Ethylene negatively regulates transcript abundance of ROP-GAP rheostat-encoding genes and affects apoplastic reactive oxygen species homeostasis in epicarps of cold stored apple fruits

Zermiani, Monica; Zonin, Elisabetta; Nonis, Alberto; Begheldo, Maura; Ceccato, Luca; Vezzaro, Alice; Baldan, Barbara; Trentin, Anna Rita; Masi, Antonio; Pegoraro, Mattia; Fadanelli, L.; Teale, William; Palme, Klaus; Quintieri, Luigi; Ruperti, Benedetto

doi:10.1093/jxb/erv422

Cited by 30 publications

(35 citation statements)

References 88 publications

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“…The skin of the control samples was characterized by the highest accumulation of phenols with antioxidant activity (such as chlorogenic acid, epicatechin, procyanidin and quercetin). These compounds have been proposed to provide a protective system activated by the fruit to prevent the accumulation of reactive oxygen species (ROS; Rao et al ., ; Pesis et al ., ; Zermiani et al ., ). Phenolic compounds are thought to be produced to scavenge the free radicals released by the oxidation of lipids in cell membranes during cold stress (Di Meo et al ., ).…”

Section: Discussionmentioning

confidence: 97%

“…Phenolic compounds are thought to be produced to scavenge the free radicals released by the oxidation of lipids in cell membranes during cold stress (Di Meo et al ., ). To this end, we note that apoplastic ROS homeostasis can be disrupted by the disruptive effect that ethylene has on the ROP‐GAP rheostat mechanism (Zermiani et al ., ). Among the phenolic compounds accumulating during scald development, the most abundant is chlorogenic acid.…”

Section: Discussionmentioning

confidence: 97%

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Apple fruit superficial scald resistance mediated by ethylene inhibition is associated with diverse metabolic processes

et al. 2017

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Fruits stored at low temperature can exhibit different types of chilling injury. In apple, one of the most serious physiological disorders is superficial scald, which is characterized by discoloration and brown necrotic patches on the fruit exocarp. Although this phenomenon is widely ascribed to the oxidation of α-farnesene, its physiology is not yet fully understood. To elucidate the mechanism of superficial scald development and possible means of prevention, we performed an integrated metabolite screen, including an analysis of volatiles, phenols and lipids, together with a large-scale transcriptome study. We also determined that prevention of superficial scald, through the use of an ethylene action inhibitor, is associated with the triggering of cold acclimation-related processes. Specifically, the inhibition of ethylene perception stimulated the production of antioxidant compounds to scavenge reactive oxygen species, the synthesis of fatty acids to stabilize plastid and vacuole membranes against cold temperature, and the accumulation of the sorbitol, which can act as a cryoprotectant. The pattern of sorbitol accumulation was consistent with the expression profile of a sorbitol 6-phosphate dehydrogenase, MdS6PDH, the overexpression of which in transgenic Arabidopsis thaliana plants confirmed its involvement in the cold acclimation and freezing tolerance.

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Section: Discussionmentioning

confidence: 97%

Section: Discussionmentioning

confidence: 97%

Apple fruit superficial scald resistance mediated by ethylene inhibition is associated with diverse metabolic processes

et al. 2017

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“…During the development of scald, the skin of the untreated (CT) samples was characterized by the largest polyphenol accumulation (Fig. 8c), compounds tentatively protecting the fruit against the accumulation of reactive oxygen species (ROS) [49][50][51] . Among the range of phenolic antioxidants, chlorogenic acid is present at relatively high concentrations in pear skin.…”

