Open Access is an initiative that aims to make scientific research freely available to all. To date our community has made over 100 million downloads. It’s based on principles of collaboration, unobstructed discovery, and, most importantly, scientific progression. As PhD students, we found it difficult to access the research we needed, so we decided to create a new Open Access publisher that levels the playing field for scientists across the world. How? By making research easy to access, and puts the academic needs of the researchers before the business interests of publishers.
We are a community of more than 103,000 authors and editors from 3,291 institutions spanning 160 countries, including Nobel Prize winners and some of the world’s most-cited researchers. Publishing on IntechOpen allows authors to earn citations and find new collaborators, meaning more people see your work not only from your own field of study, but from other related fields too.
To purchase hard copies of this book, please contact the representative in India:
CBS Publishers & Distributors Pvt. Ltd.
www.cbspd.com
|
customercare@cbspd.com
Metabolic engineering in plant can be describe as a tool using molecular biological technologies which promotes enzymatic reactions that can enhance the biosynthesis of existing compounds such as glycine betaine (GB) in plant species that are able to accumulate GB, or produce news compounds like GB in non-accumulators plants. Moreover we can include to these definition, the mediation in the degradation of diverse compounds in plant organism. For decades, one of the most popular ideas in metabolic engineering literature is the idea that the improvement of gly betaine or melatonin accumulation in plant under environmental stress can be the main window to ameliorate stress tolerance in diverse plant species. A challenging problem in this domain is the integration of different molecular technologies like transgenesis, enzyme kinetics, promoter analysis, biochemistry and genetics, protein sorting, cloning or comparative physiology to reach that objective. A large number of approaches have been developed over the last few decades in metabolic engineering to overcome this problem. Therefore, we examine some previous work and propose some understanding about the use of metabolic engineering in plant stress tolerance. Moreover, this chapter will focus on melatonin (Hormone) and gly betaine (Osmolyte) biosynthesis pathways in engineering stress resistance.
Key Laboratory of Agro-Forestry Environmental Processes and Ecological Regulation of Hainan Province, Center for Eco-Environmental Restoration Engineering of Hainan Province, School of Ecological and Environmental Sciences, Hainan University, Haikou, Hainan, China
Miao Ling-Feng
Key Laboratory of Agro-Forestry Environmental Processes and Ecological Regulation of Hainan Province, Center for Eco-Environmental Restoration Engineering of Hainan Province, School of Ecological and Environmental Sciences, Hainan University, Haikou, Hainan, China
Li Da-Dong
Key Laboratory of Agro-Forestry Environmental Processes and Ecological Regulation of Hainan Province, Center for Eco-Environmental Restoration Engineering of Hainan Province, School of Ecological and Environmental Sciences, Hainan University, Haikou, Hainan, China
Yang Fan
Key Laboratory of Agro-Forestry Environmental Processes and Ecological Regulation of Hainan Province, Center for Eco-Environmental Restoration Engineering of Hainan Province, School of Ecological and Environmental Sciences, Hainan University, Haikou, Hainan, China
*Address all correspondence to: kosmosofmalick@gmail.com
1. Introduction
The global climate change influence negatively plant growth and development via the increase of the intensity of various abiotic stresses such as drought, chilling, salinity, waterlogging or flooding. Environmental stresses are one of the most threatening factors that can cause massive losses in agricultural crop production, ranging from 50–70% [1]. Plant biotechnology and engineering are promising platform for exploring the unlimited potential of many various plants species [2]. In recent years, plant metabolism engineering provides successful pathways to increase the production of metabolites that can significantly counterattack the damages caused by diverse abiotic stresses [3]. To improve stress tolerance in plant, various metabolic engineering technologies were used to introduce or increase the synthesis of diverse osmolytes, secondary metabolites or hormones. The adaptation of various plant species to stressful environments can be managed through: (i) the identification of diverse mechanisms developed by plants to counterbalance abiotic stresses (ii) and the improvement of these processes in plants by metabolic engineering [4, 5]. Plant by-products including hormone (melatonin, MT) and osmoprotectant (glycine betaine, GB) that play a prominent roles in plant stress tolerance have been targeting in various plant species to counterattack environmental stresses. The clarification of the biosynthetic pathway of various plant compounds has provided the possibility to metabolically engineer new capabilities in plants as well as successfully engineer whole pathways into microbial systems [6]. Under environmental stresses plant is able to accumulate different molecules such as melatonin or glycine betaine to provide stress tolerance by counteracting with oxidative stress caused by drought, chilling, salinity or heavy metal stresses [7, 8, 9]. The protective properties of GB and MT in plant under abiotic stresses had made these substances targets for plant engineering resistance.
The natural biosynthesis of glycine betaine takes place in marine algae and various higher plant species belong to diverse families, counting the Gramineae, Malvaceae, Asteraceae, or Amaranthaceae [10, 11, 12, 13, 14]. Glycine betaine accumulation in non-accumulators and accumulators plant species under environmental stresses has long been a target for engineering stress resistance [15, 16]. The biosynthesis of glycine betaine passes by choline → betaine aldehyde → glycine betaine pathways. Most of the enzymes involving in these pathways such as choline monooxygenase (CMO) or betaine aldehyde dehydrogenase (BADH) have been identified, and genes for some of them have been cloned [4, 13].
Indeed, GB as a non-toxic molecule is biosynthesized through two phases of choline oxidation: the first step (Choline → betaine aldehyde) is catalyzed by CMO, and the second step (Betaine aldehyde → glycine betaine) is activated by BADH [13, 17]. The expression of CMO or BADH in tobacco has been done via the cDNA from two natural glycine betaine accumulators; spinach and sugar beet plants. The 35S promoter from plant virus, cauliflower mosaic virus which is a fundamental element of transgenic constructs in the majority of genetically modified plant species was used in transgenic tobacco to control the expression of cDNA for BADH pathway [18]. Also, a crucial tool in metabolism engineering of glycine betaine pathway is the use of a single gene codA from Arthrobacter globiformis which is involved in the synthesis of GB [19]. However, GB accumulation in transgenic plants depends on the capacity of endogenous choline uptake, the type of gene that catalyzes the GB biosynthetic pathway, and the localization of the transgene product in a particular cellular compartment [20].
