TY - JOUR

T1 - Time course of changes in the transcriptome during russet induction in apple fruit

AU - Straube, Jannis

AU - Suvarna, Shreya

AU - Chen, Yun Hao

AU - Khanal, Bishnu P.

AU - Knoche, Moritz

AU - Debener, Thomas

N1 - Funding Information: We are very grateful for advice and support from Diana Carolina Lopez Aria in the analysis of the RNA-Seq data as well as for the technical support from Julia Schröter and Simon Sitzenstock. We also thank Henryk Straube for helpful comments on an earlier version of the manuscript. Funding Information: Open Access funding enabled and organized by Projekt DEAL. This research was funded by the following grants from the German Science Foundation (DFG): DE 511/9 − 1; DE 511/9 − 2 (T.D.) and KN402/15 − 1; KN402/15 − 2 (M.K.).

PY - 2023/12

Y1 - 2023/12

N2 - 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.

AB - 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.

KW - Cuticle

KW - Fruit skin

KW - Lignin

KW - Malus x domestica

KW - Periderm

KW - Russeting

KW - Suberin

KW - Transcriptome

KW - Wounding

UR - http://www.scopus.com/inward/record.url?scp=85173564228&partnerID=8YFLogxK

U2 - 10.1186/s12870-023-04483-6

DO - 10.1186/s12870-023-04483-6

M3 - Article

C2 - 37775771

AN - SCOPUS:85173564228

VL - 23

JO - BMC plant biology

JF - BMC plant biology

SN - 1471-2229

IS - 1

M1 - 457

ER -