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Uncovering co-expression gene network modules regulating fruit acidity in diverse apples.

Bai Y, Dougherty L, Cheng L, Zhong GY, Xu K - BMC Genomics (2015)

Bottom Line: Network inferring using weighted gene co-expression network analysis (WGCNA) revealed five co-expression gene network modules of significant (P < 0.001) correlation with malate.We also identified 12 intramodular hub genes from each of the five modules and 18 enriched gene ontology (GO) terms and MapMan sub-bines, including two GO terms (GO:0015979 and GO:0009765) and two MapMap sub-bins (1.3.4 and 1.1.1.1) related to photosynthesis in module Turquoise.Using Lemon-Tree algorithms, we identified 12 regulator genes of probabilistic scores 35.5-81.0, including MDP0000525602 (a LLR receptor kinase), MDP0000319170 (an IQD2-like CaM binding protein) and MDP0000190273 (an EIN3-like transcription factor) of greater interest for being one of the 18 MSAGs or one of the 12 intramodular hub genes in Turquoise, and/or a regulator to the cluster containing Ma1.

View Article: PubMed Central - PubMed

Affiliation: Horticulture Section, School of Integrative Plant Science, Cornell University, New York State Agricultural Experiment Station, Geneva, NY, 14456, USA. yb63@cornell.edu.

ABSTRACT

Background: Acidity is a major contributor to fruit quality. Several organic acids are present in apple fruit, but malic acid is predominant and determines fruit acidity. The trait is largely controlled by the Malic acid (Ma) locus, underpinning which Ma1 that putatively encodes a vacuolar aluminum-activated malate transporter1 (ALMT1)-like protein is a strong candidate gene. We hypothesize that fruit acidity is governed by a gene network in which Ma1 is key member. The goal of this study is to identify the gene network and the potential mechanisms through which the network operates.

Results: Guided by Ma1, we analyzed the transcriptomes of mature fruit of contrasting acidity from six apple accessions of genotype Ma_ (MaMa or Mama) and four of mama using RNA-seq and identified 1301 fruit acidity associated genes, among which 18 were most significant acidity genes (MSAGs). Network inferring using weighted gene co-expression network analysis (WGCNA) revealed five co-expression gene network modules of significant (P < 0.001) correlation with malate. Of these, the Ma1 containing module (Turquoise) of 336 genes showed the highest correlation (0.79). We also identified 12 intramodular hub genes from each of the five modules and 18 enriched gene ontology (GO) terms and MapMan sub-bines, including two GO terms (GO:0015979 and GO:0009765) and two MapMap sub-bins (1.3.4 and 1.1.1.1) related to photosynthesis in module Turquoise. Using Lemon-Tree algorithms, we identified 12 regulator genes of probabilistic scores 35.5-81.0, including MDP0000525602 (a LLR receptor kinase), MDP0000319170 (an IQD2-like CaM binding protein) and MDP0000190273 (an EIN3-like transcription factor) of greater interest for being one of the 18 MSAGs or one of the 12 intramodular hub genes in Turquoise, and/or a regulator to the cluster containing Ma1.

Conclusions: The most relevant finding of this study is the identification of the MSAGs, intramodular hub genes, enriched photosynthesis related processes, and regulator genes in a WGCNA module Turquoise that not only encompasses Ma1 but also shows the highest modular correlation with acidity. Overall, this study provides important insight into the Ma1-mediated gene network controlling acidity in mature apple fruit of diverse genetic background.

No MeSH data available.


Related in: MedlinePlus

Evaluation of fruit acidity and causal organic acids. Standard deviations were shown with the error bars. a TA and malate concentrations measured in the ten apple varieties, which were abbreviated as the following: B Britegold, N Novosibirski Sweet, P PI323617, S Sweet Delicious, C Cox’s Orange Pippin, E Empire, F Fuji, G Granny Smith, J Jonathan, R Rome Beauty Law. The first four are of genotype mama whereas the last six of genotype Ma_. b Mean TA and malate concentrations in genotype groups Ma_ and mama. c Concentrations of succinate, fumarate, citrate and maleate in genotype groups Ma_ and mama. d Fruit pH readings in the ten apples
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Fig1: Evaluation of fruit acidity and causal organic acids. Standard deviations were shown with the error bars. a TA and malate concentrations measured in the ten apple varieties, which were abbreviated as the following: B Britegold, N Novosibirski Sweet, P PI323617, S Sweet Delicious, C Cox’s Orange Pippin, E Empire, F Fuji, G Granny Smith, J Jonathan, R Rome Beauty Law. The first four are of genotype mama whereas the last six of genotype Ma_. b Mean TA and malate concentrations in genotype groups Ma_ and mama. c Concentrations of succinate, fumarate, citrate and maleate in genotype groups Ma_ and mama. d Fruit pH readings in the ten apples

