Arabidopsis ERG28 tethers the sterol C4-demethylation complex to prevent accumulation of a biosynthetic intermediate that interferes with polar auxin transport

Plant Cell

Volumn 25, Issue 12, 2013, Pages 4879-4893

  Mialoundama, Alexis Samba ^a,e   Jadid, Nurul ^a,b   Brunel, Julien ^a   Di Pascoli, Thomas ^a   Heintz, Dimitri ^a   Erhardt, Mathieu ^a   Mutterer, Jérôme ^a   Bergdoll, Marc ^a   Ayoub, Daniel ^c   Van Dorsselaer, Alain ^c   Rahier, Alain ^a   Nkeng, Paul ^d   Geoffroy, Philippe ^a   Miesch, Michel ^a   Camara, Bilal ^a   Bouvier, Florence ^a  

^a UNIVERSITÉ DE STRASBOURG   (France)

^b DEPARTMENT OF ELECTRICAL ENGINEERING   (Indonesia)

^c INSTITUT DE RECHERCHES SUBATOMIQUES   (France)

^d Université de Lorraine   (France)

^e UNIVERSITY OF AVIGNON   (France)

Author keywords

[No Author keywords available]

Indexed keywords

4-CARBOXY-4-METHYL-24-METHYLENECYCLOARTANOL; ARABIDOPSIS PROTEIN; ERG28 PROTEIN, ARABIDOPSIS; INDOLEACETIC ACID DERIVATIVE; MEMBRANE PROTEIN; PHYTOSTEROL;

ARABIDOPSIS; BIOSYNTHESIS; CHEMICAL STRUCTURE; GENETICS; GROWTH, DEVELOPMENT AND AGING; METABOLISM; MOLECULAR GENETICS; PHYSIOLOGY; TRANSPORT AT THE CELLULAR LEVEL;

ARABIDOPSIS; ARABIDOPSIS PROTEINS; BIOLOGICAL TRANSPORT; BIOSYNTHETIC PATHWAYS; INDOLEACETIC ACIDS; MEMBRANE PROTEINS; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; PHYTOSTEROLS;

EID: 84893079332     PISSN: 10404651     EISSN: 1532298X     Source Type: Journal    
DOI: 10.1105/tpc.113.115576     Document Type: Article

References (101)

