Understanding the role of defective invertases in plants: Tobacco nin88 fails to degrade sucrose

Plant Physiology

Volumn 161, Issue 4, 2013, Pages 1670-1681

  Le Roy, Katrien ^a   Vergauwen, Rudy ^a   Struyf, Tom ^a   Yuan, Shuguang ^a   Lammens, Willem ^a   Mátrai, Janka ^a   De Maeyer, Marc ^a   Van den Ende, Wim ^a  

^a UNIVERSITY OF LEUVEN   (Belgium)

Author keywords

[No Author keywords available]

Indexed keywords

EID: 84875745129     PISSN: 00320889     EISSN: 15322548     Source Type: Journal    
DOI: 10.1104/pp.112.209460     Document Type: Article

References (61)

1. Alberto F, Bignon C, Sulzenbacher G, Henrissat B, Czjzek M (2004) The three-dimensional structure of invertase (beta-fructosidase) from Thermotoga maritima reveals a bimodular arrangement and an evolutionary relationship between retaining and inverting glycosidases. J Biol Chem 279: 18903-18910
2. Alvaro-Benito M, Polo A, González B, Fernández-Lobato M, Sanz- Aparicio J (2010) Structural and kinetic analysis of Schwanniomyces occidentalis invertase reveals a new oligomerization pattern and the role of its supplementary domain in substrate binding. J Biol Chem 285: 13930-13941
3. Balibrea Lara ME, Gonzalez Garcia M-C, Fatima T, Ehness R, Lee TK, Proels R, Tanner W, Roitsch T (2004) Extracellular invertase is an essential component of cytokinin-mediated delay of senescence. Plant Cell 16: 1276-1287
4. Barratt DH, Derbyshire P, Findlay K, Pike M, Wellner N, Lunn J, Feil R, Simpson C, Maule AJ, Smith AM (2009) Normal growth of Arabidopsis requires cytosolic invertase but not sucrose synthase. Proc Natl Acad Sci USA 106: 13124-13129
5. Benhamou N, Grenier J, Chrispeels MJ (1991) Accumulation of b-fructosidase in the cell walls of tomato roots following infection by a fungal wilt pathogen. Plant Physiol 97: 739-750
6. Bhaskar PB, Wu L, Busse JS, Whitty BR, Hamernik AJ, Jansky SH, Buell CR, Bethke PC, Jiang J (2010) Suppression of the vacuolar invertase gene prevents cold-induced sweetening in potato. Plant Physiol 154: 939-948
7. Bolouri-Moghaddam M-R, Le Roy K, Xiang L, Rolland F, Van den Ende W (2010) Sugar signalling and antioxidant network connections in plant cells. FEBS J 277: 2022-2037
8. Bonfig KB, Gabler A, Simon UK, Luschin-Ebengreuth N, Hatz M, Berger S, Muhammad N, Zeier J, Sinha AK, Roitsch T (2010) Post-translational derepression of invertase activity in source leaves via down-regulation of invertase inhibitor expression is part of the plant defense response. Mol Plant 3: 1037-1048
9. Chen VB, Arendall WB III, Headd JJ, Keedy DA, Immormino RM, Kapral GJ, Murray LW, Richardson JS, Richardson DC (2010) Mol- Probity: all-atom structure validation for macromolecular crystallography. Acta Crystallogr D Biol Crystallogr 66: 12-21
10. De Coninck B, Le Roy K, Francis I, Clerens S, Vergauwen R, Halliday AM, Smith SM, Van Laere A, Van den Ende W (2005) Arabidopsis AtcwINV3 and 6 are not invertases but are fructan exohydrolases (FEHs) with different substrate specificities. Plant Cell Environ 28: 432-443
11. Delano WL (2002) The PyMol molecular graphics system. DeLano Scientific. http://www.pymol.org (March 14, 2013)
12. Delhaise P, Bardiaux M, Wodak SJ (1984) Interactive computer animation of macromolecules. J Mol Graph 2: 103-106
