1932

Abstract

Tremendous chemical diversity is the hallmark of plants and is supported by highly complex biochemical machinery. Plant metabolic enzymes originated and were transferred from eukaryotic and prokaryotic ancestors and further diversified by the unprecedented rates of gene duplication and functionalization experienced in land plants. Unlike microbes, which have frequent horizontal gene transfer events and multiple inputs of energy and organic carbon, land plants predominantly rely on organic carbon generated from CO and have experienced very few, if any, gene transfers during their recent evolutionary history. As such, plant metabolic networks have evolved in a stepwise manner and on existing networks under various evolutionary constraints. This review aims to take a broader view of plant metabolic evolution and lay a framework to further explore evolutionary mechanisms of the complex metabolic network. Understanding the underlying metabolic and genetic constraints is also an empirical prerequisite for rational engineering and redesigning of plant metabolic pathways.

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2021-06-17
2024-10-03
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Literature Cited

  1. 1. 
    Alam MT, Olin-Sandoval V, Stincone A, Keller MA, Zelezniak A et al. 2017. The self-inhibitory nature of metabolic networks and its alleviation through compartmentalization. Nat. Commun. 8:16018
    [Google Scholar]
  2. 2. 
    Alifano P, Fani R, Liò P, Lazcano A, Bazzicalupo M et al. 1996. Histidine biosynthetic pathway and genes: structure, regulation, and evolution. Microbiol. Rev. 60:144–69
    [Google Scholar]
  3. 3. 
    Alonge M, Wang X, Benoit M, Soyk S, Pereira L et al. 2020. Major impacts of widespread structural variation on gene expression and crop improvement in tomato. Cell 182:1145–161.e23
    [Google Scholar]
  4. 4. 
    Arrivault S, Alexandre Moraes T, Obata T, Medeiros DB, Fernie AR et al. 2019. Metabolite profiles reveal interspecific variation in operation of the Calvin–Benson cycle in both C4 and C3 plants. J. Exp. Bot. 70:61843–58
    [Google Scholar]
  5. 5. 
    Aubry S, Kelly S, Kümpers BMC, Smith-Unna RD, Hibberd JM. 2014. Deep evolutionary comparison of gene expression identifies parallel recruitment of trans-factors in two independent origins of C4 photosynthesis. PLOS Genet 10:6e1004365
    [Google Scholar]
  6. 6. 
    Bedewitz MA, Jones AD, D'Auria JC, Barry CS 2018. Tropinone synthesis via an atypical polyketide synthase and P450-mediated cyclization. Nat. Commun. 9:15281
    [Google Scholar]
  7. 7. 
    Begley M, Gahan CGM, Kollas A-K, Hintz M, Hill C et al. 2004. The interplay between classical and alternative isoprenoid biosynthesis controls γδ T cell bioactivity of Listeria monocytogenes. FEBS Lett 561:1–399–104
    [Google Scholar]
  8. 8. 
    Beleggia R, Rau D, Laidò G, Platani C, Nigro F et al. 2016. Evolutionary metabolomics reveals domestication-associated changes in tetraploid wheat kernels. Mol. Biol. Evol. 33:71740–53
    [Google Scholar]
  9. 9. 
    Bellucci E, Bitocchi E, Ferrarini A, Benazzo A, Biagetti E et al. 2014. Decreased nucleotide and expression diversity and modified coexpression patterns characterize domestication in the common bean. Plant Cell 26:51901–12
    [Google Scholar]
  10. 10. 
    Bowman JL, Kohchi T, Yamato KT, Jenkins J, Shu S et al. 2017. Insights into land plant evolution garnered from the Marchantia polymorpha genome. Cell 171:2287–304.e15
    [Google Scholar]
  11. 11. 
    Braakman R. 2013. Mapping metabolism onto the prebiotic organic chemistry of hydrothermal vents. PNAS 110:3313236–37
    [Google Scholar]
  12. 12. 
    Bräutigam A, Schlüter U, Eisenhut M, Gowik U. 2017. On the evolutionary origin of CAM photosynthesis. Plant Physiol 174:2473–77
    [Google Scholar]
  13. 13. 
    Brockington SF, Walker RH, Glover BJ, Soltis PS, Soltis DE. 2011. Complex pigment evolution in the Caryophyllales. New Phytol 190:4854–64
    [Google Scholar]
  14. 14. 
    Buchanan BB, Arnon DI. 1990. A reverse KREBS cycle in photosynthesis: consensus at last. Photosyn. Res. 24:47–53
    [Google Scholar]
  15. 15. 
    Butelli E, Licciardello C, Ramadugu C, Durand-Hulak M, Celant A et al. 2019. Noemi controls production of flavonoid pigments and fruit acidity and illustrates the domestication routes of modern citrus varieties. Curr. Biol. 29:1158–164.e2
    [Google Scholar]
  16. 16. 
    Caetano-Anollés G, Yafremava LS, Gee H, Caetano-Anollés D, Kim HS, Mittenthal JE. 2009. The origin and evolution of modern metabolism. Int. J. Biochem. Cell Biol. 41:2285–97
    [Google Scholar]
  17. 17. 
    Cannell N, Emms DM, Hetherington AJ, MacKay J, Kelly S et al. 2020. Multiple metabolic innovations and losses are associated with major transitions in land plant evolution. Curr. Biol. 30:101783–1800.e11This innovative study used a comparative computational approach to identify metabolic gains and losses during land plant evolution.
    [Google Scholar]
  18. 18. 
    Cavalcanti JHF, Esteves-Ferreira AA, Quinhones CGS, Pereira-Lima IA, Nunes-Nesi A et al. 2014. Evolution and functional implications of the tricarboxylic acid cycle as revealed by phylogenetic analysis. Genome Biol. Evol. 6:102830–48
    [Google Scholar]
  19. 19. 
    Cheema J, Faraldos JA, O'Maille PE. 2017. REVIEW: Epistasis and dominance in the emergence of catalytic function as exemplified by the evolution of plant terpene synthases. Plant Sci 255:29–38
    [Google Scholar]
  20. 20. 
    Cheng A-X, Zhang X, Han X-J, Zhang Y-Y, Gao S et al. 2018. Identification of chalcone isomerase in the basal land plants reveals an ancient evolution of enzymatic cyclization activity for synthesis of flavonoids. New Phytol 217:2909–24
    [Google Scholar]
  21. 21. 
    Cheng S, Xian W, Fu Y, Marin B, Keller J et al. 2019. Genomes of subaerial Zygnematophyceae provide insights into land plant evolution. Cell 179:51057–1067.e14
    [Google Scholar]
  22. 22. 
    Cheng ZG, Sattler S, Maeda H, Sakuragi Y, Bryant DA, DellaPenna D. 2003. Highly divergent methyltransferases catalyze a conserved reaction in tocopherol and plastoquinone synthesis in cyanobacteria and photosynthetic eukaryotes. Plant Cell 15:102343–56
    [Google Scholar]
  23. 23. 
    Christin P-A, Arakaki M, Osborne CP, Bräutigam A, Sage RF et al. 2014. Shared origins of a key enzyme during the evolution of C4 and CAM metabolism. J. Exp. Bot. 65:133609–21
    [Google Scholar]
  24. 24. 
    Chu S, Wang J, Cheng H, Yang Q, Yu D 2014. Evolutionary study of the isoflavonoid pathway based on multiple copies analysis in soybean. BMC Genet 15:76
    [Google Scholar]
  25. 25. 
    Cohen S, Itkin M, Yeselson Y, Tzuri G, Portnoy V et al. 2014. The PH gene determines fruit acidity and contributes to the evolution of sweet melons. Nat. Commun. 5:4026
    [Google Scholar]
  26. 26. 
    Coley PD, Endara M-J, Ghabash G, Kidner CA, Nicholls JA et al. 2019. Macroevolutionary patterns in overexpression of tyrosine: an anti-herbivore defence in a speciose tropical tree genus, Inga (Fabaceae). J. Ecol. 107:41620–32
    [Google Scholar]
  27. 27. 
    Cooper G, Reed C, Nguyen D, Carter M, Wang Y 2011. Detection and formation scenario of citric acid, pyruvic acid, and other possible metabolism precursors in carbonaceous meteorites. PNAS 108:3414015–20
    [Google Scholar]
  28. 28. 
    Court SJ, Waclaw B, Allen RJ. 2015. Lower glycolysis carries a higher flux than any biochemically possible alternative. Nat. Commun. 6:8427
    [Google Scholar]
  29. 29. 
    Courtier-Orgogozo V, Martin A 2020. The coding loci of evolution and domestication: current knowledge and implications for bio-inspired genome editing. J. Exp. Biol. 223:jeb208934
    [Google Scholar]
  30. 30. 
    Cronin JR, Moore CB. 1971. Amino acid analyses of the murchison, murray, and allende carbonaceous chondrites. Science 172:39901327–29
    [Google Scholar]
  31. 31. 
    D'Ari R, Casadesús J 1998. Underground metabolism. Bioessays 20:2181–86
    [Google Scholar]
  32. 32. 
    de Vries J, de Vries S, Slamovits CH, Rose LE, Archibald JM. 2017. How embryophytic is the biosynthesis of phenylpropanoids and their derivatives in streptophyte algae?. Plant Cell Physiol 58:5934–45
    [Google Scholar]
  33. 33. 
    Del-Saz NF, Ribas-Carbo M, McDonald AE, Lambers H, Fernie AR, Florez-Sarasa I. 2018. An in vivo perspective of the role(s) of the alternative oxidase pathway. Trends Plant Sci 23:3206–19
    [Google Scholar]
  34. 34. 
    Delwiche CF, Graham LE, Thomson N. 1989. Lignin-like compounds and sporopollenin Coleochaete, an algal model for land plant ancestry. Science 245:4916399–401
    [Google Scholar]
  35. 35. 
    Deng M, Zhang X, Luo J, Liu H, Wen W et al. 2020. Metabolomics analysis reveals differences in evolution between maize and rice. Plant J 103:51710–22
    [Google Scholar]
  36. 36. 
    Dornfeld C, Weisberg AJ, Ritesh KC, Dudareva N, Jelesko JG, Maeda HA. 2014. Phylobiochemical characterization of class-Ib aspartate/prephenate aminotransferases reveals evolution of the plant arogenate phenylalanine pathway. Plant Cell 26:73101–14
    [Google Scholar]
  37. 37. 
    Edwards EJ. 2019. Evolutionary trajectories, accessibility and other metaphors: the case of C4 and CAM photosynthesis. New Phytol 223:41742–55
    [Google Scholar]
  38. 38. 
    Emiliani G, Fondi M, Fani R, Gribaldo S. 2009. A horizontal gene transfer at the origin of phenylpropanoid metabolism: a key adaptation of plants to land. Biol. Direct. 4:7
    [Google Scholar]
  39. 39. 
    Erb TJ, Zarzycki J. 2018. A short history of RubisCO: the rise and fall (?) of Nature's predominant CO2 fixing enzyme. Curr. Opin. Biotechnol. 49:100–7
    [Google Scholar]
  40. 40. 
    Evran S, Telefoncu A, Sterner R. 2012. Directed evolution of (βα)8-barrel enzymes: establishing phosphoribosylanthranilate isomerisation activity on the scaffold of the tryptophan synthase α-subunit. Protein Eng. Des. Sel. 25:6285–93
    [Google Scholar]
  41. 41. 
    Fan P, Leong BJ, Last RL. 2019. Tip of the trichome: evolution of acylsugar metabolic diversity in Solanaceae. Curr. Opin. Plant Biol. 49:8–16
    [Google Scholar]
  42. 42. 
    Fang C, Fernie AR, Luo J. 2019. Exploring the diversity of plant metabolism. Trends Plant Sci 24:183–98
    [Google Scholar]
  43. 43. 
    Fani R, Liò P, Lazcano A. 1995. Molecular evolution of the histidine biosynthetic pathway. J. Mol. Evol. 41:6760–74
    [Google Scholar]
  44. 44. 
    Fernie AR, Carrari F, Sweetlove LJ. 2004. Respiratory metabolism: glycolysis, the TCA cycle and mitochondrial electron transport. Curr. Opin. Plant Biol. 7:3254–61
    [Google Scholar]
  45. 45. 
    Fernie AR, Tadmor Y, Zamir D. 2006. Natural genetic variation for improving crop quality. Curr. Opin. Plant Biol. 9:2196–202
    [Google Scholar]
  46. 46. 
    Fernie AR, Tohge T. 2017. The genetics of plant metabolism. Annu. Rev. Genet. 51:287–310
    [Google Scholar]
  47. 47. 
    Fernie AR, Yan J 2019. De novo domestication: an alternative route toward new crops for the future. Mol. Plant 12:5615–31
    [Google Scholar]
  48. 48. 