1. Bard, M., Bruner, D.A., Pierson, C.A., Lees, N.D., Biermann, B., Frye, L., Koegel, C., and Barbuch, R. (1996). Cloning and characterization of ERG25, the Saccharomyces cerevisiae gene encoding C-4 sterol methyl oxidase. Proc. Natl. Acad. Sci. USA 93: 186-190.
2. Bennett, S.R.M., Alverz, J., Bossinger, G., and Smyth, D.R. (1995). Morphogenesis in pinoidmutants of Arabidopsis thaliana. Plant J. 8: 505-520.
3. Bensinger, S.J., Bradley, M.N., Joseph, S.B., Zelcer, N., Janssen, E.M., Hausner, M.A., Shih, R., Parks, J.S., Edwards, P.A., Jamieson, B.D., and Tontonoz, P. (2008). LXR signaling couples sterol metabolism to proliferation in the acquired immune response. Cell 134: 97-111.
4. Benveniste, P. (2004). Biosynthesis and accumulation of sterols. Annu. Rev. Plant Biol. 55: 429-457.
5. Berleth, T., and Jürgens, G. (1993). The role of the monopteros gene in organising the basal body region of the Arabidopsis embryo. Development 118: 575-587.
6. Bhalerao, R.P., Eklöf, J., Ljung, K., Marchant, A., Bennett, M., and Sandberg, G. (2002). Shoot-derived auxin is essential for early lateral root emergence in Arabidopsis seedlings. Plant J. 29: 325-332.
7. Bittman, R. (1997). Cholesterol: Its functions and metabolism in biology and medicine. In Subcellular Biochemistry, R. Bittman, ed (New York: Plenum Press), pp. 145-171.
8. Blakeslee, J.J., et al. (2007). Interactions among PIN-FORMED and P-glycoprotein auxin transporters in Arabidopsis. Plant Cell 19: 131-147.
9. Blanc, M., et al. (2011). Host defense against viral infection involves interferon mediated down-regulation of sterol biosynthesis. PLoS Biol. 9: e1000598.
10. Boutté, Y., and Grebe, M. (2009). Cellular processes relying on sterol function in plants. Curr. Opin. Plant Biol. 12: 705-713.
11. Bouvier, F., Rahier, A., and Camara, B. (2005). Biogenesis, molecular regulation and function of plant isoprenoids. Prog. Lipid Res. 44: 357-429.
12. Brown, A.J., and Galea, A.M. (2010). Cholesterol as an evolutionary response to living with oxygen. Evolution 64: 2179-2183.
13. Brown, D.E., Rashotte, A.M., Murphy, A.S., Normanly, J., Tague, B.W., Peer, W.A., Taiz, L., and Muday, G.K. (2001). Flavonoids act as negative regulators of auxin transport in vivo in Arabidopsis. Plant Physiol. 126: 524-535.
14. Byskov, A.G., Andersen, C.Y., Nordholm, L., Thøgersen, H., Xia, G., Wassmann, O., Andersen, J.V., Guddal, E., and Roed, T. (1995). Chemical structure of sterols that activate oocyte meiosis. Nature 374: 559-562.
15. Caldas, H., and Herman, G.E. (2003). NSDHL, an enzyme involved in cholesterol biosynthesis, traffics through the Golgi and accumulates on ER membranes and on the surface of lipid droplets. Hum. Mol. Genet. 12: 2981-2991.
16. Cañabate-Díaz, B., Segura Carretero, A., Fernández-Gutiérrez, A., Belmonte Vega, A., Garrido Frenich, A., Martínez Vidal, J.L., and Duran Martos, J. (2007). Separation and determination of sterols in olive oil by HPLC-MS. Food Chem. 102: 593-598.
17. Carland, F., Fujioka, S., and Nelson, T. (2010). The sterol methyltransferases SMT1, SMT2, and SMT3 influence Arabidopsis development through nonbrassinosteroid products. Plant Physiol. 153: 741-756.
18. Carland, F.M., Berg, B.L., FitzGerald, J.N., Jinamornphongs, S., Nelson, T., and Keith, B. (1999). Genetic regulation of vascular tissue patterning in Arabidopsis. Plant Cell 11: 2123-2137.
