Structure, evolution, and expression of the two invertase gene families of rice

Journal of Molecular Evolution

Volumn 60, Issue 5, 2005, Pages 615-634

  Ji, Xuemei ^a,b   Van Den Ende, Wim ^c   Van Laere, Andre ^c   Cheng, Shihua ^b   Bennett, John ^a  

^a INTERNATIONAL RICE RESEARCH INSTITUTE   (Philippines)

^b CHINA NATIONAL RICE RESEARCH INSTITUTE   (China)

^c UNIVERSITY OF LEUVEN   (Belgium)

Author keywords

Arabidopsis thaliana; Cell wall; Chloroplast; Cytosol; Intron loss; Mitochondrion; Oryza sativa; Subcellular targeting; Vacuole

Indexed keywords

BETA FRUCTOFURANOSIDASE;

AMINO TERMINAL SEQUENCE; ARABIDOPSIS; ARTICLE; CELL WALL; ENDOPLASMIC RETICULUM; GENE DUPLICATION; GENE EXPRESSION; GENE IDENTIFICATION; GENE LOSS; GENE STRUCTURE; GENETIC VARIABILITY; INTRON; NUCLEOTIDE SEQUENCE; PROTEIN MOTIF; RICE; TONOPLAST; YEAST;

AMINO ACID SEQUENCE; ARABIDOPSIS; BETA-FRUCTOFURANOSIDASE; CELL WALL; CHROMOSOME MAPPING; CLUSTER ANALYSIS; COMPUTATIONAL BIOLOGY; DATABASES, GENETIC; DNA PRIMERS; EVOLUTION, MOLECULAR; GENE COMPONENTS; GENE EXPRESSION; MOLECULAR SEQUENCE DATA; MULTIGENE FAMILY; ORYZA SATIVA; PHYLOGENY; PROTEIN SORTING SIGNALS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SEQUENCE ALIGNMENT; VACUOLES;

ARABIDOPSIS; ARABIDOPSIS THALIANA; CYANOBACTERIA; ORYZA SATIVA;

EID: 21244447375     PISSN: 00222844     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00239-004-0242-1     Document Type: Article

References (74)