Melatonin a plant hormone identified in a wide variety of animals and plants, has been extensively studied in plants for its properties to counteract with various environmental and biotic stresses [21, 22]. Transcriptome analyses indicated that melatonin primarily affects the pathways of plant hormone signal transduction and biosynthesis of secondary metabolites [23]. In plant the biosynthesis of melatonin is initiated with tryptophan which is converted in serotonin, and between the tryptophan and melatonin, the enzymes hydroxyindole-O-methyltransferase and caffeic acid O-methyltransferase (ASMT/COMT) catalyzed a reaction that produce an intermediate molecule named 5-methoxytryptamine [24, 25, 26]. The related enzymes involved in melatonin biosynthesis pathway have been targeted to improve stress tolerance in diverse plant species. The over expression of COMT like gene (TaCOMT) in a transgenic Arabidopsis via various metabolic engineering techniques (cloning, transgenesis, genetics or promoter analysis) provided drought tolerance by increasing the concentration of melatonin [27]. Other enzymes such as serotonin N-acetyltransferase (MsSNAT) involve in melatonin biosynthesis have been targeted in rice [28] or Arabidopsis [29] to provide stress tolerance, either to clarify the role of melatonin in plant. This chapter will focus on the use of glycine betaine, spermidine and melatonin in plant metabolism engineering, particularly in stress engineering.
Glycinebetaine is a quaternary ammonium compound that appears commonly in a large diversity of plants, animals and microorganisms, the first betaine discovered was trimethylglycine (Figure 1) named also N, N,N-trimethylglycine [8, 12]. The glycine betaine as a osmolytes is a crucial non-toxic molecule that is accumulated in various plant species under environmental stresses [15].
Figure 1.
N,N,N-trimethylglycine.
2.1 Glycine betaine biosynthesis
GB synthesis begins with an essential molecule named choline, synthesized through three sequential adenosyl-methionine dependent methylations of phospho-ethanolamine catalyzed by the cytosolic enzyme phosphoethanolamine methyltransferase (phosphoethanolamine N-methyltransferase) [30]. In plant, the biosynthesis of GB is two steps of oxidation initiated with choline and then betaine aldehyde (Figure 2). In plant such as Arabidopsis the biosynthesis of choline can be resume by this following line: L-serine → ethanolamine → O-phosphoethanolamine → N-methylethanolamine phosphate → N-dimethylethanolamine phosphate → phosphocholine → choline [31, 32, 33]. Pursuing the transformation of N-methylethanolamine phosphate by phosphoethanolamine methyltransferase (PeMt) the byproduct differs according to the plant species, for instance in that stage the spinach produce choline like in Arabidopsis choline biosynthesis pathway, meanwhile in tobacco PeMt catalyzed a reaction that synthesize phosphatidyl-choline in the first place then metabolized to choline [8, 15]. The first stage of GB biosynthesis is modulated by CMO which is an Fd-dependent monooxygenase with a Rieske-type iron–sulfur (2Fe-2S) cluster-binding motif. The second stage of GB biosynthesis is catalyzed by BADH, an enzyme belong to the superfamily of aldehyde dehydrogenases which is an NAD+ or NADP+ dependent [17, 34].
Figure 2.
Diagram of GB biosynthesis in brief.
2.2 Glycine betaine and environmental stress
Many plants are able to accumulate naturally GB and diverse osmoprotectants to balance the disruption of plant cell homeostasis caused by environmental stress such as drought, chilling, salinity or high temperature [8, 35, 36]. Many studies have been reported on the positive effect of endogenous GB in plants under abiotic stresses. The role of glycine betaine in osmotic adjustment was related in Amaranthus tricolor [37] and Hordeum maritimum [38] under salinity. The role of GB against oxidative stress via scavenging the reactive oxygen species and increasing the antioxidant activities was reported in many studies [39, 40, 41]. For these reasons, the use of glycine betaine in non accumulator and accumulator plant species become more popular in plant physiology. Indeed, several reports have related the positive effect of GB in transgenic plants (Table 1).
Reported roles of GB in transgenic plant under abiotic stresses.
2.3 Glycine betaine engineering
The idea of introducing GB pathway and its high accumulation in plant under environmental stresses has long been a target for metabolism engineering stress tolerance. The feasibility of this process was based on comparative physiology and genetic evidence from a maize mutant [15, 54]. Metabolic engineering of the biosynthesis of GB from choline by using various genes such as codA or BADH gene gained more attention to improve stress tolerance in crop and woody plants that are incapable of synthesizing GB under abiotic stresses [8, 18, 55]. Moreover, genetic engineering is also use to increase GB accumulation in various plant species which produce a low concentration of GB that might not be sufficient for osmoregulation to counteract with abiotic stress [56].
The genes (codA or cDNA BADH) and enzymes involve in GB biosynthesis have been identified and cloned. GB has been successfully synthesized in various targeted organisms and provided stress tolerance via genetic engineering (Table 2).
Overview of GB genetic engineering in various plant species.
2.3.1 Genetic engineering of GB via codA gene
As shown in Table 2, many species that can accumulate or not GB have been targeted via genetic engineering to synthesize or over accumulate GB under both stressed and non-stressed conditions. The choline oxidase (codA) from A. globiformis has been widely used in various transgenic plant species to synthesize GB, and codA has the ability to convert choline in one reaction [56].
The catalytic activity of choline oxidase (EC: 1.1.3.17) in A. globiformis results in this following equation: (Choline + H2O + 2 O2 = glycine betaine + H+ + 2 H2O2) [63]. The codA gene is of particular interest with respect to the engineering of desirable productive traits in crop plants and stress tolerance. In transgenic tomato and brown mustard the codA was targeted to the chloroplast and cytosol which allowed GB accumulation for an increase of stress tolerance [19, 59]. Further, transgenic indica rice showed a significant increase of water-stress tolerance and transcriptome changes via codA gene expression [51]. One of the advantages of using choline oxidase pathway as a tool for engineering GB synthesis in plant is that the addition of a single gene codA is enough for the conversion of choline to GB [8]. The codA transgenic plant has showed their abilities to counteract with environmental stresses such as salinity, high temperature, high light, cold stress and freezing in different plant growth stages [64].
