A diminution in ascorbate oxidase activity affects carbon allocation and improves yield in tomato under water deficit

Plant, Cell and Environment

Volumn 36, Issue 1, 2013, Pages 159-175

  Garchery, Cécile ^a   Gest, Noé ^a   Do, Phuc T ^b   Alhagdow, Moftah ^c,d,g   Baldet, Pierre ^c,d   Menard, Guillaume ^c,d   Rothan, Christophe ^c,d   Massot, Capucine ^e   Gautier, Hélène ^e   Aarrouf, Jawad ^f   Fernie, Alisdair R ^b   Stevens, Rebecca ^a  

^a Researches Center of Avignon   (France)

^b MAX PLANCK INSTITUTE OF MOLECULAR PLANT PHYSIOLOGY   (Germany)

^c Univ Bordeaux   (France)

^d UNIVERSITÉ DE BORDEAUX   (France)

^e Domaine Saint Paul   (France)

^f Institut Méditerranéen de Biodiversité et Ecologie   (France)

^g UNIVERSITY OF TRIPOLI   (Libyan Arab Jamahiriya)

Author keywords

Apoplast; Drought; Growth; Oxidative stress; Redox; RNAi; Solanum lycopersicum; Source sink

Indexed keywords

ASCORBATE OXIDASE; ASCORBIC ACID; HEXOSE; SUCROSE; WATER;

CARBON; DROUGHT STRESS; ENZYME ACTIVITY; GENE EXPRESSION; GROWTH; HERB; PHOTOSYNTHESIS; REDOX POTENTIAL; RESOURCE ALLOCATION; RNA; STOMATAL CONDUCTANCE; WATER SUPPLY; WILD POPULATION;

ARTICLE; BIOMASS; CARBOHYDRATE METABOLISM; ENZYMOLOGY; FRUIT; GENETICS; GROWTH, DEVELOPMENT AND AGING; METABOLISM; METABOLOME; OXIDATION REDUCTION REACTION; PHYSIOLOGY; PLANT LEAF; PLANT STOMA; RNA INTERFERENCE; TOMATO;

ASCORBATE OXIDASE; ASCORBIC ACID; BIOMASS; CARBOHYDRATE METABOLISM; FRUIT; HEXOSES; LYCOPERSICON ESCULENTUM; METABOLOME; OXIDATION-REDUCTION; PLANT LEAVES; PLANT STOMATA; RNA INTERFERENCE; SUCROSE; WATER;

LYCOPERSICON ESCULENTUM;

EID: 84870561427     PISSN: 01407791     EISSN: 13653040     Source Type: Journal    
DOI: 10.1111/j.1365-3040.2012.02564.x     Document Type: Article

References (83)