1. F Alberto C Bignon G Sulzenbacher B Henrissat M Czjzek 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. M Ares Jr L Grate MH Pauling 1999 A handful of intron-containing genes produces the lion's share of yeast mRNA RNA 5 1138 1139
3. G Avigad PM Dey 1997 Carbohydrate metabolism: storage carbohydrates PM Dey JB Harborne Plant biochemistry Academic Press San Diego 143 204
4. PA Balk AD de Boer 1999 Rapid stalk elongation in tulip (Tulipa gesneriana L. cv. Apeldoorn) and the combined action of cold-induced invertase and the water-channel protein γTIP Planta 209 346 354
5. E Baroja-Fernandez FJ Munoz T Saikusa M Rodriguez-Lopez T Akazawa J Pozueta-Romero 2003 Sucrose synthase catalyzes the de novo production of ADPglucose linked to starch biosynthesis in heterotrophic tissues of plants Plant Cell Physiol 44 500 509
6. DC Bassham NV Raikhel 1997 Molecular aspects of vacuole biogenesis Adv Bot Res 25 43 58
7. JD Bendtsen H Nielsen G von Heijne S Brunak 2004 Improved prediction of signal peptides: SignalP 3.0 J Mol Biol 340 783 795
8. AS Bournay PE Hedley A Maddison R Waugh GC Machray 1996 Exon skipping induced by cold stress in a potato invertase gene transcript Nucleic Acids Res 24 2347 2351
9. JE Bowers C Abbey S Anderson C Chang X Draye AH Hoppe R Jessup C Lemke J Lennington Z Li YR Lin SC Liu L Luo BS Marler R Ming SE Mitchell D Qiang K Reischmann SR Schulze DN Skinner YW Wang S Kresovich KF Schertz AH Paterson 2003 A high-density genetic recombination map of sequence-tagged sites for sorghum, as a framework for comparative structural and evolutionary genomics of tropical grains and grasses Genetics 165 367 386
10. S Brink UI Flugge F Chaumont M Boutry M Emmermann U Schmitz K Becker N Pfanner 1994 Preproteins of chloroplast envelope inner membrane contain targeting information for receptor-dependent import into fungal mitochondria J Biol Chem 269 16478 16485
11. C Burge S Karlin 1997 Prediction of complete gene structures in human genomic DNA J Mol Biol 268 78 94
12. BA Chapman JE Bowers SR Schulze AH Paterson 2004 A comparative phylogenetic approach for dating whole genome duplication events Bioinformatics 20 180 185
13. JQ Chen CC Black 1992 Biochemical and immunological properties of alkaline invertase isolated from sprouting soybean hypocotyls Arch Biochem Biophys 295 61 69
14. MH Chen LF Huang HM Li YR Chen SM Yu 2004 Signal peptide-dependent targeting of a rice alpha-amylase and cargo proteins to plastids and extracellular compartments of plant cells Plant Physiol 135 1367 1377
15. HL Chiang R Schekman S Hamamoto 1996 Selective uptake of cytosolic, peroxisomal, and plasma membrane proteins into the yeast lysosome for degradation J Biol Chem 271 9934 9941
16. MG Claros P Vincens 1996 Computational method to predict mitochondrially imported proteins and their targeting sequences Eur J Biochem 241 779 786
17. MJ Curtis TJ Wolpert 2002 The oat mitochondrial permeability transition and its implication in victorin binding and induced cell death Plant J 29 295 312
18. T Darsow CG Burd SD Emr 1998 Acidic di-leucine motif essential for AP-3-dependent sorting and restriction of the functional specificity of the Vam3p vacuolar t-SNARE J Cell Biol 142 913 922
19. B De Coninck K Le Roy I Francis S Clerens R Vergauwen A Halliday SM Smith A Van Laere W Van den Ende 2004 Arabidopsis AtcwINV3 and 6 are not invertases but are fructan exohydrolases (FEHs) with different substrate specificities Plant Cell Environ (in press)
20. J Ehrmann Jr A Kolek R Kod'ousek J Zapletalova S Lisova PG Murray J Drabek Z Kolar 2003 Identification of the gene for beta-fructofuranosidase of Bifidobacterium lactis DSM10140(T) and characterization of the enzyme expressed in Escherichia coli Curr Microbiol 46 391 397
21. O Emanuelsson H Nielsen S Brunak G von Heijne 2000 Predicting subcellular localization of proteins based on their N-terminal amino acid sequence J Mol Biol 300 1005 1016
22. J Farrar 1996 Regulation of shoot-root ratio is mediated by sucrose Plant Soil 185 13 19
23. AL Feiber J Rangarajan JC Vaughn 2002 The evolution of single-copy Drosophila nuclear 4f-rnp genes: spliceosomal intron losses create polymorphic alleles J Mol Evol 55 401 413
24. BS Gaut JF Doebley 1997 DNA sequence evidence for the segmental allotetraploid origin of maize Proc Natl Acad Sci USA 94 6809 6814
25. N Gerrits SCHJ Turk KPM van Dun SHD Hulleman RGF Visser PJ Weisbeek SCM Smeekens 2001 Sucrose metabolism in plastids Plant Physiol 125 926 934
26. SI Gibson 2000 Plant sugar-response pathways Part of a complex regulatory web. Plant Physiol 124 1532 1539
