Highly interwoven communities of a gene regulatory network unveil topologically important genes for maize seed development

Wenwei Xiong, Chunlei Wang, Xiangbo Zhang, Qinghua Yang, Ruixin Shao, Jinsheng Lai, Chunguang Du

Research output: Contribution to journalArticleResearchpeer-review

4 Citations (Scopus)

Abstract

The complex interactions between transcription factors (TFs) and their target genes in a spatially and temporally specific manner are crucial to all cellular processes. Reconstruction of gene regulatory networks (GRNs) from gene expression profiles can help to decipher TF-gene regulations in a variety of contexts; however, the inevitable prediction errors of GRNs hinder optimal data mining of RNA-Seq transcriptome profiles. Here we perform an integrative study of Zea mays (maize) seed development in order to identify key genes in a complex developmental process. First, we reverse engineered a GRN from 78 maize seed transcriptome profiles. Then, we studied collective gene interaction patterns and uncovered highly interwoven network communities as the building blocks of the GRN. One community, composed of mostly unknown genes interacting with opaque2, brittle endosperm1 and shrunken2, contributes to seed phenotypes. Another community, composed mostly of genes expressed in the basal endosperm transfer layer, is responsible for nutrient transport. We further integrated our inferred GRN with gene expression patterns in different seed compartments and at various developmental stages and pathways. The integration facilitated a biological interpretation of the GRN. Our yeast one-hybrid assays verified six out of eight TF-promoter bindings in the reconstructed GRN. This study identified topologically important genes in interwoven network communities that may be crucial to maize seed development.

Original languageEnglish
Pages (from-to)1143-1156
Number of pages14
JournalPlant Journal
Volume92
Issue number6
DOIs
StatePublished - 1 Dec 2017

Fingerprint

Gene Regulatory Networks
seed development
Zea mays
Seeds
corn
Genes
Transcriptome
genes
Transcription Factors
transcription factors
transcriptome
seeds
Endosperm
Data Mining
gene expression
nutrient transport
Regulator Genes
gene interaction
gene regulatory networks
endosperm

Keywords

  • Zea mays
  • gene regulatory network
  • maize seed development
  • mutual information
  • network community
  • network inference

Cite this

Xiong, Wenwei ; Wang, Chunlei ; Zhang, Xiangbo ; Yang, Qinghua ; Shao, Ruixin ; Lai, Jinsheng ; Du, Chunguang. / Highly interwoven communities of a gene regulatory network unveil topologically important genes for maize seed development. In: Plant Journal. 2017 ; Vol. 92, No. 6. pp. 1143-1156.
@article{77a6cffc46984cedbbe3fdd99fdaade0,
title = "Highly interwoven communities of a gene regulatory network unveil topologically important genes for maize seed development",
abstract = "The complex interactions between transcription factors (TFs) and their target genes in a spatially and temporally specific manner are crucial to all cellular processes. Reconstruction of gene regulatory networks (GRNs) from gene expression profiles can help to decipher TF-gene regulations in a variety of contexts; however, the inevitable prediction errors of GRNs hinder optimal data mining of RNA-Seq transcriptome profiles. Here we perform an integrative study of Zea mays (maize) seed development in order to identify key genes in a complex developmental process. First, we reverse engineered a GRN from 78 maize seed transcriptome profiles. Then, we studied collective gene interaction patterns and uncovered highly interwoven network communities as the building blocks of the GRN. One community, composed of mostly unknown genes interacting with opaque2, brittle endosperm1 and shrunken2, contributes to seed phenotypes. Another community, composed mostly of genes expressed in the basal endosperm transfer layer, is responsible for nutrient transport. We further integrated our inferred GRN with gene expression patterns in different seed compartments and at various developmental stages and pathways. The integration facilitated a biological interpretation of the GRN. Our yeast one-hybrid assays verified six out of eight TF-promoter bindings in the reconstructed GRN. This study identified topologically important genes in interwoven network communities that may be crucial to maize seed development.",
keywords = "Zea mays, gene regulatory network, maize seed development, mutual information, network community, network inference",
author = "Wenwei Xiong and Chunlei Wang and Xiangbo Zhang and Qinghua Yang and Ruixin Shao and Jinsheng Lai and Chunguang Du",
year = "2017",
month = "12",
day = "1",
doi = "10.1111/tpj.13750",
language = "English",
volume = "92",
pages = "1143--1156",
journal = "Plant Journal",
issn = "0960-7412",
publisher = "Wiley-Blackwell Publishing Ltd",
number = "6",

