Low Temperature Storage Stimulates Fruit Softening and Sugar Accumulation Without Ethylene and Aroma Volatile Production in Kiwifruit

Abstract

Fruit ripening in response to propylene (an ethylene analog), 1-methylcyclopropene (1-MCP, an ethylene action inhibitor), and low temperature (5°C) treatments was characterized in “Kosui” kiwifruit ( Actinidia rufa × A. chinensis ). Propylene treatment induced ethylene production, with increased expression levels of 1-aminocyclopropane-1-carboxylic acid ( ACC ) synthase 1 ( AcACS1 ) and ACC oxidase 2 ( AcACO2 ), and rapid fruit softening together with increased expression levels of polygalacturonase ( AcPG ) and expansin 1 ( AcEXP1 ) within 5 days (d). Fruit soluble solids concentration (SSC) and contents of sucrose, glucose, and fructose together with the expression levels of β-amylase 1 ( Acβ-AMY1 ), Acβ-AMY2 , and invertase ( AcINV3-1 ) increased rapidly after 5 d exposure to propylene. Furthermore, propylene exposure for 5 d was sufficient to induce the production of key aroma volatile compounds, ethyl- and methyl butanoate, accompanied with increased expression levels of alcohol acyl transferase ( AcAAT ). Application of 1-MCP at the start of the experiment, followed by continuous exposure to propylene, significantly delayed fruit softening, changes in SSC and sugars, and strongly suppressed the production of ethylene, aroma volatiles, and expression of associated genes. During storage, fruit softening, SSC and sugar increase, and increased expression of genes associated with cell wall modification and carbohydrate metabolism were registered without detectable ethylene production; however, these changes occurred faster at 5°C compared to 22°C. Interestingly, ethyl and methyl butanoate as well as AcAAT expression were undetectable in kiwifruit during storage, while they were rescued by post-storage propylene exposure, indicating that the production of aroma volatile compounds is strongly ethylene-dependent. Transcript levels of a NAC-related transcription factor (TF), AcNAC3 , increased in response to both propylene and low temperature treatments, while AcNAC5 was exclusively up-regulated by propylene. By contrast, transcript levels of a MADS-box TF, AcMADS2 , exclusively increased in response to low temperature. The above findings indicate that kiwifruit ripening is inducible by either ethylene or low temperature signals. However, fruit ripened by low temperature were deficient in ethylene-dependent aroma volatiles, suggesting that ethylene signaling is non-functional during low temperature-modulated ripening in kiwifruit. These data provide further evidence that ethylene-dependent a...

Low temperature transcriptionally modulates natural peel degreening in lemon (Citrus limon L.) fruit independently of endogenous ethylene

“…The regulation of fruit ripening by low temperature is not unique to citrus fruit. Previous studies have also demonstrated a role for low temperature, either independently or in concert with ethylene, in the regulation of fruit ripening in multiple fruit species such as kiwifruit (Mworia et al ., 2012; Asiche et al ., 2017; Asiche et al ., 2018; Mitalo et al, 2018a; Mitalo et al ., 2019a; Mitalo et al ., 2019b), pears (El-Sharkawy et al, 2003; Mitalo et al ., 2019c) and apples (Tacken et al ., 2010). From an ecological perspective, the primary purpose of fruit ripening is to make fruit attractive to seed-dispersing organisms.…”

“…However, promotion of fruit ripening by low temperature has been described in various fruit species such as kiwifruit (Kim et al ., 1999; Mworia et al ., 2012; Asiche et al ., 2017; Mitalo et al ., 2018a), European pears (El-Sharkawy et al ., 2003; Nham et al ., 2017), and apples (Tacken et al ., 2010). Recently, transcriptome studies have suggested that low temperature-specific genes might have regulatory roles during fruit ripening in kiwifruit (Asiche et al ., 2018; Mitalo et al ., 2018b; Mitalo et al ., 2019a; Mitalo et al ., 2019b) and European pears (Mitalo et al ., 2019c).…”

Transcriptome co-expression network analysis identifies key genes and regulators of ripening kiwifruit ester biosynthesis

“…It was suggested that the accumulation of esters during ripening were likely driven by ethylene [8,12]. The production of esters, especially ethyl butanoate and methyl butanoate, appeared to be strongly dependent on ethylene signal [3]. Additionally, in ethylene-suppressed transgenic lines kiwifruit, esters were dramatically reduced, while the major volatiles produced in ethylene-unsuppressed fruit were ethyl butanoate, methyl butanoate, and ethyl acetate [4].…”

“…Aroma, together with sweetness and acidity generate the unique flavor of kiwifruit. The production of aroma volatile compounds is strongly ethylene-dependent [3]. In ethylene-suppressed kiwifruit, fruit softening was significantly delayed and aroma volatile production was dramatically reduced, which could be re-initiated by application of exogenous ethylene [4].…”

“…In persimmon fruit, the ERFs could regulate the ADH promoter and might be key components in persimmon fruit astringency removal [19]. In kiwifruit, AcNAC5 increased significantly in response to propylene and showed correlation with aroma volatile production patterns, suggesting its potential role in the regulation of AcAAT and aroma volatile biosynthesis during ripening [3]; However, such findings only hint at the potential of TFs in ester related pathway regulation, and role of these ERFs and other TFs on esters biosynthesis remains unclear. In our previous research, three major ripening traits in kiwifruit, including texture, ethylene production and starch degradation were analyzed and a range of ethylene responsive TFs were identified [20].…”