2020) Effects of exogenous melatonin on physiology and yield of soybean during seed filling stage under drought stress. Acta Agronomica Sinica 46, 745–758.
| Effects of exogenous melatonin on physiology and yield of soybean during seed filling stage under drought stress.Crossref | GoogleScholarGoogle Scholar |
