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

Research output: Contribution to journalArticleResearchpeer review

Authors

  • Jannis Straube
  • Shreya Suvarna
  • Yun Hao Chen
  • Bishnu P. Khanal
  • Moritz Knoche
  • Thomas Debener
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Details

Original languageEnglish
Article number457
JournalBMC plant biology
Volume23
Issue number1
Early online date30 Sept 2023
Publication statusPublished - Dec 2023

Abstract

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.

Keywords

    Cuticle, Fruit skin, Lignin, Malus x domestica, Periderm, Russeting, Suberin, Transcriptome, Wounding

ASJC Scopus subject areas

Cite this

Time course of changes in the transcriptome during russet induction in apple fruit. / Straube, Jannis; Suvarna, Shreya; Chen, Yun Hao et al.
In: BMC plant biology, Vol. 23, No. 1, 457, 12.2023.

Research output: Contribution to journalArticleResearchpeer review

Straube J, Suvarna S, Chen YH, Khanal BP, Knoche M, Debener T. Time course of changes in the transcriptome during russet induction in apple fruit. BMC plant biology. 2023 Dec;23(1):457. Epub 2023 Sept 30. doi: 10.1186/s12870-023-04483-6
Straube, Jannis ; Suvarna, Shreya ; Chen, Yun Hao et al. / Time course of changes in the transcriptome during russet induction in apple fruit. In: BMC plant biology. 2023 ; Vol. 23, No. 1.
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title = "Time course of changes in the transcriptome during russet induction in apple fruit",
abstract = "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 {\textquoteleft}Pinova{\textquoteright} 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.",
keywords = "Cuticle, Fruit skin, Lignin, Malus x domestica, Periderm, Russeting, Suberin, Transcriptome, Wounding",
author = "Jannis Straube and Shreya Suvarna and Chen, {Yun Hao} and Khanal, {Bishnu P.} and Moritz Knoche and Thomas Debener",
note = "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 Schr{\"o}ter 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.). ",
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Download

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

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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 -

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