Biomechanical properties of the tomato (Solanum lycopersicum) fruit cuticle during development are modulated by changes in the relative amounts of its components

New Phytologist

Volumn 202, Issue 3, 2014, Pages 790-802

  España, Laura ^a   Heredia Guerrero, José A ^b   Segado, Patricia ^a   Benítez, José J ^b   Heredia, Antonio ^a   Domínguez, Eva ^c  

^a UNIVERSITY OF MÁLAGA   (Spain)

^b INSTITUTO DE CIENCIA DE MATERIALES DE SEVILLA   (Spain)

^c INSTITUTO DE HORTOFRUTICULTURA SUBTROPICAL Y MEDITERRÁNEA LA MAYORA   (Spain)

Author keywords

Attenuated total reflectance Fourier transform infrared (ATR FTIR); Biomechanics; Cuticle; Cutin; Flavonoids; Tomato (Solanum lycopersicum) fruit

Indexed keywords

BIOACCUMULATION; BIOMECHANICS; CULTIVAR; DEVELOPMENTAL BIOLOGY; ESTER; FRUIT; FTIR SPECTROSCOPY; GROWTH; INDEX METHOD; ORGANIC COMPOUND; PHENOL; REFLECTANCE; VISCOELASTICITY;

LYCOPERSICON ESCULENTUM;

CUTIN; MEMBRANE LIPID; PHENOL DERIVATIVE;

BIOMECHANICS; ELASTICITY; ESTERIFICATION; FRUIT; GENETICS; GENOTYPE; GROWTH, DEVELOPMENT AND AGING; INFRARED SPECTROSCOPY; METABOLISM; PHYSIOLOGY; PLANT EPIDERMIS; TOMATO; VISCOSITY;

BIOMECHANICAL PHENOMENA; ELASTICITY; ESTERIFICATION; FRUIT; GENOTYPE; LYCOPERSICON ESCULENTUM; MEMBRANE LIPIDS; PHENOLS; PLANT EPIDERMIS; SPECTROSCOPY, FOURIER TRANSFORM INFRARED; VISCOSITY;

EID: 84898051023     PISSN: 0028646X     EISSN: 14698137     Source Type: Journal    
DOI: 10.1111/nph.12727     Document Type: Article

References (65)

