Regulatory Diversification of INDEHISCENTin the Capsella Genus Directs Variationin Fruit Morphology

gold Gold open access

Evolution of gene-regulatory sequences is consid- ered the primary driver of morphological variation [1–3]. In animals, the diversity of body plans between distantly related phyla is due to the differ- ential expression patterns of conserved ‘‘toolkit’’ genes [4]. In plants, variation in expression domains similarly underlie most of the reported diversity of organ shape both in natural evolution and in the domestication of crops [5–9]. The heart-shaped fruit from members of the Capsella genus is a morpho- logical novelty that has evolved after Capselladiverged from Arabidopsis $8 mya [10]. Compara- tive studies of fruit growth in Capsella and Arabi- dopsis revealed that the difference in shape is caused by local control of anisotropic growth [11]. Here, we show that sequence variation in regu- latory domains of the fruit-tissue identity gene,INDEHISCENT (IND), is responsible for expansion of its expression domain in the heart-shaped fruits from Capsella rubella. We demonstrate that expres- sion of this CrIND gene in the apical part of the valves in Capsella contributes to the heart-shaped appearance. While studies on morphological diver- sity have revealed the importance of cis-regulatory sequence evolution, few examples exist where the downstream effects of such variation have been characterized in detail. We describe here how CrIND exerts its function on Capsella fruit shape by binding sequence elements of auxin biosynthesis genes to activate their expression and ensure auxin accumulation into highly localized maxima in the fruit valves. Thus, our data provide a direct link between changes in expression pattern and altered hormone homeostasis in the evolution of morpho- logical novelty.