Ge, Changrong, Georgiev, Alexander, Öhman, Anders, Wieslander, A. and Kelly, Amélie A.. (2011) Tryptophan residues promote membrane association for a plant lipid glycosyltransferase involved in phosphate stress. Journal of Biological Chemistry, Volume 286 (Number 8). pp. 6669-6684. ISSN 0021-9258

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Abstract

Chloroplast membranes contain a substantial excess of the nonbilayer-prone monogalactosyldiacylglycerol (GalDAG) over the biosynthetically consecutive, bilayer-forming digalactosyldiacylglycerol (GalGalDAG), yielding a high membrane curvature stress. During phosphate shortage, plants replace phospholipids with GalGalDAG to rescue phosphate while maintaining membrane homeostasis. Here we investigate how the activity of the corresponding glycosyltransferase (GT) in Arabidopsis thaliana (atDGD2) depends on local bilayer properties by analyzing structural and activity features of recombinant protein. Fold recognition and sequence analyses revealed a two-domain GT-B monotopic structure, present in other plant and bacterial glycolipid GTs, such as the major chloroplast GalGalDAG GT atDGD1. Modeling led to the identification of catalytically important residues in the active site of atDGD2 by site-directed mutagenesis. The DGD synthases share unique bilayer interface segments containing conserved tryptophan residues that are crucial for activity and for membrane association. More detailed localization studies and liposome binding analyses indicate differentiated anchor and substrate-binding functions for these separated enzyme interface regions. Anionic phospholipids, but not curvature-increasing nonbilayer lipids, strongly stimulate enzyme activity. From our studies, we propose a model for bilayer "control" of enzyme activity, where two tryptophan segments act as interface anchor points to keep the substrate region close to the membrane surface. Binding of the acceptor substrate is achieved by interaction of positive charges in a surface cluster of lysines, arginines, and histidines with the surrounding anionic phospholipids. The diminishing phospholipid fraction during phosphate shortage stress will then set the new GalGalDAG/phospholipid balance by decreasing stimulation of atDGD2.

Item Type:	Journal Article
Subjects:	Q Science > QK Botany Q Science > QP Physiology
Divisions:	Faculty of Science > Life Sciences (2010- ) > Warwick HRI (2004-2010)
Library of Congress Subject Headings (LCSH):	Tryptophan, Glycosyltransferases, Plant lipids, Escherichia coli, Bilayer lipid membranes, Phosphates, Arabidopsis thaliana
Journal or Publication Title:	Journal of Biological Chemistry
Publisher:	American Society for Biochemistry and Molecular Biology
ISSN:	0021-9258
Date:	25 February 2011
Volume:	Volume 286
Number:	Number 8
Page Range:	pp. 6669-6684
Identification Number:	10.1074/jbc.M110.138495
Status:	Peer Reviewed
Publication Status:	Published
Access rights to Published version:	Restricted or Subscription Access
Funder:	Wenner-Gren Foundation, Kungl. Svenska vetenskapsakademien [Royal Swedish Academy of Science], Sixth Framework Programme (European Commission) (FP6), Sweden. Vetenskapsrådet [Research Council]