2.3.2 Genetic engineering of GB via BADH gene
The other pathway that provided successful results in genetic engineering of GB biosynthesis in various transgenic plant species is the BADH pathway (Table 2). BADH is one of the most prominent genes involved in the biosynthetic pathway of GB, and its utilization in various plant species has led to an increased tolerance to a variety of environmental stresses [65]. Indeed, the second step of GB biosynthesis is performed by betaine aldehyde dehydrogenase (BADH) that can be encoded by betB or betA gene from E. coli. BADH is an NDA-dependent dehydrogenase that has been characterized and cloned from plants species belong to the Amaranthaceae and Gramineae families [15]. The BADH pathway has been targeted in the chloroplasts in N. tabacum [13] and in peroxisomes in Gramineae [60]. Many studies showed positive results in stress tolerance in transgenic plants with genes betA, betB or both from Escherichia coli encoding Oxygen-dependent choline dehydrogenase (CHDH) and BADH [8]. The catalytic activities of CHDH (EC: 1.1.99.1) encode by betA from E. coli can be resume by this following Eq. (A + choline = AH2 + betaine aldehyde), A (hydrogen acceptor) and AH2 (hydrogen donor) [66]. Meanwhile the catalytic activities of the NAD/NADP-dependent betaine aldehyde dehydrogenase (EC: 1.2.1.8) are done by this equation: (betaine aldehyde + H2O + NAD+ = glycine betaine +2 H+ + NADH) [66, 67]. The equation for the catalytic activities is similar for chloroplastic betaine aldehyde dehydrogenase in sugar beet or spinach compared to those of E. coli.
Melatonin (Figure 3) as an ancient pleiotropic bio-molecule which can be traced back to the origin of life, is present in both animal and plant organisms [24, 68]. In plant, melatonin has been found in diverse family and at different stage of growth: Asteraceae, papaveracea, apiaceae, linaceae, fabaceae, poaceae, rosaceae, lamiaceae, solanaceae, musaceae or vitacea etc. [69].
Figure 3.
N-acetyl-5-methoxytryptamine.
Melatonin (N-acetyl-5-methoxytryptamine), a multifunctional plant hormone, was discovered in plants in 1995 [70]. Moreover, the presence of melatonin in plant was confirmed in Chenopodium rubrum via chromatography/tandem mass spectrometry and radio-immuno-assays [71]. Melatonin has multi-functional actions that improve cellular and organ health in various plant species and it is a powerful antioxidant in both animals and plants [72].
Melatonin functions as a metabolite with numerous roles in plant, including plant stress responses such as chilling, oxidative stress, drought, salt stress and nutrients deficiency, moreover melatonin can regulates plant growth and development, such as root organogenesis, flowering, and senescence [9, 73, 74]. Plenty of studies have focused on the function and regulation of melatonin in transgenic plants because of its crucial role in plant regulation.
3.1 Melatonin biosynthesis pathways in plant
The Figure 4 shows a schematic representation of the biosynthesis of MT, in which the tryptophan is synthesized via shikimic acid pathway that is also responsible for the synthesis of vitamins and aromatic amino acids such as phenylalanine and tyrosine. In plants, tryptophan is converted to Tryptamine via a reaction catalyzed by tryptophan decarboxylase (TDC) [75], and the production of serotonin from Tryptamine is activated by tryptamine 5-hydroxylase [76]. The formation of melatonin is preceded by two reactions from serotonin; the first reaction catalyzed by ASMT transform serotonin to 5-methoxytryptamine, and the last step is catalyzed by N-acetyltransferase [77].
Figure 4.
A schematic representation of melatonin biosynthesis in brief.
As far as we know, there are 6 genes which are involved in plant melatonin biosynthesis: TDC, TPH, T5H, SNAT, ASMT, and COMT [68], and the keys enzymes they encoded are the; L-tryptophan decarboxylase, tryptophan hydroxylase, serotonin-N-acetyltransferase, N-acetylserotonin methyltransferase and hydroxyindole-O-methyltransferase [24].
3.2 Melatonin involve in abiotic stress tolerance
Melatonin is well know as a hormone which can significantly increase the plant survival rates, photosynthetic efficiency and antioxidant activities in plant under environmental stress [74, 78]. For these reasons, many studies were focused on the effects of exogenous melatonin on various plant species under abiotic stress. Indeed, exogenous melatonin could stimulate the biosynthesis of cold tolerance agents and contribute to increase the plant growth and development under cold stress [79]. As show Table 3, the alleviation of environmental stresses by melatonin has been investigated in many plant species: under drought (Zea mays) [89], under heavy metal (Caryaca thayensis) [90], under chilling stress (Cynodon dactylon) [91] and under salinity (Cucumis sativus) [82]. Compared to glycine betaine genetic engineering in plant under stress, the use of melatonin in transgenic plant to provide stress tolerance is fewer. However, there is several studies that focused on the over expression of melatonin via metabolic engineering (Table 3).
Reported roles of MT exogenously applied and in transgenic plant under abiotic stresses.
In Transgenic Arabidopsis the over expression of N-acetyltransferase gene increased salt tolerance via the increase in autophagy, and the reestablishment of redox and ion homeostasis [29]. Furthermore, increase of over-expressing N-acetyltransferase gene enhances the endogenous content in transgenic rice that provoked pleiotropic phenotypes, including enhanced seedling growth, delayed flowering, and low grain yield [28].
3.3 Melatonin in plant metabolism engineering
Previous studies using genetic engineering (transgenic plant) in various plants species with low or high MT accumulation has been achieved to determined the role of MT in plant growth regulation, stress tolerance or MT function in plant (Table 4). Indeed it was reported the implication of MT in seed germination, root development, fruit ripening, senescence, yield, circadian rhythm and plant homeostasis [98]. Ectopic over-expression (transgenesis) of human serotonin N-acetyltransferase increased endogenous melatonin that allowed transgenic rice seedlings to face chilling stress [80]. The increase of endogenous melatonin in various transgenic plant organisms compared to the wild type has been reported in Arabidopsis thaliana [29], in Lycopersicum esculentum [88] or in Medicago sativa [92].
Overview of MT metabolic engineering in diverse plants.
