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Genes Dev. 2015 Nov 15;29(22):2391-404. doi: 10.1101/gad.269050.115.

Alternate wiring of a KNOXI genetic network underlies differences in leaf development of A. thaliana and C. hirsuta.

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Department of Comparative Development and Genetics, Max Planck Institute for Plant Breeding Research, 50829 Cologne, Germany;
Department of Plant Sciences, University of Oxford, Oxford OX1 3BR, United Kingdom;
Dipartimento di Biologia e Biotecnologie, Università di Roma, Sapienza, 70-00185 Rome, Italy;
Centre for Biological Sciences, University of Southampton, Southampton SO17 1BJ, United Kingdom;
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;
Developmental Biology Unit, European Molecular Biology Laboratory, Heidelberg, Germany.


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.


CUP-SHAPED COTYLEDON; Cardamine hirsuta; KNOXI genes; compound leaf; pleiotropy; regulatory evolution

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