References:	1. Granseth, E., Daley, D. O., Rapp, M., Mele´n, K., and von Heijne, G. (2005) J. Mol. Biol. 352, 489–494 2. Booth, P. J., and Curnow, P. (2009) Curr. Opin. Struct. Biol. 19, 8–13 3. Marsh, D. (2007) Biophys. J. 93, 3884–3899 4. Kelly, A. A., and Do¨rmann, P. (2004) Curr. Opin. Plant Biol. 7, 262–269 5. Edman, M., Berg, S., Storm, P., Wikstro¨m, M., Vikstro¨m, S., Ohman, A., and Wieslander, A. (2003) J. Biol. Chem. 278, 8420–8428 6. Vikstro¨m, S., Li, L., Karlsson, O. P., and Wieslander, A. (1999) Biochemistry 38, 5511–5520 7. Alley, S. H., Ces, O., Templer, R. H., and Barahona, M. (2008) Biophys. J. 94, 2938–2954 8. Cruz-Ramírez, A., Oropeza-Aburto, A., Razo-Herna´ndez, F., Ramírez- Cha´vez, E., and Herrera-Estrella, L. (2006) Proc. Natl. Acad. Sci. U.S.A. 103, 6765–6770 9. Gaude, N., Tippmann, H., Flemetakis, E., Katinakis, P., Udvardi, M., and Do¨rmann, P. (2004) J. Biol. Chem. 279, 34624–34630 10. McMahon, H. T., and Gallop, J. L. (2005) Nature 438, 590–596 11. Zimmerberg, J., and Kozlov, M. M. (2006) Nat. Rev. Mol. Cell Biol. 7, 9–19 12. Williams, W. P., and Quinn, P. J. (1987) J. Bioenerg. Biomembr. 19, 605–624 13. Webb, M. S., and Green, B. R. (1991) Biochim. Biophys. Acta 1060, 133–158 14. Mock, T., and Kroon, B. M. (2002) Phytochemistry 61, 41–51 15. Gaude, N., Bre´he´lin, C., Tischendorf, G., Kessler, F., and Do¨rmann, P. (2007) Plant J. 49, 729–739 16. Torres-Franklin, M. L., Gigon, A., de Melo, D. F., Zuily-Fodil, Y., and Pham-Thi, A. T. (2007) Physiol. Plant. 131, 201–210 17. Su¨ss, K. H., and Yordanov, I. T. (1986) Plant Physiol. 81, 192–199 18. Chen, J., Burke, J. J., Xin, Z., Xu, C., and Velten, J. (2006) Plant Cell Environ. 29, 1437–1448 19. Moellering, E. R., Muthan, B., and Benning, C. (2010) Science 330, 226–228 20. Barkan, L., Vijayan, P., Carlsson, A. S., Mekhedov, S., and Browse, J. (2006) Plant Physiol. 141, 1012–1020 21. Cantarel, B. L., Coutinho, P. M., Rancurel, C., Bernard, T., Lombard, V., and Henrissat, B. (2009) Nucleic Acids Res. 37, D233–D238 22. Botte´, C., Jeanneau, C., Snajdrova, L., Bastien, O., Imberty, A., Breton, C., and Mare´chal, E. (2005) J. Biol. Chem. 280, 34691–34701 23. Ho¨lzl, G., Leipelt, M., Ott, C., Za¨hringer, U., Lindner, B., Warnecke, D., and Heinz, E. (2005) Glycobiology 15, 874–886 24. Lind, J., Ra¨mo¨, T., Klement, M. L., Ba´ra´ny-Wallje, E., Epand, R. M., Epand, R. F., Ma¨ler, L., and Wieslander, A. (2007) Biochemistry 46, 5664–567725. Balali-Mood, K., Bond, P. J., and Sansom, M. S. (2009) Biochemistry 48, 2135–2145 26. Guerin, M. E., Kordulakova, J., Schaeffer, F., Svetlikova, Z., Buschiazzo, A., Giganti, D., Gicquel, B., Mikusova, K., Jackson, M., and Alzari, P. M. (2007) J. Biol. Chem. 282, 20705–20714 27. Klement, M. L., Ojemyr, L., Tagscherer, K. E., Widmalm, G., and Wieslander, A. (2007) Mol. Microbiol. 65, 1444–1457 28. Matsumoto, K., Okada, M., Horikoshi, Y., Matsuzaki, H., Kishi, T., Itaya, M., and Shibuya, I. (1998) J. Bacteriol. 