Water Potential, Osmotic Potential, and Cell Turgor in Developing European Plums

Authors:
Moritz Knoche Leibniz-Universität Hannover, Institut für Gartenbauliche Produktionssysteme, Abteilung Obstbau, Herrenhäuser Str. 2, D-30419 Hannover, Germany

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Eckhard Grimm Leibniz-Universität Hannover, Institut für Gartenbauliche Produktionssysteme, Abteilung Obstbau, Herrenhäuser Str. 2, D-30419 Hannover, Germany

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Abstract

Neck shrivel is a fruit disorder of european plum (Prunus domestica L.). We investigate whether an asymmetrical distribution of osmolytes might explain the observations of a turgid stylar end and a flaccid stem end, in a selection of 17 plum cultivars sourced from two sites. The osmotic potential (ΨΠ) of the juices expressed from stem or stylar end fruit samples decreased (became more negative) during development. The cell turgor (ΨP) slightly increased during development up to 352 ± 42 kPa at 78 days after full bloom (DAFB) in the stem end and up to 331 ± 51 kPa at 92 DAFB in the stylar end, and then decreased. At maturity, ΨP averaged 22 ± 3 kPa in the stem end and 22 ± 4 kPa in the stylar end. These values are negligibly low compared with the very negative values of ΨΠ in the stylar end (−3188 ± 73 kPa) and stem end (−3060 ± 74 kPa). There was a transient gradient in ΨΠ between stylar end and stem end that almost disappeared by maturity. Marked differences in ΨΠ and its distribution were measured across 17 cultivars. In the majority (14), ΨΠ was more negative at the stylar end than at the stem end. A more negative ΨΠ in the stem was only detected in ‘Aprimira’, ‘Topfive’, and ‘Tophit’. Our results demonstrate that cell ΨP is very low and is essentially independent of ΨΠ in developing european plums. In most cultivars, ΨΠ in the stylar end is more negative than in the stem end. The absence of an axial gradient in ΨP and the small differences in ΨΠ between the stem and stylar end make both factors unlikely candidates for explaining neck shrivel.

Neck shrivel is a fruit disorder of european plum. Shriveled fruit is perceived as of low quality so there is a marked decrease in value at market. Susceptibility to neck shrivel varies among cultivars and between seasons. This complicates systematic research on cause-and-effect relationships. Earlier studies have established an elevated skin permeability to water vapor due to an increased frequency of microcracks at the stem end of the fruit, and this may contribute to neck shrivel in symptomatic fruit of susceptible ‘Hauszwetsche’ clones. The water vapor permeability of the nonshriveled, stylar end of the same cultivar was lower and had only a few, randomly oriented, microcracks. There were no differences in microcracking or in skin permeance in the stem and stylar ends of fruit of a nonsusceptible cultivar (Knoche et al. 2019). It is not known if microcracking is the only factor involved in neck shrivel. A backflow of xylem water (from fruit to the tree) has been excluded as a factor (Khanal et al. 2021; Winkler and Knoche 2021).

An alternative explanation for neck shrivel is an asymmetric distribution of the osmotic potential (ψΠ) within the plum tissues. Assuming the fruit to be at equilibrium water potential (ψ), a more negative ψΠ at the stylar end, as compared with the stem end, would result in a higher turgor potential (ψP) at the stylar end, compared with the stem end. This could lead to a turgid stylar end and a flaccid stem end.

The objective of this study was to establish (1) whether there is a gradient in ψΠ within plums, and (2) whether changes in ψΠ during development, are related to changes in ψP. We focused on the stylar end and stem end regions of the fruit because a differential response in these regions could contribute to neck shrivel.

Materials and Methods

Plant material.