1. Aarrouf J., Garcin A., Lizzi Y. & El Maataoui M. (2008) Immunolocalization and histocytopathological effects of Xanthomonas arboricola pv pruni on naturally infected leaf and fruit of peach (Prunus persica L Batsch). Journal of Phytopathology 156, 338-345.
2. Adams W.W., 3rd, Watson A.M., Mueh K.E., Amiard V., Turgeon R., Ebbert V., Logan B.A., Combs A.F. & Demmig-Adams B. (2007) Photosynthetic acclimation in the context of structural constraints to carbon export from leaves. Photosynthesis Research 94, 455-466.
3. Alhagdow M., Mounet F., Gilbert L., etal. (2007) Silencing of the mitochondrial ascorbate synthesizing enzyme L-galactono-1, 4-lactone dehydrogenase affects plant and fruit development in tomato. Plant Physiology 145, 1408-1422.
4. Ayre B.G. (2011) Membrane-transport systems for sucrose in relation to whole-plant carbon partitioning. Molecular Plant 4, 377-394.
5. Baldet P., Hernould M., Laporte F., Mounet F., Just D., Mouras A., Chevalier C. & Rothan C. (2006) The expression of cell proliferation-related genes in early developing flowers is affected by a fruit load reduction in tomato plants. Journal of Experimental Botany 57, 961-970.
6. den Boer B.G. & Murray J.A. (2000) Triggering the cell cycle in plants. Trends in Cell Biology 10, 245-250.
7. Bradford M.M. (1976) A rapid and sensitive method for the quantification of microgram quantities of protein utilizing the principle of protein-dye binding. Annals of Biochemistry 72, 248-254.
8. Burhans W.C. & Heintz N.H. (2009) The cell cycle is a redox cycle: linking phase-specific targets to cell fate. Free Radical Biology & Medicine 47, 1282-1293.
9. Carrari F., Baxter C., Usadel B., etal. (2006) Integrated analysis of metabolite and transcript levels reveals the metabolic shifts that underlie tomato fruit development and highlight regulatory aspects of metabolic network behavior. Plant Physiology 142, 1380-1396.
10. Chen Z. & Gallie D.R. (2004) The ascorbic acid redox state controls guard cell signaling and stomatal movement. The Plant Cell 16, 1143-1162.
11. Couee I., Sulmon C., Gouesbet G. & El Amrani A. (2006) Involvement of soluble sugars in reactive oxygen species balance and responses to oxidative stress in plants. Journal of Experimental Botany 57, 449-459.
12. Dahan Y., Rosenfeld R., Zadiranov V. & Irihimovitch V. (2010) A proposed conserved role for an avocado FW2.2-like gene as a negative regulator of fruit cell division. Planta 232, 663-676.
13. De Tullio M.C., Ciraci S., Liso R. & Arrigoni O. (2007) Ascorbic acid oxidase is dynamically regulated by light and oxygen. A tool for oxygen management in plants? Journal of Plant Physiology 164, 39-46.
14. De Tullio M.C., Jiang K. & Feldman L.J. (2010) Redox regulation of root apical meristem organization: connecting root development to its environment. Plant Physiology and Biochemistry 48, 328-336.
15. Do P.T., Prudent M., Sulpice R., Causse M. & Fernie A.R. (2010) The influence of fruit load on the tomato pericarp metabolome in a Solanum chmielewskii introgression line population. Plant Physiology 154, 1128-1142.
16. Dormann P. & Benning C. (1998) The role of UDP-glucose epimerase in carbohydrate metabolism of Arabidopsis. The Plant Journal 13, 641-652.
17. Ehness R., Ecker M., Godt D.E. & Roitsch T. (1997) Glucose and stress independently regulate source and sink metabolism and defense mechanisms via signal transduction pathways involving protein phosphorylation. The Plant Cell 9, 1825-1841.
18. Esaka M., Fujisawa K., Goto M. & Kisu Y. (1992) Regulation of ascorbate oxidase expression in pumpkin by auxin and copper. Plant Physiology 100, 231-237.
19. Fernie A.R., Trethewey R.N., Krotzky A.J. & Willmitzer L. (2004) Metabolite profiling: from diagnostics to systems biology. Nature Reviews in Molecular Cell Biology 5, 763-769.
20. Fotopoulos V., Sanmartin M. & Kanellis A.K. (2006) Effect of ascorbate oxidase over-expression on ascorbate recycling gene expression in response to agents imposing oxidative stress. Journal of Experimental Botany 57, 3933-3943.
21. Fotopoulos V., De Tullio M.C., Barnes J. & Kanellis A.K. (2008) Altered stomatal dynamics in ascorbate oxidase over-expressing tobacco plants suggest a role for dehydroascorbate signalling. Journal of Experimental Botany 59, 729-737.
