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Differential behavior within a grapevine cluster: decreased ethylene-related gene expression dependent on auxin transport is correlated with low abscission of first developed berries.

Kühn N, Abello C, Godoy F, Delrot S, Arce-Johnson P - PLoS ONE (2014)

Bottom Line: For this, flowers that opened in a cluster were tagged daily, which allowed to separately analyze berries, regarding their ability to persist.Use of radiolabeled auxin showed that "first berries" had higher polar auxin transport, correlated with lower ethylene content and lower ethylene-related transcript abundance than "late berries".When "first berries" were treated with a polar auxin transport inhibitor they showed higher ethylene-related transcript abundance and were more prone to abscise than control berries.

View Article: PubMed Central - PubMed

Affiliation: Departamento de Genética Molecular y Microbiología, Pontificia Universidad Católica de Chile, Santiago, Chile.

ABSTRACT
In grapevine, fruit abscission is known to occur within the first two to three weeks after flowering, but the reason why some berries in a cluster persist and others abscise is not yet understood. Ethylene sensitivity modulates abscission in several fruit species, based on a mechanism where continuous polar auxin transport across the pedicel results in a decrease in ethylene perception, which prevents abscission. In grapevine, flowering takes about four to seven days in a single cluster, thus while some flowers are developing into berries, others are just starting to open. So, in this work it was assessed whether uneven flowering accounted for differences in berry abscission dependent on polar auxin transport and ethylene-related gene expression. For this, flowers that opened in a cluster were tagged daily, which allowed to separately analyze berries, regarding their ability to persist. It was found that berries derived from flowers that opened the day that flowering started--named as "first berries"--had lower abscission rate than berries derived from flowers that opened during the following days--named as "late berries". Use of radiolabeled auxin showed that "first berries" had higher polar auxin transport, correlated with lower ethylene content and lower ethylene-related transcript abundance than "late berries". When "first berries" were treated with a polar auxin transport inhibitor they showed higher ethylene-related transcript abundance and were more prone to abscise than control berries. This study provides new insights on fruit abscission control. Our results indicate that polar auxin transport sustains the ability of "first berries" to persist in the cluster during grapevine abscission and also suggest that this could be associated with changes in ethylene-related gene expression.

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Transcript abundance of ethylene perception- and biosynthesis-related genes in “first berries” impaired in polar auxin transport.(A) Effect of blocking polar auxin transport at 14 DAF using 50 µM N-1-naphthylphthalamic acid (NPA) on transcript abundance of VvETR1, VvETR2, VvERS2, VvCTR1, VvEIN3, VvERF12 genes assessed 2 days post treatment (DPT), at 16 DAF. (B) Effect of blocking polar auxin transport at 14 DAF using 50 µM NPA on transcript abundance of VvACO3, VvACS, VvACS1 and VvACS3 genes assessed 2 DPT, at 16 DAF. Transcript abundance is relative to the mean expression of the constitutive genes VvUBI1 and VvGPDH (for more details, see Material and Methods section). (C) Effect of blocking polar auxin transport at 14 DAF on abscission using 50 µM NPA assessed 2 DPT, at 16 DAF. Treatment was done immediately after berry number per cluster was registered, and remaining berries were registered for percentage (%) of berry abscission estimation (for berry number see Table 2). Only “first berries” were analyzed. Asterisk indicates that differences are significant between NPA-treated and control berries. Significance was assessed using p value <0.05 (n = 3). Error bars are STERR±.
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pone-0111258-g005: Transcript abundance of ethylene perception- and biosynthesis-related genes in “first berries” impaired in polar auxin transport.(A) Effect of blocking polar auxin transport at 14 DAF using 50 µM N-1-naphthylphthalamic acid (NPA) on transcript abundance of VvETR1, VvETR2, VvERS2, VvCTR1, VvEIN3, VvERF12 genes assessed 2 days post treatment (DPT), at 16 DAF. (B) Effect of blocking polar auxin transport at 14 DAF using 50 µM NPA on transcript abundance of VvACO3, VvACS, VvACS1 and VvACS3 genes assessed 2 DPT, at 16 DAF. Transcript abundance is relative to the mean expression of the constitutive genes VvUBI1 and VvGPDH (for more details, see Material and Methods section). (C) Effect of blocking polar auxin transport at 14 DAF on abscission using 50 µM NPA assessed 2 DPT, at 16 DAF. Treatment was done immediately after berry number per cluster was registered, and remaining berries were registered for percentage (%) of berry abscission estimation (for berry number see Table 2). Only “first berries” were analyzed. Asterisk indicates that differences are significant between NPA-treated and control berries. Significance was assessed using p value <0.05 (n = 3). Error bars are STERR±.