Most of the studies in MT transgenesis are based on the ability of Agrobacterium to transfer DNA to plant cells by genetic engineering (Table 4). Indeed Agrobacterium tumefaciens is a widespread naturally occurring soil bacterium which demonstrated a great ability to introduce new genetic material into diverse plant cell species [99]. The Agrobacterium-mediated transformation process can be resumed in this following line: 1- Isolation of the targeted genes → 2- development of a functional transgenic construct → 3- insertion of the transgene → 4- introduction of the T-DNA-containing-plasmid into Agrobacterium → 5- mixture of the transformed Agrobacterium with plant cells → 6- regeneration of the transformed cells into transgenic plant → 7- testing for trait performance or transgene expression [99, 100, 101]. The catalytic activities of different enzymes involved in MT metabolic engineering have been elucidated in various species. The catalytic activity of Acetylserotonin O-methyltransferase (EC: 2.1.1.4) encoded by ASMT gene in Homo sapiens is done by this following line: (N-acetylserotonin + S-adenosyl-L-methionine = H+ + melatonin + S-adenosyl-L-homocysteine) [102]. The catalytic activity of Serotonin N-acetyltransferase (EC: 2.3.1.87) from Ovis aries (Sheep) encoded by AANAT gene is done by this reaction: (2-arylethylamine + acetyl-CoA = CoA + H+ + N-acetyl-2-arylethylamine) [103]. Moreover the catalytic activity of Caffeic acid 3-O-methyltransferase (EC: 2.1.1.68) implicated in many MT genetic engineering manipulations has been decoded in Medicago sativa (Alfalfa): ((E)-caffeate + S-adenosyl-L-methionine = (E)-ferulate + H+ + S-adenosyl-L-homocysteine) [104].
The elucidations of these reactions and techniques provided a huge benefit to increase the use of those compounds in metabolic engineering. There are others areas to explore and clarify to shed light the use of melatonin or glycine betaine metabolic engineering.
References
1.Francini and Sebastiani, “Abiotic Stress Effects on Performance of Horticultural Crops,” Horticulturae, vol. 5, no. 4, Sep. 2019, doi: 10.3390/horticulturae5040067
2.T. Khan, M. A. Khan, K. Karam, N. Ullah, Z.-R. Mashwani, and A. Nadhman, “Plant in vitro Culture Technologies; A Promise Into Factories of Secondary Metabolites Against COVID-19,” Front. Plant Sci., vol. 12, Mar. 2021, doi: 10.3389/fpls.2021.610194
3.Ganjewala D., Kaur G., Srivastava N. Metabolic Engineering of Stress Protectant Secondary Metabolites to Confer Abiotic Stress Tolerance in Plants. In: Singh S., Upadhyay S., Pandey A., Kumar S. (eds) Molecular Approaches in Plant Biology and Environmental Challenges. Energy, Environment, and Sustainability. 2019, Springer, Singapore. https://doi.org/10.1007/978-981-15-0690-1_11
4.S. D. McNeil, M. L. Nuccio, and A. D. Hanson, “Betaines and Related Osmoprotectants. Targets for Metabolic Engineering of Stress Resistance,” Plant Physiol., vol. 120, no. 4, Aug. 1999, doi: 10.1104/pp.120.4.945
5.S. H. Wani, V. Kumar, V. Shriram, and S. K. Sah, “Phytohormones and their metabolic engineering for abiotic stress tolerance in crop plants,” Crop J., vol. 4, no. 3, Jun. 2016, doi: 10.1016/j.cj.2016.01.010
6.A. S. Birchfield and C. A. McIntosh, “Metabolic engineering and synthetic biology of plant natural products – A minireview,” Curr. Plant Biol., vol. 24, Dec. 2020, doi: 10.1016/j.cpb.2020.100163
7.S. S. Gill and N. Tuteja, “Polyamines and abiotic stress tolerance in plants,” Plant Signal. Behav., vol. 5, no. 1, Jan. 2010, doi: 10.4161/psb.5.1.10291
8.M. G. Annunziata, L. F. Ciarmiello, P. Woodrow, E. Dell’Aversana, and P. Carillo, “Spatial and Temporal Profile of Glycine Betaine Accumulation in Plants Under Abiotic Stresses,” Front. Plant Sci., vol. 10, Mar. 2019, doi: 10.3389/fpls.2019.00230
9.J. Li, J. Liu, T. Zhu, C. Zhao, L. Li, and M. Chen, “The Role of Melatonin in Salt Stress Responses,” Int. J. Mol. Sci., vol. 20, no. 7, Apr. 2019, doi: 10.3390/ijms20071735
10.G. Blunden, S. M. Gordon, T. A. Crabb, O. G. Roch, M. G. Rowan, and B. Wood, “NMR spectra of betaines from marine algae,” Magn. Reson. Chem., vol. 24, no. 11, Nov. 1986, doi: 10.1002/mrc.1260241108
11.K. V. S. . Prasad and P. P. Saradhi, “Enhanced tolerance to photoinhibition in transgenic plants through targeting of glycinebetaine biosynthesis into the chloroplasts,” Plant Sci., vol. 166, no. 5, May 2004, doi: 10.1016/j.plantsci.2003.12.031
12.D. Rhodes and A. D. Hanson, “Quaternary Ammonium and Tertiary Sulfonium Compounds in Higher Plants,” Annu. Rev. Plant Physiol. Plant Mol. Biol., vol. 44, no. 1, Jun. 1993, doi: 10.1146/annurev.pp.44.060193.002041
13.B. Rathinasabapathi, K. McCue, D. Gage, and A. Hanson, “Metabolic engineering of glycine betaine synthesis: plant betaine aldehyde dehydrogenases lacking typical transit peptides are targeted to tobacco chloroplasts where they confer betaine aldehyde resistance,” Planta, vol. 193, no. 2, Mar. 1994, doi: 10.1007/BF00192524
14.E. A. Weretilnyk and A. D. Hanson, “Molecular cloning of a plant betaine-aldehyde dehydrogenase, an enzyme implicated in adaptation to salinity and drought.,” Proc. Natl. Acad. Sci., vol. 87, no. 7, Apr. 1990, doi: 10.1073/pnas.87.7.2745
