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Comparative Study
. 2011 Oct 17:11:138.
doi: 10.1186/1471-2229-11-138.

Transcriptomics of shading-induced and NAA-induced abscission in apple (Malus domestica) reveals a shared pathway involving reduced photosynthesis, alterations in carbohydrate transport and signaling and hormone crosstalk

Hong Zhu  1 , Chris D Dardick, Eric P Beers, Ann M Callanhan, Rui Xia, Rongcai Yuan
Affiliations
Comparative Study

Transcriptomics of shading-induced and NAA-induced abscission in apple (Malus domestica) reveals a shared pathway involving reduced photosynthesis, alterations in carbohydrate transport and signaling and hormone crosstalk

Hong Zhu et al. BMC Plant Biol. .

Abstract

Background: Naphthaleneacetic acid (NAA), a synthetic auxin analogue, is widely used as an effective thinner in apple orchards. When applied shortly after fruit set, some fruit abscise leading to improved fruit size and quality. However, the thinning results of NAA are inconsistent and difficult to predict, sometimes leading to excess fruit drop or insufficient thinning which are costly to growers. This unpredictability reflects our incomplete understanding of the mode of action of NAA in promoting fruit abscission.

Results: Here we compared NAA-induced fruit drop with that caused by shading via gene expression profiling performed on the fruit abscission zone (FAZ), sampled 1, 3, and 5 d after treatment. More than 700 genes with significant changes in transcript abundance were identified from NAA-treated FAZ. Combining results from both treatments, we found that genes associated with photosynthesis, cell cycle and membrane/cellular trafficking were downregulated. On the other hand, there was up-regulation of genes related to ABA, ethylene biosynthesis and signaling, cell wall degradation and programmed cell death. While the differentially expressed gene sets for NAA and shading treatments shared only 25% identity, NAA and shading showed substantial similarity with respect to the classes of genes identified. Specifically, photosynthesis, carbon utilization, ABA and ethylene pathways were affected in both NAA- and shading-induced young fruit abscission. Moreover, we found that NAA, similar to shading, directly interfered with leaf photosynthesis by repressing photosystem II (PSII) efficiency within 10 minutes of treatment, suggesting that NAA and shading induced some of the same early responses due to reduced photosynthesis, which concurred with changes in hormone signaling pathways and triggered fruit abscission.

Conclusions: This study provides an extensive transcriptome study and a good platform for further investigation of possible regulatory genes involved in the induction of young fruit abscission in apple, which will enable us to better understand the mechanism of fruit thinning and facilitate the selection of potential chemicals for the thinning programs in apple.

