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

McAtee PA, Richardson AC, Nieuwenhuizen NJ, Gunaseelan K, Hoong L, Chen X, Atkinson RG, Burdon JN, David KM, Schaffer RJ - BMC Plant Biol. (2015)

Bottom Line: 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.These 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.

View Article: PubMed Central - PubMed

Affiliation: The New Zealand Institute for Plant & Food Research Limited (PFR), Mt Albert Research Centre, Auckland, New Zealand. peter.mcatee@plantandfood.co.nz.

ABSTRACT

Background: Ripening 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.

Results: To 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.

Conclusions: These 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.

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A simplified model of the role of RIN-like genes during fruit maturation and ripening in different scpecies. RIN expression (blue line) correlates with ethylene production (E). Once the fruit is competent to ripen (C) RIN can induce ethylene dependent ripening (Phase 2 ripening PR2), but in the absence of ethylene (and RIN), ethylene independent ripening progresses (Phase 1 ripening PR1). In tomato RIN activates both ethylene and itself (Alba et al. 2005, Fujisawa et al. 2013) [29, 56] progressing PR1 and PR2 ripening simultaneously, while in kiwifruit and grape there is a down regulation of RIN expression following competence to ripen (and in grape veraison) (Pilati et al. 2007) [57] allowing PR1 ripening to occur independently. In kiwifruit this repression can be reversed later in maturity, or with the application of ethylene. Kiwifruit thus shows a hybrid ethylene independent-dependent mechanism with phase 2 ripening being likely to be controlled by SEP4/RIN
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Fig9: A simplified model of the role of RIN-like genes during fruit maturation and ripening in different scpecies. RIN expression (blue line) correlates with ethylene production (E). Once the fruit is competent to ripen (C) RIN can induce ethylene dependent ripening (Phase 2 ripening PR2), but in the absence of ethylene (and RIN), ethylene independent ripening progresses (Phase 1 ripening PR1). In tomato RIN activates both ethylene and itself (Alba et al. 2005, Fujisawa et al. 2013) [29, 56] progressing PR1 and PR2 ripening simultaneously, while in kiwifruit and grape there is a down regulation of RIN expression following competence to ripen (and in grape veraison) (Pilati et al. 2007) [57] allowing PR1 ripening to occur independently. In kiwifruit this repression can be reversed later in maturity, or with the application of ethylene. Kiwifruit thus shows a hybrid ethylene independent-dependent mechanism with phase 2 ripening being likely to be controlled by SEP4/RIN

Mentions: During development in all fruits, there is a period when the fruit becomes competent to ripen. This is a major change in the fruit’s properties, as it alters the fruit to be more attractive to seed-dispersing organisms, and usually coincides with seed maturation. The switch is often facilitated by large changes in phytohormone production, especially ethylene. In model fruit species such as tomato and grape there is growing molecular understanding of how some of the key switches regulate this transition. In tomato, ripening is predominantly regulated by ethylene, whilst in grape ripening ethylene has a relatively minor role. At the molecular level the best studied regulator is the RIN MADS-box gene, which acts in a heterotetrameric complex with FUL/TDR4 FUL2 and/or TAGL1 to bind and activate many genes associated with fruit ripening [21, 26, 28, 29, 50]. RIN is highly and constantly up-regulated during fruit ripening in tomato [17], banana [55], strawberry [18], and apple [19], and in tomato the FUL/TDR4 RIN complex has been shown to bind and activate the promoter of the ethylene biosynthesis genes ACS2,4 and RIN itself [26, 28, 29]. In this study we have shown that a RIN-like gene (previously published as AcSEP4 [33, 49] is associated with autocatalytic ethylene-associated ripening. Unlike tomato RIN [56], but consistent with grape VviSEP4 (GSVIVG0101051001) [57], following maturation (or veraison) the expression of this kiwifruit RIN-like gene decreases (Fig. 7b). This suggests that in grape and kiwifruit RIN cannot auto-activate itself, and even suggests the presence of an additional repression during this time. Ethylene (or propylene) is able to induce RIN expression in tomato and kiwifruit, however in kiwifruit, subsequent removal of ethylene causes this gene to be downregulated again (Fig. 7b), further supporting a repression mechanism. Transient experiments performed in tobacco indicate that the kiwifruit RIN does not activate RIN and there is no increase in RIN expression when the AcFUL is developmentally turned on, or when RIN expression is induced with ethylene, suggesting a mechanism by which the hybrid ripening is controlled (Fig. 9).Fig. 9