13. Engelke T, Hirsche J, Roitsch T (2010) Anther-specific carbohydrate supply and restoration of metabolically engineered male sterility. J Exp Bot 61: 2693-2706
14. Eswar N, Webb B, Marti-Renom MA, Madhusudhan MS, Eramian D, Shen MY, Pieper U, Sali A (2006) Comparative protein structure modeling using Modeller. Curr Protoc Bioinformatics Chapter 5: Unit 5.6
15. Fridman E, Carrari F, Liu YS, Fernie AR, Zamir D (2004) Zooming in on a quantitative trait for tomato yield using interspecific introgressions. Science 305: 1786-1789
16. Fulton DC, Stettler M, Mettler T, Vaughan CK, Li J, Francisco P, Gil M, Reinhold H, Eicke S, Messerli G, et al (2008) b-AMYLASE4, a noncatalytic protein required for starch breakdown, acts upstream of three active b-amylases in Arabidopsis chloroplasts. Plant Cell 20: 1040-1058
17. Goetz M, Godt DE, Guivarc'h A, Kahmann U, Chriqui D, Roitsch T (2001) Induction of male sterility in plants by metabolic engineering of the carbohydrate supply. Proc Natl Acad Sci USA 98: 6522-6527
18. Greiner S, Krausgrill S, Rausch T (1998) Cloning of a tobacco apoplasmic invertase inhibitor: proof of function of the recombinant protein and expression analysis during plant development. Plant Physiol 116: 733-742
19. Greiner S, Weil M, Krausgrill S, Rausch T (1995) A tobacco cDNA coding for cell-wall invertase. Plant Physiol 108: 825-826
20. Hayes MA, Feechan A, Dry IB (2010) Involvement of abscisic acid in the coordinated regulation of a stress-inducible hexose transporter (VvHT5) and a cell wall invertase in grapevine in response to biotrophic fungal infection. Plant Physiol 153: 211-221
21. Hirsche J, Engelke T, Völler D, Götz M, Roitsch T (2009) Interspecies compatibility of the anther specific cell wall invertase promoters from Arabidopsis and tobacco for generating male sterile plants. Theor Appl Genet 118: 235-245
22. Hothorn M, Van den Ende W, Lammens W, Rybin V, Scheffzek K (2010) Structural insights into the pH-controlled targeting of plant cell-wall invertase by a specific inhibitor protein. Proc Natl Acad Sci USA 107: 17427-17432
23. Jin Y, Ni D-A, Ruan Y-L (2009) Posttranslational elevation of cell wall invertase activity by silencing its inhibitor in tomato delays leaf senescence and increases seed weight and fruit hexose level. Plant Cell 21: 2072-2089
24. Kang BH, Xiong Y, Williams DS, Pozueta-Romero D, Chourey PS (2009) Miniature1-encoded cell wall invertase is essential for assembly and function of wall-in-growth in the maize endosperm transfer cell. Plant Physiol 151: 1366-1376
25. Kim JY, Mahé A, Guy S, Brangeon J, Roche O, Chourey PS, Prioul JL (2000) Characterization of two members of the maize gene family, Incw3 and Incw4, encoding cell-wall invertases. Gene 245: 89-102
26. Koch K (2004) Sucrose metabolism: regulatory mechanisms and pivotal roles in sugar sensing and plant development. Curr Opin Plant Biol 7: 235-246
27. Lammens W, Le Roy K, Schroeven L, Van Laere A, Rabijns A, Van den Ende W (2009) Structural insights into glycoside hydrolase family 32 and 68 enzymes: functional implications. J Exp Bot 60: 727-740
28. Le Roy K, Lammens W, Van Laere A, Van den Ende W (2008) Influencing the binding configuration of sucrose in the active sites of chicory fructan 1-exohydrolase and sugar beet fructan 6-exohydrolase. New Phytol 178: 572-580