    Fischer WW, Hemp J, Johnson JE. 2016. Evolution of oxygenic photosynthesis. Annu. Rev. Earth Planet. Sci. 44:647–83
    [Google Scholar]
  49. 49. 
    Flamholz A, Noor E, Bar-Even A, Liebermeister W, Milo R 2013. Glycolytic strategy as a tradeoff between energy yield and protein cost. PNAS 110:2410039–44
    [Google Scholar]
  50. 50. 
    Fondi M, Emiliani G, Fani R. 2009. Origin and evolution of operons and metabolic pathways. Res. Microbiol. 160:7502–12
    [Google Scholar]
  51. 51. 
    Fuchs G. 2011. Alternative pathways of carbon dioxide fixation: insights into the early evolution of life?. Annu. Rev. Microbiol. 65:631–58
    [Google Scholar]
  52. 52. 
    Galanie S, Thodey K, Trenchard IJ, Filsinger Interrante M, Smolke CD 2015. Complete biosynthesis of opioids in yeast. Science 349:62521095–100
    [Google Scholar]
  53. 53. 
    Gao L, Gonda I, Sun H, Ma Q, Bao K et al. 2019. The tomato pan-genome uncovers new genes and a rare allele regulating fruit flavor. Nat. Genet. 51:61044–51
    [Google Scholar]
  54. 54. 
    Goiris K, Muylaert K, Voorspoels S, Noten B, De Paepe D et al. 2014. Detection of flavonoids in microalgae from different evolutionary lineages. J. Phycol. 50:3483–92
    [Google Scholar]
  55. 55. 
    Goolsby EW, Moore AJ, Hancock LP, De Vos JM, Edwards EJ. 2018. Molecular evolution of key metabolic genes during transitions to C4 and CAM photosynthesis. Am. J. Bot. 105:3602–13
    [Google Scholar]
  56. 56. 
    Gowik U, Bräutigam A, Weber KL, Weber APM, Westhoff P. 2011. Evolution of C4 photosynthesis in the genus Flaveria: How many and which genes does it take to make C4?. Plant Cell 23:62087–105
    [Google Scholar]
  57. 57. 
    Graindorge M, Giustini C, Kraut A, Moyet L, Curien G, Matringe M. 2014. Three different classes of aminotransferases evolved prephenate aminotransferase functionality in arogenate-competent microorganisms. J. Biol. Chem. 289:63198–208
    [Google Scholar]
  58. 58. 
    Granick S. 1957. Speculations on the origins and evolution of photosynthesis. Ann. N. Y. Acad. Sci. 69:2292–308
    [Google Scholar]
  59. 59. 
    Gross W, Lenze D, Nowitzki U, Weiske J, Schnarrenberger C. 1999. Characterization, cloning, and evolutionary history of the chloroplast and cytosolic class I aldolases of the red alga Galdieria sulphuraria. Gene 230:17–14
    [Google Scholar]
  60. 60. 
    He Y, Mawhinney TP, Preuss ML, Schroeder AC, Chen B et al. 2009. A redox-active isopropylmalate dehydrogenase functions in the biosynthesis of glucosinolates and leucine in Arabidopsis. Plant J 60:4679–90
    [Google Scholar]
  61. 61. 
    Heckmann D. 2016. C4 photosynthesis evolution: the conditional Mt. Fuji. Curr. Opin. Plant Biol. 31:149–54
    [Google Scholar]
  62. 62. 
    Heyduk K, McKain MR, Lalani F, Leebens-Mack J. 2016. Evolution of a CAM anatomy predates the origins of Crassulacean acid metabolism in the Agavoideae (Asparagaceae). Mol. Phylogenet. Evol. 105:102–13
    [Google Scholar]
  63. 63. 
    Hori K, Maruyama F, Fujisawa T, Togashi T, Yamamoto N et al. 2014. Klebsormidium flaccidum genome reveals primary factors for plant terrestrial adaptation. Nat. Commun. 5:3978The first report on the charophyte algae genome revealed that many of the thought-to-be land-plant-specific metabolic pathways had emerged already from these algae in a stepwise manner.
    [Google Scholar]
  64. 64. 
    Hori K, Nobusawa T, Watanabe T, Madoka Y, Suzuki H et al. 2016. Tangled evolutionary processes with commonality and diversity in plastidial glycolipid synthesis in photosynthetic organisms. Biochim. Biophys. Acta. Mol. Cell Bio. Lipids 1861:9 Part B1294–308
    [Google Scholar]
  65. 65. 
    Horowitz NH. 1945. On the evolution of biochemical syntheses. PNAS 31:6153–57
    [Google Scholar]
  66. 66. 
    Hoshino Y, Gaucher EA. 2018. On the origin of isoprenoid biosynthesis. Mol. Biol. Evol. 35:92185–97
    [Google Scholar]
  67. 67. 
    Huang J-Q, Fang X, Tian X, Chen P, Lin J-L et al. 2020. Aromatization of natural products by a specialized detoxification enzyme. Nat. Chem. Biol. 16:3250–56
    [Google Scholar]
  68. 68. 
    Huang R, Hippauf F, Rohrbeck D, Haustein M, Wenke K et al. 2012. Enzyme functional evolution through improved catalysis of ancestrally nonpreferred substrates. PNAS 109:82966–71
    [Google Scholar]
  69. 69. 
    Huang R, O'Donnell AJ, Barboline JJ, Barkman TJ 2016. Convergent evolution of caffeine in plants by co-option of exapted ancestral enzymes. PNAS 113:3810613–18
    [Google Scholar]
  70. 70. 
    Hudson AO, Singh BK, Leustek T, Gilvarg C. 2006. An ll-diaminopimelate aminotransferase defines a novel variant of the lysine biosynthesis pathway in plants. Plant Physiol 140:1292–301
    [Google Scholar]
  71. 71. 
    Husnik F, McCutcheon JP. 2018. Functional horizontal gene transfer from bacteria to eukaryotes. Nat. Rev. Microbiol. 16:267–79
    [Google Scholar]
  72. 72. 
    Ingle RA. 2011. Histidine biosynthesis. Arabidopsis Book 9:e0141
    [Google Scholar]
  73. 73. 
    Jacobowitz JR, Weng J-K. 2020. Exploring uncharted territories of plant specialized metabolism in the postgenomic era. Annu. Rev. Plant Biol 71:631–58
    [Google Scholar]
  74. 74. 