Mentions: Low transcript abundance of genes involved in ethylene perception and biosynthesis was detected in “first berries” compared with “last berries” (Figure 3), correlated with low abscission rate and high percentage of polar auxin transport (Figure 2). Thus, we investigated whether auxin transport inhibition in “first berries” results in an increase in abscission, under the assumption that ethylene perception should be increased in response to impaired polar auxin transport. For this, first berries were treated with the auxin transport inhibitor, N-1-naphthylphthalamic acid (NPA), and changes in the transcript abundance of perception- and biosynthesis-related genes and in the abscission rate were assessed. It was found that relative transcript abundance of ethylene perception-related genes, VvETR1, VvETR2, VvEIN3, and ERF12 was significantly increased in NPA-treated “first berries” compared to untreated “first berries”, with the transcript abundance of VvCTR1 and VvERS2 genes not affected by the treatment (Figure 5A). Auxin transport impairment also affected transcript relative levels of ethylene biosynthesis-related genes, with VvACS1 and VvACS3 induced by the NPA treatment (Figure 5B). As shown in Figure 5C, polar auxin transport impairment caused by NPA treatment, resulted in a slight but significant increase in abscission percentage, indicating that polar auxin transport across the berry is required to reduce abscission. Altogether these results suggest that the ability of “first berries” to persist in a cluster is based on the capacity to sustain polar transport of auxin, which is associated with changes in the expression of genes involved in ethylene biosynthesis and perception.


Differential behavior within a grapevine cluster: decreased ethylene-related gene expression dependent on auxin transport is correlated with low abscission of first developed berries.

Kühn N, Abello C, Godoy F, Delrot S, Arce-Johnson P - PLoS ONE (2014)

Transcript abundance of ethylene perception- and biosynthesis-related genes in “first berries” impaired in polar auxin transport.(A) Effect of blocking polar auxin transport at 14 DAF using 50 µM N-1-naphthylphthalamic acid (NPA) on transcript abundance of VvETR1, VvETR2, VvERS2, VvCTR1, VvEIN3, VvERF12 genes assessed 2 days post treatment (DPT), at 16 DAF. (B) Effect of blocking polar auxin transport at 14 DAF using 50 µM NPA on transcript abundance of VvACO3, VvACS, VvACS1 and VvACS3 genes assessed 2 DPT, at 16 DAF. Transcript abundance is relative to the mean expression of the constitutive genes VvUBI1 and VvGPDH (for more details, see Material and Methods section). (C) Effect of blocking polar auxin transport at 14 DAF on abscission using 50 µM NPA assessed 2 DPT, at 16 DAF. Treatment was done immediately after berry number per cluster was registered, and remaining berries were registered for percentage (%) of berry abscission estimation (for berry number see Table 2). Only “first berries” were analyzed. Asterisk indicates that differences are significant between NPA-treated and control berries. Significance was assessed using p value <0.05 (n = 3). Error bars are STERR±.
© Copyright Policy
Related In: Results  -  Collection

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Show All Figures
getmorefigures.php?uid=PMC4218718&req=5

