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Leaf Shape Evolution Through Duplication, Regulatory Diversification, and Loss of a Homeobox Gene

Science  14 Feb 2014:
Vol. 343, Issue 6172, pp. 780-783
DOI: 10.1126/science.1248384

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Abstract

In this work, we investigate morphological differences between Arabidopsis thaliana, which has simple leaves, and its relative Cardamine hirsuta, which has dissected leaves comprising distinct leaflets. With the use of genetics, interspecific gene transfers, and time-lapse imaging, we show that leaflet development requires the REDUCED COMPLEXITY (RCO) homeodomain protein. RCO functions specifically in leaves, where it sculpts developing leaflets by repressing growth at their flanks. RCO evolved in the Brassicaceae family through gene duplication and was lost in A. thaliana, contributing to leaf simplification in this species. Species-specific RCO action with respect to its paralog results from its distinct gene expression pattern in the leaf base. Thus, regulatory evolution coupled with gene duplication and loss generated leaf shape diversity by modifying local growth patterns during organogenesis.

Developmental Complexity

Although related, the plants Arabidopsis thaliana and Cardamine hirsuta have different sorts of leaves—one, a rather plain oval and the other, a complicated multipart construction. Comparing the development of the two leaf types, Vlad et al. (p. 780) uncovered a gene that regulates developmental growth. The C. hirsuta gene encoding the REDUCED COMPLEXITY (RCO) homeodomain protein arose through gene duplication and neofunctionalization, but was lost in the A. thaliana lineage. In C. hirsuta, RCO suppresses growth in domains around the perimeter of the developing leaf, yielding complex-shaped leaves. A. thaliana, lacking RCO, produces simple leaves. When RCO was expressed in A. thaliana, the leaves became more complex. Thus, the capacity to produce complex leaves remains, despite loss of the initiator.

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