Fruit softening and pectin disassembly: An overview of nanostructural pectin modifications assessed by atomic force microscopy

Annals of Botany

Volumn 114, Issue 6, 2014, Pages 1375-1383

  Paniagua, Candelas ^a   Posé, Sara ^a   Morris, Victor J ^b   Kirby, Andrew R ^b   Quesada, Miguel A ^a   Mercado, José A ^a  

^a UNIVERSITY OF MÁLAGA   (Spain)

^b NORWICH RESEARCH PARK   (United Kingdom)

Author keywords

AFM; Atomic force microscopy; fruit ripening; fruit softening; homogalacturonan; nanostructure; pectins; plant cell wall; postharvest physiology; rhamnogalacturonan

Indexed keywords

ATOMIC FORCE MICROSCOPY; BIOCHEMICAL COMPOSITION; CELL ORGANELLE; FRUIT; FUNCTIONAL ROLE; GENE EXPRESSION; HARVESTING; PARTICLE SIZE; PHYSIOLOGY; PHYTOCHEMISTRY; POLYSACCHARIDE; RIPENING;

NANOMATERIAL; PECTIN; POLYGALACTURONASE; POLYGALACTURONIC ACID; POLYSACCHARIDE; VEGETABLE PROTEIN;

ATOMIC FORCE MICROSCOPY; CELL WALL; DOWN REGULATION; FRUIT; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; PHYSIOLOGY; PLANT; PROCEDURES; TRANSGENIC PLANT; ULTRASTRUCTURE;

CELL WALL; DOWN-REGULATION; FRUIT; GENE EXPRESSION REGULATION, ENZYMOLOGIC; GENE EXPRESSION REGULATION, PLANT; MICROSCOPY, ATOMIC FORCE; NANOSTRUCTURES; PECTINS; PLANT PROTEINS; PLANTS; PLANTS, GENETICALLY MODIFIED; POLYGALACTURONASE; POLYSACCHARIDES;

EID: 84910658005     PISSN: 03057364     EISSN: 10958290     Source Type: Journal    
DOI: 10.1093/aob/mcu149     Document Type: Review

References (90)

1. Almeida DPF, Huber DJ. 1999. Apoplastic pH and inorganic ion levels in tomato fruit: a potential means for regulation of cell wall metabolism during ripening. Physiologia Plantarum 105: 506-512.
2. Atkinson RG, Sutherland PW, Johnston SL, et al. 2012. Down-regulation of POLYGALACTURONASE1 alters firmness, tensile strength and water loss in apple (Malus × domestica) fruit. BMC Plant Biology 12: 129-142.
3. Bapat VA, Trivedi PK, Ghosh A, Sane VA, Ganapathi TR, Nath P. 2010. Ripening of fleshy fruit: molecular insight and the role of ethylene. Biotechnology Advances 28: 94-107.
4. Bourne MC. 1979. Texture of temperate fruits. Journal of Texture Studies 10: 25-44.
5. Brett C, Waldron K. 1996. Physiology and biochemistry of plant cell walls. Chapman & Hall.
6. Brummell DA. 2006. Cell wall disassembly in ripening fruit. Functional Plant Biology 33: 103-119.
7. Brummell DA, Harpster MH. 2001. Cell wall metabolisminfruit softening and quality and its manipulation in transgenic plants. Plant Molecular Biology 47: 311-340.
8. Brummell DA, Labavitch JM. 1997. Effectofantisense suppressionofendopo-lygalacturonase activity on polyuronide molecular weight in ripening tomato fruit and in fruit homogenates. Plant Physiology 115: 717-725.
9. Brummell DA, Harpster MH, Civello PM, Palys JM, Bennett AB, Dunsmuir P. 1999. Modification of expansin protein abundance in tomato fruit alters softening and cell wall polymer metabolism during ripening. Plant Cell 11: 2203-2216.
10. Brummell DA, Del Cin V, Crisosto CH, Labavitch JM. 2004. Cell wall metabolism during maturation, ripening and senescence of peach fruit. Journal of Experimental Botany 55: 2029-2039.
11. Carpita N, Gibeaut DM. 1993. Structuralmodelsofprimary cell walls inflower-ing plants: consistencyofmolecular structure with the physical properties of the walls during growth. Plant Journal 3: 1-30.
12. Carpita N, McCann M. 2000. Thecell wall. In: Buchanan B, Gruissem W, Jones R. eds. Biochemistry and molecular biology of plants. Rockville, IL: American Society of Plant Physiologists, 52-108.
13. Chen F, Liu H, Yang H, et al. 2011. Qualityattributes and cell wall properties of strawberries (Fragaria ananassa Duch.) under calcium chloride treatment. Food Chemistry 126: 450-459.
14. Chen Y, Chen F, Lai S, et al. 2013. In vitro studyof the interaction between pec-tinase and chelate-soluble pectin in postharvest apricot fruits. European Food Research and Technology 237: 987-993.
15. Figueroa CR, Rosli HG, Civello PM, Martínez GA, Herrera R, Moya-León MA. 2010. Changes in cell wall polysaccharides and cell wall degrading enzymes during ripening of Fragaria chiloensis and Fragaria × ananassa fruits. Scientia Horticulturae 124: 454-462.
16. Fishman ML, Cooke PH, Chau HK, Coffin DR, Hotchkiss AT. 2007. Global structures of high methoxyl pectin from solution and in gels. Bio-macromolecules 8: 573-578.
17. Gapper NE, McQuinn RP, Giovannoni JJ. 2013. Molecular and genetic regulation of fruit ripening. Plant Molecular Biology 82: 575-591.
18. García-Gago JA, López-Aranda JM, Muñoz-Blanco J, et al. 2009. Postharvest behaviour of transgenic strawberry with polygalacturonase or pectate lyase genes silenced. Acta Horticulturae 842: 573-576.
19. Giovannoni JJ, Della Penna D, Bennett AB, Fischer RL. 1989. Expressionofa chimeric polygalacturonase gene in transgenic rin (ripening inhibitor) tomato fruit results in polyuronide degradation but not fruit softening. Plant Cell 1: 53-63.
20. Goulao LF, Oliveira CM. 2008. Cell wall modification during fruit ripening: whenafruit isnot the fruit. Trendsin Food Science &Technology 19:4-25.
21. Goulao LF, Santos J, de Sousa I, Oliveira CM. 2007. Patterns of enzymatic ac-tivityofcell wall-modifying enzymes during growth and ripeningofapples. Postharvest Biology and Technology 43: 307-318.
22. Gross KC, Sams CE. 1984. Changes in cell wall neutral sugar composition during fruit ripening: a species survey. Phytochemistry 23: 2457-2461.
23. Hadfield KA, Bennett AB. 1998. Polygalacturonases: many genes in search ofa function. Plant Physiology 117: 337-343.
24. Harker FR, Redgwell RJ, Hallet IC, Murray SH. 1997. Texture of fresh fruit. Horticultural Reviews 20: 121-224.
