Comparative transcriptome and metabolite survey reveal key pathways involved in the control of the chilling injury disorder superficial scald in two apple cultivars, ‘Granny Smith’ and ‘Ladina’

Abstract

The low temperature normally applied to prevent fruit decay during the storage of apples, can also triggers the onset of a chilling injury disorder known as superficial scald. In this work, the etiology of this disorder and the mechanism of action of two preventing strategies, such as the application of 1-MCP (1-methylcyclopropene) and storage at low oxygen concentration in ‘Granny Smith’ and ‘Ladina’ apple cultivars were investigated. The metabolite assessment highlighted a reorganization of specific metabolites, in particular flavan-3-ols and unsaturated fatty acids, while the genome-wide transcriptomic analysis grouped the DEGs into four functional clusters. The KEGG pathway and GO enrichment analysis, together with the gene-metabolite interactome, showed that the treatment with 1-MCP prevented the development of superficial scald by actively promoting the production of unsaturated fatty acids, especially in ‘Granny Smith’. ‘Ladina’, more susceptible to superficial scald and less responsive to the preventing strategies, was instead characterized by a higher accumulation of very long chain fatty acids. Storage at low oxygen concentration stimulated a higher accumulation of ethanol and acetaldehyde together with the expression of genes involved in anaerobic respiration, such as malate, alcohol dehydrogenase and pyruvate decarboxylase in both cultivars. Low oxygen concentration, likewise 1-MCP, through a direct control on ethylene prevented the onset of superficial scald repressing the expression of PPO, a gene encoding for the polyphenol oxidase enzyme responsible of the oxidation of chlorogenic acid. Moreover, in ‘Granny Smith’ apple, the expression of three members of the VII subgroups of ERF genes, encoding for elements coordinating the acclimation process to hypoxia in plants was observed. The global RNA-Seq pattern also elucidated a specific transcriptomic signature between the two cultivars, disclosing the effect of the different genetic background in the control of this disorder.

Dissecting postharvest chilling injuries in pome and stone fruit through integrated omics

“…Lately, CI has been associated with fatty acid metabolism. Vittani et al. (2023) detected an enrichment of genes participating in fatty acid metabolism, particularly related to jasmonates.…”

“…The integration of “omics” approaches with biochemical parameters of CI allow to highlight certain metabolic pathways that have been correlated with CI, such as the farnesene (FAR) pathway ( Karagiannis et al., 2018 ; Lindo-García et al., 2020 ; Marc et al., 2020 ; He et al., 2022 ; Vittani et al., 2023 ), the ethylene pathway ( Wei et al., 2019 ; Karagiannis et al., 2020 ; Koushesh Saba and Watkins, 2020 ), the phenylpropanoid pathway ( Gapper et al., 2017 ; Koushesh Saba and Watkins, 2020 ; Marc et al., 2020 ; Busatto et al., 2021 ; He et al., 2022 ; Vittani et al., 2023 ; Zhang C. et al., 2023 ) and the fatty acid metabolism pathway ( Giné-Bordonaba et al., 2020 ; Busatto et al., 2021 ; Vittani et al., 2023 ; Zhang C. et al., 2023 ).…”

“…Many studies have linked the FAR pathway with CI. According to Vittani et al. (2023) , apples (Ladina and Granny Smith varieties) stored at low temperature were enriched in the pathway of farnesyl diphosphate, an α-FAR precursor.…”

“…As far as secondary metabolism is concerned, phenylpropanoids, a class of compounds produced from the amino acid phenylalanine acting as signal molecules both in plant development and defense ( Dixon et al., 2002 ), have been claimed to play a role in CI. Vittani et al. (2023) determined by transcriptomic analysis that CI susceptible apples (Ladina and Granny Smith) stored at low temperature were enriched for the expression of genes of the biosynthetic pathway of phenylpropanoids.…”

“…(2023) demonstrated that flavonoids (particularly kaempferol-3-O-sambubioside and luteolin-7-O-(6′-malonyl) glucoside) were more accumulated in tolerant pears and were responsible for the main differences observed between tolerant and susceptible phenotypes. Additionally, metabolome analyses pointed out high concentrations of catechin, epicatechin, and procyanidin in apples showing tolerance to CI ( Vittani et al., 2023 ). These compounds are polyphenols able to prevent oxidation, and their presence has been associated with a decrease in oxidative stress ( Fraga and Oteiza, 2011 ).…”