title: Genetic architecture of plant stress resistance: multi-trait genome-wide association mapping.
abstract: Plants are exposed to combinations of various biotic and abiotic stresses, but stress responses are usually investigated for single stresses only. Here, we investigated the genetic architecture underlying plant responses to 11 single stresses and several of their combinations by phenotyping 350 Arabidopsis thaliana accessions. A set of 214 000 single nucleotide polymorphisms (SNPs) was screened for marker-trait associations in genome-wide association (GWA) analyses using tailored multi-trait mixed models. Stress responses that share phytohormonal signaling pathways also share genetic architecture underlying these responses. After removing the effects of general robustness, for the 30 most significant SNPs, average quantitative trait locus (QTL) effect sizes were larger for dual stresses than for single stresses. Plants appear to deploy broad-spectrum defensive mechanisms influencing multiple traits in response to combined stresses. Association analyses identified QTLs with contrasting and with similar responses to biotic vs abiotic stresses, and below-ground vs above-ground stresses. Our approach allowed for an unprecedented comprehensive genetic analysis of how plants deal with a wide spectrum of stress conditions.
authors.affiliation: Laboratory of Entomology, Wageningen University and Research, PO Box 16, 6700 AA, Wageningen, the Netherlands.|Laboratory of Plant Physiology, Wageningen University and Research, PO Box 16, 6700 AA, Wageningen, the Netherlands.|Business Unit Bioscience, Wageningen Plant Research, Wageningen University and Research, PO Box 16, 6700 AA, Wageningen, the Netherlands.
authors.forename: Manus P M
authors.initials: MP
authors.lastname: Thoen
authors.affiliation: Laboratory of Entomology, Wageningen University and Research, PO Box 16, 6700 AA, Wageningen, the Netherlands.
authors.forename: Nelson H
authors.initials: NH
authors.lastname: Davila Olivas
authors.affiliation: Laboratory of Entomology, Wageningen University and Research, PO Box 16, 6700 AA, Wageningen, the Netherlands.|Laboratory of Plant Physiology, Wageningen University and Research, PO Box 16, 6700 AA, Wageningen, the Netherlands.|Business Unit Bioscience, Wageningen Plant Research, Wageningen University and Research, PO Box 16, 6700 AA, Wageningen, the Netherlands.
authors.forename: Karen J
authors.initials: KJ
authors.lastname: Kloth
authors.affiliation: Plant-Microbe Interactions, Department of Biology, Utrecht University, PO Box 800.56, 3508 TB, Utrecht, the Netherlands.
authors.forename: Silvia
authors.initials: S
authors.lastname: Coolen
authors.affiliation: Laboratory of Genetics, Wageningen University and Research, PO Box 16, 6700 AA, Wageningen, the Netherlands.
authors.forename: Ping-Ping
authors.initials: PP
authors.lastname: Huang
authors.affiliation: Laboratory of Genetics, Wageningen University and Research, PO Box 16, 6700 AA, Wageningen, the Netherlands.
authors.forename: Mark G M
authors.identifier: http://orcid.org/0000-0001-5257-0740
authors.initials: MG
authors.lastname: Aarts
authors.affiliation: Laboratory of Plant Physiology, Wageningen University and Research, PO Box 16, 6700 AA, Wageningen, the Netherlands.|Laboratory of Genetics, Wageningen University and Research, PO Box 16, 6700 AA, Wageningen, the Netherlands.
authors.forename: Johanna A
authors.initials: JA
authors.lastname: Bac-Molenaar
authors.affiliation: Laboratory of Nematology, Wageningen University and Research, PO Box 8213, 6700 ES, Wageningen, the Netherlands.
authors.forename: Jaap
authors.initials: J
authors.lastname: Bakker
authors.affiliation: Laboratory of Plant Physiology, Wageningen University and Research, PO Box 16, 6700 AA, Wageningen, the Netherlands.
authors.forename: Harro J
authors.initials: HJ
authors.lastname: Bouwmeester
authors.affiliation: Plant-Microbe Interactions, Department of Biology, Utrecht University, PO Box 800.56, 3508 TB, Utrecht, the Netherlands.|Wageningen University and Research Plant Breeding, Wageningen University and Research, PO Box 386, 6700 AJ, Wageningen, the Netherlands.