    Jensen RA. 1976. Enzyme recruitment in evolution of new function. Annu. Rev. Microbiol. 30:409–25This early review article provides a fundamental framework for understanding how the metabolic pathway evolved through gene duplication and functionalization.
    [Google Scholar]
  75. 75. 
    Jensen RA, Gu W. 1996. Evolutionary recruitment of biochemically specialized subdivisions of Family I within the protein superfamily of aminotransferases. J. Bacteriol. 178:82161–71
    [Google Scholar]
  76. 76. 
    Jiao C, Sørensen I, Sun X, Sun H, Behar H et al. 2020. The Penium margaritaceum genome: hallmarks of the origins of land plants. Cell 181:51097–111.e12
    [Google Scholar]
  77. 77. 
    Joly-Lopez Z, Bureau TE 2018. Exaptation of transposable element coding sequences. Curr. Opin. Genet. Dev. 49:34–42
    [Google Scholar]
  78. 78. 
    Jozwiak A, Sonawane PD, Panda S, Garagounis C, Papadopoulou KK et al. 2020. Plant terpenoid metabolism co-opts a component of the cell wall biosynthesis machinery. Nat. Chem. Biol. 16:7740–48This study discovered that the committed glycosyltransferase enzyme of saponin specialized metabolism was recruited from an enzyme related to classical cellulose synthase (CesAs).
    [Google Scholar]
  79. 79. 
    Kaltenbach M, Burke JR, Dindo M, Pabis A, Munsberg FS et al. 2018. Evolution of chalcone isomerase from a noncatalytic ancestor. Nat. Chem. Biol. 14:6548–55This study used ancestral protein reconstruction and revealed that the core phenylpropanoid enzyme chalcone isomerase arose from a noncatalytic ancestor, suggesting that enzymatic innovation played a key role in the evolutionary expansion of flavonoid metabolism in plants.
    [Google Scholar]
  80. 80. 
    Karpowicz SJ, Prochnik SE, Grossman AR, Merchant SS. 2011. The GreenCut2 resource, a phylogenomically derived inventory of proteins specific to the plant lineage. J. Biol. Chem. 286:2421427–39
    [Google Scholar]
  81. 81. 
    Keefe AD, Lazcano A, Miller SL. 1995. Evolution of the biosynthesis of the branched-chain amino acids. Orig. Life Evol. Biosph. 25:1–399–110
    [Google Scholar]
  82. 82. 
    Keller MA, Kampjut D, Harrison SA, Ralser M. 2017. Sulfate radicals enable a non-enzymatic Krebs cycle precursor. Nat Ecol Evol 1:483
    [Google Scholar]
  83. 83. 
    Keller MA, Zylstra A, Castro C, Turchyn AV, Griffin JL, Ralser M. 2016. Conditional iron and pH-dependent activity of a non-enzymatic glycolysis and pentose phosphate pathway. Sci. Adv. 2:1e1501235This study demonstrated strong pH- and iron-dependency of nonenzymatic glycolysis and pentose phosphate pathway–like reactions, highlighting possible nonenzymatic precursor activities of cellular carbon metabolic networks.
    [Google Scholar]
  84. 84. 
    Kelley DS, Karson JA, Blackman DK, Früh-Green GL, Butterfield DA et al. 2001. An off-axis hydrothermal vent field near the Mid-Atlantic Ridge at 30° N. Nature 412:6843145–49
    [Google Scholar]
  85. 85. 
    Khersonsky O, Tawfik DS. 2010. Enzyme promiscuity: a mechanistic and evolutionary perspective. Annu. Rev. Biochem. 79:471–505
    [Google Scholar]
  86. 86. 
    Kim CY, Mitchell AJ, Glinkerman CM, Li F-S, Pluskal T, Weng J-K. 2020. The chloroalkaloid (−)-acutumine is biosynthesized via a Fe(II)- and 2-oxoglutarate-dependent halogenase in Menispermaceae plants. Nat. Commun. 11:11867
    [Google Scholar]
  87. 87. 
    Klee HJ, Tieman DM. 2018. The genetics of fruit flavour preferences. Nat. Rev. Genet. 19:6347–56
    [Google Scholar]
  88. 88. 
    Kliebenstein DJ, Lambrix VM, Reichelt M, Gershenzon J, Mitchell-Olds T. 2001. Gene duplication in the diversification of secondary metabolism: tandem 2-oxoglutarate–dependent dioxygenases control glucosinolate biosynthesis in Arabidopsis. Plant Cell 13:3681–93
    [Google Scholar]
  89. 89. 
    Kliebenstein DJ, Osbourn A 2012. Making new molecules—evolution of pathways for novel metabolites in plants. Curr. Opin. Plant Biol. 15:4415–23
    [Google Scholar]
  90. 90. 
    Kruger NJ, von Schaewen A. 2003. The oxidative pentose phosphate pathway: structure and organisation. Curr. Opin. Plant Biol. 6:3236–46
    [Google Scholar]
  91. 91. 
    Labeeuw L, Martone PT, Boucher Y, Case RJ. 2015. Ancient origin of the biosynthesis of lignin precursors. Biol. Direct. 10:23
    [Google Scholar]
  92. 92. 
    Lange BM, Rujan T, Martin W, Croteau R 2000. Isoprenoid biosynthesis: the evolution of two ancient and distinct pathways across genomes. PNAS 97:2413172–77
    [Google Scholar]
  93. 93. 
    Lazcano A, Miller SL. 1999. On the origin of metabolic pathways. J. Mol. Evol. 49:4424–31
    [Google Scholar]
  94. 94. 
    Levsh O, Pluskal T, Carballo V, Mitchell AJ, Weng J-K. 2019. Independent evolution of rosmarinic acid biosynthesis in two sister families under the Lamiids clade of flowering plants. J. Biol. Chem. 294:4215193–205
    [Google Scholar]
  95. 95. 
    Li K, Wen W, Alseekh S, Yang X, Guo H et al. 2019. Large-scale metabolite quantitative trait locus analysis provides new insights for high-quality maize improvement. Plant J 99:2216–30Analysis of the primary metabolome of a cross between teosinte and maize that provides insight into metabolic changes underlying arguably the best-studied plant domestication process.
    [Google Scholar]
  96. 96. 
    Ljungdahl L, Irion E, Wood HG. 1965. Total synthesis of acetate from CO2. I. Co-methylcobyric acid and CO-(methyl)-5-methoxybenzimidazolylcobamide as intermediates with Clostridium thermoaceticum. Biochemistry 4:122771–80
    [Google Scholar]
  97. 97. 
