Down-regulation of an Auxin Response Factor in the tomato induces modification of fine pectin structure and tissue architecture

Journal of Experimental Botany

Volumn 59, Issue 2, 2008, Pages 273-288

  Guillon, Fabienne ^a   Philippe, Sully ^a   Bouchet, Brigitte ^a   Devaux, Marie Françoise ^a   Frasse, Pierre ^b   Jones, Brian ^b   Bouzayen, Mondher ^b   Lahaye, Marc ^a  

^a INRA   (France)

^b Ecole Nationale Superieure d'Architecture de Toulouse   (France)

Author keywords

Auxin; Cell wall; Firmness; Fruit; Pectin; Pericarp; Tomato

Indexed keywords

LYCOPERSICON ESCULENTUM;

CARBOHYDRATE; OXALIC ACID; PECTIN; PLANT EXTRACT; VEGETABLE PROTEIN;

ARTICLE; CELL WALL; CHEMISTRY; DOWN REGULATION; FRUIT; GENETICS; IMMUNOCHEMISTRY; ISOLATION AND PURIFICATION; METABOLISM; TOMATO; ULTRASTRUCTURE;

CARBOHYDRATES; CELL WALL; DOWN-REGULATION; FRUIT; IMMUNOCHEMISTRY; LYCOPERSICON ESCULENTUM; OXALIC ACID; PECTINS; PLANT EXTRACTS; PLANT PROTEINS;

EID: 41649121706     PISSN: 00220957     EISSN: 14602431     Source Type: Journal    
DOI: 10.1093/jxb/erm323     Document Type: Article

References (80)

