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Comparative network analysis reveals that tissue specificity and gene function are important factors influencing the mode of expression evolution in Arabidopsis and rice

Sara Movahedi UGent, Yves Van de Peer UGent and Klaas Vandepoele UGent (2011) PLANT PHYSIOLOGY. 156(3). p.1316-1330
abstract
Microarray experiments have yielded massive amounts of expression information measured under various conditions for the model species Arabidopsis (Arabidopsis thaliana) and rice (Oryza sativa). Expression compendia grouping multiple experiments make it possible to define correlated gene expression patterns within one species and to study how expression has evolved between species. We developed a robust framework to measure expression context conservation (ECC) and found, by analyzing 4,630 pairs of orthologous Arabidopsis and rice genes, that 77% showed conserved coexpression. Examples of nonconserved ECC categories suggested a link between regulatory evolution and environmental adaptations and included genes involved in signal transduction, response to different abiotic stresses, and hormone stimuli. To identify genomic features that influence expression evolution, we analyzed the relationship between ECC, tissue specificity, and protein evolution. Tissue-specific genes showed higher expression conservation compared with broadly expressed genes but were fast evolving at the protein level. No significant correlation was found between protein and expression evolution, implying that both modes of gene evolution are not strongly coupled in plants. By integration of cis-regulatory elements, many ECC conserved genes were significantly enriched for shared DNA motifs, hinting at the conservation of ancestral regulatory interactions in both model species. Surprisingly, for several tissue-specific genes, patterns of concerted network evolution were observed, unveiling conserved coexpression in the absence of conservation of tissue specificity. These findings demonstrate that orthologs inferred through sequence similarity in many cases do not share similar biological functions and highlight the importance of incorporating expression information when comparing genes across species.
Please use this url to cite or link to this publication:
author
organization
year
type
journalArticle (original)
publication status
published
subject
keyword
TRANSCRIPTOME, STRESS, SEQUENCE, CONSERVATION, DIVERGENCE, DUPLICATE GENES, SUBSTITUTION RATES, LOCAL COEXPRESSION DOMAINS, COMPARATIVE GENOMICS, CIS-REGULATORY ELEMENTS
journal title
PLANT PHYSIOLOGY
Plant Physiol.
volume
156
issue
3
pages
1316 - 1330
Web of Science type
Article
Web of Science id
000292294100030
JCR category
PLANT SCIENCES
JCR impact factor
6.535 (2011)
JCR rank
7/189 (2011)
JCR quartile
1 (2011)
ISSN
0032-0889
DOI
10.1104/pp.111.177865
project
Bioinformatics: from nucleotids to networks (N2N)
language
English
UGent publication?
yes
classification
A1
copyright statement
I have transferred the copyright for this publication to the publisher
id
1864506
handle
http://hdl.handle.net/1854/LU-1864506
date created
2011-08-01 17:50:49
date last changed
2013-02-27 09:11:21
@article{1864506,
  abstract     = {Microarray experiments have yielded massive amounts of expression information measured under various conditions for the model species Arabidopsis (Arabidopsis thaliana) and rice (Oryza sativa). Expression compendia grouping multiple experiments make it possible to define correlated gene expression patterns within one species and to study how expression has evolved between species. We developed a robust framework to measure expression context conservation (ECC) and found, by analyzing 4,630 pairs of orthologous Arabidopsis and rice genes, that 77\% showed conserved coexpression. Examples of nonconserved ECC categories suggested a link between regulatory evolution and environmental adaptations and included genes involved in signal transduction, response to different abiotic stresses, and hormone stimuli. To identify genomic features that influence expression evolution, we analyzed the relationship between ECC, tissue specificity, and protein evolution. Tissue-specific genes showed higher expression conservation compared with broadly expressed genes but were fast evolving at the protein level. No significant correlation was found between protein and expression evolution, implying that both modes of gene evolution are not strongly coupled in plants. By integration of cis-regulatory elements, many ECC conserved genes were significantly enriched for shared DNA motifs, hinting at the conservation of ancestral regulatory interactions in both model species. Surprisingly, for several tissue-specific genes, patterns of concerted network evolution were observed, unveiling conserved coexpression in the absence of conservation of tissue specificity. These findings demonstrate that orthologs inferred through sequence similarity in many cases do not share similar biological functions and highlight the importance of incorporating expression information when comparing genes across species.},
  author       = {Movahedi, Sara and Van de Peer, Yves and Vandepoele, Klaas},
  issn         = {0032-0889},
  journal      = {PLANT PHYSIOLOGY},
  keyword      = {TRANSCRIPTOME,STRESS,SEQUENCE,CONSERVATION,DIVERGENCE,DUPLICATE GENES,SUBSTITUTION RATES,LOCAL COEXPRESSION DOMAINS,COMPARATIVE GENOMICS,CIS-REGULATORY ELEMENTS},
  language     = {eng},
  number       = {3},
  pages        = {1316--1330},
  title        = {Comparative network analysis reveals that tissue specificity and gene function are important factors influencing the mode of expression evolution in Arabidopsis and rice},
  url          = {http://dx.doi.org/10.1104/pp.111.177865},
  volume       = {156},
  year         = {2011},
}

Chicago
Movahedi, Sara, Yves Van de Peer, and Klaas Vandepoele. 2011. “Comparative Network Analysis Reveals That Tissue Specificity and Gene Function Are Important Factors Influencing the Mode of Expression Evolution in Arabidopsis and Rice.” Plant Physiology 156 (3): 1316–1330.
APA
Movahedi, S., Van de Peer, Y., & Vandepoele, K. (2011). Comparative network analysis reveals that tissue specificity and gene function are important factors influencing the mode of expression evolution in Arabidopsis and rice. PLANT PHYSIOLOGY, 156(3), 1316–1330.
Vancouver
1.
Movahedi S, Van de Peer Y, Vandepoele K. Comparative network analysis reveals that tissue specificity and gene function are important factors influencing the mode of expression evolution in Arabidopsis and rice. PLANT PHYSIOLOGY. 2011;156(3):1316–30.
MLA
Movahedi, Sara, Yves Van de Peer, and Klaas Vandepoele. “Comparative Network Analysis Reveals That Tissue Specificity and Gene Function Are Important Factors Influencing the Mode of Expression Evolution in Arabidopsis and Rice.” PLANT PHYSIOLOGY 156.3 (2011): 1316–1330. Print.