    Lombard J, Moreira D. 2011. Origins and early evolution of the mevalonate pathway of isoprenoid biosynthesis in the three domains of life. Mol. Biol. Evol. 28:187–99
    [Google Scholar]
  98. 98. 
    Lopez-Nieves S, Yang Y, Timoneda A, Wang M, Feng T et al. 2018. Relaxation of tyrosine pathway regulation underlies the evolution of betalain pigmentation in Caryophyllales. New Phytol 217:2896–908Discovered lineage-specific alteration of tyrosine biosynthetic TyrA enzymes, which likely increased the availability of the tyrosine precursor and later facilitated the evolution of betalain biosynthesis.
    [Google Scholar]
  99. 99. 
    Lundgren MR, Osborne CP, Christin P-A. 2014. Deconstructing Kranz anatomy to understand C4 evolution. J. Exp. Bot. 65:133357–69
    [Google Scholar]
  100. 100. 
    Maeda HA. 2019. Evolutionary diversification of primary metabolism and its contribution to plant chemical diversity. Front. Plant Sci. 10:881
    [Google Scholar]
  101. 101. 
    Maeda HA. 2019. Harnessing evolutionary diversification of primary metabolism for plant synthetic biology. J. Biol. Chem. 294:4516549–66
    [Google Scholar]
  102. 102. 
    Maeda HA, Dudareva N. 2012. The shikimate pathway and aromatic amino acid biosynthesis in plants. Annu. Rev. Plant Biol. 63:73–105
    [Google Scholar]
  103. 103. 
    Martin W, Herrmann RG. 1998. Gene transfer from organelles to the nucleus: how much, what happens, and why?. Plant Physiol 118:19–17
    [Google Scholar]
  104. 104. 
    Martin WF, Bryant DA, Beatty JT. 2018. A physiological perspective on the origin and evolution of photosynthesis. FEMS Microbiol. Rev. 42:2205–31
    [Google Scholar]
  105. 105. 
    Martin WF, Cerff R. 2017. Physiology, phylogeny, early evolution, and GAPDH. Protoplasma 254:51823–34
    [Google Scholar]
  106. 106. 
    Martin WF, Garg S, Zimorski V. 2015. Endosymbiotic theories for eukaryote origin. Philos. Trans. R. Soc. B 370: 1678.20140330
    [Google Scholar]
  107. 107. 
    Matsumoto T, Awai K. 2020. Adaptations in chloroplast membrane lipid synthesis from synthesis in ancestral cyanobacterial endosymbionts. Biochem. Biophys. Res. Commun. 528:3473–77
    [Google Scholar]
  108. 108. 
    Matsuzaki M, Kuroiwa H, Kuroiwa T, Kita K, Nozaki H. 2008. A cryptic algal group unveiled: a plastid biosynthesis pathway in the oyster parasite Perkinsus marinus. Mol. Biol. Evol. 25:61167–79
    [Google Scholar]
  109. 109. 
    McDonald AE, Vanlerberghe GC. 2006. Origins, evolutionary history, and taxonomic distribution of alternative oxidase and plastoquinol terminal oxidase. Comp. Biochem. Physiol. Part D Genom. Proteom. 1:3357–64
    [Google Scholar]
  110. 110. 
    Messner CB, Driscoll PC, Piedrafita G, De Volder MFL, Ralser M 2017. Nonenzymatic gluconeogenesis-like formation of fructose 1,6-bisphosphate in ice. PNAS 114:287403–7
    [Google Scholar]
  111. 111. 
    Meyer RS, Whitaker BD, Little DP, Wu S-B, Kennelly EJ et al. 2015. Parallel reductions in phenolic constituents resulting from the domestication of eggplant. Phytochemistry 115:194–206
    [Google Scholar]
  112. 112. 
    Meyer T, Hölscher C, Schwöppe C, von Schaewen A. 2011. Alternative targeting of Arabidopsis plastidic glucose-6-phosphate dehydrogenase G6PD1 involves cysteine-dependent interaction with G6PD4 in the cytosol. Plant J 66:5745–58
    [Google Scholar]
  113. 113. 
    Mikkelsen MD, Harholt J, Ulvskov P, Johansen IE, Fangel JU et al. 2014. Evidence for land plant cell wall biosynthetic mechanisms in charophyte green algae. Ann. Bot. 114:61217–36
    [Google Scholar]
  114. 114. 
    Milo R, Last RL 2012. Achieving diversity in the face of constraints: lessons from metabolism. Science 336:60891663–67
    [Google Scholar]
  115. 115. 
    Moghe GD, Last RL. 2015. Something old, something new: conserved enzymes and the evolution of novelty in plant specialized metabolism. Plant Physiol 169:31512–23
    [Google Scholar]
  116. 116. 
    Moghe GD, Leong BJ, Hurney SM, Jones AD, Last RL. 2017. Evolutionary routes to biochemical innovation revealed by integrative analysis of a plant-defense related specialized metabolic pathway. eLife 6:e28468
    [Google Scholar]
  117. 117. 
    Morris JL, Puttick MN, Clark JW, Edwards D, Kenrick P et al. 2018. The timescale of early land plant evolution. PNAS 115:10E2274–83
    [Google Scholar]
  118. 118. 
    Muchowska KB, Varma SJ, Chevallot-Beroux E, Lethuillier-Karl L, Li G, Moran J. 2017. Metals promote sequences of the reverse Krebs cycle. Nat. Ecol. Evol. 1:111716–21
    [Google Scholar]
  119. 119. 
    Murray AW. 2020. Can gene-inactivating mutations lead to evolutionary novelty?. Curr. Biol. 30:10R465–71
    [Google Scholar]
  120. 120. 
    Ning J, Moghe GD, Leong B, Kim J, Ofner I et al. 2015. A feedback-insensitive isopropylmalate synthase affects acylsugar composition in cultivated and wild tomato. Plant. Physiol. 169:31821–35Discovered alterations of the committed enzyme of leucine biosynthesis in cultivated and wild tomatoes, which likely underlie distinct compositions of acylsugar specialized metabolites derived from leucine and valine.
    [Google Scholar]
  121. 121. 
    Nishiyama T, Sakayama H, de Vries J, Buschmann H, Saint-Marcoux D et al. 2018. The Chara genome: secondary complexity and implications for plant terrestrialization. Cell 174:2448–64.e24
    [Google Scholar]
  122. 122. 
