Biomechanics of isolated tomato (Solanum lycopersicum) fruit cuticles during ripening: the role of flavonoids
Eva Domínguez A D , Laura España B D , Gloria López-Casado B C , Jesús Cuartero A and Antonio Heredia B EA Estación Experimental ‘La Mayora’ (CSIC) Algarrobo-Costa, E-29760 Málaga, Spain.
B Departamento de Biología Molecular y Bioquímica, Universidad de Málaga, E-29071 Málaga, Spain.
C Present address: Department of Plant Biology, Cornell University, Ithaca, NY 14853, USA.
D These authors contributed equally to this work.
E Corresponding author. Email: heredia@uma.es
Functional Plant Biology 36(7) 613-620 https://doi.org/10.1071/FP09039
Submitted: 17 February 2009 Accepted: 11 May 2009 Published: 2 July 2009
Abstract
Flavonoids accumulate in tomato (Solanum lycopersicum L.) fruit cuticles during ripening. Their quantitative contribution to the biomechanical properties of the cuticle is studied in six tomato genotypes which show presence or absence of these compounds at the red ripe stage of fruit development. Tomato cuticles with flavonoids at red ripe showed a dramatic increase of these compounds between mature green and red ripe stages together with a significant increase in the elastic modulus. On the other hand, cuticles without flavonoids displayed a similar biomechanical behaviour at mature green and red ripe stages. The absence of flavonoids could also be related with a predominance of the viscoelastic performance of the cuticle. Thus, the increase of phenolics in tomato fruit cuticles during ripening is correlated with a more rigid cutin network that reinforces the mechanical function of polysaccharides which tend to diminish at this stage due to cell wall disassembly. A role of phenolics as biomechanical modulators of the cuticle behaviour is proposed.
Additional keywords: biomechanical stiffness, biomechanics, cuticle, cutin, flavonoids, phenolics, Solanum lycopersicum, tomato fruit ripening.
Acknowledgements
The authors thank Ana Rico and Toñi Núñez for technical assistance. This work has been partially supported by grant AGL2006–12494 from Plan Nacional de I+D, Ministerio de Educación y Ciencia, Spain, Fundación Cajamar and Rijk Zwaan Iberica (Almería, Spain).
Bargel H, Neinhuis C
(2004) Altered tomato (Lycopersicon esculentum Mill.) fruit cuticle. Biomechanics of a pleiotropic on ripening mutant. Journal of Plant Growth Regulation 23, 61–75.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
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.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
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.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
Domínguez E,
López-Casado G,
Cuartero J, Heredia A
(2008) Development of fruit cuticle in cherry tomato (Solanum lycopersicum). Functional Plant Biology 35(5), 403–411.
| Crossref | GoogleScholarGoogle Scholar |
Edelmann HG,
Neinhuis C, Bargel H
(2005) Influence of hydration and temperature on the rheological properties of plant cuticles and their impact on plant organ integrity. Journal of Plant Growth Regulation 24, 116–126.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
Heredia A
(2003) Biophysical and biochemical characteristics of cutin, a plant barrier biopolymer. Biochimica et Biophysica Acta 1620, 1–7.
|
CAS |
PubMed |
Hunt GM, Baker EA
(1980) Phenolic constituents of tomato fruit cuticles. Phytochemistry 19, 1415–1419.
|
CAS |
Kutschera U, Schopfer P
(1986) Effect of auxin and abscisic-acid on cell-wall extensibility in maize coleoptiles. Planta 167, 527–535.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
Laguna L,
Casado CG, Heredia A
(1999) Flavonoid biosynthesis in tomato fruit cuticles after in vivo incorporation of H3-phenylalanine precursor. Physiologia Plantarum 105, 491–498.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
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.
| Crossref | GoogleScholarGoogle Scholar | PubMed |
Luque P,
Bruque S, Heredia A
(1995) Water permeability of isolated cuticular membranes: a structural analysis. Archives of Biochemistry and Biophysics 317, 417–422.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Marga F,
Pesacreta TC, Hasenstein KH
(2001) Biochemical analysis of elastic and rigid cuticles of Cirsium horridulum. Planta 213, 841–848.
|
CAS |
Crossref |
PubMed |
Matas AJ,
Cuartero J, Heredia A
(2004) Phase transitions in the biopolyester cutin isolated from tomato fruit cuticles. Thermochimica Acta 409, 165–168.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
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.
| Crossref | GoogleScholarGoogle Scholar |
Moore S,
Vrebalov J,
Payton O, Giovannoni J
(2002) Use of genomic tools to isolate key ripening genes and analyse fruit maturation in tomato. Journal of Experimental Botany 53(377), 2023–2030.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Orgell WH
(1955) The isolation of plant cuticle with pectic enzymes. Plant Physiology 30, 78–80.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Petracek PD, Bukovac MJ
(1995) Rheological properties of enzymatically isolated tomato fruit cuticle. Plant Physiology 109, 675–679.
|
CAS |
PubMed |
Riederer M, Schreiber L
(2001) Protecting against water loss: analysis of the barrier properties of plant cuticles. Journal of Experimental Botany 52, 2023–2032.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
Round AN,
Yan B,
Dang S,
Estephan R,
Stark RE, Batteas JD
(2000) The influence of water on the nanomechanical behavior of the plant biopolyester cutin as studied by AFM and solid-state NMR. Biophysical Journal 79, 2761–2767.
| Crossref | GoogleScholarGoogle Scholar |
CAS |
PubMed |
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.
| Crossref | GoogleScholarGoogle Scholar |
Tigchelaar EC,
McGlasson WB, Buescher RW
(1978) Genetic regulation of tomato fruit ripening. HortScience 13, 508–513.
|
CAS |
Wiedemann P, Neinhuis C
(1998) Biomechanics of isolated plant cuticles. Botanica Acta 111, 28–34.
Yamada Y,
Wittwer SH, Bukovac MJ
(1964) Penetration of organic compounds through isolated cuticles with special reference to urea. Plant Physiology 39, R11.