Petaloidy and petal identity MADS-box genes in the balsaminoid genera Impatiens and Marcgravia

Koen Geuten, Annette Becker, Kerstin Kaufmann, Pieter Caris, Steven Janssens, Tom Viaene, Günter Theissen, Erik Smets
Plant Journal 2006, 47 (4): 501-18
Impatiens and Marcgravia have striking morphological innovations associated with the flowers. One of the sepals in Impatiens is spurred and petaloid, while in Marcgravia the petals are fused into a cap and nectary cups are associated with the inflorescence. Balsaminaceae (Impatiens) and Marcgraviaceae have surprisingly been shown to be closely related, since both belong to the balsaminoid clade of Ericales (basal asterids). However, several thorough morphological studies thus far have not revealed shared derived characters (synapomorphies) that support a close relationship between these families. In the balsaminoid clade, transitions from entirely green flowers to flowers with heterotopic petaloid organs can be observed. The primary role of class B genes in core eudicots is to specify the identity of petal and stamen floral organs. E-class genes, of which SEP3 is a representative, have been identified as redundant mediators that confer transcriptional activation potential on protein complexes that specify organ identity. Given the conserved function of organ-identity MADS-box genes in model plants, but the rapid molecular evolution in angiosperms, it remains controversial whether these genes have been involved in shaping floral diversity. We have identified a SEP3-like gene and a total of five class B genes from Impatiens hawkeri and Marcgravia umbellata and report their quantitative expression in the floral organs. In Impatiens, two AP3/DEF-like genes were identified with strongly divergent C-terminal domains, one truncated and one unusually long. Both genes show a gradual decrease in expression towards the outer perianth organs, but no GLO-like gene expression is observed in the petaloid sepal. Remarkably, SEP3-like gene expression in the Impatiens perianth is absent from the green sepals but present in the petaloid sepal and in the petals. Dimeric protein interactions of the cloned Impatiens genes were studied in yeast and by using gel retardation. In Marcgravia, strong overlapping class B gene expression is limited to the stamens, but a SEP3-like gene is strongly expressed in the Marcgravia nectary, indicating that both Impatiens and Marcgravia show heterotopic expression of a SEP3-like gene. We discuss several candidate mechanisms for heterotopic petaloidy involving modified gene expression and protein interaction of SEP3-like and class B genes.

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