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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 MADS box genes in response to propylene treatments during late maturation and Phase 1 ripening. Fruit were harvested from 140-224 days after full bloom (DAFB; BBCH stages 79-87) and treated in air or with 10,000 μL.L-1 propylene (P-1000) for 1 day. Expression was determined at harvest, and 1 day and 3 days after harvest (DAH) using gene-specific primers for: a. SEP4/RIN (HQ113364), b. TDR4/FUL (HQ113357), c. TAGL1 (Achn121201), d. AP3 (Achn135681). Mean expression values are given relative to ACTIN, using two independent biological replicates repeated four times. e A comparison of SEP4/RIN response to P-10000 treatment and TDR4/FUL. SEP4/RIN showed a decrease in expression through maturity (purple line) and a transient upregulation with propylene. TDR4/FUL has little increase in expression until 175 DAFB, then increases (blue line). It has no significant response to propylene. Significance response to propylene compared to harvest time point (a, b = p < 0.01)
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Fig7: Relative expression changes of MADS box genes in response to propylene treatments during late maturation and Phase 1 ripening. Fruit were harvested from 140-224 days after full bloom (DAFB; BBCH stages 79-87) and treated in air or with 10,000 μL.L-1 propylene (P-1000) for 1 day. Expression was determined at harvest, and 1 day and 3 days after harvest (DAH) using gene-specific primers for: a. SEP4/RIN (HQ113364), b. TDR4/FUL (HQ113357), c. TAGL1 (Achn121201), d. AP3 (Achn135681). Mean expression values are given relative to ACTIN, using two independent biological replicates repeated four times. e A comparison of SEP4/RIN response to P-10000 treatment and TDR4/FUL. SEP4/RIN showed a decrease in expression through maturity (purple line) and a transient upregulation with propylene. TDR4/FUL has little increase in expression until 175 DAFB, then increases (blue line). It has no significant response to propylene. Significance response to propylene compared to harvest time point (a, b = p < 0.01)

Mentions: The expression of the closest kiwifruit RIN/FUL/TAGL1- and AP3- like MADS-box genes over Phase1 ripening, with and without propylene showed that the MADS-box gene SEP4/RIN showed a decrease in expression as the fruit progressed through Phase 1 ripening, and early in Phase 1 ripening (147-168 DAFB) showed little response to the propylene treatment. However after 175 DAFB there was a transient 4-fold up-regulation in expression with the propylene treatment. This transient increase continued to 3 DAH as the fruit went into rapid softening (224 DAFB) (Fig. 7a, e). FUL-like increased four-fold as the fruit matured (Fig. 7b/e). When the fruit were treated with propylene there was no difference in this induction, showing this gene acts independently of ethylene. At early Phase 1 ripening (161-168 DAFB) the TAGL1 gene showed a two-fold increase in expression with an propylene treatment and following harvest. However this increase was not observed later in Phase 1 ripening (Fig. c, Additional file 7). The AP3-like gene was highly expressed at 140 DAFB and had a 4-fold decrease in expression as the fruit entered Phase 1 ripening. When treated with propylene this gene was rapidly downregulated (Fig. 7d, Additional file 7).Fig. 7


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 MADS box genes in response to propylene treatments during late maturation and Phase 1 ripening. Fruit were harvested from 140-224 days after full bloom (DAFB; BBCH stages 79-87) and treated in air or with 10,000 μL.L-1 propylene (P-1000) for 1 day. Expression was determined at harvest, and 1 day and 3 days after harvest (DAH) using gene-specific primers for: a. SEP4/RIN (HQ113364), b. TDR4/FUL (HQ113357), c. TAGL1 (Achn121201), d. AP3 (Achn135681). Mean expression values are given relative to ACTIN, using two independent biological replicates repeated four times. e A comparison of SEP4/RIN response to P-10000 treatment and TDR4/FUL. SEP4/RIN showed a decrease in expression through maturity (purple line) and a transient upregulation with propylene. TDR4/FUL has little increase in expression until 175 DAFB, then increases (blue line). It has no significant response to propylene. Significance response to propylene compared to harvest time point (a, b = p < 0.01)
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Fig7: Relative expression changes of MADS box genes in response to propylene treatments during late maturation and Phase 1 ripening. Fruit were harvested from 140-224 days after full bloom (DAFB; BBCH stages 79-87) and treated in air or with 10,000 μL.L-1 propylene (P-1000) for 1 day. Expression was determined at harvest, and 1 day and 3 days after harvest (DAH) using gene-specific primers for: a. SEP4/RIN (HQ113364), b. TDR4/FUL (HQ113357), c. TAGL1 (Achn121201), d. AP3 (Achn135681). Mean expression values are given relative to ACTIN, using two independent biological replicates repeated four times. e A comparison of SEP4/RIN response to P-10000 treatment and TDR4/FUL. SEP4/RIN showed a decrease in expression through maturity (purple line) and a transient upregulation with propylene. TDR4/FUL has little increase in expression until 175 DAFB, then increases (blue line). It has no significant response to propylene. Significance response to propylene compared to harvest time point (a, b = p < 0.01)
Mentions: The expression of the closest kiwifruit RIN/FUL/TAGL1- and AP3- like MADS-box genes over Phase1 ripening, with and without propylene showed that the MADS-box gene SEP4/RIN showed a decrease in expression as the fruit progressed through Phase 1 ripening, and early in Phase 1 ripening (147-168 DAFB) showed little response to the propylene treatment. However after 175 DAFB there was a transient 4-fold up-regulation in expression with the propylene treatment. This transient increase continued to 3 DAH as the fruit went into rapid softening (224 DAFB) (Fig. 7a, e). FUL-like increased four-fold as the fruit matured (Fig. 7b/e). When the fruit were treated with propylene there was no difference in this induction, showing this gene acts independently of ethylene. At early Phase 1 ripening (161-168 DAFB) the TAGL1 gene showed a two-fold increase in expression with an propylene treatment and following harvest. However this increase was not observed later in Phase 1 ripening (Fig. c, Additional file 7). The AP3-like gene was highly expressed at 140 DAFB and had a 4-fold decrease in expression as the fruit entered Phase 1 ripening. When treated with propylene this gene was rapidly downregulated (Fig. 7d, Additional file 7).Fig. 7

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