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

McAtee PA, Richardson AC, Nieuwenhuizen NJ, Gunaseelan K, Hoong L, Chen X, Atkinson RG, Burdon JN, David KM, Schaffer RJ - BMC Plant Biol. (2015)

A simplified model of the role of RIN-like genes during fruit maturation and ripening in different scpecies. RIN expression (blue line) correlates with ethylene production (E). Once the fruit is competent to ripen (C) RIN can induce ethylene dependent ripening (Phase 2 ripening PR2), but in the absence of ethylene (and RIN), ethylene independent ripening progresses (Phase 1 ripening PR1). In tomato RIN activates both ethylene and itself (Alba et al. 2005, Fujisawa et al. 2013) [29, 56] progressing PR1 and PR2 ripening simultaneously, while in kiwifruit and grape there is a down regulation of RIN expression following competence to ripen (and in grape veraison) (Pilati et al. 2007) [57] allowing PR1 ripening to occur independently. In kiwifruit this repression can be reversed later in maturity, or with the application of ethylene. Kiwifruit thus shows a hybrid ethylene independent-dependent mechanism with phase 2 ripening being likely to be controlled by SEP4/RIN
© Copyright Policy - OpenAccess
Related In: Results  -  Collection

License 1 - License 2
Show All Figures
getmorefigures.php?uid=PMC4696264&req=5

Fig9: A simplified model of the role of RIN-like genes during fruit maturation and ripening in different scpecies. RIN expression (blue line) correlates with ethylene production (E). Once the fruit is competent to ripen (C) RIN can induce ethylene dependent ripening (Phase 2 ripening PR2), but in the absence of ethylene (and RIN), ethylene independent ripening progresses (Phase 1 ripening PR1). In tomato RIN activates both ethylene and itself (Alba et al. 2005, Fujisawa et al. 2013) [29, 56] progressing PR1 and PR2 ripening simultaneously, while in kiwifruit and grape there is a down regulation of RIN expression following competence to ripen (and in grape veraison) (Pilati et al. 2007) [57] allowing PR1 ripening to occur independently. In kiwifruit this repression can be reversed later in maturity, or with the application of ethylene. Kiwifruit thus shows a hybrid ethylene independent-dependent mechanism with phase 2 ripening being likely to be controlled by SEP4/RIN
Mentions: During development in all fruits, there is a period when the fruit becomes competent to ripen. This is a major change in the fruit’s properties, as it alters the fruit to be more attractive to seed-dispersing organisms, and usually coincides with seed maturation. The switch is often facilitated by large changes in phytohormone production, especially ethylene. In model fruit species such as tomato and grape there is growing molecular understanding of how some of the key switches regulate this transition. In tomato, ripening is predominantly regulated by ethylene, whilst in grape ripening ethylene has a relatively minor role. At the molecular level the best studied regulator is the RIN MADS-box gene, which acts in a heterotetrameric complex with FUL/TDR4 FUL2 and/or TAGL1 to bind and activate many genes associated with fruit ripening [21, 26, 28, 29, 50]. RIN is highly and constantly up-regulated during fruit ripening in tomato [17], banana [55], strawberry [18], and apple [19], and in tomato the FUL/TDR4 RIN complex has been shown to bind and activate the promoter of the ethylene biosynthesis genes ACS2,4 and RIN itself [26, 28, 29]. In this study we have shown that a RIN-like gene (previously published as AcSEP4 [33, 49] is associated with autocatalytic ethylene-associated ripening. Unlike tomato RIN [56], but consistent with grape VviSEP4 (GSVIVG0101051001) [57], following maturation (or veraison) the expression of this kiwifruit RIN-like gene decreases (Fig. 7b). This suggests that in grape and kiwifruit RIN cannot auto-activate itself, and even suggests the presence of an additional repression during this time. Ethylene (or propylene) is able to induce RIN expression in tomato and kiwifruit, however in kiwifruit, subsequent removal of ethylene causes this gene to be downregulated again (Fig. 7b), further supporting a repression mechanism. Transient experiments performed in tobacco indicate that the kiwifruit RIN does not activate RIN and there is no increase in RIN expression when the AcFUL is developmentally turned on, or when RIN expression is induced with ethylene, suggesting a mechanism by which the hybrid ripening is controlled (Fig. 9).Fig. 9

Bottom Line: 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.These 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.

View Article: PubMed Central - PubMed

Affiliation: The New Zealand Institute for Plant & Food Research Limited (PFR), Mt Albert Research Centre, Auckland, New Zealand. peter.mcatee@plantandfood.co.nz.

ABSTRACT

Background: Ripening 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.

Results: To 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.

Conclusions: These 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.

Show MeSH
Related in: MedlinePlus