pone-0111258-g005: Transcript abundance of ethylene perception- and biosynthesis-related genes in “first berries” impaired in polar auxin transport.(A) Effect of blocking polar auxin transport at 14 DAF using 50 µM N-1-naphthylphthalamic acid (NPA) on transcript abundance of VvETR1, VvETR2, VvERS2, VvCTR1, VvEIN3, VvERF12 genes assessed 2 days post treatment (DPT), at 16 DAF. (B) Effect of blocking polar auxin transport at 14 DAF using 50 µM NPA on transcript abundance of VvACO3, VvACS, VvACS1 and VvACS3 genes assessed 2 DPT, at 16 DAF. Transcript abundance is relative to the mean expression of the constitutive genes VvUBI1 and VvGPDH (for more details, see Material and Methods section). (C) Effect of blocking polar auxin transport at 14 DAF on abscission using 50 µM NPA assessed 2 DPT, at 16 DAF. Treatment was done immediately after berry number per cluster was registered, and remaining berries were registered for percentage (%) of berry abscission estimation (for berry number see Table 2). Only “first berries” were analyzed. Asterisk indicates that differences are significant between NPA-treated and control berries. Significance was assessed using p value <0.05 (n = 3). Error bars are STERR±.
Mentions: Low transcript abundance of genes involved in ethylene perception and biosynthesis was detected in “first berries” compared with “last berries” (Figure 3), correlated with low abscission rate and high percentage of polar auxin transport (Figure 2). Thus, we investigated whether auxin transport inhibition in “first berries” results in an increase in abscission, under the assumption that ethylene perception should be increased in response to impaired polar auxin transport. For this, first berries were treated with the auxin transport inhibitor, N-1-naphthylphthalamic acid (NPA), and changes in the transcript abundance of perception- and biosynthesis-related genes and in the abscission rate were assessed. It was found that relative transcript abundance of ethylene perception-related genes, VvETR1, VvETR2, VvEIN3, and ERF12 was significantly increased in NPA-treated “first berries” compared to untreated “first berries”, with the transcript abundance of VvCTR1 and VvERS2 genes not affected by the treatment (Figure 5A). Auxin transport impairment also affected transcript relative levels of ethylene biosynthesis-related genes, with VvACS1 and VvACS3 induced by the NPA treatment (Figure 5B). As shown in Figure 5C, polar auxin transport impairment caused by NPA treatment, resulted in a slight but significant increase in abscission percentage, indicating that polar auxin transport across the berry is required to reduce abscission. Altogether these results suggest that the ability of “first berries” to persist in a cluster is based on the capacity to sustain polar transport of auxin, which is associated with changes in the expression of genes involved in ethylene biosynthesis and perception.

Bottom Line: For this, flowers that opened in a cluster were tagged daily, which allowed to separately analyze berries, regarding their ability to persist.Use of radiolabeled auxin showed that "first berries" had higher polar auxin transport, correlated with lower ethylene content and lower ethylene-related transcript abundance than "late berries".When "first berries" were treated with a polar auxin transport inhibitor they showed higher ethylene-related transcript abundance and were more prone to abscise than control berries.

View Article: PubMed Central - PubMed

Affiliation: Departamento de Genética Molecular y Microbiología, Pontificia Universidad Católica de Chile, Santiago, Chile.

ABSTRACT
In grapevine, fruit abscission is known to occur within the first two to three weeks after flowering, but the reason why some berries in a cluster persist and others abscise is not yet understood. Ethylene sensitivity modulates abscission in several fruit species, based on a mechanism where continuous polar auxin transport across the pedicel results in a decrease in ethylene perception, which prevents abscission. In grapevine, flowering takes about four to seven days in a single cluster, thus while some flowers are developing into berries, others are just starting to open. So, in this work it was assessed whether uneven flowering accounted for differences in berry abscission dependent on polar auxin transport and ethylene-related gene expression. For this, flowers that opened in a cluster were tagged daily, which allowed to separately analyze berries, regarding their ability to persist. It was found that berries derived from flowers that opened the day that flowering started--named as "first berries"--had lower abscission rate than berries derived from flowers that opened during the following days--named as "late berries". Use of radiolabeled auxin showed that "first berries" had higher polar auxin transport, correlated with lower ethylene content and lower ethylene-related transcript abundance than "late berries". When "first berries" were treated with a polar auxin transport inhibitor they showed higher ethylene-related transcript abundance and were more prone to abscise than control berries. This study provides new insights on fruit abscission control. Our results indicate that polar auxin transport sustains the ability of "first berries" to persist in the cluster during grapevine abscission and also suggest that this could be associated with changes in ethylene-related gene expression.

Show MeSH
Related in: MedlinePlus