nature.com

Plant cholesterol biosynthetic pathway overlaps with phytosterol metabolism - Nature Plants

  • ️Aharoni, Asaph
  • ️Thu Dec 22 2016
  • Nes, W. D. Biosynthesis of cholesterol and other sterols. Chem. Rev. 111, 6423–6451 (2011).

    Article  CAS  Google Scholar 

  • Benveniste, P. Biosynthesis and accumulation of sterols. Annu. Rev. Plant Biol. 55, 429–457 (2004).

    Article  CAS  Google Scholar 

  • Piironen, V., Lindsay, D. G., Miettinen, T. A., Toivo, J. & Lampi, A. M. Plant sterols: biosynthesis, biological function and their importance to human nutrition. J. Sci. Food Agric. 80, 939–966 (2000).

    Article  CAS  Google Scholar 

  • Schaller, H. The role of sterols in plant growth and development. Prog. Lipid Res. 42, 163–175 (2003).

    Article  CAS  Google Scholar 

  • Behrman, E. J. & Gopalan, V. Concepts in biochemistry cholesterol and plants. J. Chem. Educ. 82, 1791–1793 (2005).

    Article  CAS  Google Scholar 

  • Jäpelt, R. B. & Jakobsen, J. Vitamin D in plants: a review of occurrence, analysis, and biosynthesis. Front. Plant Sci. 4, 136 (2013).

    Article  Google Scholar 

  • Milner, S. E. et al. Bioactivities of glycoalkaloids and their aglycones from Solanum species. J. Agric. Food Chem. 59, 3454–3484 (2011).

    Article  CAS  Google Scholar 

  • Dinan, L. Phytoecdysteroids: biological aspects. Phytochemistry 57, 325–339 (2001).

    Article  CAS  Google Scholar 

  • Cárdenas, P. D. et al. The bitter side of the nightshades: genomics drives discovery in Solanaceae steroidal alkaloid metabolism. Phytochemistry 113, 24–32 (2014).

    Article  Google Scholar 

  • Bloch, K. The biological synthesis of cholesterol. Science 150, 19–28 (1965).

    Article  CAS  Google Scholar 

  • Ohyama, K., Suzuki, M., Kikuchi, J., Saito, K. & Muranaka, T. Dual biosynthetic pathways to phytosterol via cycloartenol and lanosterol in Arabidopsis. Proc. Natl Acad. Sci. USA 106, 725–730 (2009).

    Article  CAS  Google Scholar 

  • Diener, A. C. et al. STEROL METHYLTRANSFERASE 1 controls the level of cholesterol in plants. Plant Cell 12, 853–870 (2000).

    Article  CAS  Google Scholar 

  • Arnqvist, L., Dutta, P. C., Jonsson, L. & Sitbon, F. Reduction of cholesterol and glycoalkaloid levels in transgenic potato plants by overexpression of a type 1 sterol methyltransferase cDNA. Plant Physiol. 131, 1792–1799 (2003).

    Article  CAS  Google Scholar 

  • Sawai, S. et al. Sterol side chain reductase 2 is a key enzyme in the biosynthesis of cholesterol, the common precursor of toxic steroidal glycoalkaloids in potato. Plant Cell 26, 3763–3774 (2014).

    Article  CAS  Google Scholar 

  • Cárdenas, P. D. et al. GAME9 regulates the biosynthesis of steroidal alkaloids and upstream isoprenoids in the plant mevalonate pathway. Nat. Commun. 7, 10654 (2016).

    Article  Google Scholar 

  • Itkin, M. et al. Biosynthesis of antinutritional alkaloids in Solanaceous crops is mediated by clustered genes. Science 341, 175–179 (2013).

    Article  CAS  Google Scholar 

  • Itkin, M. et al. GLYCOALKALOID METABOLISM1 is required for steroidal alkaloid glycosylation and prevention of phytotoxicity in tomato. Plant Cell 23, 4507–4525 (2011).

    Article  CAS  Google Scholar 

  • Rahier, A. Dissecting the sterol C-4 demethylation process in higher plants from structures and genes to catalytic mechanism. Steroids 76, 340–352 (2011).

    Article  CAS  Google Scholar 

  • Rahier, A. & Karst, F. Plant cyclopropylsterol-cycloisomerase: key amino acids affecting activity and substrate specificity. Biochem. J. 459, 289–299 (2014).

    Article  CAS  Google Scholar 

  • Kushiro, M. et al. Obtusifoliol 14-α-demethylase (CYP51) antisense Arabidopsis shows slow growth and long life. Biochem. Biophys. Res. Commun. 285, 98–104 (2001).

    Article  CAS  Google Scholar 

  • Schrick, K. et al. FACKEL is a sterol C-14 reductase required for organized cell division and expansion in Arabidopsis embryogenesis. Genes Dev. 14, 1471–1484 (2000).

    CAS  PubMed  PubMed Central  Google Scholar 

  • Souter, M. et al. Hydra mutants of Arabidopsis are defective in sterol profiles and auxin and ethylene signaling. Plant Cell 14, 1017–1031 (2002).

    Article  CAS  Google Scholar 

  • Moses, T. et al. Combinatorial biosynthesis of sapogenins and saponins in Saccharomyces cerevisiae using a C-16α-hydroxylase from Bupleurum falcatum. Proc. Natl Acad. Sci. USA 111, 1634–1639 (2014).

    Article  CAS  Google Scholar 

  • Kushiro, T., Shibuya, M. & Ebizuka, Y. β-Amyrin synthase-cloning of oxidosqualene cyclase that catalyzes the formation of the most popular triterpene among higher plants. Eur. J. Biochem. 256, 238–244 (1998).

    Article  CAS  Google Scholar 

  • Darnet, S. & Rahier, A. Plant sterol biosynthesis: identification of two distinct families of sterol 4α-methyl oxidases. Biochem. J. 378, 889–898 (2004).

    Article  CAS  Google Scholar 

  • Suza, W. P. & Chappell, J. Spatial and temporal regulation of sterol biosynthesis in Nicotiana benthamiana. Physiol. Plant. 157, 120–134 (2016).

    Article  CAS  Google Scholar 

  • Rahier, A., Darnet, S., Bouvier, F., Camara, B. & Bard, M. Molecular and enzymatic characterizations of novel bifunctional 3β-hydroxysteroid dehydrogenases/C-4 decarboxylases from Arabidopsis thaliana. J. Biol. Chem. 281, 27264–27277 (2006).

    Article  CAS  Google Scholar 

  • Pascal, S., Taton, M. & Rahier, A. Plant sterol biosynthesis: identification of a NADPH dependant plant sterone reductase involved in the sterol-4-demethylation. Arch. Biochem. Biophys. 312, 260–271 (1994).

    Article  CAS  Google Scholar 

  • Rahier, A., Pierre, S., Riveill, G. & Karst, F. Identification of essential amino acid residues in a sterol 8,7-isomerase from Zea mays reveals functional homology and diversity with the isomerases of animal and fungal origin. Biochem. J. 414, 247–259 (2008).

    Article  CAS  Google Scholar 

  • Ashman, W. H., Barbuch, R. J., Ulbright, C. E., Jarrett, H. W. & Bard, M. Cloning and disruption of the yeast C-8 sterol isomerase gene. Lipids 26, 628–632 (1991).

    Article  CAS  Google Scholar 

  • Palermo, L. M., Leak, F. W., Tove, S. & Parks, L. W. Assessment of the essentiality of ERG genes late in ergosterol biosynthesis in Saccharomyces cerevisiae. Curr. Genet. 32, 93–99 (1997).

    Article  CAS  Google Scholar 

  • Husselstein, T., Schaller, H., Gachotte, D. & Benveniste, P. Δ7-sterol-C5-desaturase: molecular characterization and functional expression of wild-type and mutant alleles. Plant Mol. Biol. 39, 891–906 (1999).

    Article  CAS  Google Scholar 

  • Choe, S. et al. The Arabidopsis dwf7/ste1 mutant is defective in the Δ7-sterol C-5 desaturation step leading to brassinosteroid biosynthesis. Plant Cell 11, 207–221 (1999).

    CAS  PubMed  PubMed Central  Google Scholar 

  • Choe, S. et al. Lesions in the sterol delta reductase gene of Arabidopsis cause dwarfism due to a block in brassinosteroid biosynthesis. Plant J. 21, 431–443 (2000).

    Article  CAS  Google Scholar 

  • Gaylor, J. L. Membrane-bound enzymes of cholesterol synthesis from lanosterol. Biochem. Biophys. Res. Commun. 1146, 1139–1146 (2008).

    Google Scholar 

  • Caldas, H. & Herman, G. E. NSDHL, an enzyme involved in cholesterol biosynthesis, traffics through the Golgi and accumulates on ER membranes and on the surface of lipid droplets. Human Mol. Genetics 12, 2981–2991 (2003).

    Article  CAS  Google Scholar 

  • Silvestro, D., Andersen, T. G., Schaller, H. & Jensen, P. E. Plant sterol metabolism. Δ7-Sterol-C5-desaturase (STE1/DWARF7), Δ5,7-sterol-Δ7-reductase (DWARF5) and Δ24-sterol-Δ24-reductase (DIMINUTO/DWARF1) show multiple subcellular localizations in Arabidopsis thaliana (Heynh) L. PLoS ONE 8, e56429 (2013).

    Article  CAS  Google Scholar 

  • Ycas, M. On earlier states of biochemical systems. J. Theor. Biol. 44, 145–160 (1974).

    Article  CAS  Google Scholar 

  • Jensen, R. A. Enzyme recruitment in evolution of new function. Annu. Rev. Microbiol. 30, 409–425 (1976).

    Article  CAS  Google Scholar 

  • Maechler, M . et al. Cluster: Cluster Analysis Basics and Extensions. R package v.1.15.1 (CRAN, 2014); http://cran.r-project.org/web/packages/cluster/index.html

  • Ihaka, R. & Gentleman, R. R: a language for data analysis and graphics. J. Comp. Graph. Stat. 5, 299–314 (1996).

    Google Scholar 

  • Mi, H., Muruganujan, A. & Thomas, P. D. PANTHER in 2013: modeling the evolution of gene function, and other gene attributes, in the context of phylogenetic trees. Nucleic Acids Res. 41, D377–D386 (2013).

    Article  CAS  Google Scholar 

  • Larkin, M. A. et al. Clustal W and Clustal X version 2.0. Bioinformatics 23, 2947–2948 (2007).

    Article  CAS  Google Scholar 

  • Tamura, K., Stecher, G., Peterson, D., Filipski, A. & Kumar, S. MEGA6: molecular evolutionary genetics analysis version 6.0. Mol. Biol. Evol. 30, 2725–2729 (2013).

    Article  CAS  Google Scholar 

  • Itkin, M. et al. TOMATO AGAMOUS-LIKE is a component of the fruit ripening regulatory network. Plant J. 60, 1081–1095 (2009).

    Article  CAS  Google Scholar 

  • Senthil-Kumar, M. & Mysore, K. S. Tobacco rattle virus–based virus-induced gene silencing in Nicotiana benthamiana. Nat. Protoc. 9, 1549–1562 (2014).

    Article  CAS  Google Scholar 

  • Wretensjö, I. & Karlberg, B. Characterization of sterols in borage oil by GC-MS. J. Am. Chem. Oil Soc. 79, 1069–1074 (2004).

    Article  Google Scholar 

  • Zhang, X. et al. Separation of Δ5-and Δ7-phytosterols by adsorption chromatography and semipreparative reversed phase high-performance liquid chromatography for quantitative analysis of phytosterols in foods. J. Agric. Food Chem. 54, 1196–1202 (2006).

    Article  CAS  Google Scholar 

  • Yang, B., Karlsson, R. M., Oksman, P. H. & Kallio, H. P. Phytosterols in sea buckthorn (Hippophae rhamnoides L.) berries: identification and effects of different origins and harvesting times. J. Agric. Food Chem. 49, 5620–5629 (2001).

    Article  CAS  Google Scholar 

  • Kamal-Eldin, A., Appelqvist, L. A., Yousif, G. & Iskander, G. M. Seed lipids of Sesamum indicum and related wild species in Sudan. The sterols. J. Sci. Food Agric. 59, 327–334 (1992).

    Article  CAS  Google Scholar 

  • Expósito-Rodríguez, M., Borges, A. A., Borges-Pérez, A. & Pérez, J. A. Selection of internal control genes for quantitative real-time RT-PCR studies during tomato development process. BMC Plant Biol. 8, 131–142 (2008).

    Article  Google Scholar 

  • Rotenberg, D., Thompson, T. S., German, T. L. & Willis, D. K. Methods for effective real-time RT-PCR analysis of virus-induced gene silencing. J. Virol. Methods 138, 49–59 (2006).

    Article  CAS  Google Scholar 

  • Karimi, M., Inzé, D. & Depicker, A. GATEWAYTM vectors for Agrobacterium-mediated plant transformation. Trends Plant Sci. 7, 193–195 (2002).

    Article  CAS  Google Scholar 

  • Taton, M., Husselstein, T., Benveniste, P. & Rahier, A. Role of highly conserved residues in the reaction catalyzed by recombinant Δ7-sterol-C5(6)-desaturase studied by site-directed mutagenesis. Biochemistry 39, 701–711 (2000).

    Article  CAS  Google Scholar 

  • Zou, L., Li, L. & Porter, T. D. 7-dehydrocholesterol reductase activity is independent of cytochrome P450 reductase. J. Steroid Biochem. Mol. Biol. 127, 435–438 (2011).

    Article  CAS  Google Scholar 

  • Sarrion-Perdigones, A. et al. Goldenbraid 2.0: a comprehensive DNA assembly framework for plant synthetic biology. Plant Physiol. 162, 1618–1631 (2013).

    Article  CAS  Google Scholar 

  • Clough, S. & Bent, A. Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J. 16, 735–743 (1998).

    Article  CAS  Google Scholar 

  • Sparkes, I. A., Runions, J., Kearns, A. & Hawes, C. Rapid, transient expression of fluorescent fusion proteins in tobacco plants and generation of stably transformed plants. Nat. Protoc. 1, 2019–2025 (2006).

    Article  CAS  Google Scholar 

  • Nelson, B. K., Cai, X. & Nebenführ, A. A multicolored set of in vivo organelle markers for co-localization studies in Arabidopsis and other plants. Plant J. 51, 1126–1136 (2007).

    Article  CAS  Google Scholar 

  • DiCarlo, J. E. et al. Genome engineering in Saccharomyces cerevisiae using CRISPR-Cas systems. Nucleic Acids Res. 41, 4336–4343 (2013).

    Article  CAS  Google Scholar 

  • Schiestl, R. H. & Gietz, R. D. High efficiency transformation of intact yeast cells using single stranded nucleic acids as a carrier. Curr. Genet. 16, 339–346 (1989).

    Article  CAS  Google Scholar