1. Allende A, Desmet M, Vanstreels E, Verlinden BE, Nicolai BM. 2004. Micromechanical and geometrical properties of tomato skin related to differences in puncture injury susceptibility. Postharvest Biology and Technology 34, 131-141.
2. Bonnin E, Dolo E, Le Goff A, Thibault J-F. 2002. Characterisation of pectin subunits released by an optimised combinaison of enzymes. Carbohydrate Research 33, 1687-1696.
3. Brown JA, Fry SC. 1993. The preparation and susceptibility to hydrolysis of novel O-galacturonoyl derivatives of carbohydrates. Carbohydrate Research 240, 95-106.
4. Brownleader MD, Jackson P, Mobasheri A, Pantelides AT, Sumar S, Trevan M, Dey PM. 1999. Molecular aspects of cell wall modifications during ripening. Critical Review of Food Science and Nutrition 39, 149-164.
5. Brummell DA. 2006. Cell wall disassembly in ripening fruit. Functional Plant Biology 33, 103-119.
6. Brummell DA, Harpster MH. 2001. Cell wall metabolism in fruit softening and quality and its manipulation in transgenic plants. Plant Molecular Biology 47, 311-340.
7. Bush MS, McCann MC. 1999. Pectic epitopes are differentially distributed in the cell walls of potato (Solanum tuberosum) tubers. Physiologia Plantarum 107, 201-213.
8. Chaib J, Devaux MC, Grotte MG, Robini K, Causse M, Lahaye M, Marty I. 2007. Genetic and physiological relationships among physical, sensory, and morphological attributes of texture in tomato fruits. Journal of Experimental Botany 58, (in press).
9. Cheniclet C, Rong WY, Causse M, Frangne N, Bolling L, Carde JP, Renaudin JP. 2005. Cell expansion and endoreduplication show a large genetic variability in pericarp and contribute strongly to tomato fruit growing type. Plant Physiology 139, 1984-1994.
10. Clausen MH, Willats WGT, Knox JP. 2003. Synthetic methyl hexagalacturonate hapten inhibitors of anti homogalacturonan monoclonal antibodies LM7, JIM5 and JIM7. Carbohydrate Research 338, 1797-1800.
11. Devaux M-F, Barakat A, Robert P, Bouchet B, Guillon F, Navez B, Lahaye M. 2005. Mechanical breakdown and cell wall structure of mealy tomato pericarp tissue. PostHarvest 35, 209-221.
12. Devaux MF, Bouchet B, Legland D, Guillon F, Lahaye M. 2007. Macro-vision and grey level granulometry for quantification of tomato pericarp structure. Postharvest Biology and Technology 47, 199-209.
13. Dubois M, Gilles KA, Hmilton JK, Rebers PA, Smith F. 1956. Colorimetric method for determination of sugars and related substances. Analytical Chemistry 28, 350.
14. Filzmoser P, Baumgartner R, Moose E. 1999. A hierachical clustering method for analyzing functional MR image. Magnetic Resonance Imaging 17, 817-826.
15. Fry SC. 1988. The growing plant cell wall: chemical and metabolic analysis. New York: Longman and Scientific and Technical.
16. Gilsenan PM, Richardson RK, Morris ER. 2000. Thermally reversible acid induced gelation of low methoxy pectin. Carbohydrate Polymers 41, 339-349.
17. Guilfoyle T, Hagen G, Ulmasov T, Murfet J. 1998. How does auxin turn on genes? Plant Physiology 118, 341-347.
18. Guillemin F, Devaux M-F, Guillon F. 2004. Evaluation of plant histology by automatic clustering based on individual cell morphological features. Image Analysis and Stereology 23, 13-22.
19. Hejnowicz Z, Sievers A. 1995. Tissue stresses in organs of herbaceous plants. I. Poisson ratios of tissues and their role in determination of the stresses. Journal of Experimental Botany 46, 1045-1053.
20. Hoebler C, Barry J-L, David A, Delort-Laval J. 1989. Rapid acid hydrolysis of plant cell wall polysaccharides and simplified quantitative determination of their neutral monosaccharides by gas-liquid chromatography. Journal of Agricultural and Food Chemistry 37, 360-365.
21. Huber DJ, O'Donoghue EM. 1993. Polyuronides in avocado (Persea americana) and tomato (Lycopersicon esculentum) fruits exhibits markedly different patterns of molecular weight down-shifts during ripening. Plant Physiology 102, 473-480.
22. Huysamer M, Greve LC, Labavitch JM. 1997. Cell wall composition and synthetic capacity of two regions of the outer pericarp of matue green and red ripe cv. Jacpot tomatoes. Physiologia Plantarum 101, 314-322.
23. Hwang J, Kokini JL. 1992. Contribution of the side branches to rheological properties of pectins. Carbohydrate Polymers 19, 41-50.
24. Iwai H, Ishii T, Satoh S. 2001. Absence of arabinan in the side chains of the pectic polysaccharides strongly associated with cell walls of Nicotiana plumbaginifolia non-organic callus with loosely attached constituent cell. Planta 231, 907-915.
25. Jarvis MC, Briggs SPH, Knox JP. 2003. Intercellular adhesion and cell separation in plants. Plant, Cell and Environment 26, 977-989.
26. Jackman RL, Stanley DW. 1995. Perspectives in the textural evaluation of plant food. Trends in Food science and Technology 6, 187-194.
27. Jones B, Frasse P, Olmos E, Zegzouti H, Guo Li Z, Latché A, Pech J-C, Bouzayen M. 2002. Down regulation of AS-DR12, an auxin-response-factor homolog, in the tomato results in a pleiotropic phenotype including dark green and blotchy ripening fruit. The Plant Journal 32, 603-613.