19. Carland, F.M., Fujioka, S., Takatsuto, S., Yoshida, S., and Nelson, T. (2002). The identification of CVP1 reveals a role for sterols in vascular patterning. Plant Cell 14: 2045-2058.
20. Castrillo, A., Joseph, S.B., Vaidya, S.A., Haberland, M., Fogelman, A.M., Cheng, G., and Tontonoz, P. (2003). Crosstalk between LXR and toll-like receptor signaling mediates bacterial and viral antagonism of cholesterol metabolism. Mol. Cell 12: 805-816.
21. Clouse, S.D. (2000). Plant development: A role for sterols in embryogenesis. Curr. Biol. 10: R601-R604.
22. Clouse, S.D. (2002). Arabidopsis mutants reveal multiple roles for sterols in plant development. Plant Cell 14: 1995-2000.
23. Czarny, M.R., Maheshwari, K.K., Nelson, J.A., and Spencer, T.A. (1975). Synthesis of stereoisomeric 4-hydroxymethyl-4-methyl-3betahydroxy-cholestanes,-androstanes, and-10-methyl-trans-decalins. J. Org. Chem. 40: 2079-2085.
24. Desmond, E., and Gribaldo, S. (2009). Phylogenomics of sterol synthesis: Insights into the origin, evolution, and diversity of a key eukaryotic feature. Genome Biol. Evol. 1: 364-381.
25. Diener, A.C., Li, H., Zhou, W., Whoriskey, W.J., Nes, W.D., and Fink, G.R. (2000). Sterol methyltransferase 1 controls the level of cholesterol in plants. Plant Cell 12: 853-870.
26. Donner, T.J., Sherr, I., and Scarpella, E. (2009). Regulation of preprocambial cell state acquisition by auxin signaling in Arabidopsis leaves. Development 136: 3235-3246.
27. Espenshade, P.J., and Hughes, A.L. (2007). Regulation of sterol synthesis in eukaryotes. Annu. Rev. Genet. 41: 401-427.
28. Feraru, E., Feraru, M.I., Kleine-Vehn, J., Martinière, A., Mouille, G., Vanneste, S., Vernhettes, S., Runions, J., and Friml, J. (2011). PIN polarity maintenance by the cell wall in Arabidopsis. Curr. Biol. 21: 338-343.
29. Fujioka, S., and Yokota, T. (2003). Biosynthesis and metabolism of brassinosteroids. Annu. Rev. Plant Biol. 54: 137-164.
30. Gachotte, D., Eckstein, J., Barbuch, R., Hughes, T., Roberts, C., and Bard, M. (2001). A novel gene conserved from yeast to humans is involved in sterol biosynthesis. J. Lipid Res. 42: 150-154.
31. Gälweiler, L., Guan, C., Müller, A., Wisman, E., Mendgen, K., Yephremov, A., and Palme, K. (1998). Regulation of polar auxin transport by AtPIN1 in Arabidopsis vascular tissue. Science 282: 2226-2230.
32. Gaylor, J.L. (2002). Membrane-bound enzymes of cholesterol synthesis from lanosterol. Biochem. Biophys. Res. Commun. 292: 1139-1146.
33. Geldner, N., Friml, J., Stierhof, Y.D., Jürgens, G., and Palme, K. (2001). Auxin transport inhibitors block PIN1 cycling and vesicle trafficking. Nature 413: 425-428.
34. Geldner, N., Richter, S., Vieten, A., Marquardt, S., Torres-Ruiz, R. A., Mayer, U., and Jürgens, G. (2004). Partial loss-of-function alleles reveal a role for GNOM in auxin transport-related, postembryonic development of Arabidopsis. Development 131: 389-400.
35. Grebe, M., Xu, J., Möbius, W., Ueda, T., Nakano, A., Geuze, H.J., Rook, M.B., and Scheres, B. (2003). Arabidopsis sterol endocytosis involves actin-mediated trafficking via ARA6-positive early endosomes. Curr. Biol. 13: 1378-1387.
36. Hannich, J.T., Entchev, E.V., Mende, F., Boytchev, H., Martin, R., Zagoriy, V., Theumer, G., Riezman, I., Riezman, H., Knölker, H.J., and Kurzchalia, T.V. (2009). Methylation of the sterol nucleus by STRM-1 regulates dauer larva formation in Caenorhabditis elegans. Dev. Cell 16: 833-843.
