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Acta Sci. Pol., Hortorum Cultus 13(5) 2014, 91-105






Agata Konarska 

University of Life Sciences in Lublin 

Abstract. ‘Jonagold’ and ‘Szampion’ are winter apple cultivars, whose fruits are suitable 

for long-term storage. However, fruits of these cultivars differ markedly in the type of the 

surface and the rate and volume of water transpiration, which is manifested in fruit quality 

after storage and the length of apple shelf life. A majority of factors responsible for fruit 

quality and storability are genetically conditioned traits that are mainly developed before 

fruits reach harvest maturity or still develop during the storage period. The micromor-

phology, anatomy, and ultrastructure of 21-day-old fruit buds of the ‘Jonagold’ and 

‘Szampion’ were examined using light microscopy as well as scanning and transmission 

electron microscopy. The analyses were particularly focused on the traits that determine 

fruit firmness and storability, which contribute to long-term storage capacity. It was found 

that the fruit buds in both cultivars differed significantly in the number of trichome scars 

and stomata on the fruit surface, the thickness of the hypodermis layer and the hypoder-

mis cell walls, and in the content of phenolic compound deposits. At the fruit bud stage, 

the following features related to increased or decreased fruit firmness and storability were 

observed: platelet crystalline wax, cuticle microcracks, stomata and trichome scars, and 

presence of phenolic compounds.  

Key words: apple fruit buds, fruit peel, micromorphology, histology and ultrastructure, 

cuticle and epicuticular wax, microcracks, phenol compounds 


Apple cultivars are hybrids of Malus domestica (Borkh). They differ in many traits, 

e.g. the timing of reaching harvest and consumption maturity and long-term shelf life of 

fruits, which are largely dependent on the genetic background as well as on climatic and 

storage conditions [Rejman 1994, Kruczy ska 2008]. Apple fruits develop from the 

ovary of the flower and from the floral tube (receptacle). The development proceeds in 


Corresponding author: Agata Konarska, Department of Botany, University of Life Sciences in 

Lublin, Akademicka 15, 20-950 Lublin, Poland, e-mail: 


A. Konarska





Acta Sci. Pol.


two distinct stages, and the fruit growth curve has a form of a sigmoid curve [Miller et 

al. 1987, Westwood 1995]. During the development, the fruit size and weight increase 

systematically, while firmness and acidity decline [Atay et al. 2010]. The first stage of 

fruit development, i.e. the so-called fruit bud stage, is characterised by very intensive 

cell divisions (up to 8–10 weeks after anthesis). During this period, fruits are firm and 

contain a lot of starch, tannins and acids; therefore, they are tart and sour. In the second 

stage, between mid-June and harvest time, the fruit volume increases through enlarge-

ment of the intercellular spaces and cell volume. Additionally, accumulation of food 

reserves occurs, large vacuoles emerge in the cells, and the water content in fruits in-

creases in this stage. Physical changes in fruits are accompanied by chemical processes 

leading to reduction of the content of tannins and intensive accumulation of pigments, 

sugars, organic acids, fatty substances and pectins, volatile substances, vitamins, and 

minerals [Pieni ek 2000, Atay et al. 2010]. 

Fruits of different varieties of Malus vary with the the type of the fruit surface and 

peel structure and exhibit variation in the intensity of transpiration [Belding et al. 1998, 

Veraverbake et al. 2001a]. These traits are primarily associated with the amounts of 

cuticular (intra- and epicuticular) waxes as well as the number and depth of epidermal 

microcracks [Gordon et al. 1998, Maguire et al. 2000, Veraverbake et al. 2003b, Konar-

ska 2012]. A great impact on fruit transpiration is also exerted by the number of 

“opened” (active) stomata and lenticels per unit surface area and, to a small extent, by 

cuticle thickness and the number of hypodermis layers [Veraverbake 2001b, 2003b, 

Homutová and Blažek 2006]. These features prevent or promote fruit water loss, which 

is reflected in their firmness, post-storage quality (attractiveness), and the length of shelf 

life [Riederer and Schreiber 1995, Czernyszewicz 2007]. The peel morphology play 

also an important role in determining the distributions of water, carbohydrates, and 

nutrients inside the fruit [Cieslak et al. 2013]. According to Khanal and Knoche [2014] 

the epidermal and hypodermal cell layers represent the structural backbone of an apple 

peel during pre- and postharvest development, whereas cutical membrane microcrack-

ing has limited relevance to the overall mechanical properties of the peel. Recent re-

search shows that, similar to the cuticle layer, the outer layer of the cuticle (cuticle 

proper) contains polysaccharides (cellulose and pectin), which can affect the rheological 

properties of cuticles and may actively contribute to the bi-directional transport of water 

and solutes [Guzmán et al. 2014]. Moreover, optical coherence tomography which is 

a new non-destructive technique to visualize subsurface structures of materials, can be 

used to demonstrate peel structural differences between apples, as well as to measure 

structural changes that occur during storage [Verboven et al. 2013]. 

