title: Repeated evolutionary changes of leaf morphology caused by mutations to a homeobox gene.
abstract: Elucidating the genetic basis of morphological changes in evolution remains a major challenge in biology. Repeated independent trait changes are of particular interest because they can indicate adaptation in different lineages or genetic and developmental constraints on generating morphological variation. In animals, changes to "hot spot" genes with minimal pleiotropy and large phenotypic effects underlie many cases of repeated morphological transitions. By contrast, only few such genes have been identified from plants, limiting cross-kingdom comparisons of the principles of morphological evolution. Here, we demonstrate that the REDUCED COMPLEXITY (RCO) locus underlies more than one naturally evolved change in leaf shape in the Brassicaceae. We show that the difference in leaf margin dissection between the sister species Capsella rubella and Capsella grandiflora is caused by cis-regulatory variation in the homeobox gene RCO-A, which alters its activity in the developing lobes of the leaf. Population genetic analyses in the ancestral C. grandiflora indicate that the more-active C. rubella haplotype is derived from a now rare or lost C. grandiflora haplotype via additional mutations. In Arabidopsis thaliana, the deletion of the RCO-A and RCO-B genes has contributed to its evolutionarily derived smooth leaf margin, suggesting the RCO locus as a candidate for an evolutionary hot spot. We also find that temperature-responsive expression of RCO-A can explain the phenotypic plasticity of leaf shape to ambient temperature in Capsella, suggesting a molecular basis for the well-known negative correlation between temperature and leaf margin dissection.
authors.affiliation: Institut für Biochemie und Biologie, Universität Potsdam, Karl-Liebknecht Straße 24-25, 14476 Potsdam-Golm, Germany.
authors.forename: Adrien
authors.initials: A
authors.lastname: Sicard
authors.affiliation: Institut für Biochemie und Biologie, Universität Potsdam, Karl-Liebknecht Straße 24-25, 14476 Potsdam-Golm, Germany.
authors.forename: Anna
authors.initials: A
authors.lastname: Thamm
authors.affiliation: Institut für Biochemie und Biologie, Universität Potsdam, Karl-Liebknecht Straße 24-25, 14476 Potsdam-Golm, Germany.
authors.forename: Cindy
authors.initials: C
authors.lastname: Marona
authors.affiliation: Department of Ecology & Evolutionary Biology, University of Toronto, 25 Willcocks Street, Toronto, ON M5S 3B2, Canada.
authors.forename: Young Wha
authors.initials: YW
authors.lastname: Lee
authors.affiliation: Department of Metabolic Networks, Max Planck Institute of Molecular Plant Physiology, Am Mühlenberg 1, 14476 Potsdam, Germany.
authors.forename: Vanessa
authors.initials: V
authors.lastname: Wahl
authors.affiliation: Department of Ecology & Evolutionary Biology, University of Toronto, 25 Willcocks Street, Toronto, ON M5S 3B2, Canada.
authors.forename: John R
authors.initials: JR
authors.lastname: Stinchcombe
authors.affiliation: Department of Ecology & Evolutionary Biology, University of Toronto, 25 Willcocks Street, Toronto, ON M5S 3B2, Canada.
authors.forename: Stephen I
authors.initials: SI
authors.lastname: Wright
authors.affiliation: Institut für Biochemie und Biologie, Universität Potsdam, Karl-Liebknecht Straße 24-25, 14476 Potsdam-Golm, Germany.
authors.forename: Christian
authors.initials: C
authors.lastname: Kappel
authors.affiliation: Institut für Biochemie und Biologie, Universität Potsdam, Karl-Liebknecht Straße 24-25, 14476 Potsdam-Golm, Germany. Electronic address: michael.lenhard@uni-potsdam.de.
authors.forename: Michael
authors.initials: M
authors.lastname: Lenhard
mesh_terms: D000595:Amino Acid Sequence; D005075:Biological Evolution; D029687:Capsella / Q000033:anatomy & histology* / Q000235:genetics* / Q000378:metabolism; D019143:Evolution, Molecular; D005801:Genes, Homeobox; D008969:Molecular Sequence Data; D009154:Mutation; D010802:Phylogeny; D018515:Plant Leaves / Q000033:anatomy & histology / Q000235:genetics; D010940:Plant Proteins / Q000235:genetics* / Q000378:metabolism; D016415:Sequence Alignment; D013696:Temperature
chemical_list: D010940:Plant Proteins