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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

Intramodular hub genes and their total network connectivity changes in genotype groups Ma_ and mama when compared with the combined groups of both genotypes. Shown are modules Black, Blue, Brown, Turquoise and Yellow
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Fig6: Intramodular hub genes and their total network connectivity changes in genotype groups Ma_ and mama when compared with the combined groups of both genotypes. Shown are modules Black, Blue, Brown, Turquoise and Yellow

Mentions: To identify intramodular hub genes, we similarly used the guide gene Ma1, which had an MM of 0.894, ranking 11th in module Turquoise. Based on this information, we defined top 12 genes in MM values from each of the five modules as intramodular hub genes, leading to identification of 60 hub genes (Fig. 6, Additional file 7: Table S6). To evaluate how the 60 hub genes behaved in genotype groups Ma_ and in mama, their respective total network connectivity (kTotal) were calculated and compared with the overall group of both genotypes (Fig. 6, Additional file 7: Table S6). Most of the 60 hub genes showed a large increase in kTotal in mama while a marked reduction in Ma_, suggesting a major pattern of negative correlation between the hub genes’ kTotal changes and acidity levels (Fig. 6). This pattern was true in modules Blue and Yellow (both negatively correlated with acidity), largely true in Brown and Black (both positively correlated with acidity), but largely untrue in Turquoise (most positively correlated with acidity), seemingly providing another means depicting the module-acidity relationship shown early (Fig. 3c).Fig. 6


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)

Intramodular hub genes and their total network connectivity changes in genotype groups Ma_ and mama when compared with the combined groups of both genotypes. Shown are modules Black, Blue, Brown, Turquoise and Yellow
© Copyright Policy - OpenAccess
Related In: Results  -  Collection

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

Fig6: Intramodular hub genes and their total network connectivity changes in genotype groups Ma_ and mama when compared with the combined groups of both genotypes. Shown are modules Black, Blue, Brown, Turquoise and Yellow
Mentions: To identify intramodular hub genes, we similarly used the guide gene Ma1, which had an MM of 0.894, ranking 11th in module Turquoise. Based on this information, we defined top 12 genes in MM values from each of the five modules as intramodular hub genes, leading to identification of 60 hub genes (Fig. 6, Additional file 7: Table S6). To evaluate how the 60 hub genes behaved in genotype groups Ma_ and in mama, their respective total network connectivity (kTotal) were calculated and compared with the overall group of both genotypes (Fig. 6, Additional file 7: Table S6). Most of the 60 hub genes showed a large increase in kTotal in mama while a marked reduction in Ma_, suggesting a major pattern of negative correlation between the hub genes’ kTotal changes and acidity levels (Fig. 6). This pattern was true in modules Blue and Yellow (both negatively correlated with acidity), largely true in Brown and Black (both positively correlated with acidity), but largely untrue in Turquoise (most positively correlated with acidity), seemingly providing another means depicting the module-acidity relationship shown early (Fig. 3c).Fig. 6

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