37. He, J.X., Fujioka, S., Li, T.C., Kang, S.G., Seto, H., Takatsuto, S., Yoshida, S., and Jang, J.C. (2003). Sterols regulate development and gene expression in Arabidopsis. Plant Physiol. 131: 1258-1269.
38. He, M., et al. (2011). Mutations in the human SC4MOL gene encoding a methyl sterol oxidase cause psoriasiform dermatitis, microcephaly, and developmental delay. J. Clin. Invest. 121: 976-984.
39. Hughes, A.L., Lee, C.Y., Bien, C.M., and Espenshade, P.J. (2007). 4-Methyl sterols regulate fission yeast SREBP-Scap under low oxygen and cell stress. J. Biol. Chem. 282: 24388-24396.
40. Jadid, N., Mialoundama, A.S., Heintz, D., Ayoub, D., Erhardt, M., Mutterer, J., Meyer, D., Alioua, A., Van Dorsselaer, A., Rahier, A., Camara, B., and Bouvier, F. (2011). DOLICHOL PHOSPHATE MANNOSE SYNTHASE1 mediates the biogenesis of isoprenyllinked glycans and influences development, stress response, and ammonium hypersensitivity in Arabidopsis. Plant Cell 23: 1985-2005.
41. Jaillais, Y., Fobis-Loisy, I., Miège, C., Rollin, C., and Gaude, T. (2006). AtSNX1 defines an endosome for auxin-carrier trafficking in Arabidopsis. Nature 443: 106-109.
42. Jang, J.C., Fujioka, S., Tasaka, M., Seto, H., Takatsuto, S., Ishii, A., Aida, M., Yoshida, S., and Sheen, J. (2000). A critical role of sterols in embryonic patterning and meristem programming revealed by the fackel mutants of Arabidopsis thaliana. Genes Dev. 14: 1485-1497.
43. Janowski, B.A., Willy, P.J., Devi, T.R., Falck, J.R., andMangelsdorf, D.J. (1996). An oxysterol signalling pathway mediated by the nuclear receptor LXR alpha. Nature 383: 728-731.
44. Jefferson, R.A., Kavanagh, T.A., and Bevan, M.W. (1987). GUS fusions: Beta-glucuronidase as a sensitive and versatile gene fusion marker in higher plants. EMBO J. 6: 3901-3907.
45. Kim, H.B., Schaller, H., Goh, C.H., Kwon, M., Choe, S., An, C.S., Durst, F., Feldmann, K.A., and Feyereisen, R. (2005). Arabidopsis cyp51 mutant shows postembryonic seedling lethality associated with lack of membrane integrity. Plant Physiol. 138: 2033-2047.
46. Kim, J.Y., Henrichs, S., Bailly, A., Vincenzetti, V., Sovero, V., Mancuso, S., Pollmann, S., Kim, D., Geisler, M., and Nam, H.G. (2010). Identification of an ABCB/P-glycoprotein-specific inhibitor of auxin transport by chemical genomics. J. Biol. Chem. 285: 23309-23317.
47. Lewis, D.R., and Muday, G.K. (2009). Measurement of auxin transport in Arabidopsis thaliana. Nat. Protoc. 4: 437-451.
48. Lim, L., Jackson-Lewis, V., Wong, L.C., Shui, G.H., Goh, A.X., Kesavapany, S., Jenner, A.M., Fivaz, M., Przedborski, S., and Wenk, M.R. (2012). Lanosterol induces mitochondrial uncoupling and protects dopaminergic neurons from cell death in a model for Parkinson's disease. Cell Death Differ. 19: 416-427.
49. Lindsey, K., Pullen, M.L., and Topping, J.F. (2003). Importance of plant sterols in pattern formation and hormone signalling. Trends Plant Sci. 8: 521-525.
50. Livak, K.J., and Schmittgen, T.D. (2001). Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T) method. Methods 25: 402-408.
51. Ljung, K., Bhalerao, R.P., and Sandberg, G. (2001). Sites and homeostatic control of auxin biosynthesis in Arabidopsis during vegetative growth. Plant J. 28: 465-474.
52. Lu, B., Zhang, Y., Wu, X., and Shi, J. (2007). Separation and determination of diversiform phytosterols in food materials using supercritical carbon dioxide extraction and ultraperformance liquid chromatography-atmospheric pressure chemical ionization-mass spectrometry. Anal. Chim. Acta 588: 50-63.
