Gene expression predictions and networks in natural populations supports the omnigenic theory

Abstract Background Recent literature on the differential role of genes within networks distinguishes core from peripheral genes. If previous works have shown contrasting features between them, whether such categorization matters for phenotype prediction remains to be studied. Results We measured 17...

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Main Authors: Aurélien Chateigner, Marie-Claude Lesage-Descauses, Odile Rogier, Véronique Jorge, Jean-Charles Leplé, Véronique Brunaud, Christine Paysant-Le Roux, Ludivine Soubigou-Taconnat, Marie-Laure Martin-Magniette, Leopoldo Sanchez, Vincent Segura
Format: Article
Language:English
Published: BMC 2020-06-01
Series:BMC Genomics
Subjects:
Online Access:http://link.springer.com/article/10.1186/s12864-020-06809-2
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spelling doaj-ac43a819d80143bf8622f38093c0b4b32020-11-25T03:55:06ZengBMCBMC Genomics1471-21642020-06-0121111610.1186/s12864-020-06809-2Gene expression predictions and networks in natural populations supports the omnigenic theoryAurélien Chateigner0Marie-Claude Lesage-Descauses1Odile Rogier2Véronique Jorge3Jean-Charles Leplé4Véronique Brunaud5Christine Paysant-Le Roux6Ludivine Soubigou-Taconnat7Marie-Laure Martin-Magniette8Leopoldo Sanchez9Vincent Segura10BioForA, INRAE, ONFBioForA, INRAE, ONFBioForA, INRAE, ONFBioForA, INRAE, ONFBIOGECO, INRAE, Univ. BordeauxInstitute of Plant Sciences Paris-Saclay (IPS2), CNRS, INRAE, Université Paris-Sud, Université d’Evry, Université Paris-SaclayInstitute of Plant Sciences Paris-Saclay (IPS2), CNRS, INRAE, Université Paris-Sud, Université d’Evry, Université Paris-SaclayInstitute of Plant Sciences Paris-Saclay (IPS2), CNRS, INRAE, Université Paris-Sud, Université d’Evry, Université Paris-SaclayInstitute of Plant Sciences Paris-Saclay (IPS2), CNRS, INRAE, Université Paris-Sud, Université d’Evry, Université Paris-SaclayBioForA, INRAE, ONFBioForA, INRAE, ONFAbstract Background Recent literature on the differential role of genes within networks distinguishes core from peripheral genes. If previous works have shown contrasting features between them, whether such categorization matters for phenotype prediction remains to be studied. Results We measured 17 phenotypic traits for 241 cloned genotypes from a Populus nigra collection, covering growth, phenology, chemical and physical properties. We also sequenced RNA for each genotype and built co-expression networks to define core and peripheral genes. We found that cores were more differentiated between populations than peripherals while being less variable, suggesting that they have been constrained through potentially divergent selection. We also showed that while cores were overrepresented in a subset of genes statistically selected for their capacity to predict the phenotypes (by Boruta algorithm), they did not systematically predict better than peripherals or even random genes. Conclusion Our work is the first attempt to assess the importance of co-expression network connectivity in phenotype prediction. While highly connected core genes appear to be important, they do not bear enough information to systematically predict better quantitative traits than other gene sets.http://link.springer.com/article/10.1186/s12864-020-06809-2CorePeripheralBorutaMachine learningPopulus nigra
collection DOAJ
language English
format Article
sources DOAJ
author Aurélien Chateigner
Marie-Claude Lesage-Descauses
Odile Rogier
Véronique Jorge
Jean-Charles Leplé
Véronique Brunaud
Christine Paysant-Le Roux
Ludivine Soubigou-Taconnat
Marie-Laure Martin-Magniette
Leopoldo Sanchez
Vincent Segura
spellingShingle Aurélien Chateigner
Marie-Claude Lesage-Descauses
Odile Rogier
Véronique Jorge
Jean-Charles Leplé
Véronique Brunaud
Christine Paysant-Le Roux
Ludivine Soubigou-Taconnat
Marie-Laure Martin-Magniette
Leopoldo Sanchez
Vincent Segura
Gene expression predictions and networks in natural populations supports the omnigenic theory
BMC Genomics
Core
Peripheral
Boruta
Machine learning
Populus nigra
author_facet Aurélien Chateigner
Marie-Claude Lesage-Descauses
Odile Rogier
Véronique Jorge
Jean-Charles Leplé
Véronique Brunaud
Christine Paysant-Le Roux
Ludivine Soubigou-Taconnat
Marie-Laure Martin-Magniette
Leopoldo Sanchez
Vincent Segura
author_sort Aurélien Chateigner
title Gene expression predictions and networks in natural populations supports the omnigenic theory
title_short Gene expression predictions and networks in natural populations supports the omnigenic theory
title_full Gene expression predictions and networks in natural populations supports the omnigenic theory
title_fullStr Gene expression predictions and networks in natural populations supports the omnigenic theory
title_full_unstemmed Gene expression predictions and networks in natural populations supports the omnigenic theory
title_sort gene expression predictions and networks in natural populations supports the omnigenic theory
publisher BMC
series BMC Genomics
issn 1471-2164
publishDate 2020-06-01
description Abstract Background Recent literature on the differential role of genes within networks distinguishes core from peripheral genes. If previous works have shown contrasting features between them, whether such categorization matters for phenotype prediction remains to be studied. Results We measured 17 phenotypic traits for 241 cloned genotypes from a Populus nigra collection, covering growth, phenology, chemical and physical properties. We also sequenced RNA for each genotype and built co-expression networks to define core and peripheral genes. We found that cores were more differentiated between populations than peripherals while being less variable, suggesting that they have been constrained through potentially divergent selection. We also showed that while cores were overrepresented in a subset of genes statistically selected for their capacity to predict the phenotypes (by Boruta algorithm), they did not systematically predict better than peripherals or even random genes. Conclusion Our work is the first attempt to assess the importance of co-expression network connectivity in phenotype prediction. While highly connected core genes appear to be important, they do not bear enough information to systematically predict better quantitative traits than other gene sets.
topic Core
Peripheral
Boruta
Machine learning
Populus nigra
url http://link.springer.com/article/10.1186/s12864-020-06809-2
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