Natural allelic variation underlying a major fitness trade-off in Arabidopsis thaliana.
Plants can defend themselves against a wide array of enemies, from microbes to large animals, yet there is great variability in the effectiveness of such defences, both within and between species. Some of this variation can be explained by conflicting pressures from pathogens with different modes of attack. A second explanation comes from an evolutionary 'tug of war', in which pathogens adapt to evade detection, until the plant has evolved new recognition capabilities for pathogen invasion. If selection is, however, sufficiently strong, susceptible hosts should remain rare. That this is not the case is best explained by costs incurred from constitutive defences in a pest-free environment. Using a combination of forward genetics and genome-wide association analyses, we demonstrate that allelic diversity at a single locus, ACCELERATED CELL DEATH 6 (ACD6), underpins marked pleiotropic differences in both vegetative growth and resistance to microbial infection and herbivory among natural Arabidopsis thaliana strains. A hyperactive ACD6 allele, compared to the reference allele, strongly enhances resistance to a broad range of pathogens from different phyla, but at the same time slows the production of new leaves and greatly reduces the biomass of mature leaves. This allele segregates at intermediate frequency both throughout the worldwide range of A. thaliana and within local populations, consistent with this allele providing substantial fitness benefits despite its marked impact on growth.
Department of Molecular Biology, Max Planck Institute for Developmental Biology, 72076 Tübingen, Germany.
Marco
M
Todesco
Sureshkumar
S
Balasubramanian
Tina T
TT
Hu
M Brian
MB
Traw
Matthew
M
Horton
Petra
P
Epple
Christine
C
Kuhns
Sridevi
S
Sureshkumar
Christopher
C
Schwartz
Christa
C
Lanz
Roosa A E
RA
Laitinen
Yu
Y
Huang
Joanne
J
Chory
Volker
V
Lipka
Justin O
JO
Borevitz
Jeffery L
JL
Dangl
Joy
J
Bergelson
Magnus
M
Nordborg
Detlef
D
Weigel
D000483:Alleles; D017487:Ankyrins / Q000235:genetics / Q000378:metabolism; D017360:Arabidopsis / Q000235:genetics* / Q000254:growth & development / Q000378:metabolism / Q000382:microbiology; D029681:Arabidopsis Proteins / Q000235:genetics / Q000378:metabolism; D018533:Biomass; D018506:Gene Expression Regulation, Plant; D017343:Genes, Plant; D056084:Genetic Fitness / Q000235:genetics*; D014644:Genetic Variation / Q000235:genetics*; D055106:Genome-Wide Association Study; D008969:Molecular Sequence Data; D010641:Phenotype; D010935:Plant Diseases / Q000235:genetics / Q000382:microbiology; D018515:Plant Leaves / Q000033:anatomy & histology / Q000235:genetics / Q000254:growth & development / Q000469:parasitology; D040641:Quantitative Trait Loci
C480953:ACD6 protein, Arabidopsis; D017487:Ankyrins; D029681:Arabidopsis Proteins