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

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-...

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Autores principales: Bai, Yang, Dougherty, Laura, Cheng, Lailiang, Zhong, Gan-Yuan, Xu, Kenong
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2015
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4537561/
https://www.ncbi.nlm.nih.gov/pubmed/26276125
http://dx.doi.org/10.1186/s12864-015-1816-6
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author Bai, Yang
Dougherty, Laura
Cheng, Lailiang
Zhong, Gan-Yuan
Xu, Kenong
author_facet Bai, Yang
Dougherty, Laura
Cheng, Lailiang
Zhong, Gan-Yuan
Xu, Kenong
author_sort Bai, Yang
collection PubMed
description 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. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/s12864-015-1816-6) contains supplementary material, which is available to authorized users.
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spelling pubmed-45375612015-08-16 Uncovering co-expression gene network modules regulating fruit acidity in diverse apples Bai, Yang Dougherty, Laura Cheng, Lailiang Zhong, Gan-Yuan Xu, Kenong BMC Genomics Research Article 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. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (doi:10.1186/s12864-015-1816-6) contains supplementary material, which is available to authorized users. BioMed Central 2015-08-16 /pmc/articles/PMC4537561/ /pubmed/26276125 http://dx.doi.org/10.1186/s12864-015-1816-6 Text en © Bai et al. 2015 Open Access This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The Creative Commons Public Domain Dedication waiver (http://creativecommons.org/publicdomain/zero/1.0/) applies to the data made available in this article, unless otherwise stated.
spellingShingle Research Article
Bai, Yang
Dougherty, Laura
Cheng, Lailiang
Zhong, Gan-Yuan
Xu, Kenong
Uncovering co-expression gene network modules regulating fruit acidity in diverse apples
title Uncovering co-expression gene network modules regulating fruit acidity in diverse apples
title_full Uncovering co-expression gene network modules regulating fruit acidity in diverse apples
title_fullStr Uncovering co-expression gene network modules regulating fruit acidity in diverse apples
title_full_unstemmed Uncovering co-expression gene network modules regulating fruit acidity in diverse apples
title_short Uncovering co-expression gene network modules regulating fruit acidity in diverse apples
title_sort uncovering co-expression gene network modules regulating fruit acidity in diverse apples
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4537561/
https://www.ncbi.nlm.nih.gov/pubmed/26276125
http://dx.doi.org/10.1186/s12864-015-1816-6
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