In previous studies, the author of the paper found that, the peels of two apple culti-

vars ‘Jonagold’ and ‘Szampion’ differed in many quantitative and qualitative traits of 

their micromorphology, anatomy, and ultrastructure at the harvest and consumption 

maturity stage [Konarska 2013]. The most substantial differences between the cultivars 

involved the quantity and forms of epicuticular wax and the total wax weight; the depth 

of cuticular microcracks; the number of stomata and lenticels; cuticle thickness and the 

size of epidermal cells; the thickness of the hypodermis layer; and the presence of phe-

nolic compounds. The extensive literature concerning apple development and structure 

does not provide detailed information about the morphology, anatomy, and ultrastruc-

Differences in the structure of fruit buds in two apple cultivars... 





Hortorum Cultus 13(5) 2014


ture of apple fruit buds or the mechanism and time of development of traits responsible 

for fruit firmness and shelf-life. Determination of the duration of development of the 

major qualitative fruit traits may be important for growers, who could control and mod-

ify the trait development through application of appropriate fertilisation and/or irrigation 

and other agricultural treatments. Therefore, the aim of the present study was to analyse 

the structure of 21-day-old ‘Jonagold’ and ‘Szampion’ fruit buds at the intensive cell 

division stage and to present differences in the structure of the covering layer in these 

cultivars at the micromorphological, tissue, and cellular level. Particular attention was 

paid to the occurrence of traits that have an impact on subsequent quality and firmness 

of fruit. 


21-day-old (21 days after anthesis) fruit buds (ca. 1-cm diameter) of ‘Jonagold’ and 

‘Szampion’ apples were collected on May 15–20, 2012 in a commercial, conventionally 

managed orchard near Lublin. Trees of the analysed cultivars grew in close proximity 

and identical climate and soil conditions. 20 fruit buds were sampled from the crowns of 

5 randomly chosen trees of both cultivars. Further analyses were carried out on peel-

comprising fragments of fruits sampled from their equatorial part. 

Scanning electron microscopy (SEM). The fruit buds were carefully transported  

to the laboratory to avoid damage or destruction of their surface wax layer. Next,  

4 × 4 × 1-mm peel fragments were sampled from 5 fruits of each cultivar. Since fixation 

of the material for SEM induces changes in the structure and destruction of the epicu-

ticular wax layer [Reed 1982], freshly sampled material was carefully mounted onto 

stubs, sputter-coated with gold, and examined “live” under a TESCAN/VEGA LMU 

(Tescan, USA) scanning electron microscopy at an accelerating voltage of 30 kV. Quan-

tity of wax platelets was roughly determined, while the the length and the number of 

stomata and trichome scars within an area of 1 mm

of the epidermis were assessed 

using the morphology software combined with SEM. 

Light microscopy (LM). Using a razor blade, hand-cut cross-sections perpendicular 

to the fruit axis were made through fresh peel of 10 fruit buds of ‘Jonagold’ and ‘Szam-

pion’. Further, the samples were stained with Sudan III (a saturated ethanol solution of 

Sudan III) to visualize lipophilic substances in cuticle, with Lugol’s iodine in order to 

detect starch, and with FeCl


 to detect phenolic substances. Later, the samples were 

embedded in glycerol gelatine on a glass slide and observed under the Nicon SE 102 

light microscope where the thickness of the cuticle (at the mid-width of a randomly 

chosen epidermal cell), the height of the epidermal cells, the number of layers of hypo-

dermis and its overall thickness, the thickness of hypodermis cell walls, and the thick-

ness of 3 layers of the parenchyma located under the hypodermis were determined in 

five places under a Nikon SE 102 light microscopy. Hand-cut samples obtained from 

fresh material were also observed with a stereoscopic Nikon Eclipse 90i microscope 

combined with an UV filter set comprising the wavelength of EX 330–380 nm stimulat-

ing autofluorescence of cuticle and chlorophyll in order to analyse the distribution  

of that substances. Images were obtained by using a digital camera (Nikon Fi1) and 


A. Konarska





Acta Sci. Pol.


NIS-Elements Br 2 software, respectively a Zeiss Axiolmager Z1 fluorescence micro-

scope equipped with an AxioCam MR digital camera. 

0.7-μm semi-thin sections were also prepared from fragments of the fruit buds, 

which were stained with 1% methylene blue with 1% azur II in a 1% aqueous solution 

of sodium tetraborate. The material was fixed and embedded in synthetic resin with the 

standard method used in transmission electron microscope (see below). Sections were 

observed by means of a Nicon Eclipse 90i microscopy.  

