Differences in salicylic acid glucose conjugations by UGT74F1 and UGT74F2 from Arabidopsis thaliana

Scientific Reports

Volumn 7, Issue , 2017, Pages

  Thompson, Alayna M George ^a   Iancu, Cristina V ^a   Neet, Kenneth E ^a   Dean, John V ^b   Choe, Jun Yong ^a  

^a ROSALIND FRANKLIN UNIVERSITY OF MEDICINE AND SCIENCE   (United States)

^b DEPAUL UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ARABIDOPSIS PROTEIN; ESTER; GLUCOSE; GLUCOSIDE; GLUCOSYLTRANSFERASE; PROTEIN BINDING; SALICYLIC ACID; UDP-GLUCOSYLTRANSFERASE UGT74F2, ARABIDOPSIS;

ARABIDOPSIS; CELL VACUOLE; CHEMISTRY; GENETICS; METABOLISM; MOLECULAR MODEL; MUTATION; PROTEIN DOMAIN; TRANSPORT AT THE CELLULAR LEVEL;

ARABIDOPSIS; ARABIDOPSIS PROTEINS; BIOLOGICAL TRANSPORT; ESTERS; GLUCOSE; GLUCOSIDES; GLUCOSYLTRANSFERASES; MODELS, MOLECULAR; MUTATION; PROTEIN BINDING; PROTEIN DOMAINS; SALICYLIC ACID; VACUOLES;

EID: 85031688366     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/srep46629     Document Type: Article

References (46)

