Localized bursting of mesocarp cells triggers catastrophic fruit cracking

Abstract

The so-called rain-cracking of sweet cherry fruit severely threatens commercial production. Simple observation tells us that cuticular microcracking (invisible) always precedes skin macrocracking (visible). The objective here was to investigate how a macrocrack develops. Incubating detached sweet cherry fruit in deionized water induces microcracking. Incubating fruit in D 2 O and concurrent magnetic resonance imaging demonstrates that water penetration occurs only (principally) through the microcracks, with nondetectable amounts penetrating the intact cuticle. Optical coherence tomography of detached, whole fruit incubated in deionized water, allowed generation of virtual cross-sections through the zone of a developing macrocrack. Outer mesocarp cell volume increased before macrocracks developed but increased at a markedly higher rate thereafter. Little change in mesocarp cell volume occurred in a control zone distant from the crack. As water incubation continued, the cell volume in the crack zone decreased, indicating leaking/bursting of individual mesocarp cells. As incubation continued still longer, the crack propagated between cells both to form a long, deep macrocrack. Outer mesocarp cell turgor did not differ significantly before and after incubation between fruit with or without macrocracks; nor between cells within the crack zone and those in a control zone distant from the macrocrack. The cumulative frequency distribution of the log-transformed turgor pressure of a population of outer mesocarp cells reveals all cell turgor data followed a normal distribution. The results demonstrate that microcracks develop into macrocracks following the volume increase of a few outer mesocarp cells and is soon accompanied by cell bursting.

Swelling of cell walls in mature sweet cherry fruit: factors and mechanisms

“…The maximum thickness (upper asymptote) was calculated as the average cell wall thickness of all treatments with fully swollen cell walls (without turgor, 5.8 ± 0.2 µm), the minimum thickness (lower asymptote) as the average thickness of all treatments with non-swollen cell walls (with turgor, 2.7 ± 0.1 µm). The regression equation for the relationship between the percentage of plasmolyzed cells and the osmotic potential was: First, the magnitude of the pressure generated by extracted cell wall material and the turgor pressure in mature sweet cherry parenchyma cells are of the same order of magnitude (Knoche et al 2014;Schumann et al 2014;Grimm et al 2019). Hence, it is plausible that cell turgor balances and (and thus prevents) cell wall swelling in turgid cells.…”

“…The 'zipper' hypothesis offers an alternative understanding that remains consistent with the general phenomenological observations-cracking is associated with rain/dewwetted fruit skin-but is also consistent with a new body of careful experimental data which does not align well with the 'critical turgor/strain' hypothesis (Knoche and Winkler 2017). Cracking is now considered to be a multistep process comprising: (i) the formation of microcracks due to cuticular strain caused by downregulation of cutin and wax synthesis and deposition during early growth (Knoche et al 2004;Peschel and Knoche 2005;Alkio et al 2012) and the later exposure of the strained cuticle to wetness (Knoche and Peschel 2006), (ii) localized water penetration through microcracks (Winkler et al 2016), (iii) the bursting of individual mesocarp cells and the consequent leakage of malic acid into the cell-wall-free space that further damages adjacent cells including those of the epidermis (Winkler et al 2015;Grimm et al 2019), and (iv) the complete loss of the (already low) turgor that results in cell wall swelling (Grimm and Knoche 2015). Lastly, cell wall swelling decreases cell wall stiffness, fracture tension and cell:cell adhesion resulting in the separation of neighboring cells (Brüggenwirth and Knoche 2017).…”

“…The tension generated by the skin strain is sufficient to cause cells to separate along their swollen walls and to rupture the skin. Thus, the skin 'unzips'-that is, starting from a single-point failure, a skin crack propagates linearly in a manner similar to the opening up of a garment with a 'zipper' and somewhat analogous to the propagation of a 'ladder' in a piece of knitted fabric (Grimm et al 2019). Based on the 'zipper' hypothesis, the swelling of cell walls is an essential part of the decrease in the fracture stress and in cell:cell adhesion.…”

Spatial heterogeneity of flesh-cell osmotic potential in sweet cherry affects partitioning of absorbed water

“…The OCT system used was as described previously 28 . Briefly, the OCT comprised a lens (LSM03-BB; Thorlabs, NJ, USA), a pair of galvanometer scanning mirrors (6210 H; Cambridge Technology, MA, USA), a superluminescent diode having a central wave length of 835 nm (BLMS-mini-351-HP2-SM-I; Superlum Diodes, Ireland) and a long-range spectrometer (Cobra UDC, Wasatch Photonics, NC, USA).…”

“…The stylar scar region of each fruit was scanned individually, before the next cycle was initiated. Data were analysed as described previously 28 . Regions of interest (ROI) were selected in a location of the fruit that: (1) remained free of visible cracks throughout the 6 h incubation period and where (2) the cell walls were clearly visible in all planes.…”