1. Antoine C, Peyron S, Mabille F, Lapierre C, Bouchet B, Abecassis J, Rouau X. 2003. Individual contribution of grain outer layers and their cell wall structure to the mechanical properties of wheat bran. Journal of Agricultural and Food Chemistry 51: 2026-2033.
2. Baker EA, Bukovac MJ, Hunt GM. 1982. Composition of tomato fruit cuticle as related to fruit growth and development. In: Cutler DF, Alvin KL, Price CE, eds. The plant cuticle. London, UK: Academic Press, 33-44.
3. Bargel H, Koch K, Cerman Z, Neinhuis C. 2006. Structure-function relationships of the plant cuticle and cuticular waxes - a smart material? Functional Plant Biology 33: 893-910.
4. Bargel H, Neinhuis C. 2004. Altered tomato (Lycopersicon esculentum Mill.) fruit cuticle biomechanics of a pleiotropic non ripening mutant. Journal of Plant Growth Regulation 23: 61-75.
5. Bargel H, Neinhuis C. 2005. Tomato (Lycopersicon esculentum Mill.) fruit growth and ripening as related to the biomechanical properties of fruit skin and isolated cuticle. Journal of Experimental Botany 56: 1049-1060.
6. Benítez JJ, Matas AJ, Heredia A. 2004. Molecular characterization of the plant biopolyester cutin by AFM and spectroscopic techniques. Journal of Structural Biology 147: 179-184.
7. Bertin N, Lecomte A, Brunel B, Fishman S, Génard M. 2007. A model describing cell polyploidization in tissues of growing fruit as related to cessation of cell proliferation. Journal of Experimental Botany 58: 1903-1913.
8. Bianchi G. 1995. Plant waxes. In: Hamilton RJ, ed. Waxes: chemistry, molecular biology and functions. Dundee, UK: The Oily Press, 175-222.
9. Burgert I, Keplinger T. 2013. Plant micro- and nanomechanics: experimental techniques for plant cell-wall analysis. Journal of Experimental Botany 64: 4635-4649.
10. Cánovas F. 1995. Manejo del cultivo sin suelo. In: Nuez F, ed. El cultivo del tomate. Mundi Prensa: Madrid, Spain, 227-254.
11. Carnachan SM, Harris PJ. 2000. Ferulic acid is bound to the primary cell walls of all gymnosperms families. Biochemical Systematics and Ecology 28: 865-879.
12. Cosgrove DJ. 2005. Growth of the plant cell wall. Nature Reviews Molecular Cell Biology 6: 850-861.
13. Domínguez E, Cuartero J, Heredia A. 2011b. An overview on plant cuticle biomechanics. Plant Science 181: 77-84.
14. Domínguez E, España L, López-Casado G, Cuartero J, Heredia A. 2009. Biomechanics of isolated tomato (Solanum lycopersicum) fruit cuticles during ripening: the role of flavonoids. Functional Plant Biology 36: 613-620.
15. Domínguez E, Fernández MD, López Hernández JC, Pérez-Parra J, España L, Heredia A, Cuartero J. 2012. Tomato fruit continues growing while ripening, affecting cuticle properties and cracking. Physiologia Plantarum 146: 473-486.
16. Domínguez E, Heredia-Guerrero JA, Heredia A. 2011a. The biophysical design of plant cuticles: an overview. New Phytologist 189: 938-949.
17. Domínguez E, López-Casado G, Cuartero J, Heredia A. 2008. Development of fruit cuticle in cherry tomato (Solanum lycopersicum). Functional Plant Biology 35: 403-411.
18. Dorais M, Demers DA, Papadopoulos AP, Ieperen WV. 2004. Greenhouse tomato fruit cuticle cracking. Horticultural Reviews 30: 163-184.
19. Douliez JP, Barrault J, Jerome F, Heredia A, Navailles L, Nallet F. 2005. Glycerol derivatives of cutin and suberin monomers: synthesis and self-assembly. Biomacromolecules 6: 30-34.
20. Dumais J, Shaw SL, Steele CR, Long SR, Ray PM. 2006. An anisotropic-viscoelastic model of plant cell morphogenesis by tip growth. International Journal of Developmental Biology 50: 209-222.
21. Dumais J, Steele CR. 2000. New evidence for the role of mechanical forces in the shoot apical meristem. Journal of Plant Growth Regulation 19: 7-18.
22. El Modafar C, El Boustani E. 2001. Cell wall-bound phenolic acid and lignin contents in date palm as related to its resistance to Fusarium oxysporum. Biologia Plantarum 44: 125-130.
23. Foolad MR. 2007. Genome mapping and molecular breeding of tomato. International Journal of Plant Genomics 2007: 64358.
24. Geitmann A, Ortega JKE. 2009. Mechanics and modelling of plant cell growth. Trends in Plant Science 14: 467-478.
25. Gillaspy G, Ben-David HH, Gruissem W. 1993. Fruits: a developmental perspective. Plant Cell 5: 1439-1451.
26. Girard AL, Mounet F, Lemaire-Chamley M, Gaillard C, Elmorjani K, Vivancos J, Runavot JL, Quemener B, Petit J, Germain V et al. 2012. Tomato GDSL1 is required for cutin deposition in the fruit cuticle. Plant Cell 24: 3119-3134.
27. Grimm E, Peschel S, Becker T, Knoche M. 2012. Stress and strain in the sweet cherry skin. Journal of the American Society for Horticultural Science 137: 383-390.
28. Hartley RD, Harris PJ. 1981. Phenolic constituents of the cell walls of dicotyledons. Biochemical Systematics and Ecology 9: 189-203.
29. Heredia A. 2003. Biophysical and biochemical characteristics of cutin, a plant barrier biopolymer. Biochimica et Biophysica Acta 1620: 1-7.
30. Ho LC, Hewitt JD. 1986. Fruit development. In: Atherton JG, Rudich J, eds. The tomato crop. London, UK, New York, NY, USA: Chapman & Hall, 201-240.
31. Holloway PJ. 1982. The chemical constitution of plant cutins. In: Cutler DF, Alvin KL, Price CE, eds. The plant cuticle. London, UK: Academic Press, 45-85.
32. Hunt GM, Baker EA. 1980. Phenolic constituents of tomato fruit cuticles. Phytochemistry 19: 1415-1419.