27. DE Godt T Roitsch 1997 Regulation and tissue-specific distribution of mRNAs for three extracellular invertase isoenzymes of tomato suggests an important function in establishing and maintaining sink metabolism Plant Physiol 115 273 282
28. M Goetz T Roitsch 1999 The different pH optima and substrate specificities of extracellular and vacuolar invertases from plants are determined by a single amino-acid substitution Plant J 20 707 711
29. N Haouazine-Takvorian Z Tymowska-Lalanne A Takvorian J Tregear B Lejeune A Lecharny M Kreis 1997 Characterization of two members of the Arabidopsis thaliana gene family, At beta fruct3 and At beta fruct4, coding for vacuolar invertases Gene 197 239 251
30. T Hirose M Takano T Terao 2002 Cell wall invertase in developing rice caryopsis: molecular cloning of OsCIN1 and analysis of its expression in relation to its role in grain filling Plant Cell Physiol 43 452 459
31. D Iraqi FM Tremblay 2001 Analysis of carbohydrate metabolism enzymes and cellular contents of sugars and proteins during spruce somatic embryogenesis suggests a regulatory role of exogenous sucrose in embryo development J Exp Bot 52 2301 2311
32. T Itoh S Akao W Hashimoto B Mikami K Murata 2004 Crystal structure of unsaturated glucuronyl hydrolase, responsible for the degradation of glycosaminoglycan, from Bacillus sp. GL1 at 1.8 A resolution J Biol Chem 279 31804 31812
33. S Kikuchi K Satoh T Nagata N Kawagashira K Doi N Kishimoto J Yazaki M Ishikawa H Yamada H Ooka I Hotta K Kojima T Namiki E Ohneda W Yahagi K Suzuki CJ Li K Ohtsuki T Shishiki Y Otomo K Murakami Y Iida S Sugano T Fujimura Y Suzuki Y Tsunoda T Kurosaki T Kodama H Masuda M Kobayashi Q Xie M Lu R Narikawa A Sugiyama K Mizuno S Yokomizo J Niikura R Ikeda J Ishibiki M Kawamata A Yoshimura J Miura T Kusumegi M Oka R Ryu M Ueda K Matsubara J Kawai P Carninci J Adachi K Aizawa T Arakawa S Fukuda A Hara W Hashizume N Hayatsu K Imotani Y Ishii M Itoh I Kagawa S Kondo H Konno A Miyazaki N Osato Y Ota R Saito D Sasaki K Sato K Shibata A Shinagawa T Shiraki M Yoshino Y Hayashizaki A Yasunishi 2003 Rice Full-Length cDNA Consortium; National Institute of Agrobiological Sciences Rice Full-Length cDNA Project Team; Foundation of Advancement of International Science Genome Sequencing & Analysis Group; RIKEN. Collection, mapping, and annotation of over 28,000 cDNA clones from japonica rice Science 301 376 379
34. J Kim DJ Klionsky 2000 Autophagy, cytoplasm-to-vacuole targeting pathway, and pexophagy in yeast and mammalian cells Annu Rev Biochem 69 303 342
35. DJ Klionsky SD Emr 1990 A new class of lysosomal/vacuolar protein sorting signals J Biol Chem 265 5349 5352
36. HS Lee A Sturm 1996 Purification and characterization of neutral and alkaline invertase from carrot Plant Physiol 112 1513 1522
37. DG Levitt 1980 The mechanism of the sodium pump Biochim Biophys Acta 604 321 345
38. MF Liaud DX Zhang R Cerff 1990 Differential intron loss and endosymbiotic transfer of chloroplast glyceraldehyde-3-phosphate dehydrogenase genes to the nucleus Proc Natl Acad Sci USA 87 8918 8922
39. M Lynch A Kewalramani 2003 Messenger RNA surveillance and the evolutionary proliferation of introns Mol Biol Evol 20 563 571
40. L Margulis D Sagan 2003 Acquiring genomes: the theory of the origins of the species. Basic Books New York
41. W Martin T Rujan E Richly A Hansen S Cornelsen T Lins D Leister B Stoebe M Hasegawa D Penny 2002 Evolutionary analysis of Arabidopsis, cyanobacterial, and chloroplast genomes reveals plastid phylogeny and thousands of cyanobacterial genes in the nucleus Proc Natl Acad Sci USA 99 12246 12251
42. AH Millar LJ Sweetlove P Giegé CJ Leaver 2001 Analysis of the Arabidopsis mitochondrial proteome Plant Physiol 127 1711 1727
43. T Murashige F Skoog 1962 A revised medium for rapid growth and bioassays with tobacco tissue cultures Physiol Plant 15 473 497
44. K Nakai M Kanehisa 1992 A knowledge base for predicting protein localization sites in eukaryotic cells Genomics 14 897 911
45. H Nielsen Jacob Engelbrecht Søren Brunak von Gunnar Heijne 1997 Identification of prokaryotic and eukaryotic signal peptides and prediction of their cleavage sites Prot Eng 10 1 6
46. T Olsson M Thelander H Ronne 2003 A novel type of chloroplast stromal hexokinase is the major phosphorylating enzyme in the moss Physcomitrella patens J Biol Chem 278 44439 44447
47. D Perlman HO Halvorson LE Cannon 1982 Presecretory and cytoplasmic invertase polypeptides encoded by distinct mRNAs derived from the same structural gene differ by a signal sequence Proc Natl Acad Sci USA 79 781 785