authors.forename: Colette
authors.initials: C
authors.lastname: Broekgaarden
authors.affiliation: Wageningen University and Research Plant Breeding, Wageningen University and Research, PO Box 386, 6700 AJ, Wageningen, the Netherlands.
authors.forename: Johan
authors.initials: J
authors.lastname: Bucher
authors.affiliation: Laboratory of Entomology, Wageningen University and Research, PO Box 16, 6700 AA, Wageningen, the Netherlands.|Laboratory of Plant Physiology, Wageningen University and Research, PO Box 16, 6700 AA, Wageningen, the Netherlands.|Business Unit Bioscience, Wageningen Plant Research, Wageningen University and Research, PO Box 16, 6700 AA, Wageningen, the Netherlands.
authors.forename: Jacqueline
authors.initials: J
authors.lastname: Busscher-Lange
authors.affiliation: Laboratory of Plant Physiology, Wageningen University and Research, PO Box 16, 6700 AA, Wageningen, the Netherlands.
authors.forename: Xi
authors.initials: X
authors.lastname: Cheng
authors.affiliation: Laboratory of Plant Physiology, Wageningen University and Research, PO Box 16, 6700 AA, Wageningen, the Netherlands.
authors.forename: Emilie F
authors.initials: EF
authors.lastname: Fradin
authors.affiliation: Business Unit Bioscience, Wageningen Plant Research, Wageningen University and Research, PO Box 16, 6700 AA, Wageningen, the Netherlands.
authors.forename: Maarten A
authors.initials: MA
authors.lastname: Jongsma
authors.affiliation: Section of Plant Physiology, Swammerdam Institute for Life Sciences, University of Amsterdam, PO Box 94215, 1090 GE, Amsterdam, the Netherlands.|Section of Plant Cell Biology, Swammerdam Institute for Life Sciences, University of Amsterdam, PO Box 94215, 1090 GE, Amsterdam, the Netherlands.
authors.forename: Magdalena M
authors.initials: MM
authors.lastname: Julkowska
authors.affiliation: Laboratory of Genetics, Wageningen University and Research, PO Box 16, 6700 AA, Wageningen, the Netherlands.
authors.forename: Joost J B
authors.initials: JJ
authors.lastname: Keurentjes
authors.affiliation: Laboratory of Plant Physiology, Wageningen University and Research, PO Box 16, 6700 AA, Wageningen, the Netherlands.
authors.forename: Wilco
authors.initials: W
authors.lastname: Ligterink
authors.affiliation: Plant-Microbe Interactions, Department of Biology, Utrecht University, PO Box 800.56, 3508 TB, Utrecht, the Netherlands.
authors.forename: Corné M J
authors.initials: CM
authors.lastname: Pieterse
authors.affiliation: Laboratory of Plant Physiology, Wageningen University and Research, PO Box 16, 6700 AA, Wageningen, the Netherlands.
authors.forename: Carolien
authors.initials: C
authors.lastname: Ruyter-Spira
authors.affiliation: Laboratory of Nematology, Wageningen University and Research, PO Box 8213, 6700 ES, Wageningen, the Netherlands.
authors.forename: Geert
authors.initials: G
authors.lastname: Smant
authors.affiliation: Section of Plant Physiology, Swammerdam Institute for Life Sciences, University of Amsterdam, PO Box 94215, 1090 GE, Amsterdam, the Netherlands.|Section of Plant Cell Biology, Swammerdam Institute for Life Sciences, University of Amsterdam, PO Box 94215, 1090 GE, Amsterdam, the Netherlands.
authors.forename: Christa
authors.initials: C
authors.lastname: Testerink
authors.affiliation: Institute for Biology I, RWTH Aachen University, Worringer Weg 3, 52074, Aachen, Germany.
authors.forename: Björn
authors.initials: B
authors.lastname: Usadel
authors.affiliation: Laboratory of Entomology, Wageningen University and Research, PO Box 16, 6700 AA, Wageningen, the Netherlands.