25. Hiwasa K, Nakano R, Hashimoto A, et al. 2004. European, Chinese and Japanese pear fruits exhibit differential softening characteristics during ripening. Journal of Experimental Botany 55: 2281-2290.
26. Huber DJ. 1984. Strawberry fruit softening-the potential roles of polyuronides and hemicelluloses. Journal of Food Science 49: 1310-1315.
27. Huber DJ, O'Donoghue EM. 1993. Polyuronides in avocado (Persea americana) and tomato (Lycopersicon esculentum) fruits exhibit markedly different patterns of molecular weight downshifts during ripening. Plant Physiology 102: 473-480.
28. Jiménez-Bermúdez S, Redondo-Nevado J, Muñoz-Blanco J, et al. 2002. Manipulation of strawberry fruit softening by antisense expression of a pectate lyase gene. Plant Physiology 128: 751-759.
29. Kirby AR, Gunning AP, Morris VJ, Ridout MJ. 1995a. Atomic force micros-copyinfoodresearch:anewtechnique comesofage. Trendsin Food Science & Technology 6: 359-365.
30. Kirby AR, Gunning AP, Morris VJ, Ridout MJ. 1995b. Observation of the helical structure of the bacterial polysaccharide acetan by atomic force microscopy. Biophysical Journal 68: 360-363.
31. Kirby AR, Mac Dougall AJ, Morris VJ. 2008. Atomic force microscopy of tomato and sugar beet pectin molecules. Carbohydrate Polymers 71: 640-647.
32. Kramer M, Sanders R, Bolkan H, Waters C, Sheehy RE, Hiatt WR. 1992. Postharvest evaluation of transgenic tomatoes with reduced levels of poly-galacturonase: processing, firmness and disease resistance. Postharvest Biology and Technology 1: 241-255.
33. Lai S, Chen F, Zhang L, Yang H, Deng Y, Yang B. 2013. Nanostructural difference of water-soluble pectin and chelate-soluble pectin among ripening stages and cultivars of Chinese cherry. Natural Product Research 27: 379-385.
34. Lara I, Belge B, Goulao LF. 2014. The fruitcuticleasamodulatorofpostharvest quality. Postharvest Biology and Technology 87: 103-112.
35. Liu D, Cheng F. 2011. Advances in research on structural characterisation of agricultural products using atomic force microscopy. Journal of the Science of Food and Agriculture 91: 783-788.
36. Liu H, Chen F, Yang H, et al. 2009. Effectofcalciumtreatmentonnanostructure of chelate-soluble pectin and physicochemical and textural properties of apricot fruits. Food Research International 42: 1131-1140.
37. Mc Intire TM, Brant DA. 1997. Imaging of individual biopolymers and supramolecular assemblies using noncontact atomic force microscopy. Biopolymers 42: 133-146.
38. Mc Intire TM, Brant DA. 1999. Imaging of carrageenan macrocycles and amylose using noncontact atomic force microscopy. International Journal of Biological Macromolecules 26: 303-310.
39. Mc Master TJ, Miles MJ, Kasarda DD, Shewry PR, Tatham AS. 1999. Atomic force microscopy of A-gliadin fibrils and in situ degradation. Journal of Cereal Science 31: 281-286.
40. Mc Neil M, Darvill AG, Albersheim P. 1980. Structure of plant cell walls. X. Rhamnogalacturonan I, a structurally complex pectic polysaccharide in the walls of suspension-cultured sycamore cells. Plant Physiology 66: 1128-1134.
41. Mercado JA, Pliego-Alfaro F, Quesada MA. 2011. Fruit shelf life and potential for its genetic improvement. In: Jenks MA, Bebeli PJ. eds. Breedingfor fruit quality. Oxford: John Wiley & Sons, 81-104.
42. Miedes E, Lorences EP. 2009. Xyloglucan endotransglucosylase/hydrolases (XTHs) during tomato fruit growth and ripening. Journal of Plant Physiology 166: 489-498.
43. Miedes E, Herbers K, Sonnewald U, Lorences. 2010. Overexpression of a cell wall enzyme reduces xyloglucan depolymerization and softening of transgen-ic tomato fruits. Journal of Agricultural Food Chemistry 58: 5708-2713.
44. Molina-Hidalgo FJ, Franco AR, Villatoro C, et al. 2013. The strawberry (Fragaria × ananassa) fruit-specific rhamnogalacturonate lyase 1 (Fa RGLyase1) gene encodesanenzyme involved inthe degradationof cell-wall middle lamellae. Journal of Experimental Botany 64: 1471-1483.
45. Morris VJ, Gunning AP, Kirby AR, Round A, Waldron K. 1997. Atomicforce microscopy of plant cell wall, plant cell wall polysaccharides and gels. International Journal of Biological Macromolecules 21: 61-66.
46. Morris VJ, Mackie AR, Wilde PJ, Kirby AR, Mills EC, Gunning AP. 2001. Atomic force microscopyas atool for interpreting the rheologyof food bio-polymers at the molecular level. Food Science and Technology 34: 3-10.
