The hybrid non-ethylene and ethylene ripening response in kiwifruit (Actinidia chinensis) is associated with differential regulation of MADS-box transcription factors

Abstract

BackgroundRipening in tomato is predominantly controlled by ethylene, whilst in fruit such as grape, it is predominantly controlled by other hormones. The ripening response of many kiwifruit (Actinidia) species is atypical. The majority of ripening-associated fruit starch hydrolysis, colour change and softening occurs in the apparent absence of ethylene production (Phase 1 ripening) whilst Phase 2 ripening requires autocatalytic ethylene production and is associated with further softening and an increase in aroma volatiles.ResultsTo dissect the ripening response in the yellow-fleshed kiwifruit A. chinensis (‘Hort16A’), a two dimensional developmental stage X ethylene response time study was undertaken. As fruit progressed through maturation and Phase 1 ripening, fruit were treated with different concentrations of propylene and ethylene. At the start of Phase 1 ripening, treated fruit responded to ethylene, and were capable of producing endogenous ethylene. As the fruit progressed through Phase 1 ripening, the fruit became less responsive to ethylene and endogeneous ethylene production was partially repressed. Towards the end of Phase 1 ripening the fruit were again able to produce high levels of ethylene. Progression through Phase 1 ripening coincided with a developmental increase in the expression of the ethylene-unresponsive MADS-box FRUITFUL-like gene (FUL1). The ability to respond to ethylene however coincided with a change in expression of another MADS-box gene SEPALLATA4/RIPENING INHIBITOR-like (SEP4/RIN). The promoter of SEP4/RIN was shown to be transactivated by EIN3-like transcription factors, but unlike tomato, not by SEP4/RIN itself. Transient over-expression of SEP4/RIN in kiwifruit caused an increase in ethylene production.ConclusionsThese results suggest that the non-ethylene/ethylene ripening response observed in kiwifruit is a hybrid of both the tomato and grape ripening progression, with Phase 1 being akin to the RIN/ethylene inhibitory response observed in grape and Phase 2 akin to the RIN-associated autocatalytic ethylene response observed in tomato.Electronic supplementary materialThe online version of this article (doi:10.1186/s12870-015-0697-9) contains supplementary material, which is available to authorized users.

Characterization of Ripening-related Genes Involved in Ethylene-independent Low Temperature-modulated Ripening in ‘Rainbow Red’ Kiwifruit during Storage and On-vine

“…Ethylene-induced kiwifruit ripening involves the increased expression of ethylene biosynthesis and perception genes (Giovannoni, 2004(Giovannoni, , 2007Kim et al, 1999;McAtee et al, 2015;Sfakiotakis et al, 1997). In this study, transcript levels of AcACS1 and AcACO2 drastically increased in propylene-treated fruit at day 5 while no increases were observed during storage and on the vine (Fig.…”

“…However, significant ripening of kiwifruit with undetectable ethylene production has been previously reported when fruit are left on vine after commercial harvest date (McAtee et al, 2015;Murakami et al, 2015;Richardson et al, 2011). However, the mechanism of the on-vine ripening has not been elucidated.…”

“…On-vine ripening has been reported in kiwifruit without substantial ethylene production with many studies attributing it to basal "System 1" ethylene (McAtee et al, 2015;Richardson et al, 2011). Murakami et al (2015) also reported that 'Rainbow Red' fruit ripened on the vine in the absence of detectable ethylene.…”

Genetics of Fruit Softening

“…McAtee et al (2015) identified nine ethylene receptors in the 'Hongyang' genome, five of which have been published (Yin et al 2008). However, further analysis showed that two gene models did not have the all the receptor domains and one was truncated (McAtee et al 2015).…”

“…These transgenic lines should also be a useful tool to determine the role of ethylene (if any) during the rapid phase 1 of softening. McAtee et al (2015) mined the recently published kiwifruit genome (Huang et al 2013) to identify genes associated with ethylene biosynthesis and identified ten SAM synthetase genes, only one of which had previously been identified (Whittaker et al 1995). identified thirteen putative ACC synthase genes in the 'Hongyang' predicted coding sequence database, including the ACS1 gene identified by Whittaker et al (1997).…”