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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

The most significant acidity genes (MSAGs). a Expression profile (square root of RPKM) of the 18 MSAGs. Each row represents a gene as listed on right. Each column stands for a sample as specified by sample names (see the legend in Fig. 1 for keys) at lower panel. Clustering of genes and samples was shown with distance on left and top panels, respectively. The expression of genes is color coded from low (dark blue) through mean (black) and through high (bright yellow). The bright yellow color across the samples for Ma1 and M190293 indicate the expression of these two genes were all close to or exceeded the high end of the scale at bottom. b Distribution of the 18 MSAGs in modules. Modules with zero genes are not shown. Note that genes of IDs beginning with letter ‘G’ are referred to the novel transcripts [25], and the apple reference gene IDs are abbreviated (e.g. M250124 stands for MDP0000250124)
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Fig5: The most significant acidity genes (MSAGs). a Expression profile (square root of RPKM) of the 18 MSAGs. Each row represents a gene as listed on right. Each column stands for a sample as specified by sample names (see the legend in Fig. 1 for keys) at lower panel. Clustering of genes and samples was shown with distance on left and top panels, respectively. The expression of genes is color coded from low (dark blue) through mean (black) and through high (bright yellow). The bright yellow color across the samples for Ma1 and M190293 indicate the expression of these two genes were all close to or exceeded the high end of the scale at bottom. b Distribution of the 18 MSAGs in modules. Modules with zero genes are not shown. Note that genes of IDs beginning with letter ‘G’ are referred to the novel transcripts [25], and the apple reference gene IDs are abbreviated (e.g. M250124 stands for MDP0000250124)

Mentions: The 1301 FAAGs had a range of absolute gene significance (GS) for malate from 0.004 to 0.911 (Fig. 3b). We define that the most significant acidity genes (MSAGs) are those of GS for malate ≥0.801, the observed GS of the guide gene Ma1. This allowed to identify 18 MSAGs (Fig. 5a, Additional file 6: Table S5), including three transporters (M282275, M834327 and Ma1), two receptor kinases (M525602, M651862), one Ethylene-Insensitive3 (EIN3)-like transcription factor (M190273), one pyruvatedehydrogenase complex component E2 (M727725), one endo-1,4-beta-xylanase/ hydrolase (M225641), one glutamine synthetase cytosolic isozyme (G202922), one photosystem II subunit R (M800352), and seven (M364253, M442350, M345601, G103681, M230253, G106959, G104167 and G104764) of unknown function. The 18 MSAGs were distributed in three modules with 12 in Turquoise, three in Black and another three in Blue (Fig. 5b, Additional file 6: Table S5), further indicating module Turquoise is of greater relevance in acidity.Fig. 5


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)

The most significant acidity genes (MSAGs). a Expression profile (square root of RPKM) of the 18 MSAGs. Each row represents a gene as listed on right. Each column stands for a sample as specified by sample names (see the legend in Fig. 1 for keys) at lower panel. Clustering of genes and samples was shown with distance on left and top panels, respectively. The expression of genes is color coded from low (dark blue) through mean (black) and through high (bright yellow). The bright yellow color across the samples for Ma1 and M190293 indicate the expression of these two genes were all close to or exceeded the high end of the scale at bottom. b Distribution of the 18 MSAGs in modules. Modules with zero genes are not shown. Note that genes of IDs beginning with letter ‘G’ are referred to the novel transcripts [25], and the apple reference gene IDs are abbreviated (e.g. M250124 stands for MDP0000250124)
© Copyright Policy - OpenAccess
Related In: Results  -  Collection

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

Fig5: The most significant acidity genes (MSAGs). a Expression profile (square root of RPKM) of the 18 MSAGs. Each row represents a gene as listed on right. Each column stands for a sample as specified by sample names (see the legend in Fig. 1 for keys) at lower panel. Clustering of genes and samples was shown with distance on left and top panels, respectively. The expression of genes is color coded from low (dark blue) through mean (black) and through high (bright yellow). The bright yellow color across the samples for Ma1 and M190293 indicate the expression of these two genes were all close to or exceeded the high end of the scale at bottom. b Distribution of the 18 MSAGs in modules. Modules with zero genes are not shown. Note that genes of IDs beginning with letter ‘G’ are referred to the novel transcripts [25], and the apple reference gene IDs are abbreviated (e.g. M250124 stands for MDP0000250124)
Mentions: The 1301 FAAGs had a range of absolute gene significance (GS) for malate from 0.004 to 0.911 (Fig. 3b). We define that the most significant acidity genes (MSAGs) are those of GS for malate ≥0.801, the observed GS of the guide gene Ma1. This allowed to identify 18 MSAGs (Fig. 5a, Additional file 6: Table S5), including three transporters (M282275, M834327 and Ma1), two receptor kinases (M525602, M651862), one Ethylene-Insensitive3 (EIN3)-like transcription factor (M190273), one pyruvatedehydrogenase complex component E2 (M727725), one endo-1,4-beta-xylanase/ hydrolase (M225641), one glutamine synthetase cytosolic isozyme (G202922), one photosystem II subunit R (M800352), and seven (M364253, M442350, M345601, G103681, M230253, G106959, G104167 and G104764) of unknown function. The 18 MSAGs were distributed in three modules with 12 in Turquoise, three in Black and another three in Blue (Fig. 5b, Additional file 6: Table S5), further indicating module Turquoise is of greater relevance in acidity.Fig. 5

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