Molecular mechanisms underlying origin and diversification of the angiosperm flower

Abstract

Background: Understanding the mode and mechanisms of the evolution of the angiosperm flower is a long-standing and central problem of evolutionary biology and botany. It has essentially remained unsolved, however. In contrast, considerable progress has recently been made in our understanding of the genetic basis of flower development in some extant model species. The knowledge that accumulated this way has been pulled together in two major hypotheses, termed the 'ABC model' and the 'floral quartet model'. These models explain how the identity of the different types of floral organs is specified during flower development by homeotic selector genes encoding transcription factors.

Scope: We intend to explain how the 'ABC model' and the 'floral quartet model' are now guiding investigations that help to understand the origin and diversification of the angiosperm flower.

Conclusions: Investigation of orthologues of class B and class C floral homeotic genes in gymnosperms suggest that bisexuality was one of the first innovations during the origin of the flower. The transition from dimer to tetramer formation of floral homeotic proteins after establishment of class E proteins may have increased cooperativity of DNA binding of the transcription factors controlling reproductive growth. That way, we hypothesize, better 'developmental switches' