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• W2976843492 abstract "Plants produce numerous natural products that are essential to both plant and human physiology. Recent identification of genes and enzymes involved in their biosynthesis now provides exciting opportunities to reconstruct plant natural product pathways in heterologous systems through synthetic biology. The use of plant chassis, although still in infancy, can take advantage of plant cells' inherent capacity to synthesize and store various phytochemicals. Also, large-scale plant biomass production systems, driven by photosynthetic energy production and carbon fixation, could be harnessed for industrial-scale production of natural products. However, little is known about which plants could serve as ideal hosts and how to optimize plant primary metabolism to efficiently provide precursors for the synthesis of desirable downstream natural products or specialized (secondary) metabolites. Although primary metabolism is generally assumed to be conserved, unlike the highly-diversified specialized metabolism, primary metabolic pathways and enzymes can differ between microbes and plants and also among different plants, especially at the interface between primary and specialized metabolisms. This review highlights examples of the diversity in plant primary metabolism and discusses how we can utilize these variations in plant synthetic biology. I propose that understanding the evolutionary, biochemical, genetic, and molecular bases of primary metabolic diversity could provide rational strategies for identifying suitable plant hosts and for further optimizing primary metabolism for sizable production of natural and bio-based products in plants. Plants produce numerous natural products that are essential to both plant and human physiology. Recent identification of genes and enzymes involved in their biosynthesis now provides exciting opportunities to reconstruct plant natural product pathways in heterologous systems through synthetic biology. The use of plant chassis, although still in infancy, can take advantage of plant cells' inherent capacity to synthesize and store various phytochemicals. Also, large-scale plant biomass production systems, driven by photosynthetic energy production and carbon fixation, could be harnessed for industrial-scale production of natural products. However, little is known about which plants could serve as ideal hosts and how to optimize plant primary metabolism to efficiently provide precursors for the synthesis of desirable downstream natural products or specialized (secondary) metabolites. Although primary metabolism is generally assumed to be conserved, unlike the highly-diversified specialized metabolism, primary metabolic pathways and enzymes can differ between microbes and plants and also among different plants, especially at the interface between primary and specialized metabolisms. This review highlights examples of the diversity in plant primary metabolism and discusses how we can utilize these variations in plant synthetic biology. I propose that understanding the evolutionary, biochemical, genetic, and molecular bases of primary metabolic diversity could provide rational strategies for identifying suitable plant hosts and for further optimizing primary metabolism for sizable production of natural and bio-based products in plants. Plants produce diverse and often abundant chemical compounds, which play critical roles in these sessile and multicellular organisms to habitat in various environmental niches. Many of these phytochemicals are produced in a lineage-specific manner and thus are often referred to as specialized or secondary metabolites. Many of these plant natural products also provide essential nutrients and valuable resources for the production of pharmaceuticals and biomaterials to the human society (1Newman D.J. Cragg G.M. Natural products as sources of new drugs from 1981 to 2014.J. Nat. Prod. 2016; 79 (26852623): 629-66110.1021/acs.jnatprod.5b01055Crossref PubMed Scopus (2769) Google Scholar, 2McChesney J.D. Venkataraman S.K. Henri J.T. Plant natural products: back to the future or into extinction?.Phytochemistry. 