Comparative transcriptome analysis reveals distinct ethylene–independent regulation of ripening in response to low temperature in kiwifruit

Abstract

BackgroundKiwifruit are classified as climacteric since exogenous ethylene (or its analogue propylene) induces rapid ripening accompanied by ethylene production under positive feedback regulation. However, most of the ripening–associated changes (Phase 1 ripening) in kiwifruit during storage and on–vine occur largely in the absence of any detectable ethylene. This ripening behavior is often attributed to basal levels of system I ethylene, although it is suggested to be modulated by low temperature.ResultsTo elucidate the mechanisms regulating Phase 1 ripening in kiwifruit, a comparative transcriptome analysis using fruit continuously exposed to propylene (at 20 °C), and during storage at 5 °C and 20 °C was conducted. Propylene exposure induced kiwifruit softening, reduction of titratable acidity (TA), increase in soluble solids content (SSC) and ethylene production within 5 days. During storage, softening and reduction of TA occurred faster in fruit at 5 °C compared to 20 °C although no endogenous ethylene production was detected. Transcriptome analysis revealed 3761 ripening–related differentially expressed genes (DEGs), of which 2742 were up–regulated by propylene while 1058 were up–regulated by low temperature. Propylene exclusively up–regulated 2112 DEGs including those associated with ethylene biosynthesis and ripening such as AcACS1, AcACO2, AcPL1, AcXET1, Acβ–GAL, AcAAT, AcERF6 and AcNAC7. Similarly, low temperature exclusively up–regulated 467 DEGS including AcACO3, AcPL2, AcPMEi, AcADH, Acβ–AMY2, AcGA2ox2, AcNAC5 and AcbZIP2 among others. A considerable number of DEGs such as AcPG, AcEXP1, AcXET2, Acβ–AMY1, AcGA2ox1, AcNAC6, AcMADS1 and AcbZIP1 were up–regulated by either propylene or low temperature. Frequent 1–MCP treatments failed to inhibit the accelerated ripening and up–regulation of associated DEGs by low temperature indicating that the changes were independent of ethylene. On–vine kiwifruit ripening proceeded in the absence of any detectable endogenous ethylene production, and coincided with increased expression of low temperature–responsive DEGs as well as the decrease in environmental temperature.ConclusionsThese results indicate that kiwifruit possess both ethylene−dependent and low temperature–modulated ripening mechanisms that are distinct and independent of each other. The current work provides a foundation for elaborating the control of these two ripening mechanisms in kiwifruit.Electronic supplementary materialThe online version of this article (10.1186/s12870-018-1264-y) contains supplementary material, which is available to authorized users.

Low temperature modulates natural peel degreening in lemon fruit independently of endogenous ethylene

“…The regulation of fruit ripening by low temperature is not unique to citrus fruit. Previous studies have also demonstrated its role, either independently or in concert with ethylene, in the regulation of fruit ripening in various species such as kiwifruit ( Mworia et al , 2012 ; Asiche et al, 2017 , 2018 ; Mitalo et al, 2018 b , 2019 a , 2019 b ), pears ( El-Sharkawy et al , 2003 ; Mitalo et al , 2019c ), and apples ( Tacken et al , 2010 ). From an ecological perspective, the primary purpose of 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, including kiwifruit ( Kim et al , 1999 ; Mworia et al , 2012 ; Asiche et al , 2017 ; Mitalo et al , 2018 b ), 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, 2018 a , 2019 a , 2019 b ) and European pears ( Mitalo et al , 2019c ).…”

Exogenous Application of Sucrose Promotes Postharvest Ripening of Kiwifruit

“…To date, research on the regulation of postharvest ripening of kiwifruit has focused on changes in the content of endogenous hormones during this process, particularly the effects of ethylene and abscisic acid (ABA) [1][2][3]. The ripening and softening of kiwifruit were accelerated by ethylene and retarded by 1-MCP [4][5][6][7][8].…”

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).…”