Mentions: Fruit metabolite profiling was conducted using GC-MS with three biological replicates in the ten apple varieties. A total of 19 metabolites were quantified, including 12 soluble sugars and seven organic acids. Among the 12 sugars, only sorbitol showed a significantly (P = 0.026, ANOVA) higher concentration in genotype group mama (7.4 ± 2.0 mg/g FW) than in Ma_ (5.4 ± 1.9 mg/g FW). Other sugars, especially the highly abundant fructose, sucrose and glucose, had similar levels across these varieties. Among the seven organic acids (malate, dehydroascorbate, maleate, succinate, fumarate, citrate and quinate), malate was the most abundant (87.2 ± 7.2 % of the total acidity) while quinate (8.3 ± 6.7 %) and maleate (2.5 ± 0.8 %) were distantly followed as the second and third abundant, respectively. Malate concentrations varied significantly (P = 1.03E-9) in the ten apple varieties (Fig. 1a), and were more than 3-fold higher in genotype group Ma_ (7.58 ± 1.23 mg/g FW) than in mama (2.16 ± 0.41 mg/g FW) (Fig. 1b). The concentrations of maleate, succinate, fumarate and citrate were also significantly higher in genotype group Ma_ than in mama (P < 0.0001), but they were at much lower levels (at μg/g FW) (Fig. 1c). However, quinate showed no significant difference between groups Ma_ and mama. The trend of fruit juice titratable acidity (TA) was similar to that of malate in the ten varieties (Fig. 1a, b) while an expected reverse trend was observed for fruit juice pH (Fig. 1d).Fig. 1


Uncovering co-expression gene network modules regulating fruit acidity in diverse apples.

Bai Y, Dougherty L, Cheng L, Zhong GY, Xu K - BMC Genomics (2015)

Evaluation of fruit acidity and causal organic acids. Standard deviations were shown with the error bars. a TA and malate concentrations measured in the ten apple varieties, which were abbreviated as the following: B Britegold, N Novosibirski Sweet, P PI323617, S Sweet Delicious, C Cox’s Orange Pippin, E Empire, F Fuji, G Granny Smith, J Jonathan, R Rome Beauty Law. The first four are of genotype mama whereas the last six of genotype Ma_. b Mean TA and malate concentrations in genotype groups Ma_ and mama. c Concentrations of succinate, fumarate, citrate and maleate in genotype groups Ma_ and mama. d Fruit pH readings in the ten apples
© Copyright Policy - OpenAccess
Related In: Results  -  Collection

License 1 - License 2
Show All Figures
getmorefigures.php?uid=PMC4537561&req=5

Fig1: Evaluation of fruit acidity and causal organic acids. Standard deviations were shown with the error bars. a TA and malate concentrations measured in the ten apple varieties, which were abbreviated as the following: B Britegold, N Novosibirski Sweet, P PI323617, S Sweet Delicious, C Cox’s Orange Pippin, E Empire, F Fuji, G Granny Smith, J Jonathan, R Rome Beauty Law. The first four are of genotype mama whereas the last six of genotype Ma_. b Mean TA and malate concentrations in genotype groups Ma_ and mama. c Concentrations of succinate, fumarate, citrate and maleate in genotype groups Ma_ and mama. d Fruit pH readings in the ten apples
Mentions: Fruit metabolite profiling was conducted using GC-MS with three biological replicates in the ten apple varieties. A total of 19 metabolites were quantified, including 12 soluble sugars and seven organic acids. Among the 12 sugars, only sorbitol showed a significantly (P = 0.026, ANOVA) higher concentration in genotype group mama (7.4 ± 2.0 mg/g FW) than in Ma_ (5.4 ± 1.9 mg/g FW). Other sugars, especially the highly abundant fructose, sucrose and glucose, had similar levels across these varieties. Among the seven organic acids (malate, dehydroascorbate, maleate, succinate, fumarate, citrate and quinate), malate was the most abundant (87.2 ± 7.2 % of the total acidity) while quinate (8.3 ± 6.7 %) and maleate (2.5 ± 0.8 %) were distantly followed as the second and third abundant, respectively. Malate concentrations varied significantly (P = 1.03E-9) in the ten apple varieties (Fig. 1a), and were more than 3-fold higher in genotype group Ma_ (7.58 ± 1.23 mg/g FW) than in mama (2.16 ± 0.41 mg/g FW) (Fig. 1b). The concentrations of maleate, succinate, fumarate and citrate were also significantly higher in genotype group Ma_ than in mama (P < 0.0001), but they were at much lower levels (at μg/g FW) (Fig. 1c). However, quinate showed no significant difference between groups Ma_ and mama. The trend of fruit juice titratable acidity (TA) was similar to that of malate in the ten varieties (Fig. 1a, b) while an expected reverse trend was observed for fruit juice pH (Fig. 1d).Fig. 1