1. Raskin, I., Skubatz, H., Tang, W. & Meeuse, B. J. D. Salicylic Acid Levels in Thermogenic and Non-Thermogenic Plants. Ann. Bot. 66, 369-373 (1990).
2. Malamy, J., Carr, J. P., Klessig, D. F. & Raskin, I. Salicylic Acid: a likely endogenous signal in the resistance response of tobacco to viral infection. Science 250, 1002-1004 (1990).
3. Delaney, T. P. et al. A central role of salicylic Acid in plant disease resistance. Science 266, 1247-1250 (1994).
4. Métraux, J. P. et al. Increase in salicylic Acid at the onset of systemic acquired resistance in cucumber. Science 250, 1004-1006 (1990).
5. Krinke, O. et al. Phosphatidylinositol 4-kinase activation is an early response to salicylic acid in Arabidopsis suspension cells. Plant Physiol. 144, 1347-1359 (2007).
6. Rivas-San Vicente, M. & Plasencia, J. Salicylic acid beyond defence: its role in plant growth and development. J. Exp. Bot. 62, 3321-3338 (2011).
7. Klessig, D. F. et al. Induction, modification, and perception of the salicylic acid signal in plant defence. Biochem. Soc. Symp. 60, 219-229 (1994).
8. Schulz, M., Schnabl, H., Manthe, B., Schweihofen, B. & Casser, I. Uptake and detoxification of salicylic acid by Vicia faba and Fagopyrum esculentum. Phytochemistry 33, 291-294 (1993).
9. Edwards, R. Conjugation and Metabolism of Salicylic Acid in Tobacco. J. Plant Physiol. 143, 609-614 (1994).
10. Silverman, P. et al. Salicylic Acid in Rice (Biosynthesis, Conjugation, and Possible Role). Plant Physiol. 108, 633-639 (1995).
11. Tanaka, S., Hayakawa, K., Umetani, Y. & Tabata, M. Glucosylation of isomeric hydroxybenzoic acids by cell suspension cultures of Mallotus japonicus. Phytochemistry 29, 1555-1558 (1990).
12. Lee, H. I. & Raskin, I. Glucosylation of Salicylic Acid in Nicotiana tabacum Cv. Xanthi-nc. Phytopathology 88, 692-697 (1998).
13. Dean, J. V., Shah, R. P. & Mohammed, L. A. Formation and vacuolar localization of salicylic acid glucose conjugates in soybean cell suspension cultures. Physiol. Plant. 118, 328-336 (2003).
14. Dean, J. V., Mohammed, L. A. & Fitzpatrick, T. The formation, vacuolar localization, and tonoplast transport of salicylic acid glucose conjugates in tobacco cell suspension cultures. Planta 221, 287-296 (2005).
15. Lim, E.-K. et al. The activity of Arabidopsis glycosyltransferases toward salicylic acid, 4-hydroxybenzoic acid, and other benzoates. J. Biol. Chem. 277, 586-592 (2002).
16. Dean, J. V. & Delaney, S. P. Metabolism of salicylic acid in wild-type, ugt74f1 and ugt74f2 glucosyltransferase mutants of Arabidopsis thaliana. Physiol. Plant. 132, 417-425 (2008).
17. Song, J. T. et al. Overexpression of AtSGT1, an Arabidopsis salicylic acid glucosyltransferase, leads to increased susceptibility to Pseudomonas syringae. Phytochemistry 69, 1128-1134 (2008).
18. Boachon, B. et al. Role of two UDP-Glycosyltransferases from the L group of arabidopsis in resistance against pseudomonas syringae. Eur. J. Plant Pathol. 139, 707-720 (2014).
19. Quiel, J. A. & Bender, J. Glucose conjugation of anthranilate by the Arabidopsis UGT74F2 glucosyltransferase is required for tryptophan mutant blue fluorescence. J. Biol. Chem. 278, 6275-6281 (2003).
20. Cartwright, A. M., Lim, E.-K., Kleanthous, C. & Bowles, D. J. A kinetic analysis of regiospecific glucosylation by two glycosyltransferases of Arabidopsis thaliana: domain swapping to introduce new activities. J. Biol. Chem. 283, 15724-15731 (2008).
21. Caputi, L., Malnoy, M., Goremykin, V., Nikiforova, S. & Martens, S. A genome-wide phylogenetic reconstruction of family 1 UDPglycosyltransferases revealed the expansion of the family during the adaptation of plants to life on land. Plant J. Cell Mol. Biol. 69, 1030-1042 (2012).
22. Bowles, D., Lim, E.-K., Poppenberger, B. & Vaistij, F. E. Glycosyltransferases of lipophilic small molecules. Annu. Rev. Plant Biol. 57, 567-597 (2006).
23. Lim, E.-K. & Bowles, D. J. A class of plant glycosyltransferases involved in cellular homeostasis. EMBO J. 23, 2915-2922 (2004).
24. Song, C. et al. Glucosylation of 4-Hydroxy-2,5-Dimethyl-3(2H)-Furanone, the Key Strawberry Flavor Compound in Strawberry Fruit. Plant Physiol. 171, 139-151 (2016).
25. Tanaka, K. et al. UGT74D1 catalyzes the glucosylation of 2-oxindole-3-acetic acid in the auxin metabolic pathway in Arabidopsis. Plant Cell Physiol. 55, 218-228 (2014).
26. Offen, W. et al. Structure of a flavonoid glucosyltransferase reveals the basis for plant natural product modification. EMBO J. 25, 1396-1405 (2006).
27. Ross, J., Li, Y., Lim, E. & Bowles, D. J. Higher plant glycosyltransferases. Genome Biol. 2, REVIEWS3004 (2001).
28. Hiromoto, T. et al. Structural basis for acceptor-substrate recognition of UDP-glucose: anthocyanidin 3-O-glucosyltransferase from Clitoria ternatea. Protein Sci. Publ. Protein Soc. 24, 395-407 (2015).
29. Modolo, L. V., Escamilla-Treviño, L. L., Dixon, R. A. & Wang, X. Single amino acid mutations of Medicago glycosyltransferase UGT85H2 enhance activity and impart reversibility. FEBS Lett. 583, 2131-2135 (2009).
30. He, X.-Z., Wang, X. & Dixon, R. A. Mutational analysis of the Medicago glycosyltransferase UGT71G1 reveals residues that control regioselectivity for (iso)flavonoid glycosylation. J. Biol. Chem. 281, 34441-34447 (2006).
31. Brazier-Hicks, M. et al. Characterization and engineering of the bifunctional N- and O-glucosyltransferase involved in xenobiotic metabolism in plants. Proc. Natl. Acad. Sci. USA 104, 20238-20243 (2007).
32. Lin, J.-S. et al. UDP-glycosyltransferase 72B1 catalyzes the glucose conjugation of monolignols and is essential for the normal cell wall lignification in Arabidopsis thaliana. Plant J. Cell Mol. Biol. 88, 26-42 (2016).
33. Modolo, L. V. et al. Crystal structures of glycosyltransferase UGT78G1 reveal the molecular basis for glycosylation and deglycosylation of (iso)flavonoids. J. Mol. Biol. 392, 1292-1302 (2009).
34. Li, L. et al. Crystal structure of Medicago truncatula UGT85H2-insights into the structural basis of a multifunctional (iso)flavonoid glycosyltransferase. J. Mol. Biol. 370, 951-963 (2007).
35. Edgcomb, S. P. & Murphy, K. P. Variability in the pKa of histidine side-chains correlates with burial within proteins. Proteins 49, 1-6 (2002).
36. Shao, H. et al. Crystal structures of a multifunctional triterpene/flavonoid glycosyltransferase from Medicago truncatula. Plant Cell 17, 3141-3154 (2005).
37. Miroux, B. & Walker, J. E. Over-production of proteins in Escherichia coli: mutant hosts that allow synthesis of some membrane proteins and globular proteins at high levels. J. Mol. Biol. 260, 289-298 (1996).
38. Van Duyne, G. D., Standaert, R. F., Karplus, P. A., Schreiber, S. L. & Clardy, J. Atomic structures of the human immunophilin FKBP- 12 complexes with FK506 and rapamycin. J. Mol. Biol. 229, 105-124 (1993).
39. Sheldrick, G. M. Experimental phasing with SHELXC/D/E: combining chain tracing with density modification. Acta Crystallogr. D Biol. Crystallogr. 66, 479-485 (2010).
40. Langer, G. G., Hazledine, S., Wiegels, T., Carolan, C. & Lamzin, V. S. Visual automated macromolecular model building. Acta Crystallogr. D Biol. Crystallogr. 69, 635-641 (2013).
41. Emsley, P., Lohkamp, B., Scott, W. G. & Cowtan, K. Features and development of Coot. Acta Crystallogr. D Biol. Crystallogr. 66, 486-501 (2010).
42. McCoy, A. J. et al. Phaser crystallographic software. J. Appl. Crystallogr. 40, 658-674 (2007).
43. Adams, P. D., Mustyakimov, M., Afonine, P. V. & Langan, P. Generalized X-ray and neutron crystallographic analysis: more accurate and complete structures for biological macromolecules. Acta Crystallogr. D Biol. Crystallogr. 65, 567-573 (2009).
44. Murshudov, G. N. et al. REFMAC5 for the refinement of macromolecular crystal structures. Acta Crystallogr. D Biol. Crystallogr. 67, 355-367 (2011).
45. Esnouf, R. M. Further additions to MolScript version 1.4, including reading and contouring of electron-density maps. Acta Crystallogr. D Biol. Crystallogr. 55, 938-940 (1999).
46. Merritt, E. A. & Bacon, D. J. Raster3D: photorealistic molecular graphics. Methods Enzymol. 277, 505-524 (1997).