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Standing genetic variation in a tissue-specific enhancer underlies selfing-syndrome evolution in Capsella

  • 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 privateMating 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.show moreshow less

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Metadaten
Author:Adrien Sicard, Christian KappelORCiDGND, Young Wha Lee, Natalia Joanna Wozniak, Cindy Marona, John R. Stinchcombe, Stephen I. Wright, Michael Lenhard
DOI:https://doi.org/10.1073/pnas.1613394113
ISSN:0027-8424
Pubmed Id:http://www.ncbi.nlm.nih.gov/pubmed?term=27849572
Parent Title (English):Proceedings of the National Academy of Sciences of the United States of America
Publisher:National Acad. of Sciences
Place of publication:Washington
Document Type:Article
Language:English
Year of first Publication:2016
Year of Completion:2016
Release Date:2020/03/22
Tag:growth control; intronic cis-regulatory element; morphological evolution; standing variation; organ-specific evolution
Volume:113
Pagenumber:6
First Page:13911
Last Page:13916
Funder:Genome Canada and Genome Quebec Applied Bioproducts and Crops grant; Deutsche Forschungsgemeinschaft within the framework of the research priority programme "Adaptomics" [SI1967/1]; European Research Council Starting Grant [260455]
Organizational units:Mathematisch-Naturwissenschaftliche Fakultät / Institut für Biochemie und Biologie
Peer Review:Referiert