180, 100–106 29. Wikstro¨m, M., Kelly, A. A., Georgiev, A., Eriksson, H. M., Klement, M. R., Bogdanov, M., Dowhan, W., and Wieslander, A. (2009) J. Biol. Chem. 284, 954–965 30. Kelly, A. A., and Do¨rmann, P. (2002) J. Biol. Chem. 277, 1166–1173 31. Georgiev, A. (2008) Membrane Stress and the Role of GYF Domain Proteins. Ph.D. thesis, Stockholm University 32. Karlsson, O. P., Dahlqvist, A., Vikstro¨m, S., and Wieslander, A. (1997) J. Biol. Chem. 272, 929–936 33. Buser, C. A., and McLaughlin, S. (1998) Methods Mol. Biol. 84, 267–281 34. Larkin, M. A., Blackshields, G., Brown, N. P., Chenna, R., McGettigan, P. A., McWilliam, H., Valentin, F., Wallace, I. M., Wilm, A., Lopez, R., Thompson, J. D., Gibson, T. J., and Higgins, D. G. (2007) Bioinformatics 23, 2947–2948 35. Guerin, M. E., Buschiazzo, A., Kordula´kova´, J., Jackson, M., and Alzari, P. M. (2005) Acta Crystallogr. Sect. F Struct. Biol. Cryst. Commun. 61, 518–520 36. Barreras, M., Salinas, S. R., Abdian, P. L., Kampel, M. A., and Ielpi, L. (2008) J. Biol. Chem. 283, 25027–25035 37. Hu, Y., Chen, L., Ha, S., Gross, B., Falcone, B., Walker, D., Mokhtarzadeh, M., and Walker, S. (2003) Proc. Natl. Acad. Sci. U.S.A. 100, 845–849 38. Ginalski, K., Elofsson, A., Fischer, D., and Rychlewski, L. (2003) Bioinformatics 19, 1015–1018 39. Guex, N., and Peitsch, M. C. (1997) Electrophoresis 18, 2714–2723 40. Peitsch, M. C. (1995) Nature Biotechnology 13, 658–660 41. Arnold, K., Bordoli, L., Kopp, J., and Schwede, T. (2006) Bioinformatics 22, 195–201 42. Hooft, R. W., Vriend, G., Sander, C., and Abola, E. E. (1996) Nature 381, 272 43. Bru¨nger, A. T. (1992) X-PLOR, Version 3.1: A system for X-ray Crystallography and NMR, Yale University Press, New Haven, CT 44. Schu¨ttelkopf, A. W., and van Aalten, D. M. (2004) Acta Crystallogr. D Biol. Crystallogr. 60, 1355–1363 45. Koradi, R., Billeter, M., and Wuthrich, K. (1996) J. Mol. Graph. 14, 51–55 46. Dolinsky, T. J., Czodrowski, P., Li, H., Nielsen, J. E., Jensen, J. H., Klebe, G., and Baker, N. A. (2007) Nucleic Acids Res. 35, W522–W525 47. Baker, N. A., Sept, D., Joseph, S., Holst, M. J., and McCammon, J. A. (2001) Proc. Natl. Acad. Sci. U.S.A. 98, 10037–10041 48. Snider, C., Jayasinghe, S., Hristova, K., and White, S. H. (2009) Protein Sci. 18, 2624–2628 49. Lairson, L. L., Henrissat, B., Davies, G. J., and Withers, S. G. (2008) Annu. Rev. Biochem. 77, 521–555 50. Kelly, A. A., Froehlich, J. E., and Do¨rmann, P. (2003) Plant Cell 15, 2694–2706 51. Cladera, J., Rigaud, J. L., Villaverde, J., and Dun˜ach, M. (1997) Eur. J. Biochem. 243, 798–804 52. Nakamura, Y., Koizumi, R., Shui, G., Shimojima, M., Wenk, M. R., Ito, T., and Ohta, H. (2009) Proc. Natl. Acad. Sci. U.S.A. 106, 20978–20983 53. Marsico, A., Scheubert, K., Tuukkanen, A., Henschel, A., Winter, C., Winnenburg, R., and Schroeder, M. (2010) Nucleic Acids Res. 38, D181–D189 54. Li, L., Storm, P., Karlsson, O. P., Berg, S., and Wieslander, A. (2003) Biochemistry 42, 9677–9686 55. Ha, S., Walker, D., Shi, Y., and Walker, S. (2000) Protein Sci. 9, 1045–1052 56. Ferna´ndez-Vidal, M., Jayasinghe, S., Ladokhin, A. S., and White, S. H. (2007) J. Mol. Biol. 370, 459–470 57. He, J., Vora, M., Haney, R. M., Filonov, G. S., Musselman, C. A., Burd, C. G., Kutateladze, A. G., Verkhusha, V. V., Stahelin, R. V., and Kutateladze, T. G. (2009) Proteins 76, 852–860 58. Palsdottir, H., and Hunte, C. (2004) Biochim. Biophys. Acta 1666, 2–18 59. Kelly, A. A. (2003) The Biosynthesis and Function of the Galactolipid Digalactosyldiacylglycerol in Arabidopsis thaliana. Ph.D. thesis, University of Potsdam, Germany 60. Block, M. A., Dorne, A. J., Joyard, J., and Douce, R. (1983) J. Biol. Chem. 258, 13281–13286 61. Guskov, A., Kern, J., Gabdulkhakov, A., Broser, M., Zouni, A., and Saenger, W. (2009) Nat. Struct. Mol. Biol. 16, 334–342 62. Mizusawa, N., Sakurai, I., Sato, N., and Wada, H. (2009) FEBS Lett. 583, 718–722 63. Van Walraven, H. S., Koppenaal, E., Marvin, H. J., Hagendoorn, M. J., and Kraayenhof, R. (1984) Eur. J. Biochem. 