22. Foyer C.H., Pellny T.K., Locato V. & De Gara L. (2009) Analysis of redox relationships in the plant cell cycle: determinations of ascorbate, glutathione and poly (ADPribose)polymerase (PARP) in plant cell cultures. Methods in Molecular Biology 476, 193-209.
23. Frary A., Nesbitt T.C., Grandillo S., Knaap E., Cong B., Liu J., Meller J., Elber R., Alpert K.B. & Tanksley S.D. (2000) fw2.2: a quantitative trait locus key to the evolution of tomato fruit size. Science 289, 85-88.
24. Frei M., Tanaka J.P., Chen C.P. & Wissuwa M. (2010) Mechanisms of ozone tolerance in rice: characterization of two QTLs affecting leaf bronzing by gene expression profiling and biochemical analyses. Journal of Experimental Botany 61, 1405-1417.
25. Galtier N., Foyer C.H., Huber J., Voelker T.A. & Huber S.C. (1993) Effects of elevated sucrose-phosphate synthase activity on photosynthesis, assimilate partitioning, and growth in tomato (Lycopersicon esculentum var UC82B). Plant Physiology 101, 535-543.
26. Garcia V., Stevens R., Gil L., etal. (2009) An integrative genomics approach for deciphering the complex interactions between ascorbate metabolism and fruit growth and composition in tomato. Comptes Rendus Biologies 332, 1007-1021.
27. Gautier H., Varlet-Grancher C. & Membre J.M. (2001) Plasticity of petioles of white clover (Trifolium repens) to blue light. Physiologia Plantarum 112, 293-300.
28. Geigenberger P., Kolbe A. & Tiessen A. (2005) Redox regulation of carbon storage and partitioning in response to light and sugars. Journal of Experimental Botany 56, 1469-1479.
29. Gest N., Page D., Birtic S., Gouble B., Gilbert L., Garchery C., Causse M. & Stevens R. (2010) Response of the fruit antioxidant system to the post-chilling period in two different tomato lines. Functional Plant Science and Biotechnology 4, 76-83.
30. Gibon Y., Blaesing O.E., Hannemann J., Carillo P., Hohne M., Hendriks J.H., Palacios N., Cross J., Selbig J. & Stitt M. (2004) A Robot-based platform to measure multiple enzyme activities in Arabidopsis using a set of cycling assays: comparison of changes of enzyme activities and transcript levels during diurnal cycles and in prolonged darkness. The Plant Cell 16, 3304-3325.
31. Godt D. & Roitsch T. (2006) The developmental and organ specific expression of sucrose cleaving enzymes in sugar beet suggests a transition between apoplasmic and symplasmic phloem unloading in the tap roots. Plant Physiology and Biochemistry 44, 656-665.
32. Gomez L., Bancel D., Rubio E. & Vercambre G. (2007) The microplate reader: an efficient tool for the separate enzymatic analysis of sugars in plant tissues - validation of a micro-method. Journal of the Science of Food and Agriculture 87, 1893-1905.
33. Guo M., Rupe M.A., Dieter J.A., Zou J., Spielbauer D., Duncan K.E., Howard R.J., Hou Z. & Simmons C.R. (2010) Cell Number Regulator1 affects plant and organ size in maize: implications for crop yield enhancement and heterosis. The Plant Cell 22, 1057-1073.
34. Hamza S. & Chupeau Y. (1993) Re-evaluation of conditions for plant regeneration and agrobacterium-mediated transformation from tomato (Lycopersicon esculentum). Journal of Experimental Botany 44, 1837-1845.
35. Hermans C., Hammond J.P., White P.J. & Verbruggen N. (2006) How do plants respond to nutrient shortage by biomass allocation? Trends in Plant Science 11, 610-617.
36. Hidalgo A., Gonzalez-Reyes J.A. & Navas P. (1989) Ascorbate free radical enhances vacuolization in onion root meristems. Plant, Cell & Environment 12, 455-460.
37. Horemans N., Foyer C.H. & Asard H. (2000) Transport and action of ascorbate at the plant plasma membrane. Trends in Plant Science 5, 263-267.
38. Ioannidi E., Kalamaki M.S., Engineer C., Pateraki I., Alexandrou D., Mellidou I., Giovannonni J. & Kanellis A.K. (2009) Expression profiling of ascorbic acid-related genes during tomato fruit development and ripening and in response to stress conditions. Journal of Experimental Botany 60, 663-678.
39. Ishizaki K., Larson T.R., Schauer N., Fernie A.R., Graham I.A. & Leaver C.J. (2005) The critical role of Arabidopsis electron-transfer flavoprotein:ubiquinone oxidoreductase during dark-induced starvation. The Plant Cell 17, 2587-2600.
40. Karimi M., Inze D. & Depicker A. (2002) GATEWAY vectors for Agrobacterium-mediated plant transformation. Trends in Plant Science 7, 193-195.
41. Kato N. & Esaka M. (2000) Expansion of transgenic tobacco protoplasts expressing pumpkin ascorbate oxidase is more rapid than that of wild-type protoplasts. Planta 210, 1018-1022.
