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Moritz Knoche and Eckhard Grimm

Formation of microcracks in the cuticular membrane (CM) of epidermal segments (ES) of apple [Malus sylvestris (L.) Mill. var. domestica (Borkh.) Mansf., ‘Golden Delicious’, ‘Braeburn’, ‘Idared’, ‘Jonagold’, and ‘Topaz’; all grafted on ‘Malling.9’ rootstocks] fruit was studied after exposure of the surface of the ES to water. Potential strain of the CM on the ES was preserved by mounting a stainless steel washer on the fruit surface using an ethyl-cyanacrylate adhesive. Subsequently, ES were excised by tangentially cutting underneath the washer. The number of microcracks in the CM was established by light microscopy before and after a 48-h incubation period in deionized water. Within 48 h, the number of microcracks rapidly increased when the outer surface of ES of ‘Golden Delicious’ apple was exposed to water, but there was essentially no increase in microcracks when exposed to the ambient atmosphere. The occurrence of microcracks depended on the region of the fruit surface and increased from the rim of the pedicel cavity to the calyx. Increasing the relative humidity (greater than 75% relative humidity at 22 °C) above the outer surface of the ES exponentially increased the number of microcracks. Water-induced microcracking was not limited to ‘Golden Delicious’, but also occurred in ‘Braeburn’, ‘Jonagold’, ‘Topaz’, and, to a markedly smaller extent, in ‘Idared’ apple. The mechanism of formation of microcracks in the CM of apple fruit and their role in fruit russeting are discussed.

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Eckhard Grimm and Moritz Knoche

The skin is the primary load-bearing structure in a sweet cherry fruit (Prunus avium L.). Failure of the skin in rain cracking is considered to be related to water uptake. Little is known of the skin’s water potential, its osmotic potential (ΨΠ S), and turgor. The objective here was to quantify ΨΠ S relative to the osmotic potential of the flesh (ΨΠ F). Spatial resolution was achieved by monitoring plasmolysis in epidermal cells in tissue sections, incubated in selected osmotica using a light microscope method. Decreasing the osmotic potential [ΨΠ (more negative)] of the incubation medium increased the proportion (percent) of plasmolyzed epidermal cells. The pattern of increasing plasmolysis was sigmoidal with increasing osmolyte concentration. The value of ΨΠ for 50% of cells plasmolyzed, depended to some extent on the osmolyte used. The value of ΨΠ became slightly less negative for the osmolytes tested in the order: 1) mannitol, 2) sucrose, and 3) artificial cherry juice (a solution comprising the five major osmolytes of sweet cherry juice in the appropriate proportions and concentrations). There was little difference in the value of ΨΠ at 50% plasmolysis between the cultivars Hedelfinger, Sam, and Sweetheart. In all three cultivars, the value of ΨΠ F (measured for expressed juice using an osmometer) was markedly more negative than that of ΨΠ S (measured for 50% plasmolysis). Incubating skin segments in juice from the same fruit resulted in the plasmolysis of most (85.7% to 96.4%) of the epidermal cells. As fruit development progressed from stage II [27 day after full bloom (DAFB)] to the fully mature stage III (97 DAFB), plasmolysis occurred for increasingly more negative values of ΨΠ. Moreover, the difference between the osmotic potential values recorded for the flesh ΨΠ F and for the skin ΨΠ S increased. Plasmolysis of epidermal cells was accompanied by a marked swelling of their walls. The results indicate a marked difference in the osmotic potential of flesh (ΨΠ F trended more negative) and skin cells (ΨΠ S trended less negative).

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Eckhard Grimm, Stefanie Peschel, and Moritz Knoche

Mottling (pale spots) is clearly visible to the naked eye in all regions of the surface in all except for yellow cultivars of sweet cherry fruit (Prunus avium L.). The objective was to characterize these spots and their distribution on the exocarp. Within the spots, anthocyanins were limited to the epidermal cell layer but, in areas immediately adjacent to the spots, anthocyanins were present in the epidermal and in the hypodermal cell layers (making these areas darker). In ‘Sam’ sweet cherries, the median length and width of a spot in the cheek region were 390 and 162 μm, respectively, and the median area was 0.053 mm2 per spot. The spatial density in the cheek region averaged 1.94 (± 0.13) spots per mm2 and the percentage of surface area covered by the spots was 12.5% (± 1.07%). Epidermal cells within a spot had slightly larger projected surface areas than those in the adjacent region and thicker cell walls. The margins of the spots did not align with the anticlinal walls of the epidermal cells. The spots’ long axes were oriented parallel with the stem/stylar scar axis, whereas the slightly elongated epidermal cells within and adjacent to the spots were orientated perpendicular to the stem/stylar scar axis. The spatial density of spots and the cumulative spot area were highest in the region of the stylar scar, intermediate in the cheek and stem cavity, and lowest in the suture region. Spot spatial density on small fruit exceeded that on larger fruit, but the areas of individual spots was smaller. When an exocarp segment was excised from the cheek of a fruit, it contracted slightly as elastic strain was released. The projected surface area of the spots and that of the whole segment decreased to a similar extent. Our data suggest that spots result from a tensional failure during Stage III development in which the anthocyanin-containing hypodermal cell layer tears (schizogenously) and separates from the epidermis. This being the case, the pale spots (mottling) can be referred to as “strain spots.”

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Moritz Knoche, Eckhard Grimm, and Henrik Jürgen Schlegel

The pressure inside a mature sweet cherry (Prunus avium L.) fruit is thought to be an important factor in rain cracking. However, to our knowledge, this pressure has never been quantified directly. The objectives of this study are to quantify: 1) the cell turgor () in fruit using a cell pressure probe (CPP) and a vapor pressure osmometer (VPO); and 2) the tissue pressure in a fruit () using both a fruit pressure probe (FPP) and a compression-plate technique (CP). The value of in mesocarp cells of mature sweet cherry fruit averaged 28.1 kPa in ‘Samba’ and 17.5 kPa in ‘Sam’ at depths below the fruit surface between 200 and 400 μm. A (range 38 to 64 kPa for different cultivars) calculated from the tissue water potential ( = –2968 to –4035 kPa) and the osmotic potential () ( = –3020 to –4116 kPa) of excised mesocarp discs as determined by VPO was of the same order of magnitude as that by CPP. Similar low values were obtained by FPP (range 8.0 to 11.8 kPa across cultivars). The were consistently lower than the values measured by CPP or by VPO. The value in the mesocarp increased slightly with increasing depth below the surface. However, was always negligible (e.g., ‘Samba’ = 10 kPa) compared with either (‘Samba’ = –2395 kPa) or calculated water potential () (‘Samba’ = –2385 kPa). When subjecting intact fruit to CP, linear relationships were obtained between the forces applied and the resulting aplanation areas. The values obtained by CP (range in sweet cherry 18.4 to 36.1 kPa) were somewhat larger than the values obtained by FPP (range in sweet cherry 8.0 to 11.8 kPa). Incubating fruit for up to 7.5 h in deionized water or for up to 96 h in air enclosed above dry silica gel had no measurable effects on . The low and the low values are not unique to sweet cherry. Values of the same order of magnitude were obtained also in mature sour cherry (Prunus cerasus L.), european plum (Prunus domestica L.), grape (Vitis vinifera L.), gooseberry (Ribes uva-crispa L.), red currant (Ribes rubrum L.), black currant (Ribes nigrum L.), blueberry (Vaccinium corymbosum L.), and tomato (Solanum lycopersicum L.). Possible explanations for the very low values of and are discussed.

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Johannes Daniel Scharwies, Eckhard Grimm, and Moritz Knoche

Russeting is an important surface disorder in fruit and mechanical growth stresses, among other factors, are considered causal in russet induction. To test this hypothesis, fruit development and russeting were monitored on a whole fruit level and also in the calyx, cheek, and neck region of developing ‘Conference’ and ‘Condo’ pear fruit (Pyrus communis L.). To quantify growth, the pear fruit was geometrically modeled as approximating to half of a prolate spheroid for the calyx region and two truncated cones for the cheek and neck regions, respectively. Mass and surface area of ‘Conference’ and ‘Condo’ fruit increased in a single sigmoidal pattern with time. Fruit volume, determined by buoyancy, using a hydrostatic balance, and the Archimedes’ principle was closely related to that predicted by the model from fruit geometry. Growth rates of surface area in ‘Conference’ and ‘Condo’ peaked at ≈90 and 100 days after full bloom (DAFB), respectively, and were highest in the calyx followed by the cheek and neck regions. Relative growth rates, calculated by dividing growth rates by the absolute surface area present at that time, were at maximum during early development and thereafter continuously declined. In general, relative growth rates were highest for the cheek region, intermediate in the calyx, and lowest for the neck. ‘Conference’ fruit were always more russeted than ‘Condo’ with russeting generally decreasing from calyx to cheek and neck. Furthermore, russeting increased rapidly in ‘Conference’ during early development until ≈70 DAFB, particularly in the calyx and cheek regions and, to a lesser extent, in the neck region. There was little change in russeting after ≈70 DAFB. Plotting rates of russeting vs. relative growth rates in surface area indicate a positive and common relationship across regions where russeting increased when relative growth rates exceeded 0.03/day. Thus, differential growth rates between regions within ‘Conference’ or ‘Condo’, but not across the two cultivars, accounted for topical differences in russeting.

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Eckhard Grimm, Stefanie Peschel, Tobias Becker, and Moritz Knoche

Rain-cracking of sweet cherry (Prunus avium L.) fruit involves failure of the exocarp caused by excessive stress and strain. The objective of our study was to quantify exocarp strain in developing cherries. The release of linear elastic strain was followed in vivo using a gaping assay, whereas the release of biaxial elastic strain was followed in vitro after excision of small exocarp segments (ESs) that were submerged in silicone oil and strain release quantified by image analysis. When mature sweet cherry fruit were cut (by making two or more deep, longitudinal incisions parallel to the stylar/pedicel axis and on opposing sides of the fruit down to the pit), the incisions rapidly “gaped.” The gaping wounds continued to widen as they progressively released the linear elastic strain in the skin. By 24 hours the combined widths of two gapes represented 8.8% ± 0.1% of the fruit circumference. Increasing the number of cuts from two to 12 increased the cumulative gape widths to 14.9% ± 0.2%. In ES, monitoring the time course of relaxation after excision revealed a rapid release of biaxial strain, having a half-time of ≈2.7 minutes. Relaxation continued, but at a decreasing rate, for up to 48 hours. Across eight cherry cultivars, the biaxial strain in the exocarp at maturity ranged from 18.7% ± 1.9% in ‘Lapins’ to 36.0% ± 1.8% in ‘Katalin’. Elastic strain in the ES was always lower than that measured in an isolated cuticular membrane (CM). Increasing the temperature from 2 to 35 °C increased the rate of strain release and also the total percent strain released at 96 hours. In developing ‘Hedelfinger’ sweet cherry fruit, there was essentially no elastic strain in the exocarp at 45 days after full bloom (DAFB). Thereafter, significant elastic strain developed, reaching a maximum of 47.6% ± 2.5% at 87 DAFB. The effect of exocarp cell turgor on strain in the ES (evidenced by the difference in the reversible strain between ES with and without turgor) was closely and positively related to the relative area growth rate of the skin (r 2 = 0.957). Strain release peaked at ≈59 DAFB, and there was no effect of turgor on strain release in mature fruit. Our data demonstrated the following: 1) the exocarp is a viscoelastic material composite; 2) at maturity, plastic and elastic strain components make up 66% and 34% of the total percent strain, respectively; 3) elastic strain in the exocarp increases during Stage III development; and 4) the strain in the exocarp is unaffected by strain in the CM. Thus, the epidermis and hypodermis layers must represent the main, load-bearing structure in sweet cherry fruit with the cuticle making a mechanically insignificant contribution.

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Moritz Knoche, Eckhard Grimm, Andreas Winkler, Merianne Alkio, and Jürgen Lorenz

Neck shrivel is a physiological disorder of european plum (Prunus ×domestica L.) fruit, characterized by a shriveled pedicel end and a turgescent stylar end. Affected fruit are perceived as of poor quality. Little is known of the mechanistic basis of neck shrivel, but microcracking of the cuticle has been implicated. The objective of our study was to quantify transpiration through the skin surfaces of european plums with and without symptoms of neck shrivel. Cumulative transpiration increased linearly with time and was greater in the susceptible european plum cultivar Hauszwetsche Wolff with neck shrivel, compared with fruit of the same cultivar but without neck shrivel and compared with fruit of the nonsusceptible unnamed clone P5-112. Cumulative transpiration of epidermal skin segments (ES) excised from symptomatic ‘Hauszwetsche Wolff’ from near the pedicel end exceeded that from ES excised from near the stylar end. The permeance of ES from near the pedicel end of ‘Hauszwetsche Wolff’ with neck shrivel (12.4 ± 2.6 × 10−4 m·s−1) exceeded that of ES from near the stylar end (2.9 ± 0.4 × 10−4 m·s−1) 4.3-fold. However, in the clone P5-112, the same difference was only 1.6-fold (1.3 ± 0.8 × 10−4 m·s−1 vs. 0.8 ± 0.3 × 10−4 m·s−1). Microscopy revealed numerous microcracks near the pedicel end of symptomatic ‘Hauszwetsche Wolff’ fruit but markedly fewer microcracks near the stylar end. The microcracks near the pedicel end were oriented parallel to the pedicel/style axis, whereas those near the stylar end were randomly oriented. Juices extracted from near the pedicel end of susceptible cultivars had consistently more negative osmotic potentials [ψS (e.g., for Doppelte Hauszwetsche −5.1 ± 0.1 MPa)] than those from near the stylar end (e.g., for Doppelte Hauszwetsche −4.0 ± 0.1 MPa) or that from fruit without symptoms of neck shrivel (e.g., for pedicel end and stylar scar regions of Doppelte Hauszwetsche −3.8 ± 0.1 vs. −3.3 ± 0.1 MPa, respectively). Our results indicate that increased transpiration through microcracks near the pedicel end may contribute to neck shrivel but that the causes of neck shrivel are likely more complex.

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Andreas Winkler, Eckhard Grimm, Moritz Knoche, Julian Lindstaedt, and Dirk Köpcke

Skin spot is a commercially important disorder of the fruit skin of ‘Elstar’ apples (Malus ×domestica Borkh.). The disorder is characterized by patches of small brownish dots (“skin spots”) that usually appear on the skin after fruit are removed from storage. Water-induced cuticular microcracks are implicated in the etiology of skin spot. The objectives of our study were 1) to establish the effect of surface wetness on the severity of skin spot; and 2) to identify possible relationships between meteorological records of rainfall over a number of seasons and the severity of skin spot in those seasons. Surface wetness treatments were imposed on fruit using overhead sprinklers installed above trees grown under a plastic rain shelter. During early fruit development [14 to 44 days after full bloom (DAFB)], surface wetness did not affect the severity of skin spot. However, during the later part of the growing season (greater than 44 DAFB), increased surface wetness increased the incidence and severity of skin spot and also the severity of cuticular microcracking. Most skin spots and microcracks were already present at harvest before storage, but skin spots and microcracking did increase slightly during subsequent controlled atmosphere (CA) storage. Over a 9-year period, the severity of skin spot in ‘Elstar’ apples grown and stored locally under standard orchard and storage conditions was positively correlated to the number of rainy days. This correlation was greater for the period between 1 Aug. to harvest than for periods 1 June to harvest or 1 July to harvest. Fruit treated with 1-methylcyclopropene (1-MCP) were more susceptible to skin spot than untreated control fruit. Calculating regression equations for the relationship between the severity of skin spot and the number of rainy days (period 1 Aug. and harvest) revealed that the (commercially important) threshold score for skin spot of 2 is predicted to occur after 44 rainy days for control fruit and after 34 rainy days for 1-MCP-treated fruit. Our data demonstrate that skin spot arises from cuticular microcracks, which in turn result from numerous exposures to surface wetness (rain, dew), especially those occurring during later stages of fruit development.

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Christine Schumann, Henrik Jürgen Schlegel, Eckhard Grimm, Moritz Knoche, and Alexander Lang

Susceptibility of sweet cherry (Prunus avium L.) fruit to rain cracking increases toward maturity and is thought to be related to increases in both tissue pressure () and cell pressure (). Furthermore, at a given water potential (), one might expect the increase in and the to balance the decrease in osmotic potential (). The objectives of our study were to quantify and in developing sweet cherry using vapor pressure osmometry (VPO), compression plate (CP), and the cell pressure probe (CPP). In addition, the tissue water potential was determined by quantifying the bending of strips of fruit skin and the change in projected area of discs excised from the flesh when incubated in a range of sucrose solutions of varying osmotic potentials (). Fruit growth followed a sigmoid pattern with time with the Stage II/Stage III transition occurring at ≈55 days after full bloom (DAFB). The and the were constant up to ≈55 DAFB but decreased to –2.8 MPa at maturity. The calculated by subtracting the from averaged ≈350 kPa up to 48 DAFB and then decreased at a decreasing rate to ≈21 kPa toward maturity. The determined from bending assays using excised skin strips or from water uptake of excised flesh discs was essentially constant up to ≈48 DAFB, then decreased until ≈75 DAFB and remained constant thereafter. These values were in good agreement with those determined by VPO. The as determined by CP passed through a transient peak at ≈41 DAFB, then decreased until ≈63 DAFB and remained constant and low until maturity. Similarly, by CPP increased from 27 to 48 DAFB, remained constant until ≈55 DAFB, and then decreased until maturity. Our data demonstrate a consistent decrease in and that coincides with a decrease in of sweet cherry during Stage III. Because and are low relative to , the change in parallels that in . The reason for the low turgor most likely lies in the accumulation of apoplastic solutes. These prevent a catastrophic increase in pressure that would otherwise lead to the bursting of individual cells and the cracking of entire fruit.