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Phylogeny and diversification of B-function MADS-box genes in angiosperms: evolutionary and functional implications of a 260-million-year-old duplication¹

²Department of Botany, University of Florida, Gainesville, Florida 32611 USA; ³The Natural History Museums and Botanical Garden, University of Oslo, P.O. Box 1172 Blindern, NO-0318 Oslo, Norway; ⁴Molekylärsystematiska laboratoriet, Naturhistoriska riksmuseet, Box 50007, SE-104 05 Stockholm, Sweden; ⁵Florida Museum of Natural History, University of Florida, Gainesville, Florida 32611 USA

B-function MADS-box genes play crucial roles in floral development in model angiosperms. We reconstructed the structural and functional implications of B-function gene phylogeny in the earliest extant flowering plants based on analyses that include 25 new AP3 and PI sequences representing critical lineages of the basalmost angiosperms: Amborella, Nuphar (Nymphaeaceae), and Illicium (Austrobaileyales). The ancestral size of exon 5 in PI-homologues is 42 bp, typical of exon 5 in other plant MADS-box genes. This 42-bp length is found in PI-homologues from Amborella and Nymphaeaceae, successive sisters to all other angiosperms. Following these basalmost branches, a deletion occurred in exon 5, yielding a length of 30 bp, a condition that unites all other angiosperms. Several shared amino acid strings, including a prominent "DEAER" motif, are present in the AP3- and PI-homologues of Amborella. These may be ancestral motifs that were present before the duplication that yielded the AP3 and PI lineages and subsequently were modified after the divergence of Amborella. Other structural features were identified, including a motif that unites the previously described TM6 clade and a deletion in AP3-homologues that unites all Magnoliales. Phylogenetic analyses of AP3- and PI-homologues yielded gene trees that generally track organismal phylogeny as inferred by multigene data sets. With both AP3 and PI amino acid sequences, Amborella and Nymphaeaceae are sister to all other angiosperms. Using nonparametric rate smoothing (NPRS), we estimated that the duplication that produced the AP3 and PI lineages occurred approximately 260 mya (231–290). This places the duplication after the split between extant gymnosperms and angiosperms, but well before the oldest angiosperm fossils. A striking similarity in the multimer-signalling C domains of the Amborella proteins suggests the potential for the formation of unique transcription-factor complexes. The earliest angiosperms may have been biochemically flexible in their B function and "tinkered" with floral organ identity.

Key Words: Amborella • AP3 • B-class • basal angiosperms • MADS • PI

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