42. Keurentjes J.J., Sulpice R., Gibon Y., Steinhauser M.C., Fu J., Koornneef M., Stitt M. & Vreugdenhil D. (2008) Integrative analyses of genetic variation in enzyme activities of primary carbohydrate metabolism reveal distinct modes of regulation in Arabidopsis thaliana. Genome Biology 9, R129.
43. Klann E.M., Hall B. & Bennett A.B. (1996) Antisense acid invertase (TIV1) gene alters soluble sugar composition and size in transgenic tomato fruit. Plant Physiology 112, 1321-1330.
44. Koch K. (2004) Sucrose metabolism: regulatory mechanisms and pivotal roles in sugar sensing and plant development. Current Opinion in Plant Biology 7, 235-246.
45. Kopka J., Schauer N., Krueger S., etal. (2005) GMD@CSB.DB: the golm metabolome database. Bioinformatics 21, 1635-1638.
46. Lisec J., Schauer N., Kopka J., Willmitzer L. & Fernie A.R. (2006) Gas chromatography mass spectrometry-based metabolite profiling in plants. Nature Protocols 1, 387-396.
47. Livak K.J. & Schmittgen T.D. (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) method. Methods 25, 402-408.
48. Lopes M.S., Araus J.L., van Heerden P.D. & Foyer C.H. (2011) Enhancing drought tolerance in C(4) crops. Journal of Experimental Botany 62, 3135-3153.
49. Lunn J.E. & MacRae E. (2003) New complexities in the synthesis of sucrose. Current Opinion in Plant Biology 6, 208-214.
50. Morison J.I., Baker N.R., Mullineaux P.M. & Davies W.J. (2008) Improving water use in crop production. Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences 363, 639-658.
51. Muller B., Pantin F., Genard M., Turc O., Freixes S., Piques M. & Gibon Y. (2011) Water deficits uncouple growth from photosynthesis, increase C content, and modify the relationships between C and growth in sink organs. Journal of Experimental Botany 62, 1715-1729.
52. Nelson D.E., Repetti P.P., Adams T.R., etal. (2007) Plant nuclear factor Y (NF-Y) B subunits confer drought tolerance and lead to improved corn yields on water-limited acres. Proceedings of the National Academy of Sciences of the United States of America 104, 16450-16455.
53. Nesbitt T.C. & Tanksley S.D. (2001) fw2.2 directly affects the size of developing tomato fruit, with secondary effects on fruit number and photosynthate distribution. Plant Physiology 127, 575-583.
54. Pedreira J., Sanz N., Pena M.J., Sanchez M., Queijeiro E., Revilla G. & Zarra I. (2004) Role of apoplastic ascorbate and hydrogen peroxide in the control of cell growth in pine hypocotyls. Plant & Cell Physiology 45, 530-534.
55. Pignocchi C. & Foyer C.H. (2003) Apoplastic ascorbate metabolism and its role in the regulation of cell signalling. Current Opinion in Plant Biology 6, 379-389.
56. Pignocchi C., Fletcher J.M., Wilkinson J.E., Barnes J.D. & Foyer C.H. (2003) The function of ascorbate oxidase in tobacco. Plant Physiology 132, 1631-1641.
57. Pignocchi C., Kiddle G., Hernandez I., Foster S.J., Asensi A., Taybi T., Barnes J. & Foyer C.H. (2006) Ascorbate oxidase-dependent changes in the redox state of the apoplast modulate gene transcript accumulation leading to modified hormone signaling and orchestration of defense processes in tobacco. Plant Physiology 141, 423-435.
58. Piques M., Schulze W.X., Hohne M., Usadel B., Gibon Y., Rohwer J. & Stitt M. (2009) Ribosome and transcript copy numbers, polysome occupancy and enzyme dynamics in Arabidopsis. Molecular Systems Biology 5, 314.
59. Potters G., de Gara L., Asard H. & Horemans N. (2002) Ascorbate and glutathione: guardians of the cell cycle, partners in crime? Plant Physiology and Biochemistry 40, 537-548.
60. Proels R.K. & 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. Journal of Experimental Botany 60, 1555-1567.
61. Prudent M., Bertin N., Genard M., Munos S., Rolland S., Garcia V., Petit J., Baldet P., Rothan C. & Causse M. (2010) Genotype-dependent response to carbon availability in growing tomato fruit. Plant, Cell & Environment 33, 1186-1204.
62. Reynolds M. & Tuberosa R. (2008) Translational research impacting on crop productivity in drought-prone environments. Current Opinion in Plant Biology 11, 171-179.
63. Roessner U., Luedemann A., Brust D., Fiehn O., Linke T., Willmitzer L. & Fernie A. (2001) Metabolic profiling allows comprehensive phenotyping of genetically or environmentally modified plant systems. The Plant Cell 13, 11-29.