Transmission electron microscopy (TEM). Small samples (2 × 2 × 2 mm) of 

5 fruit buds of ‘Jonagold’ and ‘Szampion’ were fixed in 2% paraformaldehyde and 

2.5% glutaraldehyde buffered at pH 7.4 in 0.1 M cacodylate buffer. Fixation was per-

formed at room temperature for two hours, followed by 12 hr at 4ºC. When fixed, the 

samples were rinsed with 0.1 M cacodylate buffer at 4ºC for 24 hr and then treated with 

1% OsO


. After passage through increasing concentrations of propylene oxide in etha-

nol and finally through pure propylene oxide, the samples were embedded for 12 hr in 

Spurr Low Viscosity resin at 70ºC [Spurr 1969]. Subsequently, ultrathin sections 

(70 nm thick) obtained using the Reichert Ultracut-S ultramicrotome (Vienna, Austria) 

and a glass knife were transferred to re-distilled water and stained with a 0.5 M aqueous 

solution of uranyl acetate and lead citrate [Reynolds 1963]. Images were observed and 

recorded using the FEI Technai G2 Spirit Bio TWIN transmission electron microscopy 

at an accelerating voltage of 120 kV. Images were captured using a Megaview G2 

Olympus Soft Imaging Solutions camera. 

Statistical analyses. Means (±SD) were calculated for all the parameters measured. 

Data were analysed by one-way analysis of variance (ANOVA) and Tukey’s multiple 

range test for comparison of means, using software Statistica 7. The difference was 

considered statistically significant at the level of P < 0.05.  


SEM. The ‘Jonagold’ and ‘Szampion’ fruit buds were covered by dense, easily bro-

ken off, unicellular, ca. 1-mm-long non-glandular trichomes (figs 1A, C). The epidermis 

among the trichomes exhibited few trichome scars, i.e. traces left by broken off non-

glandular trichomes (figs 1D–E), and stomata in various developmental stages showing 

different degrees of stomatal opening (figs 1F, G). In both cultivars, the sizes of stomata 

and trichome scars were comparable, but their number per unit surface area was by ca. 

30% greater in ‘Jonagold’ (tab. 1). The cuticle of both cultivars exhibited microcracks 

of varied depths: superficial, which were more abundant, and deeper microcracks, 

which occurred sporadically and resembled a fastened zipper (fig. 1H). Moreover, the 

cuticle surface displayed vertically and horizontally oriented crystalline wax platelets 

(figs 2A–D). In ‘Jonagold’, the wax platelets were more ordered and more numerous 

than in the ‘Szampion’ cultivar. Additionally, a majority of the platelets were vertically 

or obliquely arranged (fig. 2A, B).  

LM. The surface layer of the 21-day-old ‘Jonagold’ and ‘Szampion’ fruit buds was 

composed of a single-layered epidermis covered by a cuticle layer and several hypo-

dermis layers (figs 3A–F).  

Differences in the structure of fruit buds in two apple cultivars... 





Hortorum Cultus 13(5) 2014



Fig. 1.  Epidermis surface of the fruit buds in the ‘Jonagold’ (A, C, D, F, G) and ‘Szampion’ 

cultivars (B, E, H); A, C – fragments of the epidermis surface with numerous subulate 

non-glandular trichomes; B – a fruit bud of ‘Szampion’ in stereoscopic microscopy.  

C – visible trichomes, stomata (arrows) and trichome scars (arrowheads); D, E – trichome 

scars (arrows) visible on the fruit bud surface; D – note a breaking off non-glandular 

trichome; F, G –stomata in different stages of development; H – microcrack (arrows) and 

trichome scar (arrowhead) 


A. Konarska





Acta Sci. Pol.



Fig. 2.  SEM. Fragments of the epidermis surface of the fruit buds ‘Jonagold’ (A, B) and ‘Szam-

pion’ cultivars (C, D) with vertical and horizontal crystalline wax platelets. Note ar-

rangement and a greater number of vertical and inclined wax plates in ‘Jonagold’ 


Epidermis covering the fruit buds in both cultivars had a nature of a meristematic 

tissue. Cells produced through anti- and periclinal divisions were visible among anticli-

nal elongated cells, particularly in the ‘Szampion’ cultivar (figs 3C, D). The height of 

epidermal cells was by 8% greater in ‘Jonagold’ (tab. 1). The epidermis was covered by 

a different-thickness cuticle layer which was stained orange-red by Sudan 3 (not shown) 

and exhibiting light blue fluorescence under UV light (fig. 3E). The mean cuticle thick-

ness was by 11% greater in the ‘Szampion’ cultivar (tab. 1). The epidermis of both 

cultivars had stomata with large air chambers underneath (fig. 3F). In the ‘Jonagold’ 

cultivar, the hypodermis layer was by 11% thicker than in ‘Szampion’ (tab. 1) and con-

sisted of 5–6 layers of the rectangular outline  collenchyma  cells  with  distinctly  thick- 

Differences in the structure of fruit buds in two apple cultivars... 