    Noda-Garcia L, Liebermeister W, Tawfik DS. 2018. Metabolite-enzyme coevolution: from single enzymes to metabolic pathways and networks. Annu. Rev. Biochem. 87:187–216
    [Google Scholar]
  123. 123. 
    Notebaart RA, Szappanos B, Kintses B, Pál F, Györkei Á et al. 2014. Network-level architecture and the evolutionary potential of underground metabolism. PNAS 111:3211762–67
    [Google Scholar]
  124. 124. 
    Novikov Y, Copley SD 2013. Reactivity landscape of pyruvate under simulated hydrothermal vent conditions. PNAS 110:3313283–88
    [Google Scholar]
  125. 125. 
    Nunoura T, Chikaraishi Y, Izaki R, Suwa T, Sato T et al. 2018. A primordial and reversible TCA cycle in a facultatively chemolithoautotrophic thermophile. Science 359:6375559–63
    [Google Scholar]
  126. 126. 
    Nützmann H-W, Scazzocchio C, Osbourn A 2018. Metabolic gene clusters in eukaryotes. Annu. Rev. Genet. 52:159–83
    [Google Scholar]
  127. 127. 
    One Thousand Plant Transcriptomes Initiative 2019. One thousand plant transcriptomes and the phylogenomics of green plants. Nature 574:7780679–85
    [Google Scholar]
  128. 128. 
    Orgel LE. 2004. Prebiotic chemistry and the origin of the RNA world. Crit. Rev. Biochem. Mol. Biol. 39:299–123
    [Google Scholar]
  129. 129. 
    Parween S, Anonuevo JJ, Butardo VM, Misra G, Anacleto R et al. 2020. Balancing the double-edged sword effect of increased resistant starch content and its impact on rice texture: its genetics and molecular physiological mechanisms. Plant Biotechnol. J. 18:81763–77
    [Google Scholar]
  130. 130. 
    Patron NJ, Rogers MB, Keeling PJ. 2004. Gene replacement of fructose-1,6-bisphosphate aldolase supports the hypothesis of a single photosynthetic ancestor of chromalveolates. Eukaryot. Cell 3:51169–75
    [Google Scholar]
  131. 131. 
    Perez de Souza L, Scossa F, Proost S, Bitocchi E, Papa R et al. 2019. Multi-tissue integration of transcriptomic and specialized metabolite profiling provides tools for assessing the common bean (Phaseolus vulgaris) metabolome. Plant J 97:61132–53
    [Google Scholar]
  132. 132. 
    Petersen J, Brinkmann H, Cerff R. 2003. Origin, evolution, and metabolic role of a novel glycolytic GAPDH enzyme recruited by land plant plastids. J. Mol. Evol. 57:116–26
    [Google Scholar]
  133. 133. 
    Plaxton WC. 1996. The organization and regulation of plant glycolysis. Annu. Rev. Plant Physiol. Plant Mol. Biol. 47:185–214
    [Google Scholar]
  134. 134. 
    Radwanski ER, Last RL. 1995. Tryptophan biosynthesis and metabolism: biochemical and molecular genetics. Plant Cell 7:7921–34
    [Google Scholar]
  135. 135. 
    Raff RA. 2000. Evo-devo: the evolution of a new discipline. Nat. Rev. Genet. 1:174–79
    [Google Scholar]
  136. 136. 
    Ralser M. 2014. The RNA world and the origin of metabolic enzymes. Biochem. Soc. Trans. 42:4985–88
    [Google Scholar]
  137. 137. 
    Ralser M. 2018. An appeal to magic? The discovery of a non-enzymatic metabolism and its role in the origins of life. Biochem. J. 475:162577–92
    [Google Scholar]
  138. 138. 
    Raymond J, Segrè D. 2006. The effect of oxygen on biochemical networks and the evolution of complex life. Science 311:57681764–67
    [Google Scholar]
  139. 139. 
    Reyes-Prieto A, Moustafa A 2012. Plastid-localized amino acid biosynthetic pathways of Plantae are predominantly composed of non-cyanobacterial enzymes. Sci. Rep. 2:955
    [Google Scholar]
  140. 140. 
    Richards TA, Dacks JB, Campbell SA, Blanchard JL, Foster PG et al. 2006. Evolutionary origins of the eukaryotic shikimate pathway: gene fusions, horizontal gene transfer, and endosymbiotic replacements. Eukaryot. Cell 5:91517–31
    [Google Scholar]
  141. 141. 
    Sage RF, Christin P-A, Edwards EJ. 2011. The C4 plant lineages of planet Earth. J. Exp. Bot. 62:93155–69
    [Google Scholar]
  142. 142. 
    Sato N, Awai K. 2016. Diversity in biosynthetic pathways of galactolipids in the light of endosymbiotic origin of chloroplasts. Front. Plant Sci. 7:117
    [Google Scholar]
  143. 143. 
    Sato N, Awai K. 2017. “Prokaryotic Pathway” is not prokaryotic: Noncyanobacterial origin of the chloroplast lipid biosynthetic pathway revealed by comprehensive phylogenomic analysis. Genome Biol. Evol. 9:113162–78Detailed phylogenomic and phylogenetic analyses revealed that all enzymes of plastidic glycolipid biosynthesis have been replaced by noncyanobacterial enzymes in Plantae.
    [Google Scholar]
  144. 144. 
    Sato T, Atomi H, Imanaka T. 2007. Archaeal type III RuBisCOs function in a pathway for AMP metabolism. Science 315:58141003–6
    [Google Scholar]
  145. 145. 
    Sauer FD, Erfle JD, Mahadevan S. 1975. Amino acid biosynthesis in mixed rumen cultures. Biochem. J. 150:3357–72
    [Google Scholar]
  146. 146. 
    Schenck CA, Chen S, Siehl DL, Maeda HA. 2015. Non-plastidic, tyrosine-insensitive prephenate dehydrogenases from legumes. Nat. Chem. Biol. 11:152–57
    [Google Scholar]
  147. 147. 
    Schenck CA, Holland CK, Schneider MR, Men Y, Lee SG et al. 2017. Molecular basis of the evolution of alternative tyrosine biosynthetic routes in plants. Nat. Chem. Biol. 13:1029–35
    [Google Scholar]
  148. 148. 
    Schenck CA, Last RL. 2020. Location, location! Cellular relocalization primes specialized metabolic diversification. FEBS J 287:71359–68
    [Google Scholar]
  149. 149. 