Mature fruit of Prunus domestica L. were sampled in orchards of the Federal Fruit Variety Office at Wurzen (lat. 51°22′ N; long. 12°45′ E) (cultivars Auerbacher, Bühler Frühzwetsche, Cacaks Schöne, Chrudiminer Zwetsche, Czernowitzer, Elena, Hauszwetsche Wolff, Hauszwetsche zum Felde, Italienische Zwetsche, Katinka, Lützelsachser, Oullins Reneclaude, and Tegera) or in orchards of the Horticultural research station of the Leibniz-University at Ruthe (lat. 52°14′ N, long. 9°49′ E) (cultivars Aprimira, Auerbacher, Cacaks Schöne, Elena, Hanita, Hauszwetsche Wolff, Topfive, Tophit, and Toptaste). All trees were cultivated according to current regulations for integrated fruit production. Fruit were sampled randomly from a minimum of three trees per cultivar, and held for no longer than 36 h at 2 °C.

Analyses.

Fruit used in the experiments was characterized by determining fruit mass and skin color (CM-2600d; Konica Minolta, Osaka, Japan). For determination of the ψΠ values, the fruit was cut longitudinally into halves along the suture. The pit was removed. Juice was expressed from one of the halves using a garlic press. Assuming radial (or at least bilateral) symmetry, this value represents the fruits’ mean ψΠ. To determine if an axial gradient in ψΠ existed within the fruit, the remaining half-fruit was sliced perpendicularly to its longitudinal axis. It was cut into two slices of equal thickness until 105 DAFB or into four slices of equal thickness after 105 DAFB, until maturity. Fruit from the cultivar comparison were also cut into four slices. The juice was expressed from each slice. The osmolarity of each juice sample was determined by water vapor pressure osmometry (VAPRO 5520 and 5600; Wescor, Logan, UT, USA) and the value of ψΠ was calculated.

The value of ψP was quantified in the stem end and the stylar end of developing ‘Hauszwetsche Wolff’ and ‘Elena’ fruit using a cell pressure probe (CPP) (Steudle 1993). The CPP comprised a glass capillary filled with silicone oil and was connected to a pressure transducer (26PCGFA6D; Honeywell Sensing and Control, MN, USA). The CPP was mounted on a micromanipulator. To determine the ψP, the glass capillary was carefully inserted into a parenchyma cell in the outer mesocarp under a horizontal microscope (≈200 to 400 µm below the skin surface). Upon insertion into a cell, the pressure inside the capillary equilibrated with the cell’s internal ψP. The peak pressure of the system was recorded as described previously (Knoche et al. 2014, Schumann et al. 2014). We analyzed only those insertions that (1) maintained a leak-free seal between capillary and the cell, when subjected to a small, transient, increase in pressure, and (2) where the pressure returned to atmospheric (i.e., the pressure just before the insertion) immediately after the capillary had been withdrawn from the fruit. Only when these two conditions had been met, was the peak pressure recorded and taken as an estimate of the cell’s ψP. A minimum of five fruit were measured in the two regions, per sampling date, and per cultivar.

Statistics.

Data are presented as means ± standard errors. Data were analyzed by analysis of variance using the statistical software package SAS (version 9.4; SAS Institute, Cary, NC, USA).

Results and Discussion

The time course of increase in fruit mass revealed the classical double-sigmoid growth pattern characteristic of stone fruit (Fig. 1A). The initial stage I is accompanied by a small increase in fruit mass due to cell division in the pericarp. During stage II, the endocarp and the embryo develop with little overall change in fruit mass. During stage III (also known as final swell), fruit mass increases rapidly due to cell expansion in the mesocarp (Lilleland and Newsome 1934; Tukey 1934) (Fig. 1A). Based on the changes in fruit mass and in skin color in ‘Hauszwetsche Wolff’, the stage I/II transition occurred at ≈55 DAFB, and the stage II/III transition at about 100 DAFB.

Fig. 1.
Fig. 1.

Time course of change in fruit mass (A), in skin color as indexed by the Hue angle (inset in A), in change in osmotic potential (ψΠ), in turgor (ψP) and in calculated water potential (ψ) in the stem end (B) and the stylar end (C) of ‘Hauszwetsche Wolff’ european plum. Arrows in (A) indicate the phase I/II and phase II/III transition. Insets in (B) and (C) represent the ψP redrawn on a different scale. Differences between the stem and stylar ends of the same fruit in their water potential (Δψ), and in their water potential components, osmotic potential (ΔψΠ) or turgor potential (ΔψP) (D). The Δ values were calculated by subtracting the stem end values of ψΠ, ψP, and ψ from their respective stylar end values. Because both ψ and ψΠ have negative signs, negative values for Δψ and ΔψΠ indicate that the stylar end of the fruit is more negative than the stem end. The number of replicates were as follows: 20 to 30 for mass and color, 8 to 10 for ψΠ, and 10 for turgor potential.

Citation: HortScience 57, 12; 10.21273/HORTSCI16883-22

The ψΠ value of the juice expressed from the stem end and stylar end regions generally decreased (become more negative) throughout fruit development. The rate of decrease was slower during stages I and II, but increased markedly during stage III (Fig. 1B,C). The values of ψP recorded either in the stem end or in the stylar end slightly increased to a maximum of ≈352 ± 42 kPa at 78 DAFB in the stem end and 313 ± 51 kPa at 92 DAFB in the stylar end region. Thereafter, the value of ψP decreased rapidly again during stage III and was the same in the stem end (22 ± 3 kPa) and the stylar end (22 ± 4 kPa) at maturity. The ψP values at maturity were negligibly low compared with the very negative values of ψΠ at the stylar (−3188 ± 73 kPa) and stem ends (−3060 ± 74 kPa). That is, numerically, ψP was only ≈0.7% of ψΠ, hence, the calculated value for ψ (where ψ = ψΠ + ψP) was essentially the same as that for ψΠ. Similar results were obtained for ‘Elena’ (data not shown). Neither ‘Hauszwetsche Wolff’ nor ‘Elena’ showed any symptoms of neck shriveling in the season in which these measurements were made. The ψΠ were in the same range as those reported earlier for plums (Grappadelli et al. 2019; Knoche et al. 2019; Winkler and Knoche 2018).

The low mean values for ψP, and the transient increase in ψP at the stage II/III transition, and the essential equivalence of ψΠ and ψ are not unique features of a developing plum. These three have also been reported for developing grapes (Thomas et al. 2006; Matthews et al. 2009) and sweet cherries (Knoche et al. 2014; Schumann et al. 2014). It is interesting that the transient increase in ψP in plums, in grapes, and in sweet cherries occurs when the phase of rapid solute import begins. The following explanation may be offered. The initial increase in ψP results from a more negative ψΠ at a constant ψ. The reason for the subsequent decrease in ψP while ψΠ keeps decreasing until maturity is not clear. A low value of ψP in fleshy fruits with very negative ψΠ is accounted for by an accumulation of apoplastic solutes (Wada et al. 2008, 2009). Apoplastic solutes decrease the gradient in ψΠ between symplast and apoplast, thereby decreasing turgor. Apoplastic solutes, in turn, may result from an apoplastic unloading of the phloem or a mismatch between phloem unloading and the loading of solutes into the cells. To our knowledge, there are no published studies on the mechanism of phloem unloading in european plum (for recent reviews see Falchi et al. 2020; Ma et al. 2019); however, in japanese plum (Prunus salicina L.) apoplastic and symplastic phloem unloading coexist (Grappadelli et al. 2019). In hybrid grape berries (Vitis vinifera ×Vitis labrusca L.), unloading of the phloem switches from symplastic to apoplastic unloading at or immediately before veraison, when the rapid accumulation of solutes begins (Zhang et al. 2006). If this also occurred in european plum, it would account for an accumulation of apoplastic solutes and the decrease in ψP while ψΠ decreases continuously until maturity.

