Abstract
BackgroundIn the large angiosperm order Lamiales, a diverse array of highly specialized life strategies such as carnivory, parasitism, epiphytism, and desiccation tolerance occur, and some lineages possess drastically accelerated DNA substitutional rates or miniaturized genomes. However, understanding the evolution of these phenomena in the order, and clarifying borders of and relationships among lamialean families, has been hindered by largely unresolved trees in the past.ResultsOur analysis of the rapidly evolving trnK/matK, trnL-F and rps16 chloroplast regions enabled us to infer more precise phylogenetic hypotheses for the Lamiales. Relationships among the nine first-branching families in the Lamiales tree are now resolved with very strong support. Subsequent to Plocospermataceae, a clade consisting of Carlemanniaceae plus Oleaceae branches, followed by Tetrachondraceae and a newly inferred clade composed of Gesneriaceae plus Calceolariaceae, which is also supported by morphological characters. Plantaginaceae (incl. Gratioleae) and Scrophulariaceae are well separated in the backbone grade; Lamiaceae and Verbenaceae appear in distant clades, while the recently described Linderniaceae are confirmed to be monophyletic and in an isolated position.ConclusionsConfidence about deep nodes of the Lamiales tree is an important step towards understanding the evolutionary diversification of a major clade of flowering plants. The degree of resolution obtained here now provides a first opportunity to discuss the evolution of morphological and biochemical traits in Lamiales. The multiple independent evolution of the carnivorous syndrome, once in Lentibulariaceae and a second time in Byblidaceae, is strongly supported by all analyses and topological tests. The evolution of selected morphological characters such as flower symmetry is discussed. The addition of further sequence data from introns and spacers holds promise to eventually obtain a fully resolved plastid tree of Lamiales.
Highlights
In the large angiosperm order Lamiales, a diverse array of highly specialized life strategies such as carnivory, parasitism, epiphytism, and desiccation tolerance occur, and some lineages possess drastically accelerated DNA substitutional rates or miniaturized genomes
Since one of the specific questions in our study was the relationship between Lentibulariaceae and Byblidaceae, which might have been blurred by long branch attraction (LBA) problems in previous studies, we slightly enhanced sampling for both families in one set of analyses and included two to three species for each genus
Utility of chloroplast markers for Lamiales phylogenetics Phylogenetic analysis of combined trnK/matK, trnL-F and rps16 intron sequences enhanced both resolution and statistical support compared to previous studies
Summary
In the large angiosperm order Lamiales, a diverse array of highly specialized life strategies such as carnivory, parasitism, epiphytism, and desiccation tolerance occur, and some lineages possess drastically accelerated DNA substitutional rates or miniaturized genomes. 350 spp.) belongs to Lamiales (Figure 1c, d) This family is unique for a variety of reasons: traps of Utricularia (bladderworts) are regarded as a complex modification of leaves [6,7], and the typical angiosperm body plan is strongly relaxed in members of this genus [8,9,10]. Utricularia and its sister genus, Genlisea (the corkscrew plants), are the only carnivorous angiosperms known to feed on protozoa [11] They have the smallest holoploid genome sizes among angiosperms, with some nuclear genomes as small as 63 Mbp or less [12], and exhibit the highest relative DNA substitution rates for some of the investigated chloroplast genome regions [13,14]. Pinguicula (butterworts), the third genus of Lentibulariaceae, is far less extreme in genome size, substitution rate and morphology, and exhibits glandular leaves that function as adhesive ("flypaper”) traps (Figure 1c, d)
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