33. Javelle M, Vernoud V, Rogowsky PM, Ingram GC. 2011. Epidermis; the formation and functions of a fundamental plant tissue. New Phytologist 189: 17-39.
34. Jensen WA. 1962. Botanical histochemistry. San Francisco, CA, USA: WH Freeman & Co.
35. Khanal BP, Grimm E, Finger S, Blume A, Knoche M. 2013. Intracuticular waxes fixes and restricts strain in leaf and fruit cuticles. New Phytologist 200: 134-143.
36. Knoche M, Beyer M, Peschel S, Oparlakov B, Bukovac MJ. 2004. Changes in strain and deposition of cuticle in developing sweet cherry fruit. Physiologia Plantarum 120: 667-677.
37. Kutschera U, Bergfeld R, Schopfer P. 1987. Cooperation of epidermis and inner tissues in auxin-mediated growth of maize coleoptiles. Planta 170: 168-180.
38. 3-phenylalanine precursor. Physiologia Plantarum 105: 491-498.
39. López-Casado G, Matas AJ, Domínguez E, Cuartero J, Heredia A. 2007. Biomechanics of isolated tomato (Solanum lycopersicum L.) fruit cuticles: the role of cutin matrix. Journal of Experimental Botany 58: 3875-3883.
40. Lunn D, Phan TD, Tucker GA, Lycett GW. 2013. Cell wall composition of tomato fruit changes during development and inhibition of vesicle trafficking is associated with reduced pectin levels and reduced softening. Plant Physiology and Biochemistry 66: 91-97.
41. Luque P, Bruque S, Heredia A. 1995. Water permeability of isolated cuticular membranes: a structural analysis. Archives of Biochemistry and Biophysics 317: 417-422.
42. Luque P, Heredia A. 1994. Glassy state in plant cuticles during growth. Zeitschrift für Naturforschung 49c: 273-275.
43. Matas AJ, Cobb ED, Bartsch JA, Paolillo DJ, Niklas KJ. 2004. Biomechanics and anatomy of Lycopersion esculentum fruit peels and enzyme treated samples. American Journal of Botany 91: 352-360.
44. Matas AJ, Lopez-Casado G, Cuartero J, Heredia A. 2005. Relative humidity and temperature modify the mechanical properties of isolated tomato fruit cuticles. American Journal of Botany 92: 462-468.
45. Mazurek S, Mucciolo A, Humbel BM, Nawrath C. 2013. Transmission Fourier transform infrared microspectroscopy allows simultaneous assessment of cutin and cell-wall polysaccharides of Arabidopsis petals. The Plant Journal 74: 880-891.
46. Mirabet V, Das P, Boudaoud A, Hamant O. 2011. The role of mechanical forces in plant morphogenesis. Annual Review of Plant Biology 62: 365-385.
47. Niklas KJ. 1992. Plant biomechanics: an engineering approach to plant form and function. Chicago, IL, USA: The University of Chicago Press.
48. Peschel S, Franke R, Schreiber L, Knoche M. 2007. Composition of the cuticle of developing sweet cherry fruit. Phytochemistry 68: 1017-1025.
49. Petracek PD, Bukovac MJ. 1995. Rheological properties of enzymatically isolated tomato fruit cuticle. Plant Physiology 109: 675-679.
50. Peyron S, Abecassis J, Autran JC, Rouau X. 2001. Enzymatic oxidative treatments of wheat bran layers: effects of structural heterogenity. Journal of Agricultural and Food Chemistry 49: 4694-4699.
51. Pfündel EE, Agati G, Cerovic ZG. 2006. Optical properties of plant surfaces. In: Riederer M, Müller C, eds. Biology of the plant cuticle. Oxford, UK: Blackwell Publishing, 216-249.
52. Ramírez FJ, Luque P, Heredia A, Bukovac MJ. 1992. Fourier transform IR study of enzimatically isolated tomato fruit cuticular membrane. Biopolymers 32: 1425-1429.
53. Reina JJ, Domínguez E, Heredia A. 2001. Water sorption-desorption in conifer cuticles: the role of lignin. Physiologia Plantarum 112: 372-378.
54. Riederer M. 2006. Introduction: biology of the plant cuticle. In: Riederer M, Müller C, eds. Biology of the plant cuticle. Oxford, UK: Blackwell Publishing, 1-10.
55. Savaldi-Goldstein S, Peto C, Chory J. 2007. The epidermis both drives and restricts plant shoot growth. Nature 446: 199-202.
56. Schönherr J, Bukovac MJ. 1973. Ion exchange properties of isolated tomato fruit cuticular membrane: exchange capacity, nature of fixed charges and cation selectivity. Planta 109: 73-93.
57. Schopfer P. 2006. Biomechanics of plant growth. American Journal of Botany 93: 1415-1425.
58. Schreiber L, Schonherr J. 1990. Phase transitions and thermal expansion coefficients of plant cuticles. Planta 182: 186-193.
59. Seymour GB, Østergaard L, Chapman NH, Knapp S, Martin C. 2013. Fruit development and ripening. Annual Review of Plant Biology 64: 219-241.
60. Skene DS. 1980. Growth stresses during fruit development in cox's orange pippin apples. Journal of Horticultural Science & Biotechnology 55: 27-32.
61. SPSS. 2008. SPSS for Windows, Release 17.0. Chicago, IL, USA: SPSS.
62. Takahashi Y, Tsubaki S, Sakamoto M, Watanabe S, Azuma J. 2012. Growth-dependent chemical and mechanical properties of cuticular membranes from leaves of Sonneratia alba. Plant Cell & Environment 35: 1201-1210.
63. Tsubaki S, Ozaki Y, Yonemori K, Azuma JI. 2012. Mechanical properties of fruit-cuticular membranes isolated from 27 cultivars of Diospyros kaki Thunb. Food Chemistry 132: 2135-2139.
64. Tsubaki S, Sugimura K, Teramoto Y, Yonemori K, Azuma J. 2013. Cuticular membrane of Fuyu persimmon fruit is strengthened by triterpenoid nano-fillers. PLoS One 8: e75275.
65. Villena JF, Domínguez E, Heredia A. 2000. Monitoring biopolymers present in plant cuticles by FT-IR spectroscopy. Journal of Plant Physiology 156: 419-422.