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

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 thaliana and Antirrhinum 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.

SEP-class genes in Prunus mume and their likely role in floral organ development

“…Flower emergence is a vast step in the evolutionary history of plants [1], and its diversification overtime has largely altered the interaction patterns of the plant kingdom [2]. Furthermore, floral structures are controlled by a number of environmental and genetic factors.…”

Recent advances in understanding the roles of whole genome duplications in evolution

“…These duplicated and diversified gene sets organised to generate the first now-extinct flowers, and recent reconstructions suggest that these were bisexual with petal-like tepals and pollen-bearing stamens arranged in multiple concentric whorls, and female carpels in a central spiral 25 . Among living angiosperms, the Amborella lineage evolved a ‘fading borders’ programme, such that the whole flower is a spiral that gradually transitions from bracts to outer then inner tepals (specified by ABc combinations), from inner tepals to stamens (aBC) then carpels (abC), in which upper case indicates functions of greatest influence in the respective organs 26 . Only in later-evolving flowers such as Arabidopsis and Antirrhinum did the tepals subdivide into sepals and petals, by restricting the boundaries of expression of floral identity genes.…”

“…Only in later-evolving flowers such as Arabidopsis and Antirrhinum did the tepals subdivide into sepals and petals, by restricting the boundaries of expression of floral identity genes. For example, the transcription of A and C genes became mutually exclusive 26 . Further evolutionary diversity in flower form occurred by mechanisms that include shifts in the spatial expression of ABC functions across flowers, and by further WGDs that elaborated and extended the ABC regulatory network 27 .…”

Evolution of floral diversity: genomics, genes andgamma

“…The most conspicuous key evolutionary innovation of angiosperms is the flower itself, and breakthroughs in floral developmental genetics provided new impetus for studies of floral evolution and developmentfloral evo-devo-from which have emerged numerous new hypotheses [11,12]. Among these are novel ideas about how flowers evolved from transformed gymnosperm cones [13][14][15][16], an ancestral 'fading borders' model for flower development [17][18][19][20] and floral diversification through 'sliding boundaries' of organ identity functions [21][22][23][24].…”