Calculating the difference in the value of ψΠ between the stylar end and the stem end of the fruit revealed a transient gradient in ψΠ and ψ during stage II, but this rapidly disappeared. The gradient resulted from a more negative ψΠ at the stylar end that reflected an earlier accumulation of osmolytes in the stylar end, as compared with the stem end. This observation has also been reported for grapes and is explained by a basipetal wave of maturation and ripening: the stylar end being more advanced than the stem end (Castellarin et al. 2011). As in grape, maturation is apparently initiated in the stylar end of a plum. An additional factor could be the decrease in xylem functionality during stage III development that also occurs in european plum and this too progresses basipetally: the stylar end first, then toward the stem end (Khanal et al. 2021; Winkler and Knoche 2021). It is worth noting that there was no gradient in ψP between stylar end and stem end.

The cultivar comparison at maturity revealed marked differences in the values of ψΠ and their spatial distributions (Table 1). The most negative values of ψΠ were in ‘Hauszwetsche Wolff’ and ‘Topfive’, whereas the least negative ones were in ‘Katinka’ and ‘Lützelsachser’. In most cultivars, ψΠ was more negative at the stylar end of the fruit than at the stem end. In ‘Chrudiminer Zwetsche’, ‘Elena’ (site Ruthe), ‘Hauszwetsche Wolff’ (site Ruthe), ‘Hauszwetsche zum Felde’, ‘Katinka’, ‘Lützelsachser’, and ‘Oullins Reneclaude’ there were no significant gradients. A reverse gradient, where ψΠ in the stem end was more negative than in the stylar end, was measured in ‘Aprimira’, ‘Topfive’, and ‘Tophit’. The latter was also observed in our earlier study, particularly for fruit that suffered from neck shriveling (Knoche et al. 2019). It may therefore be hypothesized that a more negative ψΠ in the stem end could result from excessive transpiration leading to a concentration of the osmolytes in the stem end region of the fruit. The excessive transpiration, in turn, resulted from severe microcracking of the stem end that probably was causal in neck shrivel.

Table 1.

Distribution of osmotic potentials of expressed juice (ψΠ) of selected cultivars of european plum along the stem/stylar scar axis. The values of ψΠ represent the mean ψΠ of the fruit at maturity. The distribution ψΠ within the fruit is indexed as the gradient of ψΠ values in a series of tissue slices taken along the stem/stylar scar axis, minus the mean ψΠ of the same fruit. Four slices of equal thickness were cut perpendicular to the longitudinal axis of the fruit. These slices are termed stem end, stem end equatorial, stylar end equatorial, and stylar end, respectively. The slice ψΠ values were normalized by subtracting the fruit mean ψΠ from the ψΠ of the slice. The range of ψΠ within a fruit (ΔψΠ) of a cultivar was calculated as the difference in ψΠ value of the stylar end slice minus that of the stem end slice. The number of replicates was 8 to 10.

Table 1.

Based on the data in this and our earlier study, a direct role of gradients in ψP or ψΠ in neck shrivel is unlikely. First, based on our hypothesis, a flaccid stem end (low ψP) and a turgescent stylar end (high ψP) would account for neck shrivel. However, there is no evidence for a gradient in ψP between the stylar end and stem end region. Also, the ψP of mature fruit were negligibly low in both regions. Second, a gradient in ψΠ toward the stem end can be accounted for by excessive transpiration through microcracks. This gradient, however, is in the opposite direction as the one expected if the ψΠ was causal (Knoche et al. 2019). Third, the lack of symptomatic fruit in the present study demonstrates that a more negative ψΠ in the stylar end is not sufficient to dehydrate the stem end. If the stylar end was dehydrating the stem end, we would expect the ψP of the stylar end to be higher than that of the stem end. This, however, was not the case, indicating that hydraulic resistance of the flesh to water movement is significant. Unfortunately, in the season in which this study was conducted, there was no fruit with neck shriveling. Thus, it is inconclusive for this hypothesis that there was no significant correlation between the gradient in ψΠ of the fruit or absolute ψΠ and the occurrence of microcracks (Knoche, unpublished data).

