A tomato vacuolar invertase inhibitor mediates sucrose metabolism and influences fruit ripening

Plant Physiology

Volumn 172, Issue 3, 2016, Pages 1596-1611

  Qin, Guozheng ^a   Zhu, Zhu ^a   Wang, Weihao ^a,b   Cai, Jianghua ^a,b   Chen, Yong ^a,b   Li, Li ^c   Tian, Shiping ^a,b  

^a INSTITUTE OF BOTANY   (China)

^b UNIVERSITY OF CHINESE ACADEMY OF SCIENCES   (China)

^c ROBERT W HOLLEY CENTER FOR AGRICULTURE AND HEALTH   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

PLANT PROTEIN; PROTEIN BINDING; SUCROSE;

CHROMATIN IMMUNOPRECIPITATION; FRUIT; GEL MOBILITY SHIFT ASSAY; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; METABOLISM; NUCLEOTIDE SEQUENCE; PLANT GENE; PROMOTER REGION; PROTEOMICS; REAL TIME POLYMERASE CHAIN REACTION; TOMATO;

BASE SEQUENCE; CHROMATIN IMMUNOPRECIPITATION; ELECTROPHORETIC MOBILITY SHIFT ASSAY; FRUIT; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION, PLANT; GENES, PLANT; LYCOPERSICON ESCULENTUM; PLANT PROTEINS; PROMOTER REGIONS, GENETIC; PROTEIN BINDING; PROTEOMICS; REAL-TIME POLYMERASE CHAIN REACTION; SUCROSE;

EID: 84994574768     PISSN: 00320889     EISSN: 15322548     Source Type: Journal    
DOI: 10.1104/pp.16.01269     Document Type: Article

References (70)

