Cargando…

Genome-wide dynamic network analysis reveals a critical transition state of flower development in Arabidopsis

BACKGROUND: The flowering transition which is controlled by a complex and intricate gene regulatory network plays an important role in the reproduction for offspring of plants. It is a challenge to identify the critical transition state as well as the genes that control the transition of flower deve...

Descripción completa

Detalles Bibliográficos
Autores principales: Zhang, Fuping, Liu, Xiaoping, Zhang, Aidi, Jiang, Zhonglin, Chen, Luonan, Zhang, Xiujun
Formato: Online Artículo Texto
Lenguaje:English
Publicado: BioMed Central 2019
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6323737/
https://www.ncbi.nlm.nih.gov/pubmed/30616516
http://dx.doi.org/10.1186/s12870-018-1589-6
_version_ 1783385825819492352
author Zhang, Fuping
Liu, Xiaoping
Zhang, Aidi
Jiang, Zhonglin
Chen, Luonan
Zhang, Xiujun
author_facet Zhang, Fuping
Liu, Xiaoping
Zhang, Aidi
Jiang, Zhonglin
Chen, Luonan
Zhang, Xiujun
author_sort Zhang, Fuping
collection PubMed
description BACKGROUND: The flowering transition which is controlled by a complex and intricate gene regulatory network plays an important role in the reproduction for offspring of plants. It is a challenge to identify the critical transition state as well as the genes that control the transition of flower development. With the emergence of massively parallel sequencing, a great number of time-course transcriptome data greatly facilitate the exploration of the developmental phase transition in plants. Although some network-based bioinformatics analyses attempted to identify the genes that control the phase transition, they generally overlooked the dynamics of regulation and resulted in unreliable results. In addition, the results of these methods cannot be self-explained. RESULTS: In this work, to reveal a critical transition state and identify the transition-specific genes of flower development, we implemented a genome-wide dynamic network analysis on temporal gene expression data in Arabidopsis by dynamic network biomarker (DNB) method. In the analysis, DNB model which can exploit collective fluctuations and correlations of different metabolites at a network level was used to detect the imminent critical transition state or the tipping point. The genes that control the phase transition can be identified by the difference of weighted correlations between the genes interested and the other genes in the global network. To construct the gene regulatory network controlling the flowering transition, we applied NARROMI algorithm which can reduce the noisy, redundant and indirect regulations on the expression data of the transition-specific genes. In the results, the critical transition state detected during the formation of flowers corresponded to the development of flowering on the 7th to 9th day in Arabidopsis. Among of 233 genes identified to be highly fluctuated at the transition state, a high percentage of genes with maximum expression in pollen was detected, and 24 genes were validated to participate in stress reaction process, as well as other floral-related pathways. Composed of three major subnetworks, a gene regulatory network with 150 nodes and 225 edges was found to be highly correlated with flowering transition. The gene ontology (GO) annotation of pathway enrichment analysis revealed that the identified genes are enriched in the catalytic activity, metabolic process and cellular process. CONCLUSIONS: This study provides a novel insight to identify the real causality of the phase transition with genome-wide dynamic network analysis. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (10.1186/s12870-018-1589-6) contains supplementary material, which is available to authorized users.
format Online
Article
Text
id pubmed-6323737
institution National Center for Biotechnology Information
language English
publishDate 2019
publisher BioMed Central
record_format MEDLINE/PubMed
