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Review
. 2016 Apr;202(4):1255-65.
doi: 10.1534/genetics.115.182964.

Evolving Ideas on the Origin and Evolution of Flowers: New Perspectives in the Genomic Era

Andre S Chanderbali  1 , Brent A Berger  2 , Dianella G Howarth  2 , Pamela S Soltis  3 , Douglas E Soltis  4
Affiliations
Review

Evolving Ideas on the Origin and Evolution of Flowers: New Perspectives in the Genomic Era

Andre S Chanderbali et al. Genetics. 2016 Apr.

Abstract

The origin of the flower was a key innovation in the history of complex organisms, dramatically altering Earth's biota. Advances in phylogenetics, developmental genetics, and genomics during the past 25 years have substantially advanced our understanding of the evolution of flowers, yet crucial aspects of floral evolution remain, such as the series of genetic and morphological changes that gave rise to the first flowers; the factors enabling the origin of the pentamerous eudicot flower, which characterizes ∼70% of all extant angiosperm species; and the role of gene and genome duplications in facilitating floral innovations. A key early concept was the ABC model of floral organ specification, developed by Elliott Meyerowitz and Enrico Coen and based on two model systems,Arabidopsis thalianaandAntirrhinum majus Yet it is now clear that these model systems are highly derived species, whose molecular genetic-developmental organization must be very different from that of ancestral, as well as early, angiosperms. In this article, we will discuss how new research approaches are illuminating the early events in floral evolution and the prospects for further progress. In particular, advancing the next generation of research in floral evolution will require the development of one or more functional model systems from among the basal angiosperms and basal eudicots. More broadly, we urge the development of "model clades" for genomic and evolutionary-developmental analyses, instead of the primary use of single "model organisms." We predict that new evolutionary models will soon emerge as genetic/genomic models, providing unprecedented new insights into floral evolution.

Keywords: ABC model; Pentapetalae; basal angiosperms; evo-devo; fading borders model: floral diversity; flower evolution.

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Figures

Figure 1
Figure 1
Summary tree of seed plant phylogeny showing the main lineages of flowering plants and the sister group, the extant gymnosperms. Species with established resources for flower developmental genetics, indicated in red, are distributed predominantly among the asterid and rosid clades of the Pentapetalae. Additional “evolutionary models,” shown in blue, are needed to address questions regarding the genetic basis of major transitions in floral evolution.
Figure 2
Figure 2
Classic ABCE model of floral organ identity vs. fading borders model. (A) The classic ABCE model specifies four morphologically discrete floral organs: sepals are produced where only A function acts, petals are produced where A and B functions overlap, stamens occur where B and C functions overlap, and carpels are produced where C function acts alone. (B) In contrast, in the fading borders model, the borders between A, B, and C functions are blurred to produce a gradual transition of organ identity programs across the floral meristem. Hence, floral organs are influenced by “ABc,” “aBC,” and “abC” activities, where lowercase font indicates lower functional influence. These three combinations of gene activities promote the development of morphologically intergrading petaloid organs (tepals), stamens, and carpels, respectively. Modified from Chanderbali et al. (2010).
Figure 3
Figure 3
Floral variation in ANA grade, magnoliid, and basal eudicot angiosperms. Although comprising only a few percent of extant angiosperm species, these lineages exhibit enormous floral variation compared to the more canalized flowers of core eudicots and monocots. (A) Nymphaea caerulea (Nymphaeaceae; basal angiosperm). (B) Austrobaileya scandens (Austrobaileyaceae; basal angiosperm). (C) Persea americana (Lauraceae; magnoliid). (D) Piper neesiasnum (Piperaceae; magnoliid). (E) Aristolochia veraguensis (Aristolociaceae; magnoliid). (F) Asimina incana (Annonaceae; magnoliid). (G) Magnolia champaca (Magnoliaceae; magnoliid). (H) Argemone albiflora (Papaveraceae; basal eudicot). (I) Anemone canadensis (Ranunculaceae; basal eudicot). (J) Ranunculus ficaria (Ranunculaceae; basal eudicot). A is courtesy of Deborah Chanderbali; B is courtesy of Douglas Soltis; C is courtesy of Andre Chanderbali; and D–J are courtesy of Walter Judd.
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