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Figures

Figure 1
Figure 1
Effect of NAA and shading treatments on fruit abscission of 'Golden Delicious' apples. (A) NAA and shading increase fruit abscission rate. (B) NAA and shading treatment also increase the percentage of total fruit drop. Results represent the mean (± SE) of three replicates. Different letters indicate significant differences among means according to Duncan's multiple range test (P ≤ 0.05).
Figure 2
Figure 2
Effect of NAA and shading treatments on ethylene production of 'Golden Delicious' apples. (A) NAA and shading induce ethylene in young fruit. (B) NAA and shading also induce ethylene in leaves. Results represent the mean (± SE) of three replicates.
Figure 3
Figure 3
Functional categories of statistically significant genes. (A) Differentially expressed genes are categorized from NAA-treated FAZ. (B) Differentially expressed genes are categorized from shading-treated FAZ. The functional categorization is based on the annotation and GO information. Category names are indicated near each pie slice, along with the proportion of each category. (C) Functional categories showing non-random expression trends. Statistically significant values are highlighted (P ≤ 0.05).
Figure 4
Figure 4
Expression of genes related to ABA biosynthesis and signaling as determined by RT-qPCR. Left column, Gene expression in fruit abscission zone (FAZ) from 'Golden Delicious' apple trees after application of NAA and shading. Red lines indicate normalized microarray values (Solid for NAA and dot for shading). Right column, Gene expression in fruit cortex (FC) from 'Golden Delicious' apple trees after application of NAA and shading. The values of transcript levels in the FAZ and FC from control trees were arbitrarily set to 1. The transcript levels were normalized using actin. Results represent the mean (± SE) of three replicates.
Figure 5
Figure 5
Expression of genes related to ethylene biosynthesis and signaling as determined by RT-qPCR. Left column, Gene expression in fruit abscission zone (FAZ) from 'Golden Delicious' apple trees after application of NAA and shading. Red lines indicate normalized microarray values (Solid for NAA and dot for shading). Right column, Gene expression in fruit cortex (FC) from 'Golden Delicious' apple trees after application of NAA and shading. The values of transcript levels in the FAZ and FC from control trees were arbitrarily set to 1. The transcript levels were normalized using actin. Results represent the mean (± SE) of three replicates.
Figure 6
Figure 6
Expression of genes related to sugar transport and polar auxin transport as determined by RT-qPCR. Left column, Gene expression in fruit abscission zone (FAZ) from 'Golden Delicious' apple trees after application of NAA and shading. Red lines indicate normalized microarray values (Solid for NAA and dot for shading). Right column, Gene expression in fruit cortex (FC) from 'Golden Delicious' apple trees after application of NAA and shading. The values of transcript levels in the FAZ and FC from control trees were arbitrarily set to 1. The transcript levels were normalized using actin. Results represent the mean (± SE) of three replicates.
Figure 7
Figure 7
Expression of genes related to abscission zone formation and cell wall degradation as determined by RT-qPCR. Gene expression in fruit abscission zone (FAZ) from 'Golden Delicious' apple trees after application of NAA and shading. Red lines indicate normalized microarray values (Solid for NAA and dot for shading). The values of transcript levels in the FAZ from control trees were arbitrarily set to 1. The transcript levels were normalized using actin. Results represent the mean (± SE) of three replicates.
Figure 8
Figure 8
Expression of genes related to photosynthesis and sugar availability as determined by RT-qPCR. Gene expression in leaf from 'Golden Delicious' apple trees after application of NAA. The values of transcript levels in the leaf from control trees were arbitrarily set to 1. The transcript levels were normalized using actin. Results represent the mean (± SE) of three replicates.
Figure 9
Figure 9
Expression of genes related to sugar metabolism as determined by RT-qPCR. Gene expression in fruit cortex (FC) from 'Golden Delicious' apple trees after application of NAA and shading. The value of transcript levels in the FC from control trees were arbitrarily set to 1. The transcript levels were normalized using actin. Results represent the mean (± SE) of three replicates.
Figure 10
Figure 10
Effect of NAA at 15 mg L-1 on apple leaf. (A) White light image of the effect of NAA at various rates on the leaves of young seedlings in growth chamber. Necrosis was observed in a concentration-dependent manner. (B-D) CFI image of the leaves of young seedlings in growth chamber treated with NAA at 15 mg L-1. Areas with pale blue color indicate PSII photoinhibition. (E-G) CFI image of the leaves of fruit-bearing trees in the field treated with NAA at 15 mg L-1. Areas with dark green color indicate PSII photoinhibition, corresponding with the numerical values (the right column) in the inserted table. Insert table: Effect of NAA at 15 mg L-1 on leaf PSII efficiency. FV/FM values were recorded three times independently from both control and NAA-affected leaves of fruit-bearing trees in the field. Results represent the mean (± SE) of three replicates. Different letters indicate significant differences among means according to Duncan's multiple range test (P ≤ 0.05).
Figure 11
Figure 11
A hypothetical model for NAA-induced young fruit abscission in apple. NAA, like shading, imposes a stress signal on leaf, or globally on any other photosynthetically-active tissues within the tree, causing photosynthesis repression and associated nutrient stress. As the nutrient stress is perceived at the fruit level, its growth is inhibited by a sugar transport block, resulting in a lower sink strength of the fruitlet. Meanwhile, ethylene and/or ABA are produced in response to photosynthesis inhibition and through sugar signaling. The elevated ethylene level decreases auxin transport to the FAZ and increases its sensitivity to ethylene, causing the differentiation of the FAZ and the execution of fruit abscission.
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References

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