29. Le Roy K, Lammens W, Verhaest M, De Coninck B, Rabijns A, Van Laere A, Van den Ende W (2007a) Unraveling the difference between invertases and fructan exohydrolases: a single amino acid (Asp-239) substitution transforms Arabidopsis cell wall invertase1 into a fructan 1-exohydrolase. Plant Physiol 145: 616-625
30. Le Roy K, Verhaest M, Rabijns A, Clerens S, Van Laere A, Van den Ende W (2007b) N-Glycosylation affects substrate specificity of chicory fructan 1-exohydrolase: evidence for the presence of an inulin binding cleft. New Phytol 176: 317-324
31. Li J, Francisco P, Zhou W, Edner C, Steup M, Ritte G, Bond CS, Smith SM (2009) Catalytically-inactive b-amylase BAM4 required for starch breakdown in Arabidopsis leaves is a starch-binding-protein. Arch Biochem Biophys 489: 92-98
32. Proels RK, Gonzalez MC, Roitsch T (2006) Gibberellin-dependent induction of tomato extracellular invertase Lin7 is required for pollen development. Funct Plant Biol 33: 547-554
33. Rausch T, Greiner S (2003) Plant protein inhibitors of invertase. Biochim Biophys Acta 1696: 253-261
34. Ritsema T, Hernández L, Verhaar A, Altenbach D, Boller T, Wiemken A, Smeekens S (2006) Developing fructan-synthesizing capability in a plant invertase via mutations in the sucrose-binding box. Plant J 48: 228-237
35. Roitsch T, González MC (2004) Function and regulation of plant invertases: sweet sensations. Trends Plant Sci 9: 606-613
36. Ruan Y-L (2012) Signaling role of sucrose metabolism in development. Mol Plant 5: 763-765
37. Ruan Y-L, Jin Y, Huang J (2009) Capping invertase activity by its inhibitor: roles and implications in sugar signaling, carbon allocation, senescence and evolution. Plant Signal Behav 4: 983-985
38. Ruan Y-L, Jin Y, Yang Y-J, Li G-J, Boyer JS (2010) Sugar input, metabolism, and signaling mediated by invertase: roles in development, yield potential, and response to drought and heat. Mol Plant 3: 942-955
39. Salerno GL, Curatti L (2003) Origin of sucrose metabolism in higher plants: when, how and why? Trends Plant Sci 8: 63-69
40. Siemens J, González MC, Wolf S, Hofmann C, Greiner S, Du Y, Rausch T, Roitsch T, Ludwig-Müller J (2011) Extracellular invertase is involved in the regulation of clubroot disease in Arabidopsis thaliana. Mol Plant Pathol 12: 247-262
41. Singh V, Louis J, Ayre BG, Reese JC, Pegadaraju V, Shah J (2011) TREHALOSE PHOSPHATE SYNTHASE11-dependent trehalose metabolism promotes Arabidopsis thaliana defense against the phloem-feeding insect Myzus persicae. Plant J 67: 94-104
42. Smeekens S, Ma J, Hanson J, Rolland F (2010) Sugar signals and molecular networks controlling plant growth. Curr Opin Plant Biol 13: 274-279
43. Sturm A (1999) Invertases: primary structures, functions, and roles in plant development and sucrose partitioning. Plant Physiol 121: 1-8
44. Sturm A, Hess D, Lee H-S, Leinhard S (1999) Neutral invertase is a novel type of sucrose-cleaving enzyme. Physiol Plant 107: 159-165
45. Tang GQ, Lüscher M, Sturm A (1999) Antisense repression of vacuolar and cell wall invertase in transgenic carrot alters early plant development and sucrose partitioning. Plant Cell 11: 177-189
46. Tarone G, Galetto G, Prat M, Comoglio PM (1982) Cell surface molecules and fibronectin-mediated cell adhesion: effect of proteolytic digestion of membrane proteins. J Cell Biol 94: 179-186