47. Morris VJ, Kirby AR, Gunning AP. 2010. Atomic force microscopy for biologists. London: Imperial College Press.
48. Morris VJ, Gromer A, Kirby AR, Bongaerts RJM, Gunning AP. 2011. Using AFM and force spectroscopy to determine pectin structure and (bio) functionality. Food Hydrocolloids 25: 230-237.
49. Orfila C, Huisman MMH, Willats WGT, et al. 2002. Altered cell wall disassembly during ripening of Cnr tomato fruit: implications for cell adhesion and fruit softening. Planta 215: 440-447.
50. Osorio S, Castillejo C, Quesada MA, et al. 2008. Partial demethylation of oli-gogalacturonidesbypectin methylesterase1isrequired forelicitingdefence responses in wild strawberry (Fragaria vesca). Plant Journal 54: 43-55.
51. Popper ZA, Fry SC. 2005. Widespreadoccurrenceofacovalentlinkagebetween xyloglucan and acidic polysaccharides in suspension-cultured angiosperm cells. Annals of Botany 96: 91-99.
52. Posé S, Kirby AR, Mercado JA, Morris VJ, Quesada MA. 2012. Structural characterization of cell wall pectin fractions in ripe strawberry fruits using AFM. Carbohydrate Polymers 88: 882-890.
53. Posé S, Paniagua C, Cifuentes M, Blanco-Portales R, Quesada MA, Mercado JA. 2013. Insights into the effects of polygalacturonase Fa PG1 gene silen-cingonpectin matrix disassembly, enhancedtissueintegrity, andfirmnessin ripe strawberry fruits. Journal of Experimental Botany 64: 3803-3815.
54. Prasanna V, Prabha TN, Tharanathan RN. 2007. Fruit ripening phenomena-an overview. Critical Reviews in Food Science and Nutrition 47: 1-19.
55. Quesada MA, Blanco-Portales R, Posé S, et al. 2009. Antisensedown-regulation of the Fa PG1 gene reveals an unexpected central role for polygalacturonase in strawberry fruit softening. Plant Physiology 150: 1022-1032.
56. Redgwell RJ, Melton LD, Brasch DJ. 1992. Cell wall dissolution in ripening kiwifruit (Actinidia deliciosa): solubilisation of the pectic polymers. Plant Physiology 98: 71-81.
57. Redgwell RJ, Macrae E, Hallett I, Fischer M, Perry J, Harker R. 1997a. In vivo and in vitro swelling of cell walls during fruit ripening. Planta 203: 162-173.
58. Redgwell RJ, Fischer M, Kendall E, Mac Rae EA, Perry J, Harker R. 1997b. Galactose loss and fruit ripening: high-molecular-weight arabinogalactans in the pectic polysaccharides of fruit cell walls. Planta 203: 174-181.
59. Rose JKC, Hadfield KA, Labavitch JM, Bennett AB. 1998. Temporal sequence of cell wall disassembly in rapidly ripening melon fruit. Plant Physiology 117: 345-361.
60. Round AN, Mac Dougall AJ, Ring SG, Morris VJ. 1997. Unexpected branch-ingin pectin observed byatomic force microscopy. Carbohydrate Research 303: 251-253.
61. Round AN, Rigby NM, Mac Dougall AJ, Ring SG, Morris VJ. 2001. Investigating the nature of branching in pectin by atomic force microscopy and carbohydrate analysis. Carbohydrate Research 331: 337-342.
62. Round AN, Rigby NM, Mac Dougall AJ, Morris VJ. 2010. A new view of pectin structure revealed by acid hydrolysis and atomic force microscopy. Carbohydrate Research 345: 487-497.
63. Saladié M, Matas AJ, Isaacson T, et al. 2007. A reevaluation of the key factors that influence tomato fruit softening and integrity. Plant Physiology 144: 1012-1028.
64. Santiago-Doménech N, Jiménez-Bermúdez S, Matas AJ, et al. 2008. Antisense inhibitionofapectatelyasegene supportsaroleforpectindepoly-merizationinstrawberryfruitsoftening. Journalof Experimental Botany 59: 2769-2779.
65. Smith CJS, Watson CF, Morris PC, et al. 1990. Inheritanceand effecton ripening of antisense polygalacturonase genes in transgenic tomatoes. Plant Molecular Biology 14: 369-379.
66. Smith DL, Abbott JA, Gross KC. 2002. Down-regulation oftomatob-galactosidase 4 results in decreased fruit softening. Plant Physiology 129: 1755-1762.
67. Thibault J-F, Renard CMGC, Axelos MAV, Roger P, Crépeau M-J. 1993. Studies of the length of homogalacturonic regions in pectins by acid hydrolysis. Carbohydrate Research 238: 271-286.
68. Thomas TR, Shackel KA, Matthews MA. 2008. Mesocarp cell turgor in Vitis vinifera L. berries throughout development and its relation to firmness, growth, and the onset of ripening. Planta 228: 1067-1076.