144, 563–569 64. Navarro, J., Toivio-Kinnucan, M., and Racker, E. (1984) Biochemistry 23, 130–135 65. Jensen, J. W., and Schutzbach, J. S. (1988) Biochemistry 27, 6315–6320 66. Demel, R. A., de Swaaf, M. E., van ’t Hof, R., Mannock, D. A., McElhaney, R. E., and de Kruijff, B. (1995) Mol. Membr. Biol. 12, 255–261 67. van den Brink-van der Laan, E., Dalbey, R. E., Demel, R. A., Killian, J. A., and de Kruijff, B. (2001) Biochemistry 40, 9677–9684 68. Goss, R., Latowski, D., Grzyb, J., Vieler, A., Lohr, M., Wilhelm, C., and Strzalka, K. (2007) Biochim. Biophys. Acta 1768, 67–75 69. Rand Doyen, J., Yucer, N., Lichtenberger, L. M., and Kulmacz, R. J. (2008) Prostaglandins Other Lipid Mediat. 85, 134–143 70. Li, M., Welti, R., and Wang, X. (2006) Plant Physiol. 142, 750–761 71. Awai, K., Xu, C., Tamot, B., and Benning, C. (2006) Proc. Natl. Acad. Sci. U.S.A. 103, 10817–10822 72. Kelly, A. A.,O¨ hman, A., Sedoud, A., and Wieslander, A. (2007) in Current Advances in the Biochemistry and Cell Biology of Plant Lipids (Benning, C., and Olhlrogge, J., eds) pp. 25–31, Aardvark Global Publishing Co., Salt Lake City, UT 73. Dubots, E., Audry, M., Yamaryo, Y., Bastien, O., Ohta, H., Breton, C., Mare´chal, E., and Block, M. A. (2010) J. Biol. Chem. 285, 6003–6011 74. Linde, K., Gro¨bner, G., and Rilfors, L. (2004) FEBS Lett. 575, 77–80 75. Zhang, Y. M., and Rock, C. O. (2008) Nat. Rev. Microbiol. 6, 222–233 76. Sakurai, I., Mizusawa, N., Wada, H., and Sato, N. (2007) Plant Physiol. 145, 1361–1370 77. Liu, W., and Caffrey, M. (2006) Biochemistry 45, 11713–11726 78. Viklund, H., Granseth, E., and Elofsson, A. (2006) J. Mol. Biol. 361, 591–603 79. Bhardwaj, N., Stahelin, R. V., Langlois, R. E., Cho, W., and Lu, H. (2006) J. Mol. Biol. 359, 486–495 80. Malik, A., and Ahmad, S. (2007) BMC Struct. Biol. 7, 1 81. Jones, J. A., Rawles, R., and Hannun, Y. A. (2005) Biochemistry 44, 13235–13245 82. Gelb, M. H., Cho, W., and Wilton, D. C. (1999) Curr. Opin. Struct. Biol. 9, 428–432 83. Beers, S. A., Buckland, A. G., Giles, N., Gelb, M. H., and Wilton, D. C. (2003) Biochemistry 42, 7326–7338 84. Sanderson, J. M., and Whelan, E. J. (2004) Phys. Chem. Chem. Phys. 6, 1012–1017 85. Johansson, A. C., and Lindahl, E. (2009) J. Chem. Phys. 130, 185101 86. MirAfzali, Z., Leipprandt, J. R., McCracken, J. L., and DeWitt, D. L. (2006) J. Biol. Chem. 281, 28354–28364 87. Spencer, A. G., Thuresson, E., Otto, J. C., Song, I., Smith, T., DeWitt, D. L., Garavito, R. M., and Smith, W. L. (1999) J. Biol. Chem. 274, 32936–32942 88. Dries, D. R., Gallegos, L. L., and Newton, A. C. (2007) J. Biol. Chem. 282, 826–830 89. Mattjus, P. (2009) Biochim. Biophys. Acta. 1788, 267–272 90. Jorasch, P., Wolter, F. P., Za¨hringer, U., and Heinz, E. (1998) Mol. Microbiol. 29, 419–430 91. Minnikin, D. E., Abdolrahimzadeh, H., and Baddiley, J. (1972) FEBS Lett. 27, 16–18 92. Eisenberg, D., Schwarz, E., Komaromy, M., and Wall, R. (1984) J. Mol. Biol. 179, 125–142
URI:	http://wrap.warwick.ac.uk/id/eprint/41581

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