15.S. D. McNeil, M. L. Nuccio, and A. D. Hanson, “Betaines and related osmoprotectants. Targets for metabolic engineering of stress resistance,” Plant Physiol., vol. 120, no. 4, pp. 945-949, 1999, doi: 10.1104/pp.120.4.945
16.D. Le Rudulier, A. R. Strom, A. M. Dandekar, L. T. Smith, and R. C. Valentine, “Molecular Biology of Osmoregulation,” Science (80-. )., vol. 224, no. 4653, Jun. 1984, doi: 10.1126/science.224.4653.1064
17.Z. Xu et al., “Glycinebetaine Biosynthesis in Response to Osmotic Stress Depends on Jasmonate Signaling in Watermelon Suspension Cells,” Front. Plant Sci., vol. 9, Oct. 2018, doi: 10.3389/fpls.2018.01469
18.A. Sakamoto and N. Murata, “Genetic engineering of glycinebetaine synthesis in plants: current status and implications for enhancement of stress tolerance,” J. Exp. Bot., vol. 51, no. 342, Jan. 2000, doi: 10.1093/jexbot/51.342.81
19.H. Hayashi, Alia, L. Mustardy, P. Deshnium, M. Ida, and N. Murata, “Transformation of Arabidopsis thaliana with the codA gene for choline oxidase; accumulation of glycinebetaine and enhanced tolerance to salt and cold stress,” Plant J., vol. 12, no. 1, Jul. 1997, doi: 10.1046/j.1365-313X.1997.12010133.x
20.M. S. Khan, X. Yu, A. Kikuchi, M. Asahina, and K. N. Watanabe, “Genetic engineering of glycine betaine biosynthesis to enhance abiotic stress tolerance in plants,” Plant Biotechnol., vol. 26, no. 1, 2009, doi: 10.5511/plantbiotechnology.26.125
21.Y. Yu et al., “The Role of Phyto-Melatonin and Related Metabolites in Response to Stress,” Molecules, vol. 23, no. 8, Jul. 2018, doi: 10.3390/molecules23081887
22.M. B. Arnao and J. Hernández-Ruiz, “Melatonin and its relationship to plant hormones,” Ann. Bot., vol. 121, no. 2, Feb. 2018, doi: 10.1093/aob/mcx114
23.W. Ma, L. Xu, S. Gao, X. Lyu, X. Cao, and Y. Yao, “Melatonin alters the secondary metabolite profile of grape berry skin by promoting VvMYB14-mediated ethylene biosynthesis,” Hortic. Res., vol. 8, no. 1, Dec. 2021, doi: 10.1038/s41438-021-00478-2
24.D. Zhao et al., “Melatonin Synthesis and Function: Evolutionary History in Animals and Plants,” Front. Endocrinol. (Lausanne)., vol. 10, Apr. 2019, doi: 10.3389/fendo.2019.00249
25.J. Axelrod and H. Weissbach, “Enzymatic O-Methylation of N-Acetylserotonin to Melatonin,” Science (80-. )., vol. 131, no. 3409, Apr. 1960, doi: 10.1126/science.131.3409.1312
26.Y. Byeon, H. Y. Lee, K. Lee, and K. Back, “Caffeic acid O -methyltransferase is involved in the synthesis of melatonin by methylating N -acetylserotonin in Arabidopsis,” J. Pineal Res., vol. 57, no. 2, Sep. 2014, doi: 10.1111/jpi.12160
27.W.-J. Yang et al., “Overexpression of TaCOMT Improves Melatonin Production and Enhances Drought Tolerance in Transgenic Arabidopsis,” Int. J. Mol. Sci., vol. 20, no. 3, Feb. 2019, doi: 10.3390/ijms20030652
28.Y. Byeon and K. Back, “An increase in melatonin in transgenic rice causes pleiotropic phenotypes, including enhanced seedling growth, delayed flowering, and low grain yield,” J. Pineal Res., vol. 56, no. 4, May 2014, doi: 10.1111/jpi.12129
29.G. Zhao et al., “Transgenic Arabidopsis overexpressing MsSNAT enhances salt tolerance via the increase in autophagy, and the reestablishment of redox and ion homeostasis,” Environ. Exp. Bot., vol. 164, Aug. 2019, doi: 10.1016/j.envexpbot.2019.04.017
30.M. L. Nuccio, S. D. McNeil, M. J. Ziemak, A. D. Hanson, R. K. Jain, and G. Selvaraj, “Choline Import into Chloroplasts Limits Glycine Betaine Synthesis in Tobacco: Analysis of Plants Engineered with a Chloroplastic or a Cytosolic Pathway,” Metab. Eng., vol. 2, no. 4, Oct. 2000, doi: 10.1006/mben.2000.0158
31.S. D. McNeil, M. L. Nuccio, M. J. Ziemak, and A. D. Hanson, “Enhanced synthesis of choline and glycine betaine in transgenic tobacco plants that overexpress phosphoethanolamine N-methyltransferase,” Proc. Natl. Acad. Sci., vol. 98, no. 17, Aug. 2001, doi: 10.1073/pnas.171228998
32.D. Rontein et al., “Plants Synthesize Ethanolamine by Direct Decarboxylation of Serine Using a Pyridoxal Phosphate Enzyme,” J. Biol. Chem., vol. 276, no. 38, Sep. 2001, doi: 10.1074/jbc.M106038200
33.P. S. Summers and E. A. Weretilnyk, “Choline Synthesis in Spinach in Relation to Salt Stress,” Plant Physiol., vol. 103, no. 4, Dec. 1993, doi: 10.1104/pp.103.4.1269
34.T. L. Fitzgerald, D. L. E. Waters, and R. J. Henry, “Betaine aldehyde dehydrogenase in plants,” Plant Biol., vol. 11, no. 2, Mar. 2009, doi: 10.1111/j.1438-8677.2008.00161.x
35.T. Demiral and I. Türkan, “Does exogenous glycinebetaine affect antioxidative system of rice seedlings under NaCl treatment?,” J. Plant Physiol., vol. 161, no. 10, Oct. 2004, doi: 10.1016/j.jplph.2004.03.009
36.P. Malekzadeh, “Influence of exogenous application of glycinebetaine on antioxidative system and growth of salt-stressed soybean seedlings (Glycine max L.),” Physiol. Mol. Biol. Plants, vol. 21, no. 2, Apr. 2015, doi: 10.1007/s12298-015-0292-4
37.Y. Wang and N. Nii, “Changes in chlorophyll, ribulose bisphosphate carboxylase-oxygenase, glycine betaine content, photosynthesis and transpiration in Amaranthus tricolor leaves during salt stress,” J. Hortic. Sci. Biotechnol., vol. 75, no. 6, Jan. 2000, doi: 10.1080/14620316.2000.11511297
