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Postharvest Biology and Technology 47 (2008) 21–26

Physiological basis of UV-C induced resistance

to Botrytis cinerea in tomato fruit
II. Modification of fruit surface and changes
in fungal colonization
Marie Thérèse Charles 1 , Joseph Makhlouf, Joseph Arul ∗
Horticultural Research Centre, Department of Food Science and Nutrition, Université Laval, Sainte-Foy, Que., Canada G1K 7P4
Received 18 May 2006; accepted 27 May 2007

Abstract
Effect of pre-storage treatment with hormic dose of UV-light and ripening on the changes in topography and fine structure of postharvest
tomato fruit during storage was studied by scanning electron microscopy (SEM). Both ripening and UV-treatment induced significant structural
modifications in tomato fruit surface. Flattening of cellular mounds associated with normal ripening process was more intense with UV-treatment,
and the fruit surface was also more wrinkled with treatment. The formation of an operculum over broken trichomes was a common feature of
ripened control fruit, while this structure was incompletely formed in the treated fruit. Surface of senescent control fruit was characterized by
the presence of an amorphous epicuticular wax, which was quasi-absent on UV-treated fruit. Surface colonization of UV-treated fruit by Botrytis
cinerea was also different from untreated control. Colonization was sparse on the treated fruit, although direct cuticle penetration as well as
penetration through damaged trichomes was observed in both cases. Fewer adhesion structures (appressoria) were observed on UV-treated fruit
than on non-irradiated control, suggesting that structural modification of the epicuticular wax induced by UV may be a factor affecting the ability
of B. cinerea to attach to the treated fruit surface. This study shows that UV-treatment causes alteration in the amount of epicuticular wax and its
ultrastructural arrangement, presumably due to changes in its chemical composition. These changes could affect light reflectance characteristics of
the fruit surface, and possibly increase transpiration loss leading to changes in fruit appearance. Another consequence of UV-induced physical and
chemical modifications of tomato fruit surface could be an improved ability of the tissue to resist infection by B. cinerea. However, the reduced
colonization of the UV-treated fruit by the pathogen cannot be attributed solely to changes in surface topography.
© 2007 Elsevier B.V. All rights reserved.

Keywords: Cuticular wax; Gray mold; UV-light; Hormesis; Lycopersicon esculentum; Postharvest; Pre-storage treatment; Scanning electron microscopy

1. Introduction tomato products. Major factors that limit the storage life of
fresh tomato are senescence, transpiration and diseases devel-
Tomato is an important vegetable crop, second only to potato, opment. Greater consumption of fresh fruit and vegetables and
and is consumed in both fresh and processed form (Schuch, consumer demands of foods that are free of pathogens and chem-
1994). Its acid-sweet taste, unique flavor and color account ical residues have stimulated the development of new approaches
for its multiple usages. Recent association of lycopene, of to postharvest preservation of fresh produce. Postharvest treat-
which tomato is the principal food source, with the preven- ment of tomato with hormic dose of UV-C has been shown to
tion of chronic diseases (Bruno and Wildman, 2001) has caused be effective not only in controlling diseases but also in delaying
an increase in per capita consumption of fresh tomato and ripening of stored produce (Wilson et al., 1994; Arul et al., 2001).
Previous work showed that UV-treatment induces disease resis-
tance in tomato fruit and that UV-induced phytoalexin, rishitin,
∗ Corresponding author. Tel.: +1 418 656 2839; fax: +1 418 656 3353. contributes to disease resistance (Charles et al., 1999). The resis-
E-mail address: [email protected] (J. Arul). tance of UV-treated tomato may also be in part, a consequence
1 Present address: Agriculture and Agri-Food Canada, Horticultural Research

and Development Centre, 430 Boulevard Gouin, Saint-Jean-sur-Richelieu, Que.,

of a delay in the ripening process (Maharaj et al., 1993, 1999;
Canada J3B 3E6. Liu et al., 1993).

0925-5214/$ – see front matter © 2007 Elsevier B.V. All rights reserved.
doi:10.1016/j.postharvbio.2007.05.014
22 M.T. Charles et al. / Postharvest Biology and Technology 47 (2008) 21–26

UV-treatment appears to produce a bronzing discoloration Forty-eight fruit were randomly assigned to two groups. One
in tomato (Liu et al., 1993; Maharaj et al., 1999); in banana group (24 fruit) was treated with UV and the other untreated
fruit (Wade et al., 1993a) and in citrus fruit (Ben-Yehoshua et group (24 fruit) consisted of the control. Fruit were kept indi-
al., 1992). This discoloration develops gradually during storage. vidually in plastic punnets, arranged on a stainless steel wire
There was a close relationship between the flavonoid catechin mesh platform, and placed in 26.7 L plastic containers covered
and the bronze pigmentation in UV-treated banana (Wade et al., with perforated plastic lids to avoid accumulation of CO2 . A
1993b). We observed that UV-treatment reduced the gloss of the layer of sterile water was placed at the bottom of the contain-
tomato fruit surface compared to the untreated fruit. The changes ers to ensure a RH value of about 95% and the containers were
in the fruit surface gloss suggested probable modifications in the stored at 13 ◦ C. To evaluate the effect of ripening and that of UV-
light reflectance characteristics which might be caused by either treatment on fruit surface, six fruit of each group (control and
loss of epicuticular wax and/or ultrastructural changes in the UV-treated) were randomly sampled on days 4, 10 and 35 after
crystalline structure of the surface wax. Any modification in the UV-treatment. On day 10 after treatment, six fruit drawn ran-
fruit surface could also contribute to a reduction in the adhesion domly from each group, were inoculated with B. cinerea spore
of the pathogen, thereby reducing the colonization. Thus, the suspension and placed in separate containers. Four inoculated
objective of this work was to examine the ultrastructure of UV- fruit were sampled 4 days after inoculation. All randomly drawn
treated fruit surface by scanning electron microscopy (SEM) fruit samples were subjected to specimen processing for SEM.
and to examine the colonization of the fruit surface by Botrytis A set of four fruit was sampled at harvest and was subjected
cinerea. to neither washing and surface sterilization nor UV-treatment.
This set of fruit served to characterize undisturbed fruit surface.
The experiment was repeated twice with fruit harvested in two
2. Materials and methods
consecutive fall seasons.
2.1. Materials
2.3. Specimen processing for SEM
Tomato fruit (Lycopersicon esculentum Mill., cv. Trust) were
Three or more tissue samples (1 cm × 0.75 cm × 0.5 cm),
manually harvested from plants grown in a commercial green-
containing the cuticle, epicarp and part of the mesocarp, were
house. The fruit were at the mature green stage, identified as
excised from each of the four randomly sampled fruit. For the
stage 1 according to the USDA Agricultural Marketing Ser-
non-inoculated fruit, tissue was excised from the top of the fruit
vice Fruit and Vegetable Classification Chart. The harvested
within about 1 cm from the stem scar. For the inoculated fruit,
fruit were sorted and only fruit free of defects were selected.
samples were collected from the inoculation site at the edge of
The selected fruit were washed in running tap water, surface
the expanding lesion. Double chemical fixation was performed
sterilized with sodium hypochlorite solution (1.0 g/L) for 5 min,
as described by Benhamou and Lafontaine (1995). The tissues
rinsed twice in sterile distilled water, and dried in ambient air.
were fixed in glutaraldehyde (3%, v/v) followed by postfixa-
The washed fruit were kept overnight at 13 ◦ C at 95% relative
tion in osmium tetroxide (1%, v/v) both in cacodylate buffer
humidity until treatment the following day.
(0.1 mol/L; pH 7.2) and dehydrated in a graded ethanol series
The B. cinerea strain used in this study was isolated from
(from 30% to 100%, v/v). Subsequently, the specimens were
diseased tomato leaves and cultured on potato dextrose agar
transferred to a critical point drying apparatus and dried with
(PDA). Spores suspension was prepared by flooding a 10-day
CO2 . The dried specimens were mounted on aluminum stubs
old culture with sterile water containing 0.02% (v/v) Tween
and coated with gold with a Nanotec sputter coater. Exami-
20 (Sigma Chemical Co., Saint Louis, MO). The spore sus-
nation was carried with a JEOL scanning electron microscope
pension was filtered through sterile cheese cloth and diluted to
(JSM-35) at 15 kV (JEOL, Tokyo, Japan). At least 12 fixed spec-
5 × 108 spores/L. Surface sterilized tomato fruit were inoculated
imens from each treatment group were thoroughly examined
by placing 1.0 mL of the prepared suspension in the hollow of
under the electron microscope. The chemicals used for scanning
the stem scar.
electron microscopy were purchased from JBEM (Pointe-Claire,
Quebec, Canada).
2.2. Treatment and fruit storage
3. Results
Top and bottom part of the fruit were exposed to hormic
UV dose of 3.7 kJ/m2 as determined by Maharaj et al. (1999). 3.1. Effects of UV-C on tomato fruit surface
UV-C radiation was produced by fluorescent germicidal lamps
(GE 30W) with peak emission at 254 nm (General Electric Cir- SEM investigation of samples from freshly harvested tomato
cleville, OH). Radiation intensity was measured with a portable fruit showed dome shape of the cellular mounds, and presence of
radiometer (UVX Digital Radiometer, UVP, Inc., San Gabriel, trichomes sparsely distributed on the fruit surface (Fig. 1A–D).
CA). Fruit were treated with the hormic UV dose by placing No significant difference between the surface of UV-treated fruit
them at approximately 30 cm from the lamp for 3 min. Treated and that of control fruit was observed on day 4 after treatment.
fruit were protected from white light by covering them with The typical features in both control (Fig. 1E) and UV-treated
black PVC sheets. (Fig. 1J) fruit were flattening of the cellular mounds, and break-
 M.T. Charles et al. / Postharvest Biology and Technology 47 (2008) 21–26 23