47. Tymowska-Lananne Z, Kreis M (1998) Plant invertases: physiology, biochemistry and molecular biology. Adv Bot Res 28: 72-117
48. Van den Ende W, De Coninck B, Clerens S, Vergauwen R, Van Laere A (2003) Unexpected presence of fructan 6-exohydrolases (6-FEHs) in nonfructan plants: characterization, cloning, mass mapping and functional analysis of a novel "cell-wall invertase-like" specific 6-FEH from sugar beet (Beta vulgaris L.). Plant J 36: 697-710
49. Van den Ende W, De Coninck B, Van Laere A (2004) Plant fructan exohydrolases: a role in signaling and defense? Trends Plant Sci 9: 523-528
50. Van den Ende W, Lammens W, Van Laere A, Schroeven L, Le Roy K (2009) Donor and acceptor substrate selectivity among plant glycoside hydrolase family 32 enzymes. FEBS J 276: 5788-5798
51. Van den Ende W, Michiels A, De Roover J, Verhaert P, Van Laere A (2000) Cloning and functional analysis of chicory root fructan 1-exohydrolase I (1-FEH I): a vacuolar enzyme derived from a cell wall invertase ancestor? Mass fingerprint of the enzyme. Plant J 23: 447-456
52. Van den Ende W, Van Laere A (1996) Fructan synthesizing and degrading activities in chicory roots (Cichorium intybus L.) during field-growth, storage and forcing. J Plant Physiol 149: 43-50
53. Vandesteene L, Ramon M, Le Roy K, Van Dijck P, Rolland F (2010) A single active trehalose-6-P synthase (TPS) and a family of putative regulatory TPS-like proteins in Arabidopsis. Mol Plant 3: 406-419
54. Vargas WA, Pontis HG, Salerno GL (2008) New insights on sucrose metabolism: evidence for an active A/N-Inv in chloroplasts uncovers a novel component of the intracellular carbon trafficking. Planta 227: 795-807
55. Vargas WA, Salerno GL (2010) The Cinderella story of sucrose hydrolysis: alkaline/neutral invertases, from cyanobacteria to unforeseen roles in plant cytosol and organelles. Plant Sci 178: 1-8
56. Verhaest M, Lammens W, Le Roy K, De Coninck B, De Ranter CJ, Van Laere A, Van den Ende W, Rabijns A (2006) X-ray diffraction structure of a cell-wall invertase from Arabidopsis thaliana. Acta Crystallogr D Biol Crystallogr 62: 1555-1563
57. Verhaest M, Lammens W, Le Roy K, De Ranter CJ, Van Laere A, Rabijns A, Van den Ende W (2007) Insights into the fine architecture of the active site of chicory fructan 1-exohydrolase: 1-kestose as substrate vs sucrose as inhibitor. New Phytol 174: 90-100
58. Verhaest M, Van den Ende W, Roy KL, De Ranter CJ, Laere AV, Rabijns A (2005) X-ray diffraction structure of a plant glycosyl hydrolase family 32 protein: fructan 1-exohydrolase IIa of Cichorium intybus. Plant J 41: 400-411
59. Wang L, Li XR, Lian H, Ni DA, He YK, Chen XY, Ruan YL (2010) Evidence that high activity of vacuolar invertase is required for cotton fiber and Arabidopsis root elongation through osmotic dependent and independent pathways, respectively. Plant Physiol 154: 744-756
60. Xiang L, Le Roy K, Bolouri-Moghaddam MR, Vanhaecke M, Lammens W, Rolland F, Van den Ende W (2011) Exploring the neutral invertaseoxidative stress defence connection in Arabidopsis thaliana. J Exp Bot 62: 3849-3862
61. Yuan S, Le Roy K, Venken T, Lammens W, Van den Ende W, De Maeyer M (2012) pKa modulation of the acid/base catalyst within GH32 and GH68: a role in substrate/inhibitor specificity? PLoS ONE 7: e37453