1. Alba R, Payton P, Fei Z, McQuinn R, Debbie P, Martin GB, Tanksley SD, Giovannoni JJ (2005) Transcriptome and selected metabolite analyses reveal multiple points of ethylene control during tomato fruit development. Plant Cell 17: 2954-2965
2. Bate NJ, Niu X, Wang Y, Reimann KS, Helentjaris TG (2004) An invertase inhibitor from maize localizes to the embryo surrounding region during early kernel development. Plant Physiol 134: 246-254
3. Borsani J, Budde CO, Porrini L, Lauxmann MA, Lombardo VA, Murray R, Andreo CS, Drincovich MF, Lara MV (2009) Carbon metabolism of peach fruit after harvest: changes in enzymes involved in organic acid and sugar level modifications. J Exp Bot 60: 1823-1837
4. Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72: 248-254
5. Brummell DA, Chen RK, Harris JC, Zhang H, Hamiaux C, Kralicek AV, McKenzie MJ (2011) Induction of vacuolar invertase inhibitor mRNA in potato tubers contributes to cold-induced sweetening resistance and includes spliced hybrid mRNA variants. J Exp Bot 62: 3519-3534
6. Carrari F, Fernie AR (2006) Metabolic regulation underlying tomato fruit development. J Exp Bot 57: 1883-1897
7. Choi ST, Huber DJ (2008) Influence of aqueous 1-methylcyclopropene concentration, immersion duration, and solution longevity on the postharvest ripening of breaker-turning tomato (Solanum lycopersicum L.) fruit. Postharvest Biol Technol 49: 147-154
8. Claeyssen E, Rivoal J (2007) Isozymes of plant hexokinase: occurrence, properties and functions. Phytochemistry 68: 709-731
9. Davies C, Robinson SP (1996) Sugar accumulation in grape berries. Cloning of two putative vacuolar invertase cDNAs and their expression in grapevine tissues. Plant Physiol 111: 275-283
10. Ecker JR (2013) Epigenetic trigger for tomato ripening. Nat Biotechnol 31: 119-120
11. Elias JE, Gygi SP (2007) Target-decoy search strategy for increased confidence in large-scale protein identifications by mass spectrometry. Nat Methods 4: 207-214
12. Elliott KJ, Butler WO, Dickinson CD, Konno Y, Vedvick TS, Fitzmaurice L, Mirkov TE (1993) Isolation and characterization of fruit vacuolar invertase genes from two tomato species and temporal differences in mRNA levels during fruit ripening. Plant Mol Biol 21: 515-524
13. Eveland AL, Jackson DP (2012) Sugars, signalling, and plant development. J Exp Bot 63: 3367-3377
14. Fraser PD, Truesdale MR, Bird CR, Schuch W, Bramley PM (1994) Carotenoid biosynthesis during tomato fruit development (evidence for tissue-specific gene expression). Plant Physiol 105: 405-413
15. Fillatti JJ, Kiser J, Rose R, Comai L (1987) Efficient transfer of a glyphosate tolerance gene into tomato using a binary Agrobacterium tumefaciens vector. Nat Biotechnol 5: 726-730
16. 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
17. Fridman E, Zamir D (2003) Functional divergence of a syntenic invertase gene family in tomato, potato, and Arabidopsis. Plant Physiol 131: 603-609
18. Fujisawa M, Nakano T, Shima Y, Ito Y (2013) A large-scale identification of direct targets of the tomato MADS box transcription factor RIPENING INHIBITOR reveals the regulation of fruit ripening. Plant Cell 25: 371-386
19. Gan CS, Chong PK, Pham TK, Wright PC (2007) Technical, experimental, and biological variations in isobaric tags for relative and absolute quantitation (iTRAQ). J Proteome Res 6: 821-827
20. German MA, Asher I, Petreikov M, Dai N, Schaffer AA, Granot D (2004) Cloning, expression and characterization of LeFRK3, the fourth tomato (Lycopersicon esculentum Mill.) gene encoding fructokinase. Plant Sci 166: 285-291
21. German MA, Dai N, Chmelnitsky I, Sobolev I, Salts Y, Barg R, Schaffer AA, Granot D (2002) LeFRK4, a novel tomato (Lycopersicon esculentum Mill.) fructokinase specifically expressed in stamens. Plant Sci 163: 607-613
22. Giovannoni JJ (2004) Genetic regulation of fruit development and ripening. Plant Cell (Suppl) 16: S170-S180
23. Giovannoni JJ (2007) Fruit ripening mutants yield insights into ripening control. Curr Opin Plant Biol 10: 283-289
24. Godt DE, Roitsch T (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