53. Mares-Sámano, S., Badhan, R., and Penny, J. (2009). Identification of putative steroid-binding sites in human ABCB1 and ABCG2. Eur. J. Med. Chem. 44: 3601-3611.
54. Masucci, J.D., Rerie, W.G., Foreman, D.R., Zhang, M., Galway, M.E., Marks, M.D., and Schiefelbein, J.W. (1996). The homeobox gene GLABRA2 is required for position-dependent cell differentiation in the root epidermis of Arabidopsis thaliana. Development 122: 1253-1260.
55. Mattsson, J., Ckurshumova, W., and Berleth, T. (2003). Auxin signaling in Arabidopsis leaf vascular development. Plant Physiol. 131: 1327-1339.
56. Mattsson, J., Sung, Z.R., and Berleth, T. (1999). Responses of plant vascular systems to auxin transport inhibition. Development 126: 2979-2991.
57. Men, S., Boutté, Y., Ikeda, Y., Li, X., Palme, K., Stierhof, Y.D., Hartmann, M.A., Moritz, T., and Grebe, M. (2008). Steroldependent endocytosis mediates post-cytokinetic acquisition of PIN2 auxin efflux carrier polarity. Nat. Cell Biol. 10: 237-244.
58. Mialoundama, A.S., Heintz, D., Debayle, D., Rahier, A., Camara, B., and Bouvier, F. (2009). Abscisic acid negatively regulates elicitorinduced synthesis of capsidiol in wild tobacco. Plant Physiol. 150: 1556-1566.
59. Mo, C., and Bard, M. (2005). Erg28p is a key protein in the yeast sterol biosynthetic enzyme complex. J. Lipid Res. 46: 1991-1998.
60. Mo, C., Milla, P., Athenstaedt, K., Ott, R., Balliano, G., Daum, G., and Bard, M. (2003). In yeast sterol biosynthesis the 3-keto reductase protein (Erg27p) is required for oxidosqualene cyclase (Erg7p) activity. Biochim. Biophys. Acta 1633: 68-74.
61. Mo, C., Valachovic, M., Randall, S.K., Nickels, J.T., and Bard, M. (2002). Protein-protein interactions among C-4 demethylation enzymes involved in yeast sterol biosynthesis. Proc. Natl. Acad. Sci. USA 99: 9739-9744.
62. Muday, G.K., Lomax, T.L., and Rayle, D.L. (1995). Characterization of the growth and auxin physiology of roots of the tomato mutant, diageotropica. Planta 195: 548-553.
63. Müller, A., Guan, C., Gälweiler, L., Tänzler, P., Huijser, P., Marchant, A., Parry, G., Bennett, M., Wisman, E., and Palme, K. (1998). AtPIN2 defines a locus of Arabidopsis for root gravitropism control. EMBO J. 17: 6903-6911.
64. Natter, K., Leitner, P., Faschinger, A., Wolinski, H., McCraith, S., Fields, S., and Kohlwein, S.D. (2005). The spatial organization of lipid synthesis in the yeast Saccharomyces cerevisiae derived from large scale green fluorescent protein tagging and high resolution microscopy. Mol. Cell. Proteomics 4: 662-672.
65. Nelson, J.A., Kahn, S., Spencer, T.A., Sharpless, K.B., and Clayton, R.B. (1975). Some aspects of substrate specificity in biological demethylation at C4 of steroids. Bioorg. Chem. 4: 363-376.
66. Noh, B., Murphy, A.S., and Spalding, E.P. (2001). Multidrug resistance-like genes of Arabidopsis required for auxin transport and auxin-mediated development. Plant Cell 13: 2441-2454.
67. Ohashi, M., Mizushima, N., Kabeya, Y., and Yoshimori, T. (2003). Localization of mammalian NAD(P)H steroid dehydrogenase-like protein on lipid droplets. J. Biol. Chem. 278: 36819-36829.
68. Okada, K., Ueda, J., Komaki, M.K., Bell, C.J., and Shimura, Y. (1991). Requirement of the auxin polar transport system in early stages of Arabidopsis floral bud formation. Plant Cell 3: 677-684.
