Bridging physiological and evolutionary time-scales in a gene regulatory network.
Gene regulatory networks (GRNs) govern phenotypic adaptations and reflect the trade-offs between physiological responses and evolutionary adaptation that act at different time-scales. To identify patterns of molecular function and genetic diversity in GRNs, we studied the drought response of the common sunflower, Helianthus annuus, and how the underlying GRN is related to its evolution. We examined the responses of 32,423 expressed sequences to drought and to abscisic acid (ABA) and selected 145 co-expressed transcripts. We characterized their regulatory relationships in nine kinetic studies based on different hormones. From this, we inferred a GRN by meta-analyses of a Gaussian graphical model and a random forest algorithm and studied the genetic differentiation among populations (FST ) at nodes. We identified two main hubs in the network that transport nitrate in guard cells. This suggests that nitrate transport is a critical aspect of the sunflower physiological response to drought. We observed that differentiation of the network genes in elite sunflower cultivars is correlated with their position and connectivity. This systems biology approach combined molecular data at different time-scales and identified important physiological processes. At the evolutionary level, we propose that network topology could influence responses to human selection and possibly adaptation to dry environments.
INRA, Laboratoire des Interactions Plantes-Microorganismes (LIPM), UMR441, F-31326, Castanet-Tolosan, France.|CNRS, Laboratoire des Interactions Plantes-Microorganismes (LIPM), UMR2594, F-31326, Castanet-Tolosan, France.
Gwenaëlle
G
Marchand
Department of Electrical Engineering and Computer Science and GIGA-R, Systems and Modeling, University of Liège, Liège, Belgium.
Vân Anh
VA
Huynh-Thu
Department of Ecology and Evolutionary Biology, University of Colorado at Boulder, Boulder, CO, 80309, USA.
Nolan C
NC
Kane
INRA, Unité de Recherche en Génomique Végétale (URGV), UMR1165 - Université d'Evry Val d'Essonne - ERL CNRS 8196, CP 5708, F-91057, Evry Cedex, France.
Sandrine
S
Arribat
INRA, Laboratoire des Interactions Plantes-Microorganismes (LIPM), UMR441, F-31326, Castanet-Tolosan, France.|CNRS, Laboratoire des Interactions Plantes-Microorganismes (LIPM), UMR2594, F-31326, Castanet-Tolosan, France.
Didier
D
Varès
INRA, Laboratoire des Interactions Plantes-Microorganismes (LIPM), UMR441, F-31326, Castanet-Tolosan, France.|CNRS, Laboratoire des Interactions Plantes-Microorganismes (LIPM), UMR2594, F-31326, Castanet-Tolosan, France.
David
D
Rengel
INRA, Unité de Recherche en Génomique Végétale (URGV), UMR1165 - Université d'Evry Val d'Essonne - ERL CNRS 8196, CP 5708, F-91057, Evry Cedex, France.
Sandrine
S
Balzergue
Department of Botany, University of British Columbia, Vancouver, BC, V6T 1Z4, Canada.|Department of Biology, Indiana University, Bloomington, IN, 47405, USA.
Loren H
LH
Rieseberg
INRA, Laboratoire des Interactions Plantes-Microorganismes (LIPM), UMR441, F-31326, Castanet-Tolosan, France.|CNRS, Laboratoire des Interactions Plantes-Microorganismes (LIPM), UMR2594, F-31326, Castanet-Tolosan, France.
Patrick
P
Vincourt
Department of Electrical Engineering and Computer Science and GIGA-R, Systems and Modeling, University of Liège, Liège, Belgium.
Pierre
P
Geurts
INRA, Mathématiques et Informatique Appliquées (MIA), UPR875, F-31326, Castanet-Tolosan, France.
Matthieu
M
Vignes
INRA, Laboratoire des Interactions Plantes-Microorganismes (LIPM), UMR441, F-31326, Castanet-Tolosan, France.|CNRS, Laboratoire des Interactions Plantes-Microorganismes (LIPM), UMR2594, F-31326, Castanet-Tolosan, France.
Nicolas B
NB
Langlade
D000040:Abscisic Acid / Q000235:genetics; D000465:Algorithms; D005075:Biological Evolution; D055864:Droughts; D018506:Gene Expression Regulation, Plant; D053263:Gene Regulatory Networks; D006368:Helianthus / Q000235:genetics* / Q000502:physiology; D008957:Models, Genetic; D009566:Nitrates / Q000378:metabolism; D010940:Plant Proteins / Q000235:genetics / Q000378:metabolism; D059467:Transcriptome
D009566:Nitrates; D010940:Plant Proteins; D000040:Abscisic Acid
CLC-A chloride channel protein; F

ST; NITRATE TRANSPORTER 1.1 (NRT1.1); abscisic acid (ABA); drought; genetic differentiation; network inference