It is interesting that for the three cultivars, ‘Cackaks Schöne’, ‘Elena’, and ‘Hauszwetsche Wolff’, obtained from two different sites, Ruthe and Wurzen, the fruit from Wurzen recorded more negative values of ψΠ and steeper gradients in ψΠ than those from Ruthe. These observations do demonstrate that site factors (soil, or management, or microenvironment, etc.) can affect gradients in ψΠ (Falchi et al. 2020).

Conclusion

Our results demonstrate that cell ψP is consistently low and is essentially independent of ψΠ in developing european plums. This observation aligns closely with nearly all fleshy fruit species so far investigated. As expected, ψΠ becomes increasingly negative during fruit development, the decrease being more rapid during stage III than during stages I and II. The absence of significant levels of ψP throughout fruit development means that the values of ψΠ and of ψ are closely similar numerically. There were no significant differences in ψP recorded between stylar end and stem end. In most cultivars examined here, ψΠ in the stylar end is more negative than in the stem end. The absence of an axial gradient in ψP and the small differences in ψΠ between the stem and stylar end make both factors unlikely candidates for explaining neck shrivel.

References

  • Castellarin, S.D., Gambetta, G.A., Wada, H., Shackel, K.A. & Matthews, M.A. 2011 Fruit ripening in Vitis vinifera: Spatiotemporal relationships among turgor, sugar accumulation, and anthocyanin biosynthesis J. Expt. Bot. 62 4345 4354 https://doi.org/10.1093/jxb/err150

    • Search Google Scholar
    • Export Citation
  • Falchi, R., Bonghi, C., Drincovich, M.F., Famiani, F., Lara, M.V., Walker, R.P. & Vizzotto, G. 2020 Sugar metabolism in stone fruit: Source-sink relationships and environmental and agronomical effects Front. Plant Sci. 11 573982 https://doi.org/10.3389/fpls.2020.573982

    • Search Google Scholar
    • Export Citation
  • Grappadelli, L.C., Morandi, B., Manfrini, L. & O’Connell, M. 2019 Apoplasmic and simplasmic phloem unloading mechanisms: Do they co-exist in Angeleno plums under demanding environmental conditions? J. Plant Physiol. 237 104 110 https://doi.org/10.1016/j.jplph.2019.04.005

    • Search Google Scholar
    • Export Citation
  • Khanal, B.P., Acharya, I. & Knoche, M. 2021 Progressive decline in xylem functionality in developing plums HortScience 56 1263 1268 https://doi.org/10.21273/HORTSCI16012-21

    • Search Google Scholar
    • Export Citation
  • Knoche, M., Grimm, E., Winkler, A., Alkio, M. & Lorenz, J. 2019 Characterizing neck shrivel in European Plum J. Amer. Soc. Hort. Sci. 144 38 44 https://doi.org/10.21273/JASHS04561-18

    • Search Google Scholar
    • Export Citation
  • Knoche, M., Grimm, E. & Schlegel, H.J. 2014 Mature sweet cherries have low turgor J. Amer. Soc. Hort. Sci. 139 3 12 https://doi.org/10.21273/JASHS.139.1.3

    • Search Google Scholar
    • Export Citation
  • Lilleland, O. & Newsome, L. 1934 A growth study of the cherry fruit Proc. Am. Soc. Hortic. Sci. 32 291 299

  • Ma, S., Li, Y., Li, X., Sui, X. & Zhang, Z. 2019 Phloem unloading strategies and mechanisms in crop fruits J. Plant Growth Regul. 38 494 500 https://doi.org/10.1007/s00344-018-9864-1

    • Search Google Scholar
    • Export Citation
  • Matthews, M.A., Thomas, T.R. & Shackel, K.A. 2009 Fruit ripening in Vitis vinifera L.: Possible relation of veraison to turgor and berry softening Aust. J. Grape Wine Res. 15 278 283 https://doi.org/10.1111/j.1755-0238.2009.00060.x

    • Search Google Scholar
    • Export Citation
  • Schumann, C., Schlegel, H.J., Grimm, E., Knoche, M. & Lang, A. 2014 Water potential and its components in developing sweet cherry J. Amer. Soc. Hort. Sci. 139 349 355 https://doi.org/10.21273/JASHS.139.4.349

    • Search Google Scholar
    • Export Citation
  • Steudle, E. 1993 Pressure probe techniques: Basic principles and application to studies of water and solute relations at the cell, tissue and organ level 5 36 Smith, J.A.C. & Griffiths, H. Water deficits: Plant responses from cell to community. Bios Scientific Publishers Oxford, UK

    • Search Google Scholar
    • Export Citation
  • Thomas, T.R., Matthews, M.A. & Shackel, K.A. 2006 Direct in situ measurement of cell turgor in grape (Vitis vinifera L.) berries during development and in response to plant water deficits Plant Cell Environ. 29 993 1001 https://doi.org/10.1111/j.1365-3040.2006.01496.x

    • Search Google Scholar
    • Export Citation
  • Tukey, H.B. 1934 Growth of the embryo, seed, and pericarp of the sour cherry (Prunus cerasus) in relation to season of fruit ripening Proc. Am. Soc. Hortic. Sci. 31 125 144

    • Search Google Scholar
    • Export Citation
  • Wada, H., Matthews, M.A. & Shackel, K.A. 2009 Seasonal pattern of apoplastic solute accumulation and loss of cell turgor during ripening of Vitis vinifera fruit under field conditions J. Expt. Bot. 60 1773 1781 https://doi.org/10.1093/jxb/erp050

    • Search Google Scholar
    • Export Citation
  • Wada, H., Shackel, K.A. & Matthews, M.A. 2008 Fruit ripening in Vitis vinifera: Apoplastic solute accumulation accounts for pre-veraison turgor loss in berries Planta 227 1351 1361 https://doi.org/10.1007/s00425-008-0707-3

    • Search Google Scholar
    • Export Citation
  • Winkler, A. & Knoche, M. 2018 Predicting osmotic potential from measurements of refractive index in cherries, grapes and plums PLoS One 13 11 E0207626 https://doi.org/10.1371/journal.pone.0207626

    • Search Google Scholar
    • Export Citation
  • Winkler, A. & Knoche, M. 2021 Xylem, phloem and transpiration flows in developing European plums PLoS One 16 5 E0252085 https://doi.org/10.1371/journal.pone.0252085

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  • Zhang, X.Y., Wang, X.L., Wang, X.F., Xia, G.H., Pan, Q.H., Fan, R.C., Wu, F.Q., Yu, X.C. & Zhang, D.P. 2006 A shift of phloem unloading from symplasmic to apoplasmic pathway is involved in developmental onset of ripening in grape berry Plant Physiol. 142 220 232 https://doi.org/10.1104/pp.106.081430

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  • Fig. 1.

    Time course of change in fruit mass (A), in skin color as indexed by the Hue angle (inset in A), in change in osmotic potential (ψΠ), in turgor (ψP) and in calculated water potential (ψ) in the stem end (B) and the stylar end (C) of ‘Hauszwetsche Wolff’ european plum. Arrows in (A) indicate the phase I/II and phase II/III transition. Insets in (B) and (C) represent the ψP redrawn on a different scale. Differences between the stem and stylar ends of the same fruit in their water potential (Δψ), and in their water potential components, osmotic potential (ΔψΠ) or turgor potential (ΔψP) (D). The Δ values were calculated by subtracting the stem end values of ψΠ, ψP, and ψ from their respective stylar end values. Because both ψ and ψΠ have negative signs, negative values for Δψ and ΔψΠ indicate that the stylar end of the fruit is more negative than the stem end. The number of replicates were as follows: 20 to 30 for mass and color, 8 to 10 for ψΠ, and 10 for turgor potential.

  • Castellarin, S.D., Gambetta, G.A., Wada, H., Shackel, K.A. & Matthews, M.A. 2011 Fruit ripening in Vitis vinifera: Spatiotemporal relationships among turgor, sugar accumulation, and anthocyanin biosynthesis J. Expt. Bot. 62 4345 4354 https://doi.org/10.1093/jxb/err150

    • Search Google Scholar
    • Export Citation
  • Falchi, R., Bonghi, C., Drincovich, M.F., Famiani, F., Lara, M.V., Walker, R.P. & Vizzotto, G. 2020 Sugar metabolism in stone fruit: Source-sink relationships and environmental and agronomical effects Front. Plant Sci. 11 573982 https://doi.org/10.3389/fpls.2020.573982

    • Search Google Scholar
    • Export Citation
  • Grappadelli, L.C., Morandi, B., Manfrini, L. & O’Connell, M. 2019 Apoplasmic and simplasmic phloem unloading mechanisms: Do they co-exist in Angeleno plums under demanding environmental conditions? J. Plant Physiol. 237 104 110 https://doi.org/10.1016/j.jplph.2019.04.005

    • Search Google Scholar
    • Export Citation
  • Khanal, B.P., Acharya, I. & Knoche, M. 2021 Progressive decline in xylem functionality in developing plums HortScience 56 1263 1268 https://doi.org/10.21273/HORTSCI16012-21

    • Search Google Scholar
    • Export Citation
  • Knoche, M., Grimm, E., Winkler, A., Alkio, M. & Lorenz, J. 2019 Characterizing neck shrivel in European Plum J. Amer. Soc. Hort. Sci. 144 38 44 https://doi.org/10.21273/JASHS04561-18

    • Search Google Scholar
    • Export Citation
  • Knoche, M., Grimm, E. & Schlegel, H.J. 2014 Mature sweet cherries have low turgor J. Amer. Soc. Hort. Sci. 139 3 12 https://doi.org/10.21273/JASHS.139.1.3

    • Search Google Scholar
    • Export Citation
  • Lilleland, O. & Newsome, L. 1934 A growth study of the cherry fruit Proc. Am. Soc. Hortic. Sci. 32 291 299

  • Ma, S., Li, Y., Li, X., Sui, X. & Zhang, Z. 2019 Phloem unloading strategies and mechanisms in crop fruits J. Plant Growth Regul. 38 494 500 https://doi.org/10.1007/s00344-018-9864-1

    • Search Google Scholar
    • Export Citation
  • Matthews, M.A., Thomas, T.R. & Shackel, K.A. 2009 Fruit ripening in Vitis vinifera L.: Possible relation of veraison to turgor and berry softening Aust. J. Grape Wine Res. 15 278 283 https://doi.org/10.1111/j.1755-0238.2009.00060.x

    • Search Google Scholar
    • Export Citation
  • Schumann, C., Schlegel, H.J., Grimm, E., Knoche, M. & Lang, A. 2014 Water potential and its components in developing sweet cherry J. Amer. Soc. Hort. Sci. 139 349 355 https://doi.org/10.21273/JASHS.139.4.349

    • Search Google Scholar
    • Export Citation
  • Steudle, E. 1993 Pressure probe techniques: Basic principles and application to studies of water and solute relations at the cell, tissue and organ level 5 36 Smith, J.A.C. & Griffiths, H. Water deficits: Plant responses from cell to community. Bios Scientific Publishers Oxford, UK

    • Search Google Scholar
    • Export Citation
  • Thomas, T.R., Matthews, M.A. & Shackel, K.A. 2006 Direct in situ measurement of cell turgor in grape (Vitis vinifera L.) berries during development and in response to plant water deficits Plant Cell Environ. 29 993 1001 https://doi.org/10.1111/j.1365-3040.2006.01496.x

