title: Alternate wiring of a KNOXI genetic network underlies differences in leaf development of A. thaliana and C. hirsuta.
abstract: Two interrelated problems in biology are understanding the regulatory logic and predictability of morphological evolution. Here, we studied these problems by comparing Arabidopsis thaliana, which has simple leaves, and its relative, Cardamine hirsuta, which has dissected leaves comprising leaflets. By transferring genes between the two species, we provide evidence for an inverse relationship between the pleiotropy of SHOOTMERISTEMLESS (STM) and BREVIPEDICELLUS (BP) homeobox genes and their ability to modify leaf form. We further show that cis-regulatory divergence of BP results in two alternative configurations of the genetic networks controlling leaf development. In C. hirsuta, ChBP is repressed by the microRNA164A (MIR164A)/ChCUP-SHAPED COTYLEDON (ChCUC) module and ChASYMMETRIC LEAVES1 (ChAS1), thus creating cross-talk between MIR164A/CUC and AS1 that does not occur in A. thaliana. These different genetic architectures lead to divergent interactions of network components and growth regulation in each species. We suggest that certain regulatory genes with low pleiotropy are predisposed to readily integrate into or disengage from conserved genetic networks influencing organ geometry, thus rapidly altering their properties and contributing to morphological divergence.
authors.affiliation: Department of Comparative Development and Genetics, Max Planck Institute for Plant Breeding Research, 50829 Cologne, Germany;
authors.forename: Madlen I
authors.initials: MI
authors.lastname: Rast-Somssich
authors.affiliation: Department of Plant Sciences, University of Oxford, Oxford OX1 3BR, United Kingdom;
authors.forename: Suvi
authors.initials: S
authors.lastname: Broholm
authors.affiliation: Department of Plant Sciences, University of Oxford, Oxford OX1 3BR, United Kingdom;
authors.forename: Huw
authors.initials: H
authors.lastname: Jenkins
authors.affiliation: Department of Plant Sciences, University of Oxford, Oxford OX1 3BR, United Kingdom;
authors.forename: Claudia
authors.initials: C
authors.lastname: Canales
authors.affiliation: Department of Plant Sciences, University of Oxford, Oxford OX1 3BR, United Kingdom;
authors.forename: Daniela
authors.initials: D
authors.lastname: Vlad
authors.affiliation: Department of Comparative Development and Genetics, Max Planck Institute for Plant Breeding Research, 50829 Cologne, Germany;
authors.forename: Michiel
authors.initials: M
authors.lastname: Kwantes
authors.affiliation: Department of Plant Sciences, University of Oxford, Oxford OX1 3BR, United Kingdom;
authors.forename: Gemma
authors.initials: G
authors.lastname: Bilsborough
authors.affiliation: Dipartimento di Biologia e Biotecnologie, Università di Roma, Sapienza, 70-00185 Rome, Italy;
authors.forename: Raffaele
authors.initials: R
authors.lastname: Dello Ioio
authors.affiliation: Centre for Biological Sciences, University of Southampton, Southampton SO17 1BJ, United Kingdom;
authors.forename: Rob M
authors.initials: RM
authors.lastname: Ewing
authors.affiliation: Institut Jean-Pierre Bourgin, UMR1318, Institut National de la Recherche Agronomique (INRA)-Institut des Sciences et Industries du Vivant et de l'Environment (AgroParisTech), INRA Centre de Versailles-Grignon, 78026 Versailles Cedex 69117, France;
authors.forename: Patrick
authors.initials: P
authors.lastname: Laufs
authors.affiliation: Department of Comparative Development and Genetics, Max Planck Institute for Plant Breeding Research, 50829 Cologne, Germany;
authors.forename: Peter
authors.initials: P
authors.lastname: Huijser
authors.affiliation: Developmental Biology Unit, European Molecular Biology Laboratory, Heidelberg, Germany.
authors.forename: Carolyn
authors.initials: C
authors.lastname: Ohno
authors.affiliation: Developmental Biology Unit, European Molecular Biology Laboratory, Heidelberg, Germany.
authors.forename: Marcus G
authors.initials: MG
authors.lastname: Heisler
authors.affiliation: Department of Comparative Development and Genetics, Max Planck Institute for Plant Breeding Research, 50829 Cologne, Germany;
authors.forename: Angela
authors.initials: A
authors.lastname: Hay
authors.affiliation: Department of Comparative Development and Genetics, Max Planck Institute for Plant Breeding Research, 50829 Cologne, Germany;
authors.forename: Miltos
authors.initials: M
authors.lastname: Tsiantis
mesh_terms: D017360:Arabidopsis / Q000033:anatomy & histology / Q000235:genetics* / Q000254:growth & development*; D029681:Arabidopsis Proteins / Q000235:genetics / Q000378:metabolism; D031217:Cardamine / Q000033:anatomy & histology / Q000235:genetics* / Q000254:growth & development*; D018506:Gene Expression Regulation, Plant; D053263:Gene Regulatory Networks / Q000235:genetics*; D018398:Homeodomain Proteins / Q000235:genetics* / Q000378:metabolism; D035683:MicroRNAs / Q000235:genetics / Q000378:metabolism; D018515:Plant Leaves / Q000033:anatomy & histology / Q000235:genetics / Q000254:growth & development; D010940:Plant Proteins / Q000235:genetics* / Q000378:metabolism
chemical_list: D029681:Arabidopsis Proteins; D018398:Homeodomain Proteins; C405985:Knox1 protein, plant; D035683:MicroRNAs; D010940:Plant Proteins; C097496:STM protein, Arabidopsis
keywords: CUP-SHAPED COTYLEDON; Cardamine hirsuta; KNOXI genes; compound leaf; pleiotropy; regulatory evolution