28. Jones L, Seymour GB, Knox JP. 1997. Localization of pectic galactan tomato cell walls using a monoclonal antibody specific to (1-4)-β-D-galactan. Plant Physiology 113, 1405-1412.
29. Knee M. 2002. Fruit quality and its biological basis. Shieffield: Academic Press.
30. Knox JP, Linstead PJ, King J, Cooper C, Roberts K. 1989. Pectin esterification is spatially regulated both within cell walls and between developing tissues of root apices. Planta 181, 512-521.
31. Koch JL, Nevins DJ. 1989. Tomato fruit cell wall, I. Use of purified tomato polygalacturonase and pectinmethylesterase to identify developmental hanges in pectins. Plant Physiology 91, 816-822.
32. Konstankiewicz K, Zdunek A. 2001. Influence of turgor and cell size on the cracking of potato tissue. International Agrophysics 15, 27-30.
33. Le Goff A, Renard CMGC, Bonnin E, Thibault J-F. 2001. Extraction, purification and chemical characterisation of xylogalacturonans from pea hulls. Carbohydrate Polymers 45, 325-334.
34. Lebart L, Morineau A, Pirin M. 1995. Statistique exploratoire multidimensionnelle. Paris: Dunod, 145-205.
35. Leboeuf E, Guillon F, Thoiron S, Lahaye M. 2005. Biochemical and immunohistochemical analysis of pectic polysaccharides in the cell walls of Arabidopsis mutant QUASIMODO 1 suspensioncultured cells: implications for cell adhesion. Journal of Experimental Botany 56, 3171-3182.
36. Lelievre J-M, Latché A, Jones B, Bouzayen M, Pech J-C. 1997. Ethylene and fruit ripening. Physiologa Plantarum 101, 727-739.
37. Lévigne S, Thomas M, Ralet M-C, Quemener B, Thibault J-F. 2002. Determination of the degrees of methylation and acetylation of pectins using C18 column internal standard. Food Hydrocolloid 16, 547-550.
38. Lin TT, Pitt RE. 1986. Rheology of apple and potato and tissue as affected by cell turgor pressure. Journal of Textural Studies 17, 291-313.
39. Liners F, Letesson JJ, Didembourg C, Van Cutsem P. 1989. Monoclonal antibodies against pectin. Recognition of a conformation induced by calcium. Plant Physiology 94, 1419-1424.
40. Liners F, Thibault J-F, Van Cutsem P. 1992. Influence of the degree of polymerization of oligogalacturonates and of esterification pattern of pectin on their recognition by monoclonal antibodies. Plant Physiology 99, 1099-1104.
41. Matas AJ, Cobb ED, Bartsch JA, Paolillo DJ, Niklas KJ. 2004. Biomechanics and anatomy of Lycopersicon esculentum fruit peels and enzyme-treated samples. American Journal of Botany 91, 352-360.
42. McCartney L, Ormerod AP, Gidley MJ, Knox JP. 2000. Temporal and spatial regulation of pectic (1 → 4)-β-D-galactan in cell walls of developing pea cotyledons: implications for mechanical properties. The Plant Journal 22, 105-113.
43. McCartney L, Knox JP. 2002. Regulation of pectic polysaccharide domains in relation to cell development and cell properties in the pea testa. Journal of Experimental Botany 53, 707-713.
44. Nara K, Kato Y, Motomura Y. 2001. Involvement of terminal arabinose and-galactose pectic compounds in mealiness of apple fruit during storage. Postharvest Biology and Technology 22, 141-150.
45. Oechslin R, Lutz MV, Amado R. 2003. Pectic subtances isolated from apple celulosic residue: structural characterization of a new type of rhamnogalacturonan I. Carbohydrate Polymers 51, 301-310.
46. Oomen RJFJ, Doeswijk-Voragen CHL, Bush MS, et al. 2002. In muro fragmentation of the rhamnogalacturonan I backbone in potato (Solanum tuberosum L.) results in a reduction and altered location of the galactan and arabinan side-chain and abnormal epiderm development. The Plant Journal 30, 403-413.
47. Orfila C, Huisman MMH, Willats WG, van Alebeek G-JWM, Schols HA, Seymour GB, Knox JP. 2002. Altered cell wall disassembly during ripening Cnr tomato fruit: implications for cell adhesion and fruit softening. Planta 30, 440-447.
48. Orfila C, Knox P. 2000. Spatial regulation of pectic polysaccharides in relation to pit field in cell walls of tomato fruit pericarp. Plant Physiology 122, 775-781.
49. Orfila C, Seymour GB, Willats WG, Huxham IM, Jarvis MC, Dover CJ, Thompson AJ, Knox JP. 2001. Altered middle lamella homogalacturonan and disrupted deposition of (1 → 5) α-L-arabinan in the pericarp Cnr, a ripening mutant of tomato. Plant Physiology 126, 210-221.
50. Pena MJ, Carpita NC. 2004. Loss of highly branched arabinans and debranching of rhamnogalacturonan I accompagny loss of firm texture and cell separation during prolonged storage of apple. Plant Physiology 135, 1305-1313.
51. Popper Z, Fry S. 2005. Widespread occurrence of a covalent linkage between xyloglucan and acidicpolysaccharides in suspension-cultured angiosperm cells. Annals of Botany 96, 91-99.
52. Qi X, Behrens BX, West PR, Mort AJ. 1995. Solubilization and partial characterization of extensin fragments from cell walls of cotton suspension cultures. Plant Physiology 108, 1691-1701.
53. Quéméner B, Cabrera Pino JC, Ralet M-C, Bonnin B, Thibault J-F. 2003. Assignment of acetyl groups to O-2 and/or O-3 of pectic oligogalacturonides using negative Electrospray-Ion Trap Mass Spectrometry. Journal of Mass Spectrometry 38, 641-658.
54. Redgwell RJ, Fischer M. 2002. Fruit texture, cell wall metabolism and consumer perceptions. In: Knee M, ed. Fruit quality and its biological basis. Sheffield: Sheffield Academic Press, 46-88.