    • Search Google Scholar
    • Export Citation
  • Tukey, H.B. 1934 Growth of the embryo, seed, and pericarp of the sour cherry (Prunus cerasus) in relation to season of fruit ripening Proc. Am. Soc. Hortic. Sci. 31 125 144

    • Search Google Scholar
    • Export Citation
  • Wada, H., Matthews, M.A. & Shackel, K.A. 2009 Seasonal pattern of apoplastic solute accumulation and loss of cell turgor during ripening of Vitis vinifera fruit under field conditions J. Expt. Bot. 60 1773 1781 https://doi.org/10.1093/jxb/erp050

    • Search Google Scholar
    • Export Citation
  • Wada, H., Shackel, K.A. & Matthews, M.A. 2008 Fruit ripening in Vitis vinifera: Apoplastic solute accumulation accounts for pre-veraison turgor loss in berries Planta 227 1351 1361 https://doi.org/10.1007/s00425-008-0707-3

    • Search Google Scholar
    • Export Citation
  • Winkler, A. & Knoche, M. 2018 Predicting osmotic potential from measurements of refractive index in cherries, grapes and plums PLoS One 13 11 E0207626 https://doi.org/10.1371/journal.pone.0207626

    • Search Google Scholar
    • Export Citation
  • Winkler, A. & Knoche, M. 2021 Xylem, phloem and transpiration flows in developing European plums PLoS One 16 5 E0252085 https://doi.org/10.1371/journal.pone.0252085

    • Search Google Scholar
    • Export Citation
  • Zhang, X.Y., Wang, X.L., Wang, X.F., Xia, G.H., Pan, Q.H., Fan, R.C., Wu, F.Q., Yu, X.C. & Zhang, D.P. 2006 A shift of phloem unloading from symplasmic to apoplasmic pathway is involved in developmental onset of ripening in grape berry Plant Physiol. 142 220 232 https://doi.org/10.1104/pp.106.081430

    • Search Google Scholar
    • Export Citation
Moritz Knoche Leibniz-Universität Hannover, Institut für Gartenbauliche Produktionssysteme, Abteilung Obstbau, Herrenhäuser Str. 2, D-30419 Hannover, Germany

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Eckhard Grimm Leibniz-Universität Hannover, Institut für Gartenbauliche Produktionssysteme, Abteilung Obstbau, Herrenhäuser Str. 2, D-30419 Hannover, Germany

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Contributor Notes

This research was funded in part by grant KN 402/20-1 from the Deutsche Forschungsgemeinschaft. The publication of this article was funded by the Open Access fund of the Leibniz Universität Hannover.

We thank Mrs. Anne Grund, Mr. Andreas Zschammer, and Dr. Erik Schulte of the Federal Plant Variety Office for the fruit samples; Mr. Rajesh Mehta and Mr. Simon Sitzenstock for technical help; and Drs. Andreas Winkler and Sandy Lang for helpful comments on an earlier version of this manuscript.

M.K. is the corresponding author. E-mail: moritz.knoche@obst.uni-hannover.de.

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  • Fig. 1.

    Time course of change in fruit mass (A), in skin color as indexed by the Hue angle (inset in A), in change in osmotic potential (ψΠ), in turgor (ψP) and in calculated water potential (ψ) in the stem end (B) and the stylar end (C) of ‘Hauszwetsche Wolff’ european plum. Arrows in (A) indicate the phase I/II and phase II/III transition. Insets in (B) and (C) represent the ψP redrawn on a different scale. Differences between the stem and stylar ends of the same fruit in their water potential (Δψ), and in their water potential components, osmotic potential (ΔψΠ) or turgor potential (ΔψP) (D). The Δ values were calculated by subtracting the stem end values of ψΠ, ψP, and ψ from their respective stylar end values. Because both ψ and ψΠ have negative signs, negative values for Δψ and ΔψΠ indicate that the stylar end of the fruit is more negative than the stem end. The number of replicates were as follows: 20 to 30 for mass and color, 8 to 10 for ψΠ, and 10 for turgor potential.

 

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