TY  - JOUR
A1  - Sicard, Adrien
A1  - Kappel, Christian
A1  - Lee, Young Wha
A1  - Wozniak, Natalia Joanna
A1  - Marona, Cindy
A1  - Stinchcombe, John R.
A1  - Wright, Stephen I.
A1  - Lenhard, Michael
T1  - Standing genetic variation in a tissue-specific enhancer underlies
selfing-syndrome evolution in Capsella
JF  - Proceedings of the National Academy of Sciences of the United States of America
N2  - 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.
KW  - morphological evolution
KW  - growth control
KW  - standing variation;
 organ-specific evolution
KW  - intronic cis-regulatory element
Y1  - 2016
U6  - https://doi.org/10.1073/pnas.1613394113
SN  - 0027-8424
VL  - 113
SP  - 13911
EP  - 13916
PB  - National Acad. of Sciences
CY  - Washington
ER  - 
TY  - JOUR
A1  - Sicard, Adrien
A1  - Thamm, Anna
A1  - Marona, Cindy
A1  - Lee, Young Wha
A1  - Wahl, Vanessa
A1  - Stinchcombe, John R.
A1  - Wright, Stephen I.
A1  - Kappel, Christian
A1  - Lenhard, Michael
T1  - Repeated evolutionary changes of leaf morphology caused by mutations to a homeobox gene
JF  - Current biology
N2  - Elucidating the genetic basis of morphological changes in evolution remains a major challenge in biology [1-3]. 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 [4-6]. In animals, changes to "hot spot" genes with minimal pleiotropy and large phenotypic effects underlie many cases of repeated morphological transitions [4-8]. By contrast, only few such genes have been identified from plants [8-11], limiting cross-kingdom comparisons of the principles of morphological evolution. Here, we demonstrate that the REDUCED COMPLEXITY (RCO) locus [12] 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 [12], 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.
Y1  - 2014
U6  - https://doi.org/10.1016/j.cub.2014.06.061
SN  - 0960-9822
SN  - 1879-0445
VL  - 24
IS  - 16
SP  - 1880
EP  - 1886
PB  - Cell Press
CY  - Cambridge
ER  - 
TY  - JOUR
A1  - Sicard, Adrien
A1  - Kappel, Christian
A1  - Josephs, Emily B.
A1  - Lee, Young Wha
A1  - Marona, Cindy
A1  - Stinchcombe, John R.
A1  - Wright, Stephen I.
A1  - Lenhard, Michael
T1  - Divergent sorting of a balanced ancestral polymorphism underlies the establishment of gene-flow barriers in Capsella
JF  - Nature Communications
N2  - In the Bateson-Dobzhansky-Muller model of genetic incompatibilities post-zygotic gene-flow barriers arise by fixation of novel alleles at interacting loci in separated populations. Many such incompatibilities are polymorphic in plants, implying an important role for genetic drift or balancing selection in their origin and evolution. Here we show that NPR1 and RPP5 loci cause a genetic incompatibility between the incipient species Capsella grandiflora and C. rubella, and the more distantly related C. rubella and C. orientalis. The incompatible RPP5 allele results from a mutation in C. rubella, while the incompatible NPR1 allele is frequent in the ancestral C. grandiflora. Compatible and incompatible NPR1 haplotypes are maintained by balancing selection in C. grandiflora, and were divergently sorted into the derived C. rubella and C. orientalis. Thus, by maintaining differentiated alleles at high frequencies, balancing selection on ancestral polymorphisms can facilitate establishing gene-flow barriers between derived populations through lineage sorting of the alternative alleles.
Y1  - 2015
U6  - https://doi.org/10.1038/ncomms8960
SN  - 2041-1723
VL  - 6
PB  - Nature Publ. Group
CY  - London
ER  - 
TY  - GEN
A1  - Sicard, Adrien
A1  - Kappel, Christian
A1  - Josephs, Emily B.
A1  - Wha Lee, Young
A1  - Marona, Cindy
A1  - Stinchcombe, John R.
A1  - Wright, Stephen I.
A1  - Lenhard, Michael
T1  - Divergent sorting of a balanced ancestral polymorphism underlies the establishment of gene-flow barriers in Capsella
N2  - In the Bateson–Dobzhansky–Muller model of genetic incompatibilities post-zygotic gene-flow barriers arise by fixation of novel alleles at interacting loci in separated populations. Many such incompatibilities are polymorphic in plants, implying an important role for genetic drift or balancing selection in their origin and evolution. Here we show that NPR1 and RPP5 loci cause a genetic incompatibility between the incipient species Capsella grandiflora and C. rubella, and the more distantly related C. rubella and C. orientalis. The incompatible RPP5 allele results from a mutation in C. rubella, while the incompatible NPR1 allele is frequent in the ancestral C. grandiflora. Compatible and incompatible NPR1 haplotypes are maintained by balancing selection in C. grandiflora, and were divergently sorted into the derived C. rubella and C. orientalis. Thus, by maintaining differentiated alleles at high frequencies, balancing selection on ancestral polymorphisms can facilitate establishing gene-flow barriers between derived populations through lineage sorting of the alternative alleles.
T3  - Zweitveröffentlichungen der Universität Potsdam : Mathematisch-Naturwissenschaftliche Reihe - 231 
Y1  - 2015
U6  - http://nbn-resolving.de/urn/resolver.pl?urn:nbn:de:kobv:517-opus4-93568
ER  - 
TY  - JOUR
A1  - Sicard, Adrien
A1  - Kappel, Christian
A1  - Josephs, Emily B.
A1  - Wha Lee, Young
A1  - Marona, Cindy
A1  - Stinchcombe, John R.
A1  - Wright, Stephen I.
A1  - Lenhard, Michael
T1  - Divergent sorting of a balanced ancestral polymorphism underlies the establishment of gene-flow barriers in Capsella
JF  - Nature Communications
N2  - In the Bateson–Dobzhansky–Muller model of genetic incompatibilities post-zygotic gene-flow
barriers arise by fixation of novel alleles at interacting loci in separated populations. Many such incompatibilities are polymorphic in plants, implying an important role for genetic drift or balancing selection in their origin and evolution. Here we show that NPR1 and RPP5 loci cause a genetic incompatibility between the incipient species Capsella grandiflora and C. rubella, and the more distantly related C. rubella and C. orientalis. The incompatible RPP5 allele results from a mutation in C. rubella, while the incompatible NPR1 allele is frequent in the ancestral C. grandiflora. Compatible and incompatible NPR1 haplotypes are maintained by balancing selection in C. grandiflora, and were divergently sorted into the derived C. rubella and
C. orientalis. Thus, by maintaining differentiated alleles at high frequencies, balancing selection
on ancestral polymorphisms can facilitate establishing gene-flow barriers between derived populations through lineage sorting of the alternative alleles.
Y1  - 2015
U6  - https://doi.org/10.1038/ncomms8960
SN  - 2041-1723
VL  - 6
PB  - Nature Publishing Group
CY  - London
ER  -