Hortorum Cultus 13(5) 2014




Fig. 3.  LM. Fragments of the cross-sections through the ‘Jonagold’ (A, B, E, F) and ‘Szam-

pion’(C–D) surface layer of the fruit bud. A, B – in hypodermis and parenchymatic cells 

visible large deposits of phenolic substances (arrowheads) and thickened tangential cell 

walls in the hypodermis cells (arrows with two heads). Note epidermis cells after mitotic 

divisions (asterisks); B – visible chloroplasts (arrows) in the hypodermis; C, D – visible 

chloroplasts (arrows) (D) and cells after mitotic divisions in the epidermis, hypodermis 

and parenchyma layer (asterisks); E – visible blue-fluorescent cuticle and red – fluores-

cent chloroplasts (fluorescence microscopy); F – visible stoma (S) with the air space (as-

terisk). Note chloroplasts (arrows) and deposits of phenolic substances (arrowheads) in 

the hypodermis cells; C – cuticle, E – epidermis, H – hypodermis, P – parenchyma 


A. Konarska





Acta Sci. Pol.




Fig. 4.  TEM. Ultrastructure of ‘Jonagold’ (A, D, E) and ‘Szampion’ (B, C) fruit peel at the fruit 

bud stage; A, B – visible cuticle composed of lamellar cuticle proper (CP) and a reticulate 

cuticular layer (CL); A, C – plastids (P) with starch grains visible in the epidermis and 

hypodermis cells; D – chloroplasts (Ch) with starch grains and electron-dense deposits of 

phenolic substances (arrowheads) visible in the hypodermis cells; E – deposit of phenolic 

substances visible in the vacuole; N – nucleus, M – mitochondrion, V – vacuoles,  

CW – cell wall 

Differences in the structure of fruit buds in two apple cultivars... 





Hortorum Cultus 13(5) 2014


ened tangential walls (tab. 1, figs 3A, B). In turn, the hypodermis cells in the ‘Szam-

pion’ fruit buds exhibited local and only slight cell wall thickenings or they were still at 

the differentiation stage and had an oval outline characteristic of parenchymatic cells 

(tab. 1, figs 3C, D). The diameters of parenchymal cells located below the hypodermis 

were comparable in both cultivars (tab. 1, figs 3A, C). Likewise in the epidermis, cells 

after mitotic divisions were also observed in hypodermal and parenchymal layers, par-

ticularly in the ‘Szampion’ cultivar (figs 3C, D). Numerous chloroplasts that produced 

red fluorescence under the fluorescence microscopy (fig. 3E) and contained starch (re-

action with IKI) were visible in the cytoplasm of these tissues in both cultivars (figs 3B, 

D, F). Additionally, the hypodermis and parenchymal cells in the ‘Jonagold’ fruit buds 

contained oval deposits of phenolic compounds (figs 3A, B, F) characterised by dark 

brown staining in FeCl



Table 1. Characteristics of fruit buds of ‘Jonagold’ and ‘Szampion’ cultivars 

Parameters (n = 10) 



Number of stomata and trichome scars (per mm


23 ±5.0 a 

18 ±4.0 b 

Length of stomata pores (μm) 

27.8 ±3.3 a 

30.1 ±2.9 a 

Length of trichome scars (μm) 

23.32 ±4.6 a 

22.56 ±4.2 a 

Thickness of cuticle (μm) 

8.64 ±0.7 a 

9.77 ±0.9 a 

Height of the epidermis cells (μm) 

22.93 ±1.7 a 

21.1 ±1.2 a 

Number of the hypodermis layers 

6 ±1.0 a 

4 ±1.0 a 

Thickness of the hypodermis layer (μm) 

85.51 ±9.7 a 

76.18 ±5.8 b 

Thickness of the hypodermis cell walls 

3.65 ±1.0 a 

0.09 ±0.4 b 

Thickness of the three parenchyma layers (μm) 

65.71 ±11.1 a 

67.98 ±6.0 a 

Total thickness of peel (μm) 

114.0 ±23.6 a 

106.3 ±18.4 a 


Values are mean ±SD (standard deviation). The same letters within a row mean no statistically 

differences (P < 0.05) 



TEM.  Only slight differences in the ultrastructure of epidermal, hypodermal, and 

parenchymal cells were found between the analysed cultivars. The cuticle on the surface 

of the fruit buds was composed of two layers: a substantially larger internal reticulate 

layer, the so-called cuticular layer and an external lamellate layer, the so-called cuticle 

proper, accounting for ca. 8–10% of the total cuticle thickness (figs 4A, B). The epi-

dermal cells exhibited a thin layer of parietal cytoplasm with visible mitochondria, and 

plastids containing starch grains (figs 4A, C). Similarly, the cytoplasm of hypodermal 

and parenchymal cells had plastids containing starch grains, whereas the vacuoles in the 

‘Jonagold’ cultivar exhibited numerous, large electron-dense deposits of phenolic com-

pounds (figs 4D, E). They usually adhered to the tonoplast and had different sizes.  


A. Konarska





Acta Sci. Pol.



Most traits related to fruit quality and firmness are genetically conditioned [Faust 

and Shear 1972a]. In the fruits of ‘Jonagold’ and ‘Szampion’, these traits were fully 

developed at harvest and consumption maturity [Konarska 2013]. 3-week-old fruit buds 

of the ‘Jonagold’ and ‘Szampion’ cultivars exhibited most features associated with the 

protective function of the surface covering layer. Differences in the structure of the fruit 

buds between the cultivars were visible primarily at the level of anatomy and micro-

morphology and were less evident than in the stage of harvest and consumption matur-


Babos et al. [1984] and Zamorsky [2007] report that protection of the fruit interior is 

ensured by fruit peel composed of an epidermis covered by a cuticle and a multi-layered 

hypodermis. In the early stage of ‘Jonagold’ and ‘Szampion’ fruit development, the 

protective role of this layer is additionally strengthened by abundant non-glandular 

trichomes densely distributed in the fruit bud epidermis. Similar non-glandular 

trichomes with a similar function were found to cover fruits of other plant species in 

different developmental stages [Bain 1961, Miller 1984, Bednorz and Wojciechowicz 

2009, Celano et al. 2009]. In 21 day-old ‘Jonagold’ and ‘Szampion’ fruit buds only few 

trichome scars remaining after broken off trichomes were visible. Maguire et al. [1999] 

and Veraverbake et al. [2003b] report that trichome scars, stomata and lenticels, present 

in the fruit epidermis at all developmental stages facilitate gas exchange and promote 

fruit transpiration, thereby contributing to wilting, softening and quality deterioration 

during storage and shelf life. However, the total number of trichome scars and stomata 

in the ‘Szampion’ fruit buds was lower than that in ‘Jonagold’. As reported by Konarska 

[2013], this relationship persisted in the consumption maturity stage, although ‘Szam-

pion’ fruits exhibit worse and shorter storability. According to Veraverbake et al. 

[2003a], at the consumption maturity stage, approximately 60% of ‘Jonagold’ lenticels 

are “closed” (non-transpiring), while only “opened” lenticels promote transpiration. 

A vast majority of the ‘Szampion’ lenticels may have been “opened”; yet, no such in-

vestigations have been conducted. The author of the present study considers that the 

intensity of fruit transpiration is dependent on a set of several water-loss promoting 

traits rather than on a single feature.  

The surface of the fruit buds in both cultivars examined showed few microcracks 

present mostly on the surface cuticle layers. The presence of the microcracks indicated 

the onset of the cell expansion process, although cells after mitotic divisions were still 

found by the author in all the layers of the fruit bud tissues, i.e. the epidermis, hypoder-

mis, and parenchyma. Microcracks appearing in the cuticle may indicate more rapid 

expansion of the volume and turgor of epidermal and internal fruit cells, while the 

amount of cuticle per fruit is constant [Faust and Shear 1972a, Roy et al. 1994, Knoche 

et al. 2004]. Similar results were obtained by Harker and Ferguson [1988], who found 

that the fruit bud stage in apples is a period of dynamic cell divisions, particularly in the 

epidermis, and the beginning of intensive cell growth. According to many authors, mi-

crocracks enhance water loss and reduce fruit firmness and weight [H hn 1990, Lau and 

Lane 1998, Maguire et al. 1999, De Bellie 2000, Link et al. 2004]. 

Differences in the structure of fruit buds in two apple cultivars... 





Hortorum Cultus 13(5) 2014


The surface of the fruit buds in the cultivars examined was covered by a layer of 

crystalline epicuticular waxes arranged in vertical and horizontal platelets, which were 

more abundant and ordered in the ‘Jonagold’ cultivar. Unlike the trichome scars, sto-

mata as well as microcracks, cuticular waxes are an efficient protective barrier against 

excessive transpiration [Faust and Shear 1972b, Babos et al. 1984, Roy et al. 1994, 

Belding et al. 1998, Veraverbeke et al. 2001a, b]. The number of wax platelets increases 

together with fruit maturation, reaching a maximum value during the storage period, 

particularly in varieties with a greasy and smooth peel, which was observed by Konar-

ska [2013] in ‘Jonagold’ fruits stored in a controlled-atmosphere storehouse for 

6 months. Koch et al. [2004] and Curry [2009] suggest that production of the highest 

possible numbers of vertically oriented platelets is especially important for reduction of 

transpiration, since this form of wax promotes healing and “repair” of microcracks. 

According to Curry [2001, 2005] and Müller [2005], apple trees employ a ‘Tear and 

Repair’ mechanism involving continuous synthesis of epicuticular waxes and closure of 

microcracks appearing along with fruit growth.  

The surface of the fruit buds of the cultivars examined had a characteristic reticulate-

lamellate cuticle, whose layer was thicker in the ‘Szampion’ cultivar. As shown by 

Konarska [2013], ‘Szampion’ fruits were characterised by greater weight loss and more 

intensive transpiration during the storage period. A thicker cuticle does not restrict the 

decline in fruit firmness and their better quality after storage. Similar results concerning 

the role of the cuticle in fruits of other apple varieties were obtained by Riederer and 

Schreiber [1995] and Knoche et al. [2000]. 