Fig. 1. Scanning electron micrographs of tomato fruit surface. Effect of ripening and UV-C treatment. (A–D) Tomato fruit surface at harvest day. Note the presence
of sound trichomes (B and C) and the dome shape of the cellular mounds (D, arrow). (E–I) Surface of control fruit (non-irradiated) during storage. Non-irradiated
control 4 (E and F), 10 (G) and 35 (H and I) days after irradiation. (J–N) Surface of UV-treated fruit during storage. UV-C treated fruit 4 (J and K), 10 (L) and 35
(M and N) days after irradiation. Note the flattening of the cellular mounds, alteration of the trichomes and wrinkling of the fruit surface in both the control and
UV-treated fruit. The epicuticular wax appears more flaky and crystalline in the control than in the UV-treated fruit. Arrows (H and M) indicate the formation of an
opercule over brocken trichomes (T: trichome). Bars: (A), (C), (E), (G), (H), (J), (L) and (M): 10 ␮m; (B): 20 ␮m; (D) and (I): 5 ␮m; (F), (K) and (N): 1 ␮m.

down and/or wilting of some trichomes, attributable to either fruit surface appeared unadorned and bare of any crystalline wax
washing and surface sterilization of the fruit or to ongoing senes- (Fig. 1I versus N). Any wax present is likely to be in amorphous
cence. Occasionally, the altered trichomes (Fig. 1E) appeared form.
like open craters on the fruit surface. The surface wax of the
UV-treated fruit (Fig. 1K) appeared more ridged than that of the 3.2. Surface colonization
control (Fig. 1F). After 10 days of storage, flattening of the cellu-
lar mounds was more intense in the UV-C treated fruit (Fig. 1L) The overall growth of B. cinerea on tomato fruit appeared to
than in the control (Fig. 1G). On the other hand, the control fruit be greatly affected by pre-storage UV-C irradiation. Four days
surface appeared more wrinkled after 10 days of storage than after inoculation, mycelial growth at the inoculation site was
it was after 4 days of storage (not shown). However, the differ- heavier on the control (Fig. 2A) compared to UV-treated fruit
ence in ultrastructural features between treated and control fruit (Fig. 2B). Although fungal attachment was secured by the pres-
were more striking after 35 days of storage (Fig. 1M versus H). ence of an extracellular matrix associated with hyphae, adhesion
The flattening of the cellular mounds was more extensive on the and penetration of the pathogen were moderate in irradiated
surface of the treated fruit than the control. Although formation fruit as indicated by hyphal tips forming appressoria to a lesser
of an operculum covering the crater left behind by the degener- extent (Fig. 2F) than in the control (Fig. 2C, arrowheads). Pin-
ated trichome was evident in both UV-treated and control fruit, hole beneath the hyphal tip indicated direct cuticular penetration
the formation of the protective operculum appeared more com- (Fig. 2C, single arrow). The fungus also took advantage of the
plete in the control fruit (Fig. 1M versus H). While the control opening on the fruit surface left by the broken trichomes to gain
fruit surface appeared uneven and flaky or crystalline, the treated its entrance into the fruit tissue both in the control (Fig. 2B)
24 M.T. Charles et al. / Postharvest Biology and Technology 47 (2008) 21–26