69. Tieman DM, Handa AK. 1994. Reduction in pectin methylesterase activity modifies tissue integrity and cation levels in ripening tomato (Lycopersicon esculentum Mill.) fruits. Plant Physiology 106: 429-436.
70. Toivonen PM, Brummell DA. 2008. Biochemical bases of appearance and texture changes in fresh-cut fruit and vegetables. Postharvest Biology and Technology 48: 1-14.
71. Vicente AR, Ortugno C, Powell ALT, Greve LC, Labavitch JM. 2007. Temporal sequence of cell wall disassembly events in developing fruits. 1. Analysis of raspberry (Rubus idaeus). Journal of Agricultural and Food Chemistry 55: 4119-4124.
72. Vincken JP, Schols HA, Oomen RJFJ, et al. 2003. Ifhomogalacturonan were a side chain of rhamnogalacturonan I. Implications for cell wall architecture. Plant Physiology 132: 1781-1789.
73. Voragen A, Coenen G, Verhoef R, Schols H. 2009. Pectin, a versatile polysac-charide present in plant cell walls. Structural Chemistry 20: 263-275.
74. Wada H, Matthews MA, Shackel KA. 2009. Seasonal pattern of apoplastic solute accumulation and loss of cell turgor during ripening of Vitis vinifera fruit under field conditions. Journal of Experimental Botany 60: 1773-1781.
75. Wakabayashi K. 2000. Changes in cell wall polysaccharides during fruit ripening. Journal of Plant Research 113: 231-237.
76. Wakabayashi K, Chun J-P, Huber DJ. 2000. Extensive solubilization and depolymerization of cell wall polysaccharides during avocado (Persea americana) ripening involves concerted action of polygalacturonase and pectinmethylesterase. Physiologia Plantarum 108: 345-352.
77. Walkinshaw MD, Arnott S. 1981. Conformations and interactions of pectins. I. X-ray diffraction analyses of sodium pectate in neutral and acidified forms. Journal of Molecular Biology 153: 1055-1073.
78. Wang H, Chen F, Yang H, Chen Y, Zhang L, An H. 2012. Effects of ripening stageand cultivaronphysicochemical propertiesandpectinnanostructureof jujubes. Carbohydrate Polymers 89: 1180-1188.
79. Willats WG, McCartney L, Mackie W, Knox JP. 2001. Pectin: cell biologyand prospects for functional analysis. Plant Molecular Biology 47: 9-27.
80. Xin Y, Chen F, Yang H, Zhang P, Deng Y, Yang B. 2010. Morphology, profile and role of chelate-soluble pectin on tomato properties during ripening. Food Chemistry 121: 372-380.
81. Yang H, An H, Feng G, Li Y, Lai S. 2005. Atomic forcemicroscopyofthewater-soluble pectin of peaches during storage. European Food Research and Technology 220: 587-591.
82. Yang H, Lai S, An H, Li Y. 2006a. Atomic force microscopy study of the ultra-structural changes of chelate-soluble pectin in peaches under controlled atmosphere storage. Postharvest Biology and Technology 39: 75-83.
83. Yang H-S, Feng G-P, An H-J, Li Y-F. 2006b. Microstructure changesofsodium carbonate-soluble pectin of peach by AFM during controlled atmosphere storage. Food Chemistry 94: 179-192.
84. Yang H, Chen F, An H, Lai S. 2009. Comparative studies on nanostructures of three kindsof pectins in two peach cultivars using atomic force microscopy. Postharvest Biology and Technology 51: 391-398.
85. Yapo BM, Lerouge P, Thibault J-F, Ralet M-C. 2007. Pectins from citrus peel cell walls contain homogalacturonans homogeneous with respect to molar mass, rhamnogalacturonan I and rhamnogalacturonan II. Carbohydrate Polymers 69: 426-435.
86. Zareie MH, Gokmen V, Javadipour I. 2003. Investigating network, branching, gelation and enzymatic degradation in pectin by atomic force microscopy. Journal of Food Science and Technology 40: 169-172.
87. Zhang L, Chen F, An H, et al. 2008. Physicochemical properties, firmness, and nanostructures of sodium carbonate-soluble pectin of 2 Chinese cherry cul-tivars at 2 ripening stages. Journal of Food Science 73: N17-N22.
88. Zhang L, Chen F, Yang H, et al. 2010. Changes in firmness, pectin content and nanostructure of two crisp peach cultivars after storage. Food Science and Technology 43: 26-32.
89. Zhang L, Chen F, Yang H, et al. 2012. Effects of temperature and cultivar on nanostructural changes of water-soluble and chelate-soluble pectin in peaches. Carbohydrate Polymers 87: 816-821.
90. Zykwinska AW, Ralet MCJ, Garnier CD, Thibault JFJ. 2005. Evidence for in vitro binding of pectin side chainsto cellulose. Plant Physiology 139: 397-407.