Numerous deposits of phenolic compounds were found in the hypodermis and par-

enchymal cells in the ‘Jonagold’ fruit buds; these, however, were not observed in 

‘Szampion’. Similarly, the deposits were visible, although in smaller numbers, only in 

the harvest and consumption maturity stage in ‘Jonagold’ [Konarska 2013]. The results 

obtained by the author correspond to the findings of Mehrabani and Hassanpouraghdam 

[2012], who reported that the content of phenolic compounds was higher in younger 

fruits than in the harvest maturity stage. Additionally, a varied content of polyphenols in 

different apple and pear cultivars has been described by other researchers [Solovchenko 

and Schmitz-Elberger 2003, Drogoudi et al. 2008,  ata et al. 2009]. Absence of poly-

phenols in the ‘Szampion’ cultivar may be one of the causes of the poorer quality and 

storability of its fruits, as evidenced by literature data indicating that presence of poly-

phenols improves and extends fruit storage by increasing resistance to pathogens [Garry 

et al. 1995, Lattanzio et al. 2001, Cheynier 2005]. 


1. The fruit buds in the ‘Jonagold’ and ‘Szampion’ cultivars differed significantly in 

the number of trichome scars and stomata, thickness of hypodermis layer and hypoder-

mis cell walls, as well as the quantities of deposits of phenolic compounds. 

2. The following factors exert an impact on the fruit quality and storability in the 

fruit bud stage: trichome scars and stomata, microcracks, crystalline wax platelets and 

phenols compounds. 


A. Konarska





Acta Sci. Pol.



This work was supported by the Ministry of Science and Higher Education of Po-

land as part of the statutory activities of the Department of Botany, University of Life 

Sciences in Lublin. 


Atay E., Pirlak L., Atay A.N., 2010. Determination of fruit growth in some apple varieties. 

J. Agric. Sci., 16, 1–8. 

Babos K., Sass P., Mohácsy P., 1984. Relationship between the peel structure and storability of 

apples. Acta Agron. Acad. Sci. Hung., 33, 41–50. 

Bain J.M., 1961. Some morphological, anatomical, and physiological changes in the pear fruit 

(Pyrus communis var. Williams Bon Chrétien) during development and following harvest. 

Aust. J. Bot., 9, 99–123. 

Bednorz L., Wojciechowicz M.K., 2009. Development of the multilayered epidermis covering 

fruit of Sorbus torminalis (Rosaceae). Dendrobiology, 62, 11–16.  

Belding R.D., Blankenship S.M., Young E., Leidy R.B., 1998. Composition and variability of 

epicuticular waxes in apple cultivars. J. Amer. Soc. Hort. Sci., 123, 348–356. 

Celano G., Minnocci A., Sebastiani L., D’Auria M., Xiloyannis C., 2009. Changes in the structure 

of the skin of kiwifruit in a relation to water. J. Hortic. Sci. Biotech., 84, 41–46. 

Cieslak M., Génard M., Boudon F., Baldazzi V., Godin C., Bertin N., 2013. Integrating architec-

ture and physiological perspectives in fruit development. Proceedings of the 7th International 

Conference on Functional-Structural Plant Models. 9–14 June 2013, Saariselkä, Finland,  


Cheynier V., 2005. Polyphenols in foods are more complex than often thought. Am. J. Clin. Nutr., 

81, 2235–2295. 

Curry E.A., 2001. Lenticel and cuticle disorders: a survey. Proceedings of the Washington Tree 

Fruit Postharvest Conference. 13–14 March 2001, Wenatchee, WA, USA. 

Curry E.A., 2005. Ultrastructure of epicuticular wax aggregates during fruit development in apple 

(Malus domestica Borkh). J. Hortic. Sci. Biotech., 80, 668–676. 

Curry E.A., 2009. Growth-induced microcracking and repair mechanisms of fruit cuticles. Plant 

Physiology. Proceedings of the SEM Annual Conference. 1–4 June 2009, Albuquereque New 

Mexico, USA.  

Czernyszewicz E., 2007. A consumer’s look at the apple quality. Annales UMCS, sec. EEE, 

Horticultura, 17, 70–82. 

De Bellie N., Schotte S., Soucke P., De Baerdemaeker J., 2000. Development of an automated 

monitoring device to quantify changes in firmness of apples during storage. Postharv. Biol. 

Technol., 18, 1–8.  

Drogoudi P.D., Michailidis Z., Pantelidis G., 2008. Peel and flesh antioxidant content and harvest 

quality characteristics of seven apple cultivars. Sci. Hortic., 115, 149–153. 

Faust M., Shear C.B., 1972a. Russeting of apples, an interpretive review. HortSci., 7, 233–235.  

Faust M., Shear C.B., 1972b. Fine structure of the fruit surface of three apple cultivars. J. Am. 

Soc. Hortic. Sci., 97, 351–355. 

Garry L.L., Suttill N.H., Wall K.M., Beveridge T.H., 1995. Localization of condensed tannins in 

apple fruit peel, pulp, and seeds. Can. J. Bot., 73, 1897–1904. 

Differences in the structure of fruit buds in two apple cultivars... 





Hortorum Cultus 13(5) 2014


Gordon D.C., Percy K.E., Riding R.T., 1998. effects of uv-radiation on epicuticular wax produc-

tion and chemical composition of four Picea species. New Phytol., 138, 441–449.  

Guzmán P., Fernández V., García M.L., Khayet M., Fernández A., Gil L., 2014. Localization of 

polysaccharides in isolated and intact cuticles of eucalypt, poplar and pear leaves by enzyme-

gold labelling. Plant Physiol. Biochem., 76, 1–6. 

Harker F.R., Ferguson I.B., 1988. Transport of calcium across cuticles isolated from apple fruit. 

Sci. Hortic., 36, 205–217. 

Homutová I., Blažek J., 2006. Differences In fruit skin thickness between selected apple (Malus 

domestica Borkh.) cultivars assessed by histological and sensory methods. Hort. Sci. (Prague), 

33, 108–113. 

H hn E., 1990. Quality of apples. Acta Hort., 285, 111–118. 

Khanal B.P., Knoche M., 2014. Mechanical properties of apple skin are determined by epidermis 

and hypodermis. J. Am. Soc. Hortic. Sci., 139(2), 139–147. 

Knoche M., Peschel S., Hinz M., Bukovac M.J., 2000. Studies on water transport through the 

sweet cherry fruit surface: Characterizing conductance of the cuticular membrane using peri-

carp segments. Planta, 212, 127–135. 

Knoche M., Beyer M., Peschel S., Oparlakov B., Bukovac M.J., 2004. Changes in strain and 

deposition of cuticle in developing sweet cherry fruit. Physiol. Plant., 120, 667–677. 

Koch K., Neinhuis C., Ensikat H.J., Barthlott W., 2004. Self assembly of epicuticular waxes on 

living plant surfaces imaged by atomic force microscopy (AFM). J. Exp. Bot., 55, 711–718. 

Konarska A., 2012. Differences in the fruit peel structures between two apple cultivars during 

storage. Acta Sci. Pol., Hort. Cult., 11(2), 105–116. 

Konarska A., 2013. The structure of the fruit peel in two varieties of Malus domestica Borkh. 

(Rosaceae) before and after storage. Protoplasma, 250, 701–714. 

Kruczy ska D., 2008. Jab onie: nowe odmiany. Hortpress Warszawa.  

Lattanzio V., Di-Venere D., Linsalata V., Bertolini P., Ippolito A., Salerno M., 2001. Low tem-

perature metabolism of apple phenolics and quiescence of Phlyctaena vagabunda. J. Agric. 

Food Chem., 49, 5817–5821. 

Lau O.L., Lane W.D., 1998. Harvest indices, storability, and poststorage refrigeration require-

ments of ‘Sunrise’ apple. HortSci., 33, 302–304. 

Link S.O., Drake S.R., Thiede M.E., 2004. Prediction of apple firmness from mass loss and 

shrinkage. J. Food Quality, 27, 13–26. 

ata B., Trampczy ska A., Paczesna J., 2009. Cultivar variation in apple peel and whole fruit 

phenolic composition. Sci. Hortic., 121, 176–181. 

Maguire K.M., Lang A., Banks N.H., Hall A., Hopcroft D., Benneti R., 1999. Relationship be-

tween water vapour permeance of apples and micro-cracking of the cuticle, Postharv. Biol. 

Technol., 17, 89–96. 

Maguire K.M., Banks N.H., Lang A., Gordon I.L., 2000. Harvest date, cultivar, orchard and tree 

effects on water vapour permeance in apples. J. Am. Soc. Hort. Sci., 125, 100–104. 

Mehrabani L.V., Hassanpouraghdam M.B., 2012. Developmental variation of phenolic com-

pounds in fruit tissue of two apple cultivarsActa Sci. Pol., Technol. Aliment., 11(3), 259–264. 

Miller A.N., Walsh C.S., Cohen C.D., 1987. Measurement of indole-3-acetic acid in peach fruits 

(Prunus persica L. Batsch cv Redhaven) during development. Plant Physiol., 84, 491–494. 

Miller R.H., 1984. The multiple epidermis-cuticle complex of Medlar fruit Mespilus germanica L. 

(Rosaceae). Ann. Bot., 53, 779–792. 

Müller I., 2005. Relationship between preharvest soybean oil application and postharvest behav-

ior apples. Dissertation, Washington State University.  

Pieni ek S.A., 2000. Sadownictwo. PWRiL Warszawa. 


A. Konarska





Acta Sci. Pol.


Reed D.W., 1982. Wax alteration and extraction Turing electron microscopy preparation of leaf 

cuticles. In: The plant cuticle. Cultler, D.F., Alvin K.L., Price C.E., eds. Academic Press, Lon-


Rejman A., 1994. Pomologia. PWRiL Warszawa.  