38.S. Kishitani, K. Watanabe, S. Yasuda, K. Arakawa, and T. Takabe, “Accumulation of glycinebetaine during cold acclimation and freezing tolerance in leaves of winter and spring barley plants,” Plant, Cell Environ., vol. 17, no. 1, Jan. 1994, doi: 10.1111/j.1365-3040.1994.tb00269.x
39.Q.-Q. Ma, W. Wang, Y.-H. Li, D.-Q. Li, and Q. Zou, “Alleviation of photoinhibition in drought-stressed wheat (Triticum aestivum) by foliar-applied glycinebetaine,” J. Plant Physiol., vol. 163, no. 2, Feb. 2006, doi: 10.1016/j.jplph.2005.04.023
40.S. H. Raza, H. R. Athar, M. Ashraf, and A. Hameed, “Glycinebetaine-induced modulation of antioxidant enzymes activities and ion accumulation in two wheat cultivars differing in salt tolerance,” Environ. Exp. Bot., vol. 60, no. 3, Jul. 2007, doi: 10.1016/j.envexpbot.2006.12.009
41.M. A. . Raza, M. . Saleem, G. . Shah, I. . Khan, and A. Raza, “Exogenous application of glycinebetaine and potassium for improving water relations and grain yield of wheat under drought,” J. soil Sci. plant Nutr., no. ahead, 2014, doi: 10.4067/S0718-95162014005000028
42.K. O. Holmström, S. Somersalo, A. Mandal, T. E. Palva, and B. Welin, “Improved tolerance to salinity and low temperature in transgenic tobacco producing glycine betaine,” J. Exp. Bot., vol. 51, no. 343, pp. 177-185, 2000, doi: 10.1093/jexbot/51.343.177
43.R. Quan, M. Shang, H. Zhang, Y. Zhao, and J. Zhang, “Improved chilling tolerance by transformation with betA gene for the enhancement of glycinebetaine synthesis in maize,” Plant Sci., vol. 166, no. 1, Jan. 2004, doi: 10.1016/j.plantsci.2003.08.018
44.P. Deshnium, Z. Gombos, Y. Nishiyama, and N. Murata, “The action in vivo of glycine betaine in enhancement of tolerance of Synechococcus sp. strain PCC 7942 to low temperature.,” J. Bacteriol., vol. 179, no. 2, 1997, doi: 10.1128/JB.179.2.339-344.1997
45.A. Sakamoto and A. and N. Murata, “Metabolic engineering of rice leading to biosynthesis of glycinebetaine and tolerance to salt and cold,” Plant Mol. Biol., vol. 38, no. 6, 1998, doi: 10.1023/A:1006095015717
46.S. Lv, A. Yang, K. Zhang, L. Wang, and J. Zhang, “Increase of glycinebetaine synthesis improves drought tolerance in cotton,” Mol. Breed., vol. 20, no. 3, Aug. 2007, doi: 10.1007/s11032-007-9086-x
47.G. Lilius, N. Holmberg, and L. Bülow, “Enhanced NaCl Stress Tolerance in Transgenic Tobacco Expressing Bacterial Choline Dehydrogenase,” Nat. Biotechnol., vol. 14, no. 2, Feb. 1996, doi: 10.1038/nbt0296-177
48.G. P. Wang, X. Y. Zhang, F. Li, Y. Luo, and W. Wang, “Overaccumulation of glycine betaine enhances tolerance to drought and heat stress in wheat leaves in the protection of photosynthesis,” Photosynthetica, vol. 48, no. 1, Mar. 2010, doi: 10.1007/s11099-010-0016-5
49.E.-J. Park, Z. Jeknic, M.-T. Pino, N. Murata, and T. H.-H. Chen, “Glycinebetaine accumulation is more effective in chloroplasts than in the cytosol for protecting transgenic tomato plants against abiotic stress,” Plant. Cell Environ., vol. 30, no. 8, Aug. 2007, doi: 10.1111/j.1365-3040.2007.01694.x
50.S. LI et al., “Glycinebetaine enhances the tolerance of tomato plants to high temperature during germination of seeds and growth of seedlings,” Plant. Cell Environ., vol. 34, no. 11, Nov. 2011, doi: 10.1111/j.1365-3040.2011.02389.x
51.H. Kathuria, J. Giri, K. N. Nataraja, N. Murata, M. Udayakumar, and A. K. Tyagi, “Glycinebetaine-induced water-stress tolerance in codA -expressing transgenic indica rice is associated with up-regulation of several stress responsive genes,” Plant Biotechnol. J., vol. 7, no. 6, Aug. 2009, doi: 10.1111/j.1467-7652.2009.00420.x
52.E.-J. Park et al., “Genetic engineering of glycinebetaine synthesis in tomato protects seeds, plants, and flowers from chilling damage,” Plant J., vol. 40, no. 4, Oct. 2004, doi: 10.1111/j.1365-313X.2004.02237.x
53.Q. Wang, W. Xu, Q. Xue, and W. Su, “Transgenic Brassica chinensis plants expressing a bacterial codA gene exhibit enhanced tolerance to extreme temperature and high salinity,” J. Zhejiang Univ. Sci. B, vol. 11, no. 11, Nov. 2010, doi: 10.1631/jzus.B1000137
54.P. Yancey, “Compatible and counteracting solutes, in cellular and molecular physiology,” Acad. Press, 1994
55.H. J. M. Hou et al., “Inducers of glycinebetaine synthesis in barley,” Plant Physiol., vol. 120, no. 4, pp. 856-865, 2019, doi: 10.1104/pp.120.4.945
56.J. Giri, “Glycinebetaine and abiotic stress tolerance in plants,” Plant Signal. Behav., vol. 6, no. 11, pp. 1746-1751, 2011, doi: 10.4161/psb.6.11.17801
57.P. Castiglioni et al., “Identification of GB1 , a gene whose constitutive overexpression increases glycinebetaine content in maize and soybean,” Plant Direct, vol. 2, no. 2, Feb. 2018, doi: 10.1002/pld3.40
58.D. Li et al., “Genetic Engineering of the Biosynthesis of Glycine Betaine Modulates Phosphate Homeostasis by Regulating Phosphate Acquisition in Tomato,” Front. Plant Sci., vol. 9, Jan. 2019, doi: 10.3389/fpls.2018.01995
59.E.-J. Park, Z. Jeknić, T. H. H. Chen, and N. Murata, “The codA transgene for glycinebetaine synthesis increases the size of flowers and fruits in tomato,” Plant Biotechnol. J., vol. 5, no. 3, May 2007, doi: 10.1111/j.1467-7652.2007.00251.x
