Abstract
The majority of angiosperms are syncarpous- their gynoecium is composed of two or more fused carpels. In Arabidopsis thaliana, this fusion is regulated through the balance of expression between CUP SHAPED COTYLEDON (CUC) genes, which are orthologs of the Petunia hybrida transcription factor NO APICAL MERISTEM (NAM), and their post-transcriptional regulator miR164. Accordingly, the expression of a miR164-insensitive form of A. thaliana CUC2 causes a radical breakdown of carpel fusion. Here, we investigate the role of the NAM/miR164 genetic module in carpel closure in monocarpous plants. We show that the disruption of this module in monocarpous flowers of A. thaliana aux1-22 mutants causes a failure of carpel closure, similar to the failure of carpel fusion observed in the wild-type genetic background. This observation suggested that closely related mechanisms may bring about carpel closure and carpel fusion, at least in A. thaliana. We therefore tested whether these mechanisms were conserved in a eurosid species that is monocarpous in its wild-type form. We observed that expression of MtNAM, the NAM ortholog in the monocarpous eurosid Medicago truncatula, decreases during carpel margin fusion, suggesting a role for the NAM/miR164 module in this process. We transformed M. truncatula with a miR164-resistant form of MtNAM and observed, among other phenotypes, incomplete carpel closure in the resulting transformants. These data confirm the underlying mechanistic similarity between carpel closure and carpel fusion which we observed in A. thaliana. Our observations suggest that the role of the NAM/miR164 module in the fusion of carpel margins has been conserved at least since the most recent common ancestor of the eurosid clade, and open the possibility that a similar mechanism may have been responsible for carpel closure at much earlier stages of angiosperm evolution. We combine our results with studies of early diverging angiosperms to speculate on the role of the NAM/miR164 module in the origin and further evolution of the angiosperm carpel.
Highlights
The female whorl, or gynoecium, of the angiosperm flower consists of one or more carpels which enclose the ovules
We tested whether the introduction of a miR164-resistant version of CUC2 (CUC2g-m4) could cause a breakdown in the closure of the single carpels that are produced in A. thaliana aux1-22 mutants (Bennett et al, 1996), as compared to control plants transformed with a wild-type construct (CUC2g-wt)
We show that a previously characterized developmental module involving the post-transcriptional regulation of NO APICAL MERISTEM (NAM) orthologs by miR164 is involved in carpel fusion in syncarpous A. thaliana (Nikovics et al, 2006; Sieber et al, 2007), and in the closure of the single carpels present in two species whose lineages diverged at the base of the eurosid clade, some 114–113 million years ago (MYA)
Summary
The female whorl, or gynoecium, of the angiosperm flower consists of one or more carpels which enclose the ovules. If only one carpel is produced per flower, the gynoecium is termed monocarpous. Carpels in apocarpous or monocarpous gynoecia may emerge from the floral meristem with their margins already fused together, in which case they are described as ascidiate (bottle-shaped), or may emerge with unfused margins that subsequently fuse by folding, in which case they are described as plicate. Mapping of character states onto angiosperm phylogeny indicates that syncarpy has arisen at least 17 times in the angiosperms, while the evolution of apocarpy from syncarpy is much less frequent (Armbruster et al, 2002)
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