Reynolds E.S., 1963. The use of lead citrate at high pH as an electron-opaque stain for electron 

microscopy. J. Cell Biol., 17, 208–212. 

Riederer M., Schreiber L., 1995. Waxes – the transport barriers of plant cuticles. In: Waxes: 

Chemistry, molecular biology and functions, Hamilton R.J (ed.). The Oily Press, Scotland, 


Roy S., Conway W.S., Watada A.E., Sams C.E., Erbe E.F., Wergin W.P., 1994. Heat treatment 

affects epicuticular wax structure and postharvest calcium uptake in ‘Golden Delicious’ ap-

ples. Hort. Sci., 29, 1056–1058. 

Solovchenko A., Schmitz-Eiberger M.J., 2003. Significance of skin flavonoids for 


UV-B-protection in apple fruits. Exp. Bot., 54, 1977–1984. 

Spurr A.R., 1969. A low-viscosity epoxy resin embedding medium for electron microscopy. 

J. Ultra. Res., 26, 31–43. 

Veraverbake E.A., van Bruaene N., van Oostveldt P., Nicolaï B.M., 2001a. Non destructive 

analysis of the wax layer off apple (Malus domestica Borkh.) by means of confocal laser scan-

ning microscopy. Planta, 213, 525–533.  

Veraverbake E.A., Lammertyn J., Saevels S., Nicolaï B.M., 2001b. Changes in chemical wax 

composition of three different apple (Malus domestica Borkh.) cultivars during storage. Post-

harv. Biol. Technol., 23, 197–208. 

Veraverbake E.A., Verboven P., van Oostveldt P., Nicolaï B.M., 2003a. Prediction of moisture 

loss across the cuticle of apple (Malus sylvestris subsp. Mitis (Wallr.)) during storage: part 1. 

Model development and determination of diffusion coefficients, Postharv. Biol. Technol., 30, 


Veraverbeke E.A., Verboven P., van Oostveldt P., Nicolaï B.M., 2003b. Prediction of moisture 

loss across the cuticle of apple (Malus sylvestris subsp. Mitis (Wallr.)) during storage: part 2. 

Model simulations and practical applications. Postharv. Biol. Technol., 30, 89–97. 

Verboven P., Nemeth A., Abera M.K., Bongaers E., Daelemans D., Estrade P., Herremans E., 

Hertog M., Saeys W., Vanstreels E., Verlinden B., Leitner M., Nicolaï B., 2013. Optical co-

herence tomography visualizes microstructure of apple peel. Postharv. Biol. Technol., 78, 


Westwood M.N., 1995. Temperate zone pomology: Physiology and culture. (Third Edition). 

Timber Press, Oregon.  

Zamorskyi V., 2007. The role of the anatomical structure of apple fruits as fresh cut produce. 

Acta Hort., 746, 509–512. 





Streszczenie. ‘Jonagold’ i ‘Szampion’ nale  do zimowych odmian jab oni, których owo-

ce s  przystosowane do d ugotrwa ego przechowywania. Jednak owoce ró ni  si  wyra -

nie rodzajem powierzchni oraz tempem i ilo ci  transpirowanej wody, co przek ada si  na 

Differences in the structure of fruit buds in two apple cultivars... 





Hortorum Cultus 13(5) 2014


jako  owoców po wyj ciu z przechowalni oraz na d ugo   ycia jab ek na pó ce sklepo-

wej. Wi kszo  cech odpowiedzialnych za jako  i trwa o  owoców to cechy uwarun-

kowane genetycznie, rozwijaj ce si  w ró nym czasie. Mikromorfologi , anatomi  oraz 

ultrastruktur  21-dniowych zawi zków owoców odmian ‘Jonagold’ i ‘Szampion’ badano 

za pomoc  mikroskopii  wietlnej oraz elektronowej: skaningowej i transmisyjnej. Szcze-

góln  uwag  zwrócono na cechy maj ce wp yw na j drno  oraz trwa o  owoców. 

Stwierdzono,  e zawi zki badanych odmian ró ni y si  istotnie liczb  szparek i blizn w o-

skowych obecnych na jednostce powierzchni owocu, grubo ci  pok adu hipodermy oraz 

jej  cian komórkowych, a tak e zawarto ci  depozytów zwi zków fenolowych. Na etapie 

zawi zka u obydwu odmian zaobserwowano nast puj ce cechy maj ce zwi zek ze wzro-

stem lub obni eniem j drno ci i trwa o ci owoców: wosk krystaliczny w postaci p ytek, 

mikrosp kania w kutykuli, szparki i blizny w oskowe oraz obecno  zwi zków fenolo-



S owa kluczowe: zawi zki jab ek, skórka owoców, mikromorfologia, anatomia i ultra-

struktura, kutykula, wosk epikutykularny, mikrosp kania, zwi zki fenolowe  





Accepted for print: 6.06.2014 

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