title: Standing genetic variation in a tissue-specific enhancer underlies selfing-syndrome evolution in Capsella.
abstract: Mating system shifts recurrently drive specific changes in organ dimensions. The shift in mating system from out-breeding to selfing is one of the most frequent evolutionary transitions in flowering plants and is often associated with an organ-specific reduction in flower size. However, the evolutionary paths along which polygenic traits, such as size, evolve are poorly understood. In particular, it is unclear how natural selection can specifically modulate the size of one organ despite the pleiotropic action of most known growth regulators. Here, we demonstrate that allelic variation in the intron of a general growth regulator contributed to the specific reduction of petal size after the transition to selfing in the genus Capsella Variation within this intron affects an organ-specific enhancer that regulates the level of STERILE APETALA (SAP) protein in the developing petals. The resulting decrease in SAP activity leads to a shortening of the cell proliferation period and reduced number of petal cells. The absence of private polymorphisms at the causal region in the selfing species suggests that the small-petal allele was captured from standing genetic variation in the ancestral out-crossing population. Petal-size variation in the current out-crossing population indicates that several small-effect mutations have contributed to reduce petal-size. These data demonstrate how tissue-specific regulatory elements in pleiotropic genes contribute to organ-specific evolution. In addition, they provide a plausible evolutionary explanation for the rapid evolution of flower size after the out-breeding-to-selfing transition based on additive effects of segregating alleles.
authors.affiliation: Institut für Biochemie und Biologie, Universität Potsdam, 14476 Potsdam-Golm, Germany; adrien.sicard@uni-potsdam.de michael.lenhard@uni-potsdam.de.
authors.forename: Adrien
authors.initials: A
authors.lastname: Sicard
authors.affiliation: Institut für Biochemie und Biologie, Universität Potsdam, 14476 Potsdam-Golm, Germany.
authors.forename: Christian
authors.identifier: 0000-0002-1450-1864
authors.initials: C
authors.lastname: Kappel
authors.affiliation: Department of Ecology & Evolutionary Biology, University of Toronto, Toronto, ON, Canada M5S 3B2.
authors.forename: Young Wha
authors.initials: YW
authors.lastname: Lee
authors.affiliation: Institut für Biochemie und Biologie, Universität Potsdam, 14476 Potsdam-Golm, Germany.
authors.forename: Natalia Joanna
authors.initials: NJ
authors.lastname: Woźniak
authors.affiliation: Institut für Biochemie und Biologie, Universität Potsdam, 14476 Potsdam-Golm, Germany.
authors.forename: Cindy
authors.initials: C
authors.lastname: Marona
authors.affiliation: Department of Ecology & Evolutionary Biology, University of Toronto, Toronto, ON, Canada M5S 3B2.
authors.forename: John R
authors.initials: JR
authors.lastname: Stinchcombe
authors.affiliation: Department of Ecology & Evolutionary Biology, University of Toronto, Toronto, ON, Canada M5S 3B2.
authors.forename: Stephen I
authors.initials: SI
authors.lastname: Wright
authors.affiliation: Institut für Biochemie und Biologie, Universität Potsdam, 14476 Potsdam-Golm, Germany; adrien.sicard@uni-potsdam.de michael.lenhard@uni-potsdam.de.
authors.forename: Michael
authors.initials: M
authors.lastname: Lenhard
mesh_terms: D005075:Biological Evolution; D029687:Capsella / Q000235:genetics* / Q000254:growth & development; D004742:Enhancer Elements, Genetic / Q000235:genetics; D035264:Flowers / Q000235:genetics / Q000254:growth & development; D019684:Magnoliopsida / Q000235:genetics* / Q000254:growth & development; D009928:Organ Specificity; D010641:Phenotype; D054817:Pollination / Q000235:genetics; D040641:Quantitative Trait Loci / Q000235:genetics*; D012098:Reproduction / Q000235:genetics*; D012641:Selection, Genetic / Q000235:genetics*; D057945:Self-Fertilization / Q000235:genetics
keywords: growth control; intronic cis-regulatory element; morphological evolution; organ-specific evolution; standing variation