60.T. Nakamura et al., “Expression of a betaine aldehyde dehydrogenase gene in rice, a glycinebetaine nonaccumulator, and possible localization of its protein in peroxisomes,” Plant J., vol. 11, no. 5, May 1997, doi: 10.1046/j.1365-313X.1997.11051115.x
61.N.-H. T. Tran, T. Oguchi, E. Matsunaga, A. Kawaoka, K. N. Watanabe, and A. Kikuchi, “Transcriptional enhancement of a bacterial choline oxidase A gene by an HSP terminator improves the glycine betaine production and salinity stress tolerance of Eucalyptus camaldulensis trees,” Plant Biotechnol., vol. 35, no. 3, Sep. 2018, doi: Arthrobacter globiformis
62.E. Matsunaga et al., “Agrobacterium-mediated transformation of Eucalyptus globulus using explants with shoot apex with introduction of bacterial choline oxidase gene to enhance salt tolerance,” Plant Cell Rep., vol. 31, no. 1, Jan. 2012, doi: 10.1007/s00299-011-1159-y
63.T. Rand, T. Halkier, and O. C. Hansen, “Structural Characterization and Mapping of the Covalently Linked FAD Cofactor in Choline Oxidase from Arthrobacter globiformis,” Biochemistry, vol. 42, no. 23, Jun. 2003, doi: 10.1021/bi0274266
64.S. Hussain Wani, N. Brajendra Singh, A. Haribhushan, and J. Iqbal Mir, “Compatible Solute Engineering in Plants for Abiotic Stress Tolerance - Role of Glycine Betaine,” Curr. Genomics, vol. 14, no. 3, Apr. 2013, doi: 10.2174/1389202911314030001
65.M. Niazian, S. A. Sadat-Noori, M. Tohidfar, S. M. M. Mortazavian, and P. Sabbatini, “Betaine Aldehyde Dehydrogenase (BADH) vs. Flavodoxin (Fld): Two Important Genes for Enhancing Plants Stress Tolerance and Productivity,” Front. Plant Sci., vol. 12, Apr. 2021, doi: 10.3389/fpls.2021.650215
66.B. Landfald and A. R. Strøm, “Choline-glycine betaine pathway confers a high level of osmotic tolerance in Escherichia coli.,” J. Bacteriol., vol. 165, no. 3, 1986, doi: 10.1128/JB.165.3.849-855.1986
67.P. Falkenberg and A. R. Strøm, “Purification and characterization of osmoregulatory betaine aldehyde dehydrogenase of Escherichiacoli,” Biochim. Biophys. Acta - Gen. Subj., vol. 1034, no. 3, Jun. 1990, doi: 10.1016/0304-4165(90)90046-Y
68.K. Back, “Melatonin metabolism, signaling and possible roles in plants,” Plant J., vol. 105, no. 2, Jan. 2021, doi: 10.1111/tpj.14915
69.M. A. Nawaz et al., “Melatonin: Current Status and Future Perspectives in Plant Science,” Front. Plant Sci., vol. 6, Jan. 2016, doi: 10.3389/fpls.2015.01230
70.R. Dubbels et al., “Melatonin in edible plants identified by radioimmunoassay and by high performance liquid chromatography-mass spectrometry,” J. Pineal Res., vol. 18, no. 1, Jan. 1995, doi: 10.1111/j.1600-079X.1995.tb00136.x
71.J. Kolář et al., “Melatonin: Occurrence and daily rhythm in Chenopodium rubrum,” Phytochemistry, vol. 44, no. 8, Apr. 1997, doi: 10.1016/S0031-9422(96)00568-7
72.G. Cheng et al., “Plant-derived melatonin from food: a gift of nature,” Food Funct., vol. 12, no. 7, 2021, doi: 10.1039/D0FO03213A
73.R. Sharif et al., “Melatonin and its effects on plant systems,” Molecules, vol. 23, no. 9, pp. 1-20, 2018, doi: 10.3390/molecules23092352
74.M. B. Arnao and J. Hernández-Ruiz, “Melatonin: A New Plant Hormone and/or a Plant Master Regulator?,” Trends Plant Sci., vol. 24, no. 1, Jan. 2019, doi: 10.1016/j.tplants.2018.10.010
75.V. De Luca, C. Marineau, and N. Brisson, “Molecular cloning and analysis of cDNA encoding a plant tryptophan decarboxylase: comparison with animal dopa decarboxylases.,” Proc. Natl. Acad. Sci., vol. 86, no. 8, Apr. 1989, doi: 10.1073/pnas.86.8.2582
76.M. PARK, K. KANG, S. PARK, and K. BACK, “Conversion of 5-Hydroxytryptophan into Serotonin by Tryptophan Decarboxylase in Plants, Escherichia coli , and Yeast,” Biosci. Biotechnol. Biochem., vol. 72, no. 9, Sep. 2008, doi: 10.1271/bbb.80220
77.D. Zhao, R. Wang, D. Liu, Y. Wu, J. Sun, and J. Tao, “Melatonin and Expression of Tryptophan Decarboxylase Gene (TDC) in Herbaceous Peony (Paeonia lactiflora Pall.) Flowers,” Molecules, vol. 23, no. 5, May 2018, doi: 10.3390/molecules23051164
78.E. H. M. Cisse, L.-F. Miao, F. Yang, J.-F. Huang, D.-D. Li, and J. Zhang, “Gly Betaine Surpasses Melatonin to Improve Salt Tolerance in Dalbergia odorifera,” Front. Plant Sci., vol. 12, Feb. 2021
79.H. Shi et al., “Comparative physiological, metabolomic, and transcriptomic analyses reveal mechanisms of improved abiotic stress resistance in bermudagrass [Cynodon dactylon (L). Pers.] by exogenous melatonin,” J. Exp. Bot., vol. 66, no. 3, Feb. 2015, doi: 10.1093/jxb/eru373
80.K. Kang, K. Lee, S. Park, Y. S. Kim, and K. Back, “Enhanced production of melatonin by ectopic overexpression of human serotonin N-acetyltransferase plays a role in cold resistance in transgenic rice seedlings,” J. Pineal Res., Jun. 2010, doi: 10.1111/j.1600-079X.2010.00783.x
81.C. Li et al., “The mitigation effects of exogenous melatonin on salinity-induced stress in Malus hupehensis,” J. Pineal Res., vol. 53, no. 3, Oct. 2012, doi: 10.1111/j.1600-079X.2012.00999.x
82.H.-J. Zhang et al., “Melatonin promotes seed germination under high salinity by regulating antioxidant systems, ABA and GA 4 interaction in cucumber ( Cucumis sativus L.),” J. Pineal Res., vol. 57, no. 3, Oct. 2014, doi: 10.1111/jpi.12167