55. Redgwell J, MacRae EA, Hallet I, Fischer M, Perry J, Harker R. 1997. In vivo and in vitro swelling of cell walls during fruit ripening. Planta 203, 162-173.
56. Rondeau-Mouro C, Crépeau M-J, Lahaye M. 2003. Application of CP-MAS liquid-like solid state NMR experiments for the study of the ripening-associated cell wall changes in tomato. International Journal of Biological Macromolecules 31, 235-244.
57. Rose JKC, Bennet AB. 1999. Cooperative disassembly of the cellulose-xyloglucan network of plant cell walls: parallels between cell expansion and frit ripening. Trends in Plant Science 4, 176-183.
58. Selvendran RR. 1985. Developments in the chemistry and biochemistry of pectic and hemicellulosic polymers. Journal of Cell Science Supplement 2, 51-88.
59. Seymour GB, Colquhoun IJ, Dupont MS, Parsley KR, Selvendran RR. 1990. Composition and structural features of cell-wall polysaccharides from tomato fruits. Phytochemistry 29, 725-731.
60. Seymour GB, Gross KC. 1996. Cell wall disassembly and fruit softening. PostHarvest News and Information 7, 45N-52N.
61. Seymour GB, Manning K, Erikson E, Popovich A, King G. 2002. Genetic indentification and genomic organization of factors affecting fruit texture. Journal of Experimental Botany 53, 2065-2071.
62. Shackel KA, Greve C, Labavitch JM, Ahmadi H. 1991. Cell turgor changes associated with ripening in tomato pericarp tissue. Plant Physiology 97, 814-816.
63. Smith DL, Abbott JA, Gross KC. 2002. Down-regulation of tomato β galactosidase 4 results in decreased fruit softening. Plant Physiology 129, 1755-1762.
64. Soille P. 2003. Morphological image analysis. Principles and applications. Berlin: Springer-Verlag.
65. Sorensen SO, Pauly M, Bush M, Skjot M, McCann MC, Borkhardt B, Ulvskov P. 2000. Pectin engineering: modification of potato pectin by in vivo expression of an endo-1,4-β-D-galactanase. Proceedings of the National Academy of Sciences, USA 97, 7639-7644.
66. Thibault J-F. 1979. Automatisation du dosage des substances pectiques par la méthode au métahydroxydiphényle. Lebensmittel-Wissenschaft und Technologie 12, 247-251.
67. Tibbits CW, MacDougall AJ, Ring SG. 1998. Calcium binding and swelling behaviour of a high methoxyl pectin gel. Carbohydrate Research 310, 101-107.
68. Ulmasov T, Hagen G, Guilfoyle T. 1999. Activation and repression of transcription by auxin response factors. Proceedings of the National Academy of Sciences, USA 96, 5844-5849.
69. Ulvskov P, Wium H, Bruce D, Jørgensen B, Bruun Qvist K, Skjøt Hepworth D, Borkhardt B, Oxenbøll Sørensen S. 2005. Biophysical consequences of remodeling the neutral side chains of rhamnogalacturonan I in tubers of transgenic potatoes. Planta 220, 609-620.
70. Vincken JP, Schols HA, Oomen RJFJ, Beldman G, Visser RGF, Voragen AGJ. 2003. Pectin: the hairy thing. In: Voragen AGJ, Schols HA, Visser R, eds. Advances in pectin and pectinase research. Dordrecht: Kluwer Academic Publishers, 47-59.
71. Wakabayashi K, Hoson T, Huber D. 2003. Methyl de-esterification as a major factor regulating the extent of pectin depolymerization during fruit rieping: a comparison of the actions of avocado (Persea americana) and tomato (Lycopersicon esculentum) polygalacturonases. Journal of Plant Physiology 160, 667-673.
72. Waldron KW. 2004. Plant structure and fruit and vegetable texture. In: Kilcast D, ed. Texture in foods. Boca Raton: Woodhead Publishing, Cambridge, 242-258.
73. Willats WG, McCartney L, Mackie W, Knox JP. 2001a. Pectin: cell biology and prospects for functional analysis. Plant Molecular Biology 47, 9-27.
74. Willats WG, Steele-King CG, Marcus SE, Knox JP. 1999. Side chains of pectic polysaccharides are regulated in relation to cell proliferation and cell differentiation. The Plant Journal 20, 619-628.
75. Willats WG, Steele-King CG, McCartney L, Orfila C, Marcus SE, Knox JP. 2000. Making and using antibody probes to study plant cell walls. Plant Physiology and Biochemistry 38, 27-36.
76. Willats WGT, Marcus SE, Knox JP. 1998. Generation of monoclonal antibody specific to (1-5)-α-L-arabinan. Carbohydrate Research 308, 149-152.
77. Willats WGT, Orfila C, Limberg G, et al. 2001b. Modulation of the degree and pattern of methyl-esterification of pectic homogalacturonan in plant cell walls. Implications for pectin methyl esterase action, matrix properties, and cell adhesion. Journal of Biological Chemistry 276, 19404-19413.
78. Zegzouti H, Jones B, Frasse P, Marty C, Maitre B, Latché A, Pech J-C, Bouzayen M. 1999. Ethylene-regulated gene expression in tomato fruit: characterization of novel ethylene-responsive and ripening related genes isolated by differential display. The Plant Journal 18, 589-600.
79. Zykwinska AW, Ralet M-C, Garnier CD, Thibault JF. 2005. Evidence for in vitro binding of pectic side chains to cellulose. Plant Physiology 139, 397-407.
80. Zykwinska AW, Rondeau-Mouro C, Garnier CD, Thibault JF, Ralet M-C. 2006. Alkaline extractability of pectic arabinan and galactan and their mobility in sugar beet and potato cell walls. Carbohydrate Polymers 65, 510-520.