Abstract
BackgroundThe ABC model of flower development describes the molecular basis for specification of floral organ identity in model eudicots such as Arabidopsis and Antirrhinum. According to this model, expression of C-class genes is linked to stamen and gynoecium organ identity. The Zingiberales is an order of tropical monocots in which the evolution of floral morphology is characterized by a marked increase in petaloidy in the androecium. Petaloidy is a derived characteristic of the ginger families and seems to have arisen in the common ancestor of the ginger clade. We hypothesize that duplication of the C-class AGAMOUS (AG) gene followed by divergence of the duplicated AG copies during the diversification of the ginger clade lineages explains the evolution of petaloidy in the androecium. In order to address this hypothesis, we carried out phylogenetic analyses of the AG gene family across the Zingiberales and investigated patterns of gene expression within the androecium.ResultsPhylogenetic analysis supports a scenario in which Zingiberales-specific AG genes have undergone at least one round of duplication. Gene duplication was immediately followed by divergence of the retained copies. In particular, we detect positive selection in the third alpha-helix of the K domain of Zingiberales AGAMOUS copy 1 (ZinAG-1). A single fixed amino acid change is observed in ZinAG-1 within the ginger clade when compared to the banana grade. Expression analyses of AG and APETALA1/FRUITFULL (AP1/FUL) in Musa basjoo is similar to A- and C-class gene expressions in the Arabidopsis thaliana model, while Costus spicatus exhibits simultaneous expression of AG and AP1/FUL in most floral organs. We propose that this novel expression pattern could be correlated with the evolution of androecial petaloidy within the Zingiberales.ConclusionsOur results present an intricate story in which duplication of the AG lineage has lead to the retention of at least two diverged Zingiberales-specific copies, ZinAG-1 and Zingiberales AGAMOUS copy 2 (ZinAG-2). Positive selection on ZinAG-1 residues suggests a mechanism by which AG gene divergence may explain observed morphological changes in Zingiberales flowers. Expression data provides preliminary support for the proposed mechanism, although further studies are required to fully test this hypothesis.
Highlights
The ABC model of flower development describes the molecular basis for specification of floral organ identity in model eudicots such as Arabidopsis and Antirrhinum
In order to further explore the role of the AG gene in the evolution of androecial petaloidy across angiosperms, we focus our study on the Zingiberales, a group of monocots that exhibits extensive petaloidy in the androecial organs
Zingiberales AGAMOUS copy 2 (ZinAG-2) sequences form a monophyletic group, suggesting an orthologous relationship between copies found in the banana and ginger lineages, while Zingiberales AGAMOUS copy 1 (ZinAG-1) sequences formed a grade at the base of the ZinAG-2 clade
Summary
The ABC model of flower development describes the molecular basis for specification of floral organ identity in model eudicots such as Arabidopsis and Antirrhinum. According to this model, expression of C-class genes is linked to stamen and gynoecium organ identity. With the exception of AP2, all other genetic components of the ABC model are type-II MIKCc MADS-box genes as determined by their arrangement of protein domains Their proper function as transcriptional regulators is dependent on the protein-protein interactions that occur between the A-, B-, and C-class genes, as well as with the SEPALLATA genes [2], to form protein dimers and functional tetramers. The protein-level explanation for A-, B-, and Cclass functions is known as the quartet model, and asserts that only in tetramers are the A-, B-, and C-class proteins capable of regulating downstream genes (for review, [3])
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