69. Ovecka, M., Berson, T., Beck, M., Derksen, J., Samaj, J., Baluska, F., and Lichtscheidl, I.K. (2010). Structural sterols are involved in both the initiation and tip growth of root hairs in Arabidopsis thaliana. Plant Cell 22: 2999-3019.
70. Panicker, S.P., Ganguly, T., Consolo, M., Price, V., Mirmirani, P., Honda, K., and Karnik, P. (2012). Sterol intermediates of cholesterol biosynthesis inhibit hair growth and trigger an innate immune response in cicatricial alopecia. PLoS ONE 7: e38449.
71. Parent, N., Winstall, E., Beauchemin, M., Paquet, C., Poirier, G.G., and Bertrand, R. (2009). Proteomic analysis of enriched lysosomes at early phase of camptothecin-induced apoptosis in human U-937 cells. J. Proteomics 72: 960-973.
72. Peer, W.A., and Murphy, A.S. (2007). Flavonoids and auxin transport: Modulators or regulators? Trends Plant Sci. 12: 556-563.
73. Petrásek, J., and Friml, J. (2009). Auxin transport routes in plant development. Development 136: 2675-2688.
74. Pullen, M., Clark, N., Zarinkamar, F., Topping, J., and Lindsey, K. (2010). Analysis of vascular development in the hydra sterol biosynthetic mutants of Arabidopsis. PLoS ONE 5: e12227.
75. Reinhardt, D., Pesce, E.R., Stieger, P., Mandel, T., Baltensperger, K., Bennett, M., Traas, J., Friml, J., and Kuhlemeier, C. (2003). Regulation of phyllotaxis by polar auxin transport. Nature 426: 255-260.
76. Rhourri-Frih, B., Chaimbault, P., Claude, B., Lamy, C., André, P., and Lafosse, M. (2009). Analysis of pentacyclic triterpenes by LC-MS. A comparative study between APCI and APPI. J. Mass Spectrom. 44: 71-80.
77. Růzicka, K., Ljung, K., Vanneste, S., Podhorská, R., Beeckman, T., Friml, J., and Benková, E. (2007). Ethylene regulates root growth through effects on auxin biosynthesis and transport-dependent auxin distribution. Plant Cell 19: 2197-2212.
78. Schmidt, A.W., Doert, T., Goutal, S., Gruner, M., Mende, F., Kurzchalia, T.V., and Knoelker, H.J. (2006). Regio-and stereospecific synthesis of cholesterol derivatives and their hormonal activity in Caenorhabditis elegans. Eur. J. Org. Chem. 2006: 3687-3706.
79. Schmitt, L., Benabdelhak, H., Blight, M.A., Holland, I.B., and Stubbs, M.T. (2003). Crystal structure of the nucleotide-binding domain of the ABC-transporter haemolysin B: Identification of a variable region within ABC helical domains. J. Mol. Biol. 330: 333-342.
80. Schneider, C., Newman, R.A., Sutherland, D.R., Asser, U., and Greaves, M.F. (1982). A one-step purification of membrane proteins using a high efficiency immunomatrix. J. Biol. Chem. 257: 10766-10769.
81. Schrick, K., Fujioka, S., Takatsuto, S., Stierhof, Y.D., Stransky, H., Yoshida, S., and Jürgens, G. (2004b). A link between sterol biosynthesis, the cell wall, and cellulose in Arabidopsis. Plant J. 38: 227-243.
82. Schrick, K., Mayer, U., Horrichs, A., Kuhnt, C., Bellini, C., Dangl, J., Schmidt, J., and Jürgens, G. (2000). FACKEL is a sterol C-14 reductase required for organized cell division and expansion in Arabidopsis embryogenesis. Genes Dev. 14: 1471-1484.
83. Schrick, K., Mayer, U., Martin, G., Bellini, C., Kuhnt, C., Schmidt, J., and Jürgens, G. (2002). Interactions between sterol biosynthesis genes in embryonic development of Arabidopsis. Plant J. 31: 61-73.
84. Schrick, K., Nguyen, D., Karlowski, W.M., and Mayer, K.F. (2004a). START lipid/sterol-binding domains are amplified in plants and are predominantly associated with homeodomain transcription factors. Genome Biol. 5: R41.
