Aquilegia as a model system for the evolution and ecology of petals

Abstract

The ranunculid genus Aquilegia holds extraordinary promise as a model system for investigating a wide range of questions relating to the evolution and ecology of petals. New genetic and genomic resources, including an extensive EST database, BAC libraries and physical maps, as well as virus-induced gene silencing are facilitating this research on multiple fronts. At the developmental genetic level, Aquilegia has been important for elucidating the developmental programme for specifying petals and petaloid characteristics. Data suggest that duplication events among the petal and stamen identity genes have resulted in sub- and neofunctionalization. This expansion of gene function does not include the petaloidy of Aquilegia sepals, however, which does not depend on the same loci that control identity of the second whorl petals. Of special interest is the elaboration of the petal into a nectar spur, a major innovation for the genus. Intra- and interspecific variation in the shape and colour of petals, especially the spurs, has been shown to be adaptative for different pollinators. Thus, understanding the genetic basis of these traits will help us connect the ecological interactions driving speciation with the genetic changes responsible for remodelling morphology. Progress in this area has focused on the multiple, parallel transitions in flower colour and nectar spur length across the genus. For flower colour, upstream transcription factors appear to be primarily targets of natural selection. Thus research in Aquilegia spans the initial evolution of petals and petaloidy to the diversification of petal morphology to the ecological basis of petal form, thereby providing a comprehensive picture of the evolutionary biology of this critical angiosperm feature.

Figure 1.

(a) The classic ABC model with the addition of the E function. (b) The corresponding ABCE genes from Arabidopsis. The A class genes APETALA1 (AP1) and APETALA2 (AP2) specify sepals (SEP) and with the B class genes, APETALA3 (AP3) and PISTALLATA (PI), specify petals (PET). The B class genes with the C class gene AGAMOUS (AG) specify stamens (STA) and the C class gene alone specifies carpels (CAR). (c,d) The modified ABC model of Aquilegia based on expression studies of the B gene homologues: (c) corresponds to early developmental stages while (d) reflects expression after carpel initiation.

Figure 2.

Floral variation across natural species and one cultivar of Aquilegia. (a) A. caerulea. (b) A. shockleyi. (c) A. pubescens. (d) A. chrysantha. (e) A. caerulea var. daileyae, which lacks spurs. (f) A. vulgaris ‘Black Tower’, which has stamens transformed into petals. Photos: (a) Nathan Derieg; (b–e) Scott Hodges and (f) Elena Kramer.

Figure 3.

Simplified phylogeny of the angiosperms based on Moore et al. (2007) showing the position of Aquilegia relative to other major model systems.

Figure 4.

Frequency distribution of the length of tentative consensus (TC) sequences in the AqGI.

Figure 5.

Classification of sequences from the AqGI to GO vocabularies. (a) Molecular function, (b) biological processes and (c) cellular component.

Figure 6.

Comparison of individual petals among species of Aquilegia. (a) Aquilegia longissima, (b) Aquilegia pinetorum, (c) Aquilegia chrysantha, (d,e) A. formosa and (f) Aquilegia flabellata (scale bar, 1 cm).