Fig. 2. Scanning electron micrographs of B. cinerea-inoculated tomato fruit surface, 4 days after challenge. (A–C) Interaction between B. cinerea and control
(untreated) fruit. (D–F) Interaction between B. cinerea and UV-treated fruit. Note the more intense colonization on control (non-irradiated) fruit at the site of
inoculation (A) compared to that of UV-treated tissue (D). The fungus gains its entrance into the fruit tissue via the broken trichomes (B and E), or through direct
sub-cuticular penetration (C, arrow). More hyphal forming appressoria (C, arrowheads) are seen on the control than on the UV-treated fruit (F). The flaky or crystalline
deposit seen on the fruit surface is more abundant on the control (A–C) than on UV-treated fruit (D–F). F: fungus; Ap: appressoria; FD: flaky deposit. Bars: 10 ␮m.

and the treated fruit (Fig. 2E). The presence of flaky deposits surface of mature fruit. The observed presence of trichomes is
appeared to be associated with B. cinerea on the fruit surface. attributable to the site of tissue sampling, i.e., in the vicinity of
This material was generally less abundant on the UV-treated stem scar, and that the maturation process is slower at this site
surface (Fig. 2D–F) than on the control fruit surface (Fig. 2A–C). compared with the rest of the fruit.
The morphology and chemical composition of waxes cov-
4. Discussion ering plant surface undergo changes during development and
storage, light playing a dominant role in wax biosynthesis
SEM investigations showed that both the ripening process and (Juniper and Jeffree, 1983). In the present work, fruit were stored
UV-treatment affected the topography as well as the fine struc- in the dark and therefore it is less likely for wax biosynthesis to
ture of the tomato fruit surface. During ripening, the mounds of occur during storage. However, regeneration of the waxy layer,
the epidermal cells flattened and the ridges on the fruit surface disturbed during washing and surface sterilization, might have
became more abrupt, and this was in line with earlier studies by taken place in stored tomato. The latter possibility is known
Wilson and Sterling (1976). Such topographical changes were to occur in stored apple fruit which are polished before stor-
amplified in UV-treated fruit, probably due to UV-induced plas- age (Skene, 1963). The regenerated epicuticular wax layer of
molysis of the underlying epidermal cells (Charles et al., 2008a). polished apple is structurally different from that of unpolished
An interesting feature of the surface of untreated senescent fruit apple, which enhances the gloss of the polished apple. The struc-
was the presence of a flaky epicuticular wax which was not evi- ture and morphology of epicuticular wax is related to the gloss
dent on the UV-treated fruit at equivalent storage time. Since of fruit and vegetable surfaces, with smoother wax deposits dis-
these wax deposits were apparently absent on the surface of the playing higher gloss (Blanke, 1986; Ward and Nussinovitch,
freshly harvested fruit, it could be assumed that this wax layer 1996; Nussinovitch et al., 1996a). Nussinovitch et al. (1996b)
was exuded during storage. reported a decrease in the gloss of tomato peel during ripening.
Although trichome density decreases as the fruit matures in Furthermore, changes in gloss may result from variations in the
modern tomato cultivars, and it tends to be completely absent in epicuticular wax quantity (Corey and Schlimme, 1988), struc-
ripe fruit (Getz et al., 1983; Li et al., 2004), Cruickshank (1995) ture (Corey and Schlimme, 1988; Corey et al., 1988; Ward and
observed the presence of irregularly distributed trichomes on the Nussinovitch, 1996) as well as chemical composition (Hunt and
 M.T. Charles et al. / Postharvest Biology and Technology 47 (2008) 21–26 25