83.L. Wang et al., “Changes in melatonin levels in transgenic ‘Micro-Tom’ tomato overexpressing ovine AANAT and ovine HIOMT genes,” J. Pineal Res., vol. 56, no. 2, Mar. 2014, doi: 10.1111/jpi.12105
84.Y. Byeon, H. Y. Lee, O. J. Hwang, H.-J. Lee, K. Lee, and K. Back, “Coordinated regulation of melatonin synthesis and degradation genes in rice leaves in response to cadmium treatment,” J. Pineal Res., vol. 58, no. 4, May 2015, doi: 10.1111/jpi.12232
85.S. Park, D.-E. Lee, H. Jang, Y. Byeon, Y.-S. Kim, and K. Back, “Melatonin-rich transgenic rice plants exhibit resistance to herbicide-induced oxidative stress,” J. Pineal Res., vol. 54, no. 3, Apr. 2013, doi: 10.1111/j.1600-079X.2012.01029.x
86.L. Zhang, J. jia, Y. Xu, Y. Wang, J. Hao, and T. Li, “Production of transgenic Nicotiana sylvestris plants expressing melatonin synthetase genes and their effect on UV-B-induced DNA damage,” Vitr. Cell. Dev. Biol. - Plant, vol. 48, no. 3, Jun. 2012, doi: 10.1007/s11627-011-9413-0
87.I. Tiryaki and H. Keles, “Reversal of the inhibitory effect of light and high temperature on germination of Phacelia tanacetifolia seeds by melatonin,” J. Pineal Res., vol. 52, no. 3, Apr. 2012, doi: 10.1111/j.1600-079X.2011.00947.x
88.Liu, Sun, Liu, Shi, Chen, and Zhao, “Overexpression of the Melatonin Synthesis-Related Gene SlCOMT1 Improves the Resistance of Tomato to Salt Stress,” Molecules, vol. 24, no. 8, Apr. 2019, doi: 10.3390/molecules24081514
89.X. Ma, J. Zhang, P. Burgess, S. Rossi, and B. Huang, “Interactive effects of melatonin and cytokinin on alleviating drought-induced leaf senescence in creeping bentgrass ( Agrostis stolonifera ),” Environ. Exp. Bot., vol. 145, Jan. 2018, doi: 10.1016/j.envexpbot.2017.10.010
90.A. Sharma et al., “Melatonin regulates the functional components of photosynthesis, antioxidant system, gene expression, and metabolic pathways to induce drought resistance in grafted Carya cathayensis plants,” Sci. Total Environ., vol. 713, Apr. 2020, doi: 10.1016/j.scitotenv.2020.136675
91.J. Fan et al., “Alleviation of cold damage to photosystem II and metabolisms by melatonin in Bermudagrass,” Front. Plant Sci., vol. 6, Nov. 2015, doi: 10.3389/fpls.2015.00925
92.H. Cen et al., “Overexpression of MsASMT1 Promotes Plant Growth and Decreases Flavonoids Biosynthesis in Transgenic Alfalfa (Medicago sativa L.),” Front. Plant Sci., vol. 11, Apr. 2020, doi: 10.3389/fpls.2020.00489
93.Y.-H. Huang et al., “Overexpression of ovine AANAT and HIOMT genes in switchgrass leads to improved growth performance and salt-tolerance,” Sci. Rep., vol. 7, no. 1, Dec. 2017, doi: 10.1038/s41598-017-12566-2
94.K. Lee, O. J. Hwang, and K. Back, “Rice N-acetylserotonin deacetylase regulates melatonin levels in transgenic rice,” Melatonin Res., vol. 3, no. 1, Mar. 2020, doi: 10.32794/mr11250046
95.Y. Byeon, H. Y. Lee, and K. Back, “Chloroplastic and cytoplasmic overexpression of sheep serotonin N -acetyltransferase in transgenic rice plants is associated with low melatonin production despite high enzyme activity,” J. Pineal Res., vol. 58, no. 4, May 2015, doi: 10.1111/jpi.12231
96.B. Zuo et al., “Overexpression of MzASMT improves melatonin production and enhances drought tolerance in transgenic Arabidopsis thaliana plants,” J. Pineal Res., vol. 57, no. 4, Nov. 2014, doi: 10.1111/jpi.12180
97.S. Yuan et al., “Comparative Transcriptomic Analyses of Differentially Expressed Genes in Transgenic Melatonin Biosynthesis Ovine HIOMT Gene in Switchgrass,” Front. Plant Sci., vol. 7, Nov. 2016, doi: 10.3389/fpls.2016.01613
98.H. Shi, K. Chen, Y. Wei, and C. He, “Fundamental Issues of Melatonin-Mediated Stress Signaling in Plants,” Front. Plant Sci., vol. 7, Jul. 2016, doi: 10.3389/fpls.2016.01124
99.S. B. Gelvin, “Agrobacterium-Mediated Plant Transformation: the Biology behind the ‘Gene-Jockeying’ Tool,” Microbiol. Mol. Biol. Rev., vol. 67, no. 1, Mar. 2003, doi: 10.1128/MMBR.67.1.16-37.2003
100.K. K. Kumar, S. Maruthasalam, M. Loganathan, D. Sudhakar, and P. Balasubramanian, “An improved Agrobacterium-mediated transformation protocol for recalcitrant elite indica rice cultivars,” Plant Mol. Biol. Report., vol. 23, no. 1, Mar. 2005, doi: 10.1007/BF02772648
101.H. D. Jones, A. Doherty, and H. Wu, “Review of methodologies and a protocol for the Agrobacterium-mediated transformation of wheat,” Plant Methods, vol. 1, no. 1, 2005, doi: 10.1186/1746-4811-1-5
102.H. G. Botros et al., “Crystal structure and functional mapping of human ASMT, the last enzyme of the melatonin synthesis pathway,” J. Pineal Res., vol. 54, no. 1, Jan. 2013, doi: 10.1111/j.1600-079X.2012.01020.x
103.J. Pavlicek et al., “Evidence That Proline Focuses Movement of the Floppy Loop of Arylalkylamine N-Acetyltransferase (EC 2.3.1.87),” J. Biol. Chem., vol. 283, no. 21, May 2008, doi: 10.1074/jbc.M800593200
104.R. Edwards and R. A. Dixon, “Purification and characterization of S-adenosyl-l-methionine: Caffeic acid 3-O-methyltransferase from suspension cultures of alfalfa (Medicago sativa L.),” Arch. Biochem. Biophys., vol. 287, no. 2, Jun. 1991, doi: 10.1016/0003-9861(91)90492-2
Written By
Cisse El Hadji Malick, Miao Ling-Feng, Li Da-Dong and Yang Fan
Submitted: 27 February 2021Reviewed: 17 April 2021Published: 24 November 2021
Open access peer-reviewed chapter