25. Goren S, Huber SC, Granot D (2011) Comparison of a novel tomato sucrose synthase, SlSUS4, with previously described SlSUS isoforms reveals distinct sequence features and differential expression patterns in association with stem maturation. Planta 233: 1011-1023
26. 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
27. Greiner S, Rausch T, Sonnewald U, Herbers K (1999) Ectopic expression of a tobacco invertase inhibitor homolog prevents cold-induced sweetening of potato tubers. Nat Biotechnol 17: 708-711
28. Hothorn M, Wolf S, Aloy P, Greiner S, Scheffzek K (2004) Structural insights into the target specificity of plant invertase and pectin methylesterase inhibitory proteins. Plant Cell 16: 3437-3447
29. Huber SC, Huber JL (1996) Role and regulation of sucrose-phosphate synthase in higher plants. Annu Rev Plant Physiol Plant Mol Biol 47: 431-444
30. Iglesias DJ, Tadeo FR, Legaz F, Primo-Millo E, Talon M (2001) In vivo sucrose stimulation of colour change in citrus fruit epicarps: interactions between nutritional and hormonal signals. Physiol Plant 112: 244-250
31. Ito Y, Kitagawa M, Ihashi N, Yabe K, Kimbara J, Yasuda J, Ito H, Inakuma T, Hiroi S, Kasumi T (2008) DNA-binding specificity, transcriptional activation potential, and the rin mutation effect for the tomato fruit-ripening regulator RIN. Plant J 55: 212-223
32. Jin Y, Ni DA, Ruan YL (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
33. Kanayama Y, Dai N, Granot D, Petreikov M, Schaffer A, Bennett AB (1997) Divergent fructokinase genes are differentially expressed in tomato. Plant Physiol 113: 1379-1384
34. Kandel-Kfir M, Damari-Weissler H, German MA, Gidoni D, Mett A, Belausov E, Petreikov M, Adir N, Granot D (2006) Two newly identified membrane-associated and plastidic tomato HXKs: characteristics, predicted structure and intracellular localization. Planta 224: 1341-1352
35. Karimi M, Inzé D, Depicker A (2002) GATEWAY vectors for Agrobacterium-mediated plant transformation. Trends Plant Sci 7: 193-195
36. Klann EM, Chetelat RT, Bennett AB (1993) Expression of acid invertase gene controls sugar composition in tomato (Lycopersicon) fruit. Plant Physiol 103: 863-870
37. Klann EM, Hall B, Bennett AB (1996) Antisense acid invertase (TIV1) gene alters soluble sugar composition and size in transgenic tomato fruit. Plant Physiol 112: 1321-1330
38. Klann E, Yelle S, Bennett AB (1992) Tomato fruit acid invertase complementary DNA: nucleotide and deduced amino acid sequences. Plant Physiol 99: 351-353
39. Klee HJ, Giovannoni JJ (2011) Genetics and control of tomato fruit ripening and quality attributes. Annu Rev Genet 45: 41-59
40. Kocal N, Sonnewald U, Sonnewald S (2008) Cell wall-bound invertase limits sucrose export and is involved in symptom development and inhibition of photosynthesis during compatible interaction between tomato and Xanthomonas campestris pv vesicatoria. Plant Physiol 148: 1523-1536
41. Koch K (2004) Sucrose metabolism: regulatory mechanisms and pivotal roles in sugar sensing and plant development. Curr Opin Plant Biol 7: 235-246
42. Li Z, Palmer WM, Martin AP, Wang R, Rainsford F, Jin Y, Patrick JW, Yang Y, Ruan YL (2012) High invertase activity in tomato reproductive organs correlates with enhanced sucrose import into, and heat tolerance of, young fruit. J Exp Bot 63: 1155-1166
43. Link M, Rausch T, Greiner S (2004) In Arabidopsis thaliana, the invertase inhibitors AtC/VIF1 and 2 exhibit distinct target enzyme specificities and expression profiles. FEBS Lett 573: 105-109
44. Long JC, Zhao W, Rashotte AM, Muday GK, Huber SC (2002) Gravitystimulated changes in auxin and invertase gene expression in maize pulvinal cells. Plant Physiol 128: 591-602
45. Lunn JE, MacRae E (2003) New complexities in the synthesis of sucrose. Curr Opin Plant Biol 6: 208-214
46. Martel C, Vrebalov J, Tafelmeyer P, Giovannoni JJ (2011) The tomato MADS-box transcription factor RIPENING INHIBITOR interacts with promoters involved in numerous ripening processes in a COLORLESS NONRIPENING-dependent manner. Plant Physiol 157: 1568-1579