Baker, 1980). Changes in wax structure are related to surface favor penetration of tomato fruit by Colletotrichum gloeospo-
expansion and to desaturation of saturated fatty acids (Blanke, rioides (Cruickshank, 1995). Penetration of surface-modified
1986). We observed significant differences in the epicuticular tomato fruit occurred rapidly and formation of appressoria was
wax crystallinity between the start and the end of the storage not essential to assist the formation of penetration pegs. On
period, i.e., with ripening. The crystalline materials cannot be the contrary, we observed an extensive mycelial growth on the
salt crystals since there is no evidence for the existence of either untreated fruit (Fig. 2A) with greater amount of epicuticular wax
salt glands for ion secretion or hydathodes for water extrusion (Fig. 1I), while mycelial growth in treated fruit (Fig. 2D) was
in tomato fruit. In fact, amorphous wax platelets (Fig. 1I) were greatly reduced in spite of reduced epicuticular wax (Fig. 1N).
seen on the surface of the untreated senescent fruit. The decrease This suggests that epicuticular wax either plays only a minor role
in gloss of ripening tomato fruit is likely due to alterations in the as a physical barrier or the resistance offered may be variable
wax morphology and increase in the total epicuticular wax. depending on the ability of the pathogen to secrete hydrolytic
In UV-treated fruit, the modification in wax morphology asso- enzymes to digest the components of the fruit surface. B. cinerea
ciated with ripening appears to have been hindered or at least is known for its ability to secrete cutinases to hydrolyze cuticular
delayed. If the modification in wax morphology associated with wax during pathogenesis (Pezet, 1996). The marked reduction
ripening leads to a decrease in gloss, then the quasi-absence of in fungal colonization in UV-treated fruit cannot be attributed
epicuticular wax in UV-treated fruit should result in accentuated solely to changes in fruit surface topology. It is likely that modifi-
loss of gloss. Scanning electron micrographs indicate a lower cations in the pattern of disease development are manifestations
level of epicuticular wax deposit on UV-treated fruit (Fig. 1N) of biochemical differences in the wax composition and changes
during the course of storage than the untreated control (Fig. 1I), in the epicarp cells of the UV-treated fruit compared to that of
which can lead to less glossy appearance. However, exposure of the control.
barley, bean and cucumber seedlings to enhanced UV-B radia- Ultraviolet radiation affects the production of various sec-
tion (at a daily dose of 7.93 kJ/m2 for 14 days) caused an increase ondary metabolites (Rozema et al., 1997) some of which can be
of total cuticular wax in leaves by about 25% (Steinmüller and incorporated to the cuticle and wax layer. Among the secondary
Tevini, 1985). Enhanced UV-B radiation affected the distribution metabolites elicited by UV, some act as UV-filters (flavonoids),
pattern of alkanes, aldehydes and primary alcohols, and induced while others play a significant role in defense against micro-
branching and a shift toward shorter acyl chain lengths of the wax bial invasion (phenolic acids and lignin). Then, it is reasonable
components (Steinmüller and Tevini, 1985; Barnes et al., 1996). to presume that chemical modification of the plant surface can
The greater deposition of epicuticular wax and changes in its account, in part, for the reduced growth rate of B. cinerea on
chemical composition may function as a mechanism to attenu- UV-treated tomato fruit. In addition, plasmolysis and collapse
ate enhanced UV-B damages, as shown for epidermal flavonoids of the epidermal and first mesocarp cells, resembling HR-like
(Robberecht and Caldwell, 1978). The increase in the amount cell death generate a physical barrier composed of dead cells
of wax surface is possible by exudation from healthy epidermal (Charles et al., 2008a) which limits the availability of nutrients
cells which are known to be the site of wax synthesis (Juniper to the pathogen due to rapid dehydration that often accompanies
and Jeffree, 1983). Reduced accumulation of epicuticular wax cell death (Greenberg, 1996). The desiccation of the infection
on UV-treated tomato fruit surface must be related to damages to court impairs the growth and survival of the fungus within the
the epicarp cells, causing a loss of their ability to regenerate sur- plant tissue. Maharaj et al. (1999) observed a higher moisture
face wax. It appears to be the case, since collapse of epicarp cells loss in UV-treated tomato compared to the control. Moreover,
in UV-treated fruit has been observed (Charles et al., 2008a). The several studies have correlated UV-induced disease resistance
implications of the reduced amount of epicuticular wax on senes- to the accumulation of phytoalexins in treated tissue (Rodov et
cent UV-treated tomato would be altered light reflectance and al., 1992; Mercier et al., 1993; Charles et al., 1999; Charles et
reduction in gloss. Although most of the cuticular waxes do not al., 2008b). Therefore, the presence of substances with antifun-
absorb within the visible spectrum, the structural arrangement gal activity in both the cuticle and pericarp of UV-treated tomato
of wax enhances light reflectance and light scattering (Cameron, may have reduced its sensitivity to fungal invasion. Further work
1970). When wax was removed mechanically from leaves, the is necessary to establish differences in the biochemistry of sur-
reflectance of leaves was reduced compared to that of leaves face wax of UV-treated tomato compared to that of untreated
with normal wax deposition (Sinclair and Thomas, 1970). In fruit.
addition, diffusion coefficient of water should be enhanced with
less profuse wax layer (Denna, 1970). But the weight loss of 5. Conclusion
UV-treated fruit was higher (6.7%) than control fruit (5.5%) at
the end of a 35-day storage period, but it was not significant We provide evidence that UV-treatment affects the morphol-
enough to cause shriveling (Maharaj et al., 1999). ogy of tomato fruit surface wax. Surface colonization of the
Surface colonization of the irradiated fruit was reduced, com- UV-treated fruit was lower than that of non-irradiated fruit. UV-
pared with untreated fruit. The physical and chemical nature of treatment may have induced biochemical modifications of the
plant surface is known to greatly influence adhesion, germina- surface wax layers. The overall impact of these changes are
tion, growth and penetration of fungal spores (Prusky, 1996; two contrasting effects. On one hand, changes in the physical
Jenks and Ashworth, 1999). Minor abrasion of the epicuticu- and biochemical modifications occurring in epidermal cell in
lar wax of tomato fruit or its removal by solvent was shown to response to UV-treatment may be conducive to an improved
26 M.T. Charles et al. / Postharvest Biology and Technology 47 (2008) 21–26