authors.forename: Joop J A
authors.initials: JJ
authors.lastname: van Loon
authors.affiliation: Plant-Microbe Interactions, Department of Biology, Utrecht University, PO Box 800.56, 3508 TB, Utrecht, the Netherlands.
authors.forename: Johan A
authors.initials: JA
authors.lastname: van Pelt
authors.affiliation: Laboratory of Nematology, Wageningen University and Research, PO Box 8213, 6700 ES, Wageningen, the Netherlands.
authors.forename: Casper C
authors.initials: CC
authors.lastname: van Schaik
authors.affiliation: Plant-Microbe Interactions, Department of Biology, Utrecht University, PO Box 800.56, 3508 TB, Utrecht, the Netherlands.
authors.forename: Saskia C M
authors.initials: SC
authors.lastname: van Wees
authors.affiliation: Wageningen University and Research Plant Breeding, Wageningen University and Research, PO Box 386, 6700 AJ, Wageningen, the Netherlands.
authors.forename: Richard G F
authors.initials: RG
authors.lastname: Visser
authors.affiliation: Wageningen University and Research Plant Breeding, Wageningen University and Research, PO Box 386, 6700 AJ, Wageningen, the Netherlands.
authors.forename: Roeland
authors.initials: R
authors.lastname: Voorrips
authors.affiliation: Wageningen University and Research Plant Breeding, Wageningen University and Research, PO Box 386, 6700 AJ, Wageningen, the Netherlands.
authors.forename: Ben
authors.initials: B
authors.lastname: Vosman
authors.affiliation: Laboratory of Plant Physiology, Wageningen University and Research, PO Box 16, 6700 AA, Wageningen, the Netherlands.
authors.forename: Dick
authors.initials: D
authors.lastname: Vreugdenhil
authors.affiliation: Laboratory of Nematology, Wageningen University and Research, PO Box 8213, 6700 ES, Wageningen, the Netherlands.
authors.forename: Sonja
authors.initials: S
authors.lastname: Warmerdam
authors.affiliation: Laboratory of Entomology, Wageningen University and Research, PO Box 16, 6700 AA, Wageningen, the Netherlands.|Business Unit Bioscience, Wageningen Plant Research, Wageningen University and Research, PO Box 16, 6700 AA, Wageningen, the Netherlands.
authors.forename: Gerrie L
authors.initials: GL
authors.lastname: Wiegers
authors.affiliation: Biometris, Wageningen University and Research, PO Box 16, 6700 AA, Wageningen, the Netherlands.
authors.forename: Joost
authors.initials: J
authors.lastname: van Heerwaarden
authors.affiliation: Biometris, Wageningen University and Research, PO Box 16, 6700 AA, Wageningen, the Netherlands.
authors.forename: Willem
authors.initials: W
authors.lastname: Kruijer
authors.affiliation: Biometris, Wageningen University and Research, PO Box 16, 6700 AA, Wageningen, the Netherlands.
authors.forename: Fred A
authors.initials: FA
authors.lastname: van Eeuwijk
authors.affiliation: Laboratory of Entomology, Wageningen University and Research, PO Box 16, 6700 AA, Wageningen, the Netherlands.
authors.forename: Marcel
authors.initials: M
authors.lastname: Dicke
mesh_terms: D017360:Arabidopsis / Q000235:genetics* / Q000502:physiology*; D002874:Chromosome Mapping; D004269:DNA, Bacterial / Q000235:genetics; D017343:Genes, Plant; D056726:Genetic Association Studies; D055106:Genome-Wide Association Study; D040582:Inheritance Patterns / Q000235:genetics; D008957:Models, Genetic; D009154:Mutation / Q000235:genetics; D010641:Phenotype; D010937:Plant Growth Regulators / Q000378:metabolism; D040641:Quantitative Trait Loci / Q000235:genetics; D015203:Reproducibility of Results; D013312:Stress, Physiological / Q000235:genetics*
chemical_list: D004269:DNA, Bacterial; D010937:Plant Growth Regulators; C036483:T-DNA
keywords: abiotic stress; biotic stress; genetic architecture; genome-wide association mapping; multiple stresses