47. Mason G, Provero P, Vaira AM, Accotto GP (2002) Estimating the number of integrations in transformed plants by quantitative real-time PCR. BMC Biotechnol 2: 20
48. Menu T, Rothan C, Dai N, Petreikov M, Etienne C, Destrac-Irvine A, Schaffer A, Granot D, Ricard B (2001) Cloning and characterization of a cDNA encoding hexokinase from tomato. Plant Sci 160: 209-218
49. Miron D, Schaffer AA (1991) Sucrose phosphate synthase, sucrose synthase, and invertase activities in developing fruit of Lycopersicon esculentum Mill. and the sucrose accumulating Lycopersicon hirsutum Humb. and Bonpl. Plant Physiol 95: 623-627
50. Moore S, Payton P, Wright M, Tanksley S, Giovannoni J (2005) Utilization of tomato microarrays for comparative gene expression analysis in the Solanaceae. J Exp Bot 56: 2885-2895
51. Murashige T, Skoog F (1962) A revised medium for rapid growth and bio assays with tobacco tissue cultures. Physiol Plant 15: 473-497
52. Proels RK, Roitsch T (2009) Extracellular invertase LIN6 of tomato: a pivotal enzyme for integration of metabolic, hormonal, and stress signals is regulated by a diurnal rhythm. J Exp Bot 60: 1555-1567
53. Qin G, Wang Y, Cao B, Wang W, Tian S (2012) Unraveling the regulatory network of the MADS box transcription factor RIN in fruit ripening. Plant J 70: 243-255
54. Rausch T, Greiner S (2004) Plant protein inhibitors of invertases. Biochim Biophys Acta 1696: 253-261
55. Rolland F, Moore B, Sheen J (2002) Sugar sensing and signaling in plants. Plant Cell (Suppl) 14: S185-S205
56. Ruan YL, Jin Y, Yang YJ, Li GJ, 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
57. Saravanan RS, Rose JKC (2004) A critical evaluation of sample extraction techniques for enhanced proteomic analysis of recalcitrant plant tissues. Proteomics 4: 2522-2532
58. Schmittgen TD, Livak KJ (2008) Analyzing real-time PCR data by the comparative C(T) method. Nat Protoc 3: 1101-1108
59. Sturm A (1999) Invertases. Primary structures, functions, and roles in plant development and sucrose partitioning. Plant Physiol 121: 1-8
60. Sumner JB (1921) Dinitrosalicylic acid: a reagent for the estimation of sugar in normal and diabetic urine. J Biol Chem 47: 5-9
61. Télef N, Stammitti-Bert L, Mortain-Bertrand A, Maucourt M, Carde JP, Rolin D, Gallusci P (2006) Sucrose deficiency delays lycopene accumulation in tomato fruit pericarp discs. Plant Mol Biol 62: 453-469
62. Vaughn MW, Harrington GN, Bush DR (2002) Sucrose-mediated transcriptional regulation of sucrose symporter activity in the phloem. Proc Natl Acad Sci USA 99: 10876-10880
63. Vrebalov J, Ruezinsky D, Padmanabhan V, White R, Medrano D, Drake R, Schuch W, Giovannoni J (2002) A MADS-box gene necessary for fruit ripening at the tomato ripening-inhibitor (rin) locus. Science 296: 343-346
64. Wang F, Smith AG, Brenner ML (1993) Isolation and sequencing of tomato fruit sucrose synthase cDNA. Plant Physiol 103: 1463-1464
65. Wang Y, Wang W, Cai J, Zhang Y, Qin G, Tian S (2014) Tomato nuclear proteome reveals the involvement of specific E2 ubiquitin-conjugating enzymes in fruit ripening. Genome Biol 15: 548
66. Wi_sniewski JR, Zougman A, Nagaraj N, Mann M (2009) Universal sample preparation method for proteome analysis. Nat Methods 6: 359-362
67. Yu X, Wang X, Zhang W, Qian T, Tang G, Guo Y, Zheng C (2008) Antisense suppression of an acid invertase gene (MAI1) in muskmelon alters plant growth and fruit development. J Exp Bot 59: 2969-2977
68. Zhong S, Fei Z, Chen YR, Zheng Y, Huang M, Vrebalov J, McQuinn R, Gapper N, Liu B, Xiang J, et al (2013) Single-base resolution methylomes of tomato fruit development reveal epigenome modifications associated with ripening. Nat Biotechnol 31: 154-159
69. Zhu Z, Liu R, Li B, Tian S (2013) Characterisation of genes encoding key enzymes involved in sugar metabolism of apple fruit in controlled atmosphere storage. Food Chem 141: 3323-3328
70. Zhu Z, Zhang ZQ, Qin GZ, Tian SP (2010) Effects of brassinosteroids on postharvest disease and senescence of jujube fruit in storage. Postharvest Biol Technol 56: 50-55