2007; 68 (17574638): 2015-202210.1016/j.phytochem.2007.04.032Crossref PubMed Scopus (220) Google Scholar3Kutchan T.M. Gershenzon J. Moller B.L. Gang D.R. Buchanan B.B. Gruissem W. Jones R.L. Biochemistry and Molecular Biology of Plants. 2nd Ed. American Society of Plant Physiologists, Rockville, MD2015Google Scholar). 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Microbial hosts, having well-developed genetic tools and industrial-scale culture methods (e.g. yeast), have been engineered to build chemical production platforms that are optimized for a certain primary metabolic branch on which various downstream pathways, including plant specialized metabolic pathways, have been introduced (8Ajikumar P.K. Xiao W.-H. Tyo K.E. Wang Y. Simeon F. Leonard E. Mucha O. Phon T.H. Pfeifer B. Stephanopoulos G. Isoprenoid pathway optimization for Taxol precursor overproduction in Escherichia coli.Science. 2010; 330 (20929806): 70-7410.1126/science.1191652Crossref PubMed Scopus (1086) Google Scholar9Brown S. Clastre M. Courdavault V. O'Connor S.E. De novo production of the plant-derived alkaloid strictosidine in yeast.Proc. Natl. Acad. Sci. U.S.A. 2015; 112 (25675512): 3205-321010.1073/pnas.1423555112Crossref PubMed Scopus (202) Google Scholar, 10Galanie S. Thodey K. Trenchard I.J. Filsinger Interrante M. Smolke C.D. 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Isoprenoid pathway optimization for Taxol precursor overproduction in Escherichia coli.Science. 2010; 330 (20929806): 70-7410.1126/science.1191652Crossref PubMed Scopus (1086) Google Scholar, 14Paddon C.J. Westfall P.J. Pitera D.J. Benjamin K. Fisher K. McPhee D. Leavell M.D. Tai A. Main A. Eng D. Polichuk D.R. Teoh K.H. Reed D.W. Treynor T. Lenihan J. et al.High-level semi-synthetic production of the potent antimalarial artemisinin.Nature. 2013; 496 (23575629): 528-53210.1038/nature12051Crossref PubMed Scopus (1086) Google Scholar), microbial production of certain classes of plant natural products, such as alkaloids and phenolics, appear to be more challenging, likely due to their toxicity, pathway complexity, and inefficiency of plant-derived enzymes (10Galanie S. Thodey K. Trenchard I.J. Filsinger Interrante M. Smolke C.D. Complete biosynthesis of opioids in yeast.Science. 2015; 349 (26272907): 1095-110010.1126/science.aac9373Crossref PubMed Scopus (444) Google Scholar, 16Li S. 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Biofuel and energy crops: high-yield Saccharinae take center stage in the post-genomics era.Genome Biol. 2013; 14 (23805917): 21010.1186/gb-2013-14-6-210Crossref PubMed Scopus (19) Google Scholar). Plant hosts may also have better storage capacity and toxicity resistance for phytochemical production compared with microbial hosts (Fig. 1B). Thus, plant chassis potentially provide promising alternative platforms to produce some of these metabolites that are difficult to produce in microbes, especially if tailored plant hosts (or chassis) are carefully selected and generated depending on downstream target compounds. Many specialized metabolic pathways have been successfully introduced to heterologous plants (29Farhi M. Marhevka E. Ben-Ari J. Algamas-Dimantov A. Liang Z. Zeevi V. Edelbaum O. Spitzer-Rimon B. Abeliovich H. Schwartz B. Tzfira T. Vainstein A. Generation of the potent anti-malarial drug artemisinin in tobacco.Nat. 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Microbial metabolic engineering and synthetic biology studies demonstrated that redirection of carbon flux and efficient supply of a specific primary precursor(s) are critical to achieve efficient production of downstream target products (Fig. 1A) (16Li S. Li Y. Smolke C.D. Strategies for microbial synthesis of high-value phytochemicals.Nat. Chem. 2018; 10 (29568052): 395-40410.1038/s41557-018-0013-zCrossref PubMed Scopus (40) Google Scholar, 35Huccetogullari D. Luo Z.W. Lee S.Y. Metabolic engineering of microorganisms for production of aromatic compounds.Microb. Cell Fact. 2019; 18 (30808357): 4110.1186/s12934-019-1090-4Crossref PubMed Scopus (20) Google Scholar36Kirby J. Keasling J.D. Biosynthesis of plant isoprenoids: perspectives for microbial engineering.Annu. Rev. Plant Biol. 2009; 60 (19575586): 335-35510.1146/annurev.arplant.043008.091955Crossref PubMed Scopus (302) Google Scholar, 37Nielsen J. Keasling J.D. Engineering cellular metabolism.Cell. 2016; 164 (26967285): 1185-119710.1016/j.cell.2016.02.004Abstract Full Text Full Text PDF PubMed Scopus (470) Google Scholar38Vickers C.E. Williams T.C. Peng B. Cherry J. Recent advances in synthetic biology for engineering isoprenoid production in yeast.Curr. Opin. Chem. Biol. 2017; 40 (28623722): 47-5610.1016/j.cbpa.2017.05.017Crossref PubMed Scopus (57) Google Scholar). Thus, holistic understanding and engineering of both primary and specialized metabolisms are crucial for efficient and sizable production of natural products in plants. Unlike in microbes, engineering of plant primary metabolism poses several major challenges (Fig. 1B). (i) There is a much more limited capacity to conduct genetic engineering and mutagenesis screening in plants than in microbes, due to low transformation efficiency and long generation cycles of most plants (months to years versus hours to days). (ii) Plant metabolism is likely more constrained due to almost exclusive reliance on the carbon input from photosynthetic CO2 fixation, unlike microbes that can utilize multiple carbon sources. (iii) Plant primary metabolic pathways are tightly integrated with each other and directly linked to the growth and development of these complex multicellular organisms, and their manipulation often compromises overall growth and yield (39Shaul O. Galili G. Concerted regulation of lysine and threonine synthesis in tobacco plants expressing bacterial feedback-insensitive aspartate kinase and dihydrodipicolinate synthase.Plant Mol. Biol. 1993; 23 (8251629): 759-76810.1007/BF00021531Crossref PubMed Google Scholar40Bartlem D. Lambein I. Okamoto T. Itaya A. Uda Y. Kijima F. Tamaki Y. Nambara E. Naito S. 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Here, I discuss one promising approach to achieve this goal by learning from millions of years of experimentations that nature has done. Although primary metabolism is generally assumed to be conserved across the plant kingdom, unlike highly-diversified specialized metabolism (45Moghe G.D. Last R.L. Something old, something new: conserved enzymes and the evolution of novelty in plant specialized metabolism.Plant Physiol. 2015; 169 (26276843): 1512-152310.1104/pp.15.00994PubMed Google Scholar46Pichersky E. Lewinsohn E. Convergent evolution in plant specialized metabolism.Annu. Rev. Plant Biol. 2011; 62 (21275647): 549-56610.1146/annurev-arplant-042110-103814Crossref PubMed Scopus (225) Google Scholar, 47Weng J.-K. Philippe R.N. Noel J.P. The rise of chemodiversity in plants.Science. 2012; 336 (22745420): 1667-167010.1126/science.1217411Crossref PubMed Scopus (187) Google Scholar48Bathe U. Tissier A. Cytochrome P450 enzymes: a driving force of plant diterpene diversity.Phytochemistry. 2019; 161 (30733060): 149-16210.1016/j.phytochem.2018.12.003Crossref PubMed Scopus (17) Google Scholar), there are some examples of evolutionary diversification of primary metabolic pathways, especially at the interface between primary and specialized metabolism (49Maeda H.A. Evolutionary diversification of primary metabolism and its contribution to plant chemical diversity.Front. Plant Sci. 2019; 10 (31354760): 88110.3389/fpls.2019.00881Crossref PubMed Scopus (8) Google Scholar). Exploring and harnessing such relatively-rare but key evolutionary innovations of plant metabolism will provide useful tools and strategies to optimize plant primary metabolism in coordination with downstream specialized metabolic pathways, in order to achieve efficient production of plant natural products in carefully-selected plant hosts. Despite the general conservation of primary metabolic pathways among different kingdoms of life, some of them are unique in plants, which likely contributed to the tremendous chemical diversity seen in the plant kingdom today. Understanding such fundamental differences provides a critical basis for constructing plant chemical production platforms through metabolic engineering. Here, I highlight prominent examples found in primary metabolic pathways that support two major classes of plant natural products, terpenoid (isoprenoid) and phenylpropanoid compounds. Isopentenyl diphosphate (IPP), 2The abbreviations used are: IPPisopentenyl diphosphateMVAmevalonateDMAPPdimethylallyl diphosphateDMAPdimethylallyl phosphateMEP2-C-methyl-d-erythritol 4-phosphateMPDCmevalonate diphosphate decarboxylasePMKphosphomevalonate kinaseERendoplasmic reticulumIDIIPP:DMAPP isomeraseDXP1-deoxy-d-xylulose 5-phosphateDXRDXP reductaseDXSDXP synthaseHMBPP4-hydroxy-3-methyl-butenyl 1-diphosphateMEcPP2-C-methyl-d-erythritol-2,4-cyclodiphosphateHMG–CoA3-hydroxy-3-methylglutaryl–CoAHMGRHMG–CoA reductaseMVPmevalonate 5-phosphatePMDphosphomevalonate decarboxylaseIPisopentenyl phosphateIPKisopentenyl phosphate kinaseCMchorismate mutaseHDSHMBPP synthaseHDRHMBPP reductasePPA-ATprephenate aminotransferaseADTarogenate dehydratasePDTprephenate dehydratasePPY-ATphenylpyruvate aminotransferaseASanthranilate synthaseTyrAaarogenate TyrA dehydrogenasencTyrAanoncanonical TyrAaPheHPhe hydroxylaseTyrApprephenate TyrA dehydrogenaseIPMSisopropylmalate synthase3MOB3-methyl-2-oxobutanoate4MOP4-methyl-2-oxopropanoate. and its allylic isomer dimethylallyl diphosphate (DMAPP), is the precursor and building blocks of diverse isoprenoid compounds, such as sterols (e.g. cholesterols), dolichol, and quinones (e.g. ubiquinone). In plants, IPP and DMAPP are also used to synthesize photosynthetic pigments (i.e. chlorophylls and carotenoids) and quinones (i.e. plastoquinone and phylloquinone), plant hormones (e.g. gibberellins, brassinosteroids, and abscisic acid), rubbers, isoprene, mono- and sesquiterpene volatiles, and diverse di- and tri-terpenoids (50Rodríguez-Concepción M. Boronat A. Breaking new ground in the regulation of the early steps of plant isoprenoid biosynthesis.Curr. Opin. Plant Biol. 2015; 25 (25909859): 17-2210.1016/j.pbi.2015.04.001Crossref PubMed Scopus (59) Google Scholar51Tholl D. Biosynthesis and biological functions of terpenoids in plants.Adv. Biochem. Eng. Biotechnol. 2015; 148 (25583224): 63-10610.1007/10_2014_295PubMed Google Scholar, 52Croteau R. Kutchan T.M. Lewis N.G. Buchanan B.B. Gruissem W. Jones R.L. Biochemistry and Molecular Biology of Plants. American Society of Plant Physiologists, Rockville, MD200010.4236/ajmb.2013.32010Google Scholar, 53Gershenzon J. Dudareva N. The function of terpene natural products in the natural world.Nat. Chem. Biol. 2007; 3 (17576428): 408-41410.1038/nchembio.2007.5Crossref PubMed Scopus (1050) Google Scholar54Zi J. Mafu S. Peters R.J. To gibberellins and beyond! Surveying the evolution of (di)terpenoid metabolism.Annu. Rev. Plant Biol. 2014; 65 (24471837): 259-28610.1146/annurev-arplant-050213-035705Crossref PubMed Scopus (135) Google Scholar). IPP (and DMAPP) can be synthesized via two different routes, the mevalonate (MVA) and 2-C-methyl-d-erythritol 4-phosphate (MEP) pathways (Fig. 2) (36Kirby J. Keasling J.D. Biosynthesis of plant isoprenoids: perspectives for microbial engineering.Annu. Rev. Plant Biol. 2009; 60 (19575586): 335-35510.1146/annurev.arplant.043008.091955Crossref PubMed Scopus (302) Google Scholar, 50Rodríguez-Concepción M. Boronat A. Breaking new ground in the regulation of the early steps of plant isoprenoid biosynthesis.Curr. Opin. 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• W2976843492 created "2019-10-03" @default.
• W2976843492 creator A5040429486 @default.
• W2976843492 date "2019-11-01" @default.
• W2976843492 modified "2023-10-06" @default.
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