48. RMD Page 1996 TREEVIEW: An application to display phylogenetic trees on personal computers Comput Appl Biosci 12 357 358
49. RC Piper NJ Bryant TH Stevens 1997 The membrane protein alkaline phosphatase is delivered to the vacuole by a route that is distinct from the VPS-dependent pathway J Cell Biol 138 531 545
50. T Pons O Olmea G Chinea A Beldarrain G Marquez N Acosta L Rodriguez A Valencia 1998 Structural model for family 32 of glycosyl-hydrolase enzymes Proteins 33 383 395
51. A Reddy F Maley 1996 Studies on identifying the catalytic role of Glu-204 in the active site of yeast invertase J Biol Chem 271 13953 13957
52. F Rook N Gerrits A Kortstee M van Kampen M Borrias P Weisbeek S Smeekens 1998 Sucrose-specific signalling represses translation of the Arabidopsis ATB2 bZIP transcription factor gene Plant J 15 253 263
53. B Rost J Liu 2003 The PredictProtein server Nucleic Acids Res 31 3300 3304
54. SM Sherson HL Alford SM Forbes G Wallace SM Smith 2003 Roles of cell-wall invertases and monosaccharide transporters in the growth and development of Arabidopsis J Exp Bot 54 525 531
55. JCM Smeekens 2000 Sugar-induced signal transduction in plants Ann Rev Plant Physiol Plant Mol Biol 51 49 81
56. A Sturm 1999 Invertases. Primary structures, functions, and roles in plant development and sucrose partitioning Plant Physiol 121 1 8
57. A Sturm MJ Chrispeels 1990 cDNA cloning of carrot extracellular β-fructosidase and its expression in response to wounding and bacterial infection Plant Cell 2 1107 1119
58. DL Swofford 2002 PAUP*. Phylogenetic analysis using parsimony (*and other methods). Version 4 Sinauer Associates Sunderland, MA
59. BW Tague CD Dickinson MJ Chrispeels 1990 A short domain of the plant vacuolar protein phytohemagglutinin targets invertase to the yeast vacuole Plant Cell 2 533 546
60. KA Tucker F Reggiori WA Dunn Jr DJ Klionsky 2003 Atg23 is essential for the cytoplasm to vacuole targeting pathway and efficient autophagy but not pexophagy J Biol Chem 278 48445 48452
61. C Unger M Hardegger S Lienhard A Sturm 1994 cDNA cloning of carrot (Daucus carota) soluble acid beta-fructofuranosidases and comparison with the cell wall isoenzyme Plant Physiol 104 1351 1357
62. W Van den Ende B De Coninck S Clerens R Vergauwen A Van Laere 2003 Unexpected presence of fructan 6-exohydrolases (6-FEHs) in non-fructan 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
63. W Van den Ende A Michiels J De Roover P Verhaert A Van Laere 2000 Cloning and functional analysis of chicory root fructanl-exohydrolase I (1-FEH I): A vacuolar enzyme derived from a cell-wall invertase ancestor? Mass fingerprint of the 1-FEH I enzyme Plant J 24 447 456
64. W Van den Ende A Michiels D Van Wonterghem SP Clerens J De Roover AJ Van Laere 2001 Defoliation induces fructan 1-exohydrolase II in Witloof chicory roots. Cloning and purification of two isoforms, fructan 1-exohydrolase IIa and fructan 1-exohydrolase IIb. Mass fingerprint of the fructan 1-exohydrolase II enzymes Plant Physiol 126 1186 1195
65. W Van den Ende AJ Van Laere 1995 Purification and properties of a neutral invertase from the roots of Cichorium intybus Physiol Plant 93 241 248
66. W Vargas A Cumino GL Salerno 2003 Cyanobacterial alkaline/neutral invertases Origin of sucrose hydrolysis in the plant cytosol? Planta 216 951 960
67. I Vijn S Smeekens 1999 Fructan: More than a reserve carbohydrate? Plant Physiol 120 351 360
68. A Vitale MJ Chrispeels 1992 Sorting of proteins to the vacuoles of plant cells Bioessays 14 151 160
69. JJ Vowels GS Payne 1998 A dileucine-like sorting signal directs transport into an AP-3-dependent, clathrin-independent pathway to the yeast vacuole EMBO J 17 2482 2493
70. M Warchol S Perrin JP Grill F Schneider 2002 Characterization of a purified beta-fructofuranosidase from Bifidobacterium infantis ATCC 15697 Lett Appl Microbiol 35 462 467
71. LE Williams SJ Nelson JL Hall 1992 Solute/proton co-transport in plasma membrane vesicles from Ricinus cotyledons, and a comparison with other tissues Planta 22 541 550
72. J Xu WT Avigne DR McCarty KE Koch 1996 A similar dichotomy of sugar modulation and development expression affects both paths of sucrose metabolism: evidence from maize invertase gene family Plant Cell 8 1209 1220
73. EM Zdobnov R Apweiler 2001 InterProScan-an integration platform for the signature-recognition methods in InterPro Bioinformatics 17 847 848
74. M Zoratti I Szabo 1995 The mitochondrial permeability transition Biochim Biophys Acta 1241 139 176