Russeting (periderm formation) is a critical fruit-surface disorder in apple (Malus × domestica Borkh.). The first symptom of insipient russeting is cuticular microcracking. Humid and rainy weather increases russeting. The aim was to determine the ontogeny of moisture-induced russeting in ‘Pinova’ apple. We recorded the effects of duration of exposure to water and the stage of fruit development at exposure on microcracking, periderm formation and cuticle deposition. Early on (21 or 31 days after full bloom; DAFB) short periods (2 to 12 d) of moisture exposure induced cuticular microcracking—but not later on (66 or 93 DAFB). A periderm was not formed during moisture exposure but 4 d after exposure ended. A periderm was formed in the hypodermis beneath a microcrack. Russeting frequency and severity were low for up to 4 d of moisture exposure but increased after 6 d. Cuticle thickness was not affected by moisture for up to 8 d but decreased for longer exposures. Cuticular ridge thickness decreased around a microcrack. In general, moisture did not affect cuticular strain release. We conclude that a hypodermal periderm forms after termination of moisture exposure and after microcrack formation. Reduced cuticle deposition may cause moisture-induced microcracking and, thus, russeting.

Exposure of the fruit surface to moisture during early development is causal in russeting of apple (Malus × domestica Borkh.). Moisture exposure results in formation of microcracks and decreased cuticle thickness. Periderm differentiation begins in the hypodermis, but only after discontinuation of moisture exposure. Expressions of selected genes involved in cutin, wax and suberin synthesis were quantified, as were the wax, cutin and suberin compositions. Experiments were conducted in two phases. In Phase I (31 days after full bloom) the fruit surface was exposed to moisture for 6 or 12 d. Phase II was after moisture exposure had been discontinued. Unexposed areas on the same fruit served as unexposed controls. During Phase I, cutin and wax synthesis genes were down-regulated only in the moisture-exposed patches. During Phase II, suberin synthesis genes were up-regulated only in the moisture-exposed patches. The expressions of cutin and wax genes in the moisture-exposed patches increased slightly during Phase II, but the levels of expression were much lower than in the control patches. Amounts and compositions of cutin, wax and suberin were consistent with the gene expressions. Thus, moisture-induced russet is a two-step process: moisture exposure reduces cutin and wax synthesis, moisture removal triggers suberin synthesis.

Background: Russeting is a major problem in many fruit crops. Russeting is caused by environmental factors such as wounding or moisture exposure of the fruit surface. Despite extensive research, the molecular sequence that triggers russet initiation remains unclear. Here, we present high-resolution transcriptomic data by controlled russet induction at very early stages of fruit development. During Phase I, a patch of the fruit surface is exposed to surface moisture. For Phase II, moisture exposure is terminated, and the formerly exposed surface remains dry. We targeted differentially expressed transcripts as soon as 24 h after russet induction. Results: During moisture exposure (Phase I) of ‘Pinova’ apple, transcripts associated with the cell cycle, cell wall, and cuticle synthesis (SHN3) decrease, while those related to abiotic stress increase. NAC35 and MYB17 were the earliest induced genes during Phase I. They are therefore linked to the initial processes of cuticle microcracking. After moisture removal (Phase II), the expression of genes related to meristematic activity increased (WOX4 within 24 h, MYB84 within 48 h). Genes related to lignin synthesis (MYB52) and suberin synthesis (MYB93, WRKY56) were upregulated within 3 d after moisture removal. WOX4 and AP2B3 are the earliest differentially expressed genes induced in Phase II. They are therefore linked to early events in periderm formation. The expression profiles were consistent between two different seasons and mirrored differences in russet susceptibility in a comparison of cultivars. Furthermore, expression profiles during Phase II of moisture induction were largely identical to those following wounding. Conclusions: The combination of a unique controlled russet induction technique with high-resolution transcriptomic data allowed for the very first time to analyse the formation of cuticular microcracks and periderm in apple fruit immediately after the onset of triggering factors. This data provides valuable insights into the spatial-temporal dynamics of russeting, including the synthesis of cuticles, dedifferentiation of cells, and impregnation of cell walls with suberin and lignin.