    Schlüter U, Weber APM. 2020. Regulation and evolution of C4 photosynthesis. Annu. Rev. Plant Biol. 71:183–215
    [Google Scholar]
  150. 150. 
    Schnarrenberger C, Martin W. 2002. Evolution of the enzymes of the citric acid cycle and the glyoxylate cycle of higher plants. A case study of endosymbiotic gene transfer. Eur. J. Biochem. 269:3868–83
    [Google Scholar]
  151. 151. 
    Schopf JW, Kitajima K, Spicuzza MJ, Kudryavtsev AB, Valley JW 2018. SIMS analyses of the oldest known assemblage of microfossils document their taxon-correlated carbon isotope compositions. PNAS 115:153–58
    [Google Scholar]
  152. 152. 
    Scossa F, Fernie AR. 2020. The evolution of metabolism: How to test evolutionary hypotheses at the genomic level. Comput. Struct. Biotechnol. J. 18:482–500
    [Google Scholar]
  153. 153. 
    Seto H, Watanabe H, Furihata K. 1996. Simultaneous operation of the mevalonate and non-mevalonate pathways in the biosynthesis of isopentenly diphosphate in Streptomyces aeriouvifer. Tetrahedron Lett 37:447979–82
    [Google Scholar]
  154. 154. 
    Shameer S, Baghalian K, Cheung CYM, Ratcliffe RG, Sweetlove LJ. 2018. Computational analysis of the productivity potential of CAM. Nat. Plants 4:3165–71
    [Google Scholar]
  155. 155. 
    Shan Q, Zhang Y, Chen K, Zhang K, Gao C. 2015. Creation of fragrant rice by targeted knockout of the OsBADH2 gene using TALEN technology. Plant Biotechnol. J. 13:6791–800
    [Google Scholar]
  156. 156. 
    Shih PM. 2018. Towards a sustainable bio-based economy: redirecting primary metabolism to new products with plant synthetic biology. Plant Sci 273:84–91
    [Google Scholar]
  157. 157. 
    Singh BK, Shaner DL. 1995. Biosynthesis of branched chain amino acids: from test tube to field. Plant Cell 7:7935–44
    [Google Scholar]
  158. 158. 
    Sojo V, Herschy B, Whicher A, Camprubí E, Lane N. 2016. The origin of life in alkaline hydrothermal vents. Astrobiology 16:2181–97
    [Google Scholar]
  159. 159. 
    Somerville C, Browse J. 1991. Plant lipids: metabolism, mutants, and membranes. Science 252:500280–87
    [Google Scholar]
  160. 160. 
    Sonawane PD, Jozwiak A, Panda S, Aharoni A. 2020.. “ Hijacking” core metabolism: a new panache for the evolution of steroidal glycoalkaloids structural diversity. Curr. Opin. Plant Biol. 55:118–28
    [Google Scholar]
  161. 161. 
    Soo RM, Hemp J, Parks DH, Fischer WW, Hugenholtz P. 2017. On the origins of oxygenic photosynthesis and aerobic respiration in Cyanobacteria. Science 355:63321436–40
    [Google Scholar]
  162. 162. 
    Sørensen I, Pettolino FA, Bacic A, Ralph J, Lu F et al. 2011. The charophycean green algae provide insights into the early origins of plant cell walls. Plant J 68:2201–11
    [Google Scholar]
  163. 163. 
    Springsteen G, Yerabolu JR, Nelson J, Rhea CJ, Krishnamurthy R. 2018. Linked cycles of oxidative decarboxylation of glyoxylate as protometabolic analogs of the citric acid cycle. Nat. Commun. 9:191
    [Google Scholar]
  164. 164. 
    Studart-Guimarães C, Gibon Y, Frankel N, Wood CC, Zanor MI et al. 2005. Identification and characterisation of the α and β subunits of succinyl CoA ligase of tomato. Plant Mol. Biol. 59:5781–91
    [Google Scholar]
  165. 165. 
    Swanson-Wagner R, Briskine R, Schaefer R, Hufford MB, Ross-Ibarra J et al. 2012. Reshaping of the maize transcriptome by domestication. PNAS 109:2911878–83
    [Google Scholar]
  166. 166. 
    Sweetlove LJ, Fernie AR. 2005. Regulation of metabolic networks: understanding metabolic complexity in the systems biology era. New Phytol 168:19–24
    [Google Scholar]
  167. 167. 
    Sweetlove LJ, Fernie AR. 2013. The spatial organization of metabolism within the plant cell. Annu. Rev. Plant Biol. 64:723–46
    [Google Scholar]
  168. 168. 
    Tabita FR, Hanson TE, Li H, Satagopan S, Singh J, Chan S 2007. Function, structure, and evolution of the RubisCO-like proteins and their RubisCO homologs. Microbiol. Mol. Biol. Rev. 71:4576–99
    [Google Scholar]
  169. 169. 
    Tabita FR, Hanson TE, Satagopan S, Witte BH, Kreel NE. 2008. Phylogenetic and evolutionary relationships of RubisCO and the RubisCO-like proteins and the functional lessons provided by diverse molecular forms. Philos. Trans. R. Soc. B 363:15042629–40
    [Google Scholar]
  170. 170. 
    Tohge T, Wendenburg R, Ishihara H, Nakabayashi R, Watanabe M et al. 2016. Characterization of a recently evolved flavonol-phenylacyltransferase gene provides signatures of natural light selection in Brassicaceae. Nat. Commun. 7:12399
    [Google Scholar]
  171. 171. 
    Varma SJ, Muchowska KB, Chatelain P, Moran J. 2018. Native iron reduces CO2 to intermediates and end-products of the acetyl-CoA pathway. Nat. Ecol. Evol. 2:61019–24Discovered that several native metals can facilitate pyruvate and acetate from CO2, which may provide nonenzymatic precursor reactions of the reductive acetyl-CoA pathway.
    [Google Scholar]
  172. 172. 
    Velasco AM, Leguina JI, Lazcano A. 2002. Molecular evolution of the lysine biosynthetic pathways. J. Mol. Evol. 55:4445–59
    [Google Scholar]
  173. 173. 
    Verschueren KHG, Blanchet C, Felix J, Dansercoer A, De Vos D et al. 2019. Structure of ATP citrate lyase and the origin of citrate synthase in the Krebs cycle. Nature 568:7753571–75
    [Google Scholar]
  174. 174. 
    Vranová E, Coman D, Gruissem W. 2013. Network analysis of the MVA and MEP pathways for isoprenoid synthesis. Annu. Rev. Plant Biol. 64:665–700
    [Google Scholar]
  175. 175. 