64. Roitsch T. (1999) Source-sink regulation by sugar and stress. Current Opinion in Plant Biology 2, 198-206.
65. Rosa M., Prado C., Podazza G., Interdonato R., Gonzalez J.A., Hilal M. & Prado F.E. (2009) Soluble sugars - metabolism, sensing and abiotic stress: a complex network in the life of plants. Plant Signaling and Behavior 4, 388-393.
66. Sanmartin M., Drogoudi P.A., Lyons T., Pateraki I., Barnes J. & Kanellis A.K. (2003) Over-expression of ascorbate oxidase in the apoplast of transgenic tobacco results in altered ascorbate and glutathione redox states and increased sensitivity to ozone. Planta 216, 918-928.
67. Sanmartin M., Pateraki I., Chatzopoulou F. & Kanellis A.K. (2007) Differential expression of the ascorbate oxidase multigene family during fruit development and in response to stress. Planta 225, 873-885.
68. Schauer N., Steinhauser D., Strelkov S., etal. (2005) GC-MS libraries for the rapid identification of metabolites in complex biological samples. FEBS Letters 579, 1332-1337.
69. Seifert G.J., Barber C., Wells B., Dolan L. & Roberts K. (2002) Galactose biosynthesis in Arabidopsis: genetic evidence for substrate channeling from UDP-D-galactose into cell wall polymers. Current Biology 12, 1840-1845.
70. Sinha A.K., Hofmann M.G., Romer U., Kockenberger W., Elling L. & Roitsch T. (2002) Metabolizable and non-metabolizable sugars activate different signal transduction pathways in tomato. Plant Physiology 128, 1480-1489.
71. Smirnoff N. & Wheeler G.L. (2000) Ascorbic acid in plants: biosynthesis and function. Critical Reviews in Biochemistry and Molecular Biology 35, 291-314.
72. Stevens R., Buret M., Garchery C., Carretero Y. & Causse M. (2006) Technique for rapid, small-scale analysis of vitamin C levels in fruit and application to a tomato mutant collection. Journal of Agricultural and Food Chemistry 54, 6159-6165.
73. Stevens R., Buret M., Duffe P., Garchery C., Baldet P., Rothan C. & Causse M. (2007) Candidate genes and quantitative trait loci affecting fruit ascorbic acid content in three tomato populations. Plant Physiology 143, 1943-1953.
74. Stevens R., Page D., Gouble B., Garchery C., Zamir D. & Causse M. (2008) Tomato fruit ascorbic acid content is linked with monodehydroascorbate reductase activity and tolerance to chilling stress. Plant, Cell & Environment 31, 1086-1096.
75. Turcsanyi E., Lyons T., Plochl M. & Barnes J. (2000) Does ascorbate in the mesophyll cell walls form the first line of defence against ozone? Testing the concept using broad bean (Vicia faba L.). Journal of Experimental Botany 51, 901-910.
76. Veljovic-Jovanovic S.D., Pignocchi C., Noctor G. & Foyer C.H. (2001) Low ascorbic acid in the vtc-1 mutant of Arabidopsis is associated with decreased growth and intracellular redistribution of the antioxidant system. Plant Physiology 127, 426-435.
77. Viola R., Roberts A.G., Haupt S., Gazzani S., Hancock R.D., Marmiroli N., Machray G.C. & Oparka K.J. (2001) Tuberization in potato involves a switch from apoplastic to symplastic phloem unloading. The Plant Cell 13, 385-398.
78. Witt S., Galicia L., Lisec J., Cairns J., Tiessen A., Araus J.L., Palacios-Rojas N. & Fernie A.R. (2012) Metabolic and phenotypic responses of greenhouse-grown maize hybrids to experimentally controlled drought stress. Molecular Plant 5, 401-417.
79. Worrell A.C., Bruneau J.M., Summerfelt K., Boersig M. & Voelker T.A. (1991) Expression of a maize sucrose phosphate synthase in tomato alters leaf carbohydrate partitioning. The Plant Cell 3, 1121-1130.
80. Yamamoto A., Bhuiyan M.N., Waditee R., Tanaka Y., Esaka M., Oba K., Jagendorf A.T. & Takabe T. (2005) Suppressed expression of the apoplastic ascorbate oxidase gene increases salt tolerance in tobacco and Arabidopsis plants. Journal of Experimental Botany 56, 1785-1796.
81. Zhang C.J. & Guo Y. (2012) OsTRXh1 regulates the redox state of the apoplast and influences stress responses in rice. Plant Signaling & Behavior 7, 441-443.
82. Zhang X.Y., Wang X.L., Wang X.F., Xia G.H., Pan Q.H., Fan R.C., Wu F.Q., Yu X.C. & Zhang D.P. (2006) A shift of Phloem unloading from symplasmic to apoplasmic pathway is involved in developmental onset of ripening in grape berry. Plant Physiology 142, 220-232.
83. Zou L., Li H., Ouyang B., Zhang J. & Ye Z. (2006) Cloning and mapping of genes involved in tomato ascorbic acid biosynthesis and metabolism. Plant Science 170, 120-127.