ability of the plant tissue to resist pathogen attack. On the other Greenberg, J.T., 1996. Programmed cell death: a way of life for plants. Proc.
hand, altered wax layers can affect light reflectance character- Natl. Acad. Sci. U.S.A. 93, 12094–12097.
istics of the fruit surface, and can also contribute to increased Hunt, G.M., Baker, E.A., 1980. Phenolic constituents of tomato fruit cuticles.
Phytochemistry 19, 1415–1419.
water loss from cuticular transpiration, both leading to changes Jenks, M.A., Ashworth, E.N., 1999. Plant epicuticular waxes: function, produc-
in the appearance of the fruit. tion and genetics. Hortic. Rev. 23, 1–68.
Juniper, B.E., Jeffree, C.E., 1983. Plant Surfaces. Edward Arnold, London, p.
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Acknowledgements Li, L., Zhao, Y., McCaig, B.C., Wingerd, B.A., Wang, J., Whalon, M.E., Picher-
sky, E., Howe, G.A., 2004. The tomato homolog of coronatine-insensitive 1
This work was supported by Natural Sciences and Engineer- is required for the maternal control of seed maturation, jasmonate-signaled
ing Research Council (NSERC) and Conseil des Recherches defense responses, and glandular trichome development. Plant Cell 16,
126–143.
en Pêche et en Agro-Alimentaire du Québec (CORPAQ). The Liu, J., Stevens, C., Khan, V.A., Lu, J.Y., Wilson, C.L., Adeyeye, O., Kabwe,
authors wish to thank Ms. Odette Desbiens and Mr. Ronan Cor- M.K., Pusey, P.L., Chalutz, E., Sultana, T., Droby, S., 1993. Application of
cuff for technical assistance. ultraviolet-C light on storage rots and ripening of tomatoes. J. Food Prot. 56,
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