Evolution of floral diversity: genomics, genes and gamma

Abstract

A salient feature of flowering plant diversification is the emergence of a novel suite of floral features coinciding with the origin of the most species-rich lineage, Pentapetalae. Advances in phylogenetics, developmental genetics and genomics, including new analyses presented here, are helping to reconstruct the specific evolutionary steps involved in the evolution of this clade. The enormous floral diversity among Pentapetalae appears to be built on a highly conserved ground plan of five-parted (pentamerous) flowers with whorled phyllotaxis. By contrast, lability in the number and arrangement of component parts of the flower characterize the early-diverging eudicot lineages subtending Pentapetalae. The diversification of Pentapetalae also coincides closely with ancient hexaploidy, referred to as the gamma whole-genome triplication, for which the phylogenetic timing, mechanistic details and molecular evolutionary consequences are as yet not fully resolved. Transcription factors regulating floral development often persist in duplicate or triplicate in gamma-derived genomes, and both individual genes and whole transcriptional programmes exhibit a shift from broadly overlapping to tightly defined expression domains in Pentapetalae flowers. Investigations of these changes associated with the origin of Pentapetalae can lead to a more comprehensive understanding of what is arguably one of the most important evolutionary diversification events within terrestrial plants.This article is part of the themed issue 'Evo-devo in the genomics era, and the origins of morphological diversity'.

Keywords: Gunneridae; Pentapetalae; eudicots; floral evolution; gamma palaeohexaploidy.

Figure 1.

Phylogenetic relationships among the main lineages of flowering plants and their sister group, the extant gymnosperms, based on nuclear, mitochondrial and chloroplast DNA sequence data. Amborellales, Nymphaeales and Austrobaileyales form a basal grade below all other flowering plants (Mesangiospermae). Relationships among the three major clades of Mesangiospermae (magnoliids, monocots and eudicots) and Ceratophyllales are currently unresolved. Among eudicots, Ranunculales diverge first, followed by Proteales before a trichotomy comprising Buxales, Trochodendrales and core eudicots. Among core eudicots, Gunnerales are sister to Pentapetalae, which comprise the large Superrosidae and Superasteridae clades and Dilleniales in an unresolved a trichotomy. Superrosidae includes Saxifragales plus Rosidae (rosids), while Superasteridae comprises a basal grade of Santalales, Berberidopsidales and Caryophyllales subtending the large Asteridae (asterids) clade.

Figure 2.

Representatives of eudicot floral diversity. (a) Saxifraga rotundifolia (Saxifragales) displays the five-part flowers typical of the Superrosidae clade of Pentapetalae. (b) The five petals are fused in Petunia sp. (Solanales), as is characteristic of the Asteridae clade of Pentapetalae. (c) Antirrhinum majus (snapdragon; Lamiales), a model species for floral symmetry developmental genetics, has zygomorphic flowers in which dorsal, lateral and ventral petal lobes emerge from the corolla tube. (d) Gunnera (Gunnerales) flowers are minute and densely packed in spicate inflorescences. (e) Trochodendron aralioides (Trochodendrales) flowers are polymerous with numerous stamens and carpels. (f) Inflorescences of Pachysandra procumbens (Buxales) bearing dimerous flowers, each with two pairs of stamens. (g) Grevillea sericea (Proteales) flowers displaying four sepal lobes (dimerous) to which stamens are fused, and an elongated pistil. (h) Nelumbo nucifera (Proteales) flowers are polymerous with numerous petals, stamens and carpels. (i) Eschscholzia californica (Ranunculales) flowers are dimerous with two pairs of decussate petals. Photo credits: (a) ‘Saxifraga rotundifolia’ (CC BY-NC 2.0) by cetp; (b) ‘Petunia’ (CC BY-NC-ND 2.0) by Ava Babili; (c) ‘Antirrhinum majus ‘ (CC BY-NC-SA 2.0) by francesco_43; (d) ‘Gunnera’ (CC BY-NC-ND 2.0) by allisoncake; (e) ‘Trochodendron aralioides ‘ (CC BY-NC-SA 2.0) by dogtooth77; (f) ‘Pachysandra procumbens (Allegheny spurge)’ (CC BY-NC-SA 2.0) by tgpotterfield; (g) ‘Grevillea sericea’ (CC BY-NC-SA 2.0) by Marine Explorer; (h) ‘sacred lotus’ (CC BY-NC-SA 2.0) by faria!; (i) ‘Eschscholzia’ (CC BY-NC 2.0) by Nickiz77.

Figure 3.

Evolutionary origin of gamma-derived Vitis paralogues. The branch labels along the backbone of the phylogenetic tree [total(no. with greater than 50% BS)] indicate the number of Vitis paralogues estimated to have arisen along the respective stem linages assuming strict tetraploidy events. Possible phylogenetic origins of the third subgenome via the two-step model of gamma hexaploidy are indicated by 1, 2 and 3. Scenarios in which a tetraploid is crossed with a close relative that branched off the core eudicot stem lineage (position 1) or off an older stem lineage (position 2) can be reconciled with our gene trees if extensive gene loss and/or extinction is invoked. The scenario of a wide cross between the core eudicot tetraploid and a species that branched off the stem lineage ‘below’ Buxales and Trochodendrales (position 3) is less complex evolutionarily.