}

Highly interwoven communities of a gene regulatory network unveil topologically important genes for maize seed development. / Xiong, Wenwei; Wang, Chunlei; Zhang, Xiangbo; Yang, Qinghua; Shao, Ruixin; Lai, Jinsheng; Du, Chunguang.

In: Plant Journal, Vol. 92, No. 6, 01.12.2017, p. 1143-1156.

Research output: Contribution to journalArticleResearchpeer-review

TY - JOUR

T1 - Highly interwoven communities of a gene regulatory network unveil topologically important genes for maize seed development

AU - Xiong, Wenwei

AU - Wang, Chunlei

AU - Zhang, Xiangbo

AU - Yang, Qinghua

AU - Shao, Ruixin

AU - Lai, Jinsheng

AU - Du, Chunguang

PY - 2017/12/1

Y1 - 2017/12/1

N2 - The complex interactions between transcription factors (TFs) and their target genes in a spatially and temporally specific manner are crucial to all cellular processes. Reconstruction of gene regulatory networks (GRNs) from gene expression profiles can help to decipher TF-gene regulations in a variety of contexts; however, the inevitable prediction errors of GRNs hinder optimal data mining of RNA-Seq transcriptome profiles. Here we perform an integrative study of Zea mays (maize) seed development in order to identify key genes in a complex developmental process. First, we reverse engineered a GRN from 78 maize seed transcriptome profiles. Then, we studied collective gene interaction patterns and uncovered highly interwoven network communities as the building blocks of the GRN. One community, composed of mostly unknown genes interacting with opaque2, brittle endosperm1 and shrunken2, contributes to seed phenotypes. Another community, composed mostly of genes expressed in the basal endosperm transfer layer, is responsible for nutrient transport. We further integrated our inferred GRN with gene expression patterns in different seed compartments and at various developmental stages and pathways. The integration facilitated a biological interpretation of the GRN. Our yeast one-hybrid assays verified six out of eight TF-promoter bindings in the reconstructed GRN. This study identified topologically important genes in interwoven network communities that may be crucial to maize seed development.

AB - The complex interactions between transcription factors (TFs) and their target genes in a spatially and temporally specific manner are crucial to all cellular processes. Reconstruction of gene regulatory networks (GRNs) from gene expression profiles can help to decipher TF-gene regulations in a variety of contexts; however, the inevitable prediction errors of GRNs hinder optimal data mining of RNA-Seq transcriptome profiles. Here we perform an integrative study of Zea mays (maize) seed development in order to identify key genes in a complex developmental process. First, we reverse engineered a GRN from 78 maize seed transcriptome profiles. Then, we studied collective gene interaction patterns and uncovered highly interwoven network communities as the building blocks of the GRN. One community, composed of mostly unknown genes interacting with opaque2, brittle endosperm1 and shrunken2, contributes to seed phenotypes. Another community, composed mostly of genes expressed in the basal endosperm transfer layer, is responsible for nutrient transport. We further integrated our inferred GRN with gene expression patterns in different seed compartments and at various developmental stages and pathways. The integration facilitated a biological interpretation of the GRN. Our yeast one-hybrid assays verified six out of eight TF-promoter bindings in the reconstructed GRN. This study identified topologically important genes in interwoven network communities that may be crucial to maize seed development.

KW - Zea mays

KW - gene regulatory network

KW - maize seed development

KW - mutual information

KW - network community

KW - network inference

UR - http://www.scopus.com/inward/record.url?scp=85034595700&partnerID=8YFLogxK

U2 - 10.1111/tpj.13750

DO - 10.1111/tpj.13750

M3 - Article

VL - 92

SP - 1143

EP - 1156

JO - Plant Journal

JF - Plant Journal

SN - 0960-7412

IS - 6

ER -