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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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Relative expression changes of five selected kiwifruit genes in response to propylene treatments during late maturation and Phase 1 ripening. Fruit were harvested from 140-224 days after full bloom (DAFB) and left in air or treated with 10,000 μL.L-1 propylene (P-10000) for 1 day. Expression was determined at harvest, and 1 day and 3 days after harvest (DAH) using gene-specific primers for a. CBP: CHLOROPHYLL BINDING PROTEIN (FG05168), associated with colour change; b. PE: PECTIN ESTERASE (Achn064451) and c. EXP: EXPANSIN (FG442832), both associated with softening and d. β-AM: β-AMYLASE (Achn387071) and e. SUSA: SUCROSE SYNTHASE (Achn024141), both associated with sugar metabolism. Mean expression values are given relative to AcACTIN, using two independent biological replicates repeated four times. Arrows show periods where expression is repressed
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Fig4: Relative expression changes of five selected kiwifruit genes in response to propylene treatments during late maturation and Phase 1 ripening. Fruit were harvested from 140-224 days after full bloom (DAFB) and left in air or treated with 10,000 μL.L-1 propylene (P-10000) for 1 day. Expression was determined at harvest, and 1 day and 3 days after harvest (DAH) using gene-specific primers for a. CBP: CHLOROPHYLL BINDING PROTEIN (FG05168), associated with colour change; b. PE: PECTIN ESTERASE (Achn064451) and c. EXP: EXPANSIN (FG442832), both associated with softening and d. β-AM: β-AMYLASE (Achn387071) and e. SUSA: SUCROSE SYNTHASE (Achn024141), both associated with sugar metabolism. Mean expression values are given relative to AcACTIN, using two independent biological replicates repeated four times. Arrows show periods where expression is repressed

Mentions: In the ‘at-harvest’ samples through the maturation period, there were only small transcriptional changes observed in two soluble sugar-related genes (β-AMYLASE (β-AM) and SUCROSE SYNTHASE (SUSA)) and the two softening-related genes (PECTIN ESTERASE (PE) and EXPANSIN (EXP)) (Fig. 4, Additional file 2). The colour-related gene CHLOROPHYLL BINDING PROTEIN (CBP) showed a decrease in expression through Phase 1 ripening. In fruit that were not treated with propylene the effect of harvest over three days was initially minimal, but at 224 DAFB the sugar and cell wall related genes showed an increase in expression 1-3 days post harvest.Fig. 4


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)

Relative expression changes of five selected kiwifruit genes in response to propylene treatments during late maturation and Phase 1 ripening. Fruit were harvested from 140-224 days after full bloom (DAFB) and left in air or treated with 10,000 μL.L-1 propylene (P-10000) for 1 day. Expression was determined at harvest, and 1 day and 3 days after harvest (DAH) using gene-specific primers for a. CBP: CHLOROPHYLL BINDING PROTEIN (FG05168), associated with colour change; b. PE: PECTIN ESTERASE (Achn064451) and c. EXP: EXPANSIN (FG442832), both associated with softening and d. β-AM: β-AMYLASE (Achn387071) and e. SUSA: SUCROSE SYNTHASE (Achn024141), both associated with sugar metabolism. Mean expression values are given relative to AcACTIN, using two independent biological replicates repeated four times. Arrows show periods where expression is repressed
© Copyright Policy - OpenAccess
Related In: Results  -  Collection

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

Fig4: Relative expression changes of five selected kiwifruit genes in response to propylene treatments during late maturation and Phase 1 ripening. Fruit were harvested from 140-224 days after full bloom (DAFB) and left in air or treated with 10,000 μL.L-1 propylene (P-10000) for 1 day. Expression was determined at harvest, and 1 day and 3 days after harvest (DAH) using gene-specific primers for a. CBP: CHLOROPHYLL BINDING PROTEIN (FG05168), associated with colour change; b. PE: PECTIN ESTERASE (Achn064451) and c. EXP: EXPANSIN (FG442832), both associated with softening and d. β-AM: β-AMYLASE (Achn387071) and e. SUSA: SUCROSE SYNTHASE (Achn024141), both associated with sugar metabolism. Mean expression values are given relative to AcACTIN, using two independent biological replicates repeated four times. Arrows show periods where expression is repressed
Mentions: In the ‘at-harvest’ samples through the maturation period, there were only small transcriptional changes observed in two soluble sugar-related genes (β-AMYLASE (β-AM) and SUCROSE SYNTHASE (SUSA)) and the two softening-related genes (PECTIN ESTERASE (PE) and EXPANSIN (EXP)) (Fig. 4, Additional file 2). The colour-related gene CHLOROPHYLL BINDING PROTEIN (CBP) showed a decrease in expression through Phase 1 ripening. In fruit that were not treated with propylene the effect of harvest over three days was initially minimal, but at 224 DAFB the sugar and cell wall related genes showed an increase in expression 1-3 days post harvest.Fig. 4

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