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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

Analysis of module Turquoise. a Module eigengene values across the 29 samples, including 17 in Ma_ on left and 12 in mama on right. Samples are represented by the combination of a letter (abbreviated cultivar name, see Fig. 1’s legend) and a number (replicate 1, 2 or 3). b Correlation between module membership (MM) and gene significance (GS) for malate
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Fig4: Analysis of module Turquoise. a Module eigengene values across the 29 samples, including 17 in Ma_ on left and 12 in mama on right. Samples are represented by the combination of a letter (abbreviated cultivar name, see Fig. 1’s legend) and a number (replicate 1, 2 or 3). b Correlation between module membership (MM) and gene significance (GS) for malate

Mentions: Further WGCNA analysis identified ten network modules in the co-expression network, designated Turquoise, Black, Brown, Pink, Magenta, Red, Green, Blue, Yellow, and Grey (for four unassigned genes) (Fig. 3a, c). Investigating the relationships between module eigengene and acidity uncovered that the correlation coefficients varied widely from −0.67 to 0.79 in malate and from −0.55 to 0.75 in TA (Fig. 3c). The eigengenes (Fig. 4a, Additional file 5: Figure S1A) of five modules Turquoise, Black, Brown, Blue and Yellow showed significant correlations (p < 0.001) with malate, suggesting these five modules had greater relevance in fruit acidity although Blue and Yellow were negatively correlated (Fig. 3c). The five modules comprised 943 genes with module Turquoise being the largest of 336 genes. Notably, the guide gene Ma1 was assigned to Turquoise, which also had the highest modular correlation (r = 0.75–0.79) with acidity (Fig. 3c). Inspecting the correlation between the module memberships (MM) and gene significance (GS) revealed that all modules were significant except Blue (Fig. 4b, Additional file 5: Figure S1B). Again, module Turquoise had the most significant correlation between MM and GS (r =0.49, p = 1.1E-21), indicating genes of higher MM values were more likely of greater GS in Turquoise than in others.Fig. 4


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)

Analysis of module Turquoise. a Module eigengene values across the 29 samples, including 17 in Ma_ on left and 12 in mama on right. Samples are represented by the combination of a letter (abbreviated cultivar name, see Fig. 1’s legend) and a number (replicate 1, 2 or 3). b Correlation between module membership (MM) and gene significance (GS) for malate
© Copyright Policy - OpenAccess
Related In: Results  -  Collection

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getmorefigures.php?uid=PMC4537561&req=5

Fig4: Analysis of module Turquoise. a Module eigengene values across the 29 samples, including 17 in Ma_ on left and 12 in mama on right. Samples are represented by the combination of a letter (abbreviated cultivar name, see Fig. 1’s legend) and a number (replicate 1, 2 or 3). b Correlation between module membership (MM) and gene significance (GS) for malate
Mentions: Further WGCNA analysis identified ten network modules in the co-expression network, designated Turquoise, Black, Brown, Pink, Magenta, Red, Green, Blue, Yellow, and Grey (for four unassigned genes) (Fig. 3a, c). Investigating the relationships between module eigengene and acidity uncovered that the correlation coefficients varied widely from −0.67 to 0.79 in malate and from −0.55 to 0.75 in TA (Fig. 3c). The eigengenes (Fig. 4a, Additional file 5: Figure S1A) of five modules Turquoise, Black, Brown, Blue and Yellow showed significant correlations (p < 0.001) with malate, suggesting these five modules had greater relevance in fruit acidity although Blue and Yellow were negatively correlated (Fig. 3c). The five modules comprised 943 genes with module Turquoise being the largest of 336 genes. Notably, the guide gene Ma1 was assigned to Turquoise, which also had the highest modular correlation (r = 0.75–0.79) with acidity (Fig. 3c). Inspecting the correlation between the module memberships (MM) and gene significance (GS) revealed that all modules were significant except Blue (Fig. 4b, Additional file 5: Figure S1B). Again, module Turquoise had the most significant correlation between MM and GS (r =0.49, p = 1.1E-21), indicating genes of higher MM values were more likely of greater GS in Turquoise than in others.Fig. 4

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