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

Abstract

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.

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

“…The efficacy of 1-MCP was initially assigned to its role in reducing α-farnesene production by downregulating the expression of the α-farnesene synthase 1 gene (AFS1). However, recent findings 3,8 support that 1-MCP protects apples from developing scald not only by inhibiting ethylene-related physiological processes, but also by stimulating complex cold-acclimation reactions within the fruit. For instance, 1-MCP induced the expression of the sorbitol-6phosphate dehydrogenase 8 , a key element in the production of the cryoprotectant compound sorbitol 16 .…”

“…Symptoms of superficial scald are consistent among most susceptible varieties of pome fruit, and shown as brown-dark patches on the fruit skin, resulting from the necrosis of the epidermis and hypodermal cortical tissues 1,3 . While the molecular and physiological mechanisms underlying scald in apples have been largely studied over the past few years 2,3,[6][7][8] , scarce information is available regarding this disorder in pears. The most accepted theory for scald development focuses on the auto-oxidation of the acylic sesquiterpene α-farnesene into conjugate trienols (CTols), which leads to the production and release of the ketone 6methyl-5-hepten-2-one 4,[9][10][11] .…”

“…Nevertheless, the physiological basis of scald has been recently revisited, suggesting complex metabolic changes being involved in the development of the disorder. Among them, the oxidation of chlorogenic acid by the enzyme polyphenol oxidase (PPO) was one of the most important process correlated to the development of the scald symptoms 3,8 . Storage at low temperature can compromise the integrity of the cellular organelles' internal membranes, promoting the reaction between PPO (stored in the plastid) and chlorogenic acid (stored in the vacuole), leading to the production of quinones and melanin, which finally leads to the dark-discolored areas on the fruit skin.…”

Pre-harvest climate and post-harvest acclimation to cold prevent from superficial scald development in Granny Smith apples

“…It was shown that in addition to reduced ethylene and α-farnesene production, 1-MCP also reduced the accumulation of reactive oxygen species (ROS) in fruit peel, probably by promoting cell-membrane integrity 6 . Further studies revealed that 1-MCP stimulates the production of ROS scavengers, synthesis of fatty acids that could stabilize plastid and vacuole membranes against cold, and the accumulation of sorbitol that can act as a cryoprotectant 7 . In the proposed model, ROS production in response to cold stress plays a central role in scald development by disrupting membrane integrity and promoting the accumulation of phenolic compounds.…”

“…Although superficial scald was intensively studied for several years, its molecular or biochemical determinism was mainly analysed after long time cold storage during symptom development 3,9 , or under 1-MCP or DPA treatments 4,7,8,[10][11][12] . Thus, early determinisms linked to the pre-harvest conditions, in particular to climate or fruit maturity stages remain poorly understood.…”