spelling pubmed-63237372019-01-10 Genome-wide dynamic network analysis reveals a critical transition state of flower development in Arabidopsis Zhang, Fuping Liu, Xiaoping Zhang, Aidi Jiang, Zhonglin Chen, Luonan Zhang, Xiujun BMC Plant Biol Research Article BACKGROUND: The flowering transition which is controlled by a complex and intricate gene regulatory network plays an important role in the reproduction for offspring of plants. It is a challenge to identify the critical transition state as well as the genes that control the transition of flower development. With the emergence of massively parallel sequencing, a great number of time-course transcriptome data greatly facilitate the exploration of the developmental phase transition in plants. Although some network-based bioinformatics analyses attempted to identify the genes that control the phase transition, they generally overlooked the dynamics of regulation and resulted in unreliable results. In addition, the results of these methods cannot be self-explained. RESULTS: In this work, to reveal a critical transition state and identify the transition-specific genes of flower development, we implemented a genome-wide dynamic network analysis on temporal gene expression data in Arabidopsis by dynamic network biomarker (DNB) method. In the analysis, DNB model which can exploit collective fluctuations and correlations of different metabolites at a network level was used to detect the imminent critical transition state or the tipping point. The genes that control the phase transition can be identified by the difference of weighted correlations between the genes interested and the other genes in the global network. To construct the gene regulatory network controlling the flowering transition, we applied NARROMI algorithm which can reduce the noisy, redundant and indirect regulations on the expression data of the transition-specific genes. In the results, the critical transition state detected during the formation of flowers corresponded to the development of flowering on the 7th to 9th day in Arabidopsis. Among of 233 genes identified to be highly fluctuated at the transition state, a high percentage of genes with maximum expression in pollen was detected, and 24 genes were validated to participate in stress reaction process, as well as other floral-related pathways. Composed of three major subnetworks, a gene regulatory network with 150 nodes and 225 edges was found to be highly correlated with flowering transition. The gene ontology (GO) annotation of pathway enrichment analysis revealed that the identified genes are enriched in the catalytic activity, metabolic process and cellular process. CONCLUSIONS: This study provides a novel insight to identify the real causality of the phase transition with genome-wide dynamic network analysis. ELECTRONIC SUPPLEMENTARY MATERIAL: The online version of this article (10.1186/s12870-018-1589-6) contains supplementary material, which is available to authorized users. BioMed Central 2019-01-07 /pmc/articles/PMC6323737/ /pubmed/30616516 http://dx.doi.org/10.1186/s12870-018-1589-6 Text en © The Author(s). 2019 Open AccessThis 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
Zhang, Fuping
Liu, Xiaoping
Zhang, Aidi
Jiang, Zhonglin
Chen, Luonan
Zhang, Xiujun
Genome-wide dynamic network analysis reveals a critical transition state of flower development in Arabidopsis
title Genome-wide dynamic network analysis reveals a critical transition state of flower development in Arabidopsis
title_full Genome-wide dynamic network analysis reveals a critical transition state of flower development in Arabidopsis
title_fullStr Genome-wide dynamic network analysis reveals a critical transition state of flower development in Arabidopsis
title_full_unstemmed Genome-wide dynamic network analysis reveals a critical transition state of flower development in Arabidopsis
title_short Genome-wide dynamic network analysis reveals a critical transition state of flower development in Arabidopsis
title_sort genome-wide dynamic network analysis reveals a critical transition state of flower development in arabidopsis
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC6323737/
https://www.ncbi.nlm.nih.gov/pubmed/30616516
http://dx.doi.org/10.1186/s12870-018-1589-6
work_keys_str_mv AT zhangfuping genomewidedynamicnetworkanalysisrevealsacriticaltransitionstateofflowerdevelopmentinarabidopsis
AT liuxiaoping genomewidedynamicnetworkanalysisrevealsacriticaltransitionstateofflowerdevelopmentinarabidopsis
AT zhangaidi genomewidedynamicnetworkanalysisrevealsacriticaltransitionstateofflowerdevelopmentinarabidopsis
AT jiangzhonglin genomewidedynamicnetworkanalysisrevealsacriticaltransitionstateofflowerdevelopmentinarabidopsis
AT chenluonan genomewidedynamicnetworkanalysisrevealsacriticaltransitionstateofflowerdevelopmentinarabidopsis
AT zhangxiujun genomewidedynamicnetworkanalysisrevealsacriticaltransitionstateofflowerdevelopmentinarabidopsis