Section: The Role Of Antioxidants In the Prevention Of Superficial Scaldmentioning

confidence: 99%

Investigation of the transcriptomic and metabolic changes associated with superficial scald physiology impaired by lovastatin and 1-methylcyclopropene in pear fruit (cv. “Blanquilla”)

et al. 2020

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To elucidate the physiology underlying the development of superficial scald in pears, susceptible "Blanquilla" fruit was treated with different compounds that either promoted (ethylene) or repressed (1-methylcyclopropene and lovastatin) the incidence of this disorder after 4 months of cold storage. Our data show that scald was negligible for the fruit treated with 1-methylcyclopropene or lovastatin, but highly manifested in untreated (78% incidence) or ethylenetreated fruit (97% incidence). The comparison between the fruit metabolomic profile and transcriptome evidenced a distinct reprogramming associated with each treatment. In all treated samples, cold storage led to an activation of a cold-acclimation-resistance mechanism, including the biosynthesis of very-long-chain fatty acids, which was especially evident in 1-methylcyclopropane-treated fruit. Among the treatments applied, only 1-methylcyclopropene inhibited ethylene production, hence supporting the involvement of this hormone in the development of scald. However, a common repression effect on the PPO gene combined with higher sorbitol content was found for both lovastatin and 1-methylcyclopropene-treated samples, suggesting also a non-ethylene-mediated process preventing the development of this disorder. The results presented in this work represent a step forward to better understand the physiological mechanisms governing the etiology of superficial scald in pears.

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“…qPCR is used to verify that, generally, the estimates of gene expression are concordant between the two technologies. This ranges from excellent correlations of R 2 > 0.9 for genes of interest (Honaas et al, 2016;Zermiani et al, 2015) to nonmathematical visualization meant to show concordance (Busatto et al, 2018). Here, we show that disagreement may simply result from misidentification of the corresponding homologous gene, but we note that it is also variable from gene to gene.…”

Section: Discussionmentioning

confidence: 55%

Leveraging Transcriptome Data for Enhanced Gene Expression Analysis in Apple

Hargarten¹,

Waliullah²,

Kalcsits³

et al. 2018

J. Amer. Soc. Hort. Sci.

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Complex changes in gene expression occur during postharvest storage of apple (Malus ×domestica) and often precede or accompany changes in ripening and disorder development. Targeted gene expression analysis fundamentally relies on previous knowledge of the targeted gene. Minimally, a substantial fragment of the gene sequence must be known with high accuracy so that primers and probes, which bind to their targets in a complimentary fashion, are highly specific. Here, we describe a workflow that leverages publicly available transcriptome data to discover apple cultivar–specific gene sequences to guide primer design for quantitative real-time polymerase chain reaction (qPCR). We find that problematic polymorphisms occur frequently in ‘Granny Smith’ and ‘Honeycrisp’ apple when candidate primer binding sites were selected using the ‘Golden Delicious’ genome. We attempted to validate qPCR-based gene expression measurements with RNA sequencing (RNA-Seq) analysis of the same RNA samples. However, we found that agreement between the two technologies was highly variable and positively correlated with the similarity between cultivar-specific genes and RNA-Seq reference genes. Thus, we offer insight that 1) improves the accuracy and efficiency of qPCR primer design in cultivars that lack sufficient sequence resources and 2) better guides the essential step of validation of RNA-Seq data with a subset of genes of interest examined via qPCR.

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Ethylene negatively regulates transcript abundance of ROP-GAP rheostat-encoding genes and affects apoplastic reactive oxygen species homeostasis in epicarps of cold stored apple fruits

Abstract: HighlightIn cold-stressed apple skins, the ethylene-dependent negative regulation of ROP-GAP rheostat transcripts and apoplastic H2O2 homeostasis suggests an unprecedented putative crosstalk between ROS and ethylene in abiotic stress.

Cited by 30 publications

References 88 publications

Apple fruit superficial scald resistance mediated by ethylene inhibition is associated with diverse metabolic processes

Apple fruit superficial scald resistance mediated by ethylene inhibition is associated with diverse metabolic processes

Investigation of the transcriptomic and metabolic changes associated with superficial scald physiology impaired by lovastatin and 1-methylcyclopropene in pear fruit (cv. “Blanquilla”)

Leveraging Transcriptome Data for Enhanced Gene Expression Analysis in Apple

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