Bottom Line: Network inferring using weighted gene co-expression network analysis (WGCNA) revealed five co-expression gene network modules of significant (P < 0.001) correlation with malate.We also identified 12 intramodular hub genes from each of the five modules and 18 enriched gene ontology (GO) terms and MapMan sub-bines, including two GO terms (GO:0015979 and GO:0009765) and two MapMap sub-bins (1.3.4 and 1.1.1.1) related to photosynthesis in module Turquoise.Using Lemon-Tree algorithms, we identified 12 regulator genes of probabilistic scores 35.5-81.0, including MDP0000525602 (a LLR receptor kinase), MDP0000319170 (an IQD2-like CaM binding protein) and MDP0000190273 (an EIN3-like transcription factor) of greater interest for being one of the 18 MSAGs or one of the 12 intramodular hub genes in Turquoise, and/or a regulator to the cluster containing Ma1.

View Article: PubMed Central - PubMed

Affiliation: Horticulture Section, School of Integrative Plant Science, Cornell University, New York State Agricultural Experiment Station, Geneva, NY, 14456, USA. yb63@cornell.edu.

ABSTRACT

Background: Acidity is a major contributor to fruit quality. Several organic acids are present in apple fruit, but malic acid is predominant and determines fruit acidity. The trait is largely controlled by the Malic acid (Ma) locus, underpinning which Ma1 that putatively encodes a vacuolar aluminum-activated malate transporter1 (ALMT1)-like protein is a strong candidate gene. We hypothesize that fruit acidity is governed by a gene network in which Ma1 is key member. The goal of this study is to identify the gene network and the potential mechanisms through which the network operates.

Results: Guided by Ma1, we analyzed the transcriptomes of mature fruit of contrasting acidity from six apple accessions of genotype Ma_ (MaMa or Mama) and four of mama using RNA-seq and identified 1301 fruit acidity associated genes, among which 18 were most significant acidity genes (MSAGs). Network inferring using weighted gene co-expression network analysis (WGCNA) revealed five co-expression gene network modules of significant (P < 0.001) correlation with malate. Of these, the Ma1 containing module (Turquoise) of 336 genes showed the highest correlation (0.79). We also identified 12 intramodular hub genes from each of the five modules and 18 enriched gene ontology (GO) terms and MapMan sub-bines, including two GO terms (GO:0015979 and GO:0009765) and two MapMap sub-bins (1.3.4 and 1.1.1.1) related to photosynthesis in module Turquoise. Using Lemon-Tree algorithms, we identified 12 regulator genes of probabilistic scores 35.5-81.0, including MDP0000525602 (a LLR receptor kinase), MDP0000319170 (an IQD2-like CaM binding protein) and MDP0000190273 (an EIN3-like transcription factor) of greater interest for being one of the 18 MSAGs or one of the 12 intramodular hub genes in Turquoise, and/or a regulator to the cluster containing Ma1.

Conclusions: The most relevant finding of this study is the identification of the MSAGs, intramodular hub genes, enriched photosynthesis related processes, and regulator genes in a WGCNA module Turquoise that not only encompasses Ma1 but also shows the highest modular correlation with acidity. Overall, this study provides important insight into the Ma1-mediated gene network controlling acidity in mature apple fruit of diverse genetic background.

No MeSH data available.


Related in: MedlinePlus