85. Shui, G., Cheong, W.F., Jappar, I.A., Hoi, A., Xue, Y., Fernandis, A.Z., Tan, B.K., and Wenk, M.R. (2011). Derivatization-independent cholesterol analysis in crude lipid extracts by liquid chromatography/ mass spectrometry: Applications to a rabbit model for atherosclerosis. J. Chromatogr. A 1218: 4357-4365.
86. Sieburth, L.E. (1999). Auxin is required for leaf vein pattern in Arabidopsis. Plant Physiol. 121: 1179-1190.
87. Souter, M., Topping, J., Pullen, M., Friml, J., Palme, K., Hackett, R., Grierson, D., and Lindsey, K. (2002). hydra mutants of Arabidopsis are defective in sterol profiles and auxin and ethylene signaling. Plant Cell 14: 1017-1031.
88. Souter, M.A., Pullen, M.L., Topping, J.F., Zhang, X., and Lindsey, K. (2004). Rescue of defective auxin-mediated gene expression and root meristem function by inhibition of ethylene signalling in sterol biosynthesis mutants of Arabidopsis. Planta 219: 773-783.
89. Spann, N.J., et al. (2012). Regulated accumulation of desmosterol integrates macrophage lipid metabolism and inflammatory responses. Cell 151: 138-152.
90. Sukhanova, A., et al. (2013). Targeting C4-demethylating genes in the cholesterol pathway sensitizes cancer cells to EGF receptor inhibitors via increased EGF receptor degradation. Cancer Discov. 3: 96-111.
91. Tohge, T., and Fernie, A.R. (2012). Co-expression and co-responses: Within and beyond transcription. Front. Plant Sci. 3: 248.
92. Turner, S.R., and Somerville, C.R. (1997). Collapsed xylem phenotype of Arabidopsis identifies mutants deficient in cellulose deposition in the secondary cell wall. Plant Cell 9: 689-701.
93. Ulmasov, T., Murfett, J., Hagen, G., and Guilfoyle, T.J. (1997). Aux/IAA proteins repress expression of reporter genes containing natural and highly active synthetic auxin response elements. Plant Cell 9: 1963-1971.
94. Vinci, G., Xia, X., and Veitia, R.A. (2008). Preservation of genes involved in sterol metabolism in cholesterol auxotrophs: facts and hypotheses. PLoS ONE 3: e2883.
95. Wang, H., Jones, B., Li, Z., Frasse, P., Delalande, C., Regad, F., Chaabouni, S., Latché, A., Pech, J.C., and Bouzayen, M. (2005). The tomato Aux/IAA transcription factor IAA9 is involved in fruit development and leaf morphogenesis. Plant Cell 17: 2676-2692.
96. Wenzel, C.L., Hester, Q., and Mattsson, J. (2008). Identification of genes expressed in vascular tissues using NPA-induced vascular overgrowth in Arabidopsis. Plant Cell Physiol. 49: 457-468.
97. Willemsen, V., Friml, J., Grebe, M., van den Toorn, A., Palme, K., and Scheres, B. (2003). Cell polarity and PIN protein positioning in Arabidopsis require STEROL METHYLTRANSFERASE1 function. Plant Cell 15: 612-625.
98. Xue, T., Zhang, Y., Zhang, L., Yao, L., Hu, X., and Xu, L.X. (2013). Proteomic analysis of two metabolic proteins with potential to translocate to plasma membrane associated with tumor metastasis development and drug targets. J. Proteome Res. 12: 1754-1763.
99. Zaitseva, J., Jenewein, S., Jumpertz, T., Holland, I.B., and Schmitt, L. (2005). H662 is the linchpin of ATP hydrolysis in the nucleotide-binding domain of the ABC transporter HlyB. EMBO J. 24: 1901-1910.
100. Zhong, R., and Ye, Z.H. (2001). Alteration of auxin polar transport in the Arabidopsis ifl1 mutants. Plant Physiol. 126: 549-563.
101. Zhu, J.Y., Sae-Seaw, J., and Wang, Z.Y. (2013). Brassinosteroid signalling. Development 140: 1615-1620.