    Washburn JD, Bird KA, Conant GC, Pires JC. 2016. Convergent evolution and the origin of complex phenotypes in the age of systems biology. Int. J. Plant Sci. 177:4305–18
    [Google Scholar]
  176. 176. 
    Wasternack C, Feussner I. 2018. The oxylipin pathways: biochemistry and function. Annu. Rev. Plant Biol. 69:363–86
    [Google Scholar]
  177. 177. 
    Weiss MC, Sousa FL, Mrnjavac N, Neukirchen S, Roettger M et al. 2016. The physiology and habitat of the last universal common ancestor. Nat. Microbiol. 1:916116
    [Google Scholar]
  178. 178. 
    Weng J-K. 2014. The evolutionary paths towards complexity: a metabolic perspective. New Phytol 201:41141–49
    [Google Scholar]
  179. 179. 
    Weng J-K, Philippe RN, Noel JP 2012. The rise of chemodiversity in plants. Science 336:60891667–70
    [Google Scholar]
  180. 180. 
    Widhalm JR, Ducluzeau A-L, Buller NE, Elowsky CG, Olsen LJ, Basset GJC. 2012. Phylloquinone (vitamin K1) biosynthesis in plants: two peroxisomal thioesterases of Lactobacillales origin hydrolyze 1,4-dihydroxy-2-naphthoyl-CoA. Plant J 71:2205–15
    [Google Scholar]
  181. 181. 
    Wilmanns M, Hyde CC, Davies DR, Kirschner K, Jansonius JN. 1991. Structural conservation in parallel β/α-barrel enzymes that catalyze three sequential reactions in the pathway of tryptophan biosynthesis. Biochemistry 30:389161–69
    [Google Scholar]
  182. 182. 
    Wong JT. 1975. A co-evolution theory of the genetic code. PNAS 72:51909–12
    [Google Scholar]
  183. 183. 
    Xie G, Keyhani NO, Bonner CA, Jensen RA. 2003. Ancient origin of the tryptophan operon and the dynamics of evolutionary change. Microbiol. Mol. Biol. Rev. 67:3303–42
    [Google Scholar]
  184. 184. 
    Xing A, Last RL. 2017. A regulatory hierarchy of the Arabidopsis branched-chain amino acid metabolic network. Plant Cell 29:61480–99
    [Google Scholar]
  185. 185. 
    Xiong J, Bauer CE. 2002. Complex evolution of photosynthesis. Annu. Rev. Plant Biol. 53:503–21
    [Google Scholar]
  186. 186. 
    Xu G, Cao J, Wang X, Chen Q, Jin W et al. 2019. Evolutionary metabolomics identifies substantial metabolic divergence between maize and its wild ancestor, teosinte. Plant Cell 31:91990–2009
    [Google Scholar]
  187. 187. 
    Yang W, Simpson JP, Li-Beisson Y, Beisson F, Pollard M, Ohlrogge JB. 2012. A land-plant-specific glycerol-3-phosphate acyltransferase family in Arabidopsis: substrate specificity, sn-2 preference, and evolution. Plant Physiol 160:2638–52
    [Google Scholar]
  188. 188. 
    Yang X, Hu R, Yin H, Jenkins J, Shu S et al. 2017. The Kalanchoë genome provides insights into convergent evolution and building blocks of crassulacean acid metabolism. Nat. Commun. 8:11899
    [Google Scholar]
  189. 189. 
    Yasutake Y, Yao M, Sakai N, Kirita T, Tanaka I. 2004. Crystal structure of the Pyrococcus horikoshii isopropylmalate isomerase small subunit provides insight into the dual substrate specificity of the enzyme. J. Mol. Biol. 344:2325–33
    [Google Scholar]
  190. 190. 
    Yokota T, Ohnishi T, Shibata K, Asahina M, Nomura T et al. 2017. Occurrence of brassinosteroids in non-flowering land plants, liverwort, moss, lycophyte and fern. Phytochemistry 136:46–55
    [Google Scholar]
  191. 191. 
    Yoon HS, Hackett JD, Ciniglia C, Pinto G, Bhattacharya D. 2004. A molecular timeline for the origin of photosynthetic eukaryotes. Mol. Biol. Evol. 21:5809–18
    [Google Scholar]
  192. 192. 
    Yuzawa Y, Shimojima M, Sato R, Mizusawa N, Ikeda K et al. 2014. Cyanobacterial monogalactosyldiacylglycerol-synthesis pathway is involved in normal unsaturation of galactolipids and low-temperature adaptation of Synechocystis sp. PCC 6803. Biochim. Biophys. Acta Mol. Cell Biol. Lipids 1841:4475–83
    [Google Scholar]
  193. 193. 
    Zhang J. 2003. Evolution by gene duplication: an update. Trends Ecol. Evol. 18:6292–98
    [Google Scholar]
  194. 194. 
    Zhang L, Su W, Tao R, Zhang W, Chen J et al. 2017. RNA sequencing provides insights into the evolution of lettuce and the regulation of flavonoid biosynthesis. Nat. Commun. 8:12264
    [Google Scholar]
  195. 195. 
    Zhang S, Bryant DA. 2011. The tricarboxylic acid cycle in cyanobacteria. Science 334:60621551–53
    [Google Scholar]
  196. 196. 
    Zhang XV, Martin ST. 2006. Driving parts of Krebs cycle in reverse through mineral photochemistry. J. Am. Chem. Soc. 128:5016032–33
    [Google Scholar]
  197. 197. 
    Zhao G, Lian Q, Zhang Z, Fu Q, He Y et al. 2019. A comprehensive genome variation map of melon identifies multiple domestication events and loci influencing agronomic traits. Nat. Genet. 51:111607–15
    [Google Scholar]
  198. 198. 
    Zhao Q, Yang J, Cui M-Y, Liu J, Fang Y et al. 2019. The reference genome sequence of Scutellaria baicalensis provides insights into the evolution of wogonin biosynthesis. Mol. Plant. 12:7935–50
    [Google Scholar]
  199. 199. 
    Zhu G, Wang S, Huang Z, Zhang S, Liao Q et al. 2018. Rewiring of the fruit metabolome in tomato breeding. Cell 172:1–2249–61.e12A comprehensive analysis of the effect of domestication and improvement processes on the tomato metabolome revealing the sites of selection for removal of toxic steroidal glycoalkaloids.
    [Google Scholar]
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