Journal
GENES & DEVELOPMENT
Volume 29, Issue 22, Pages 2391-2404Publisher
COLD SPRING HARBOR LAB PRESS, PUBLICATIONS DEPT
DOI: 10.1101/gad.269050.115
Keywords
KNOXI genes; regulatory evolution; CUP-SHAPED COTYLEDON; Cardamine hirsuta; pleiotropy; compound leaf
Categories
Funding
- Biotechnology and Biological Sciences Research Council [BB/H011455/1, BB/H006974/1]
- Deutsche Forschungsgemeinschaft [TS 229/1-1, SFB 680]
- Gatsby Charitable Foundation
- Human Frontier Science Program [RGP0047/2010]
- Max Planck Society
- Cluster of Excellence on Plant Sciences
- Biotechnology and Biological Sciences Research Council [BB/H011455/1, BB/H006974/1] Funding Source: researchfish
- Engineering and Physical Sciences Research Council [EP/M020517/1] Funding Source: researchfish
- BBSRC [BB/H006974/1, BB/H011455/1] Funding Source: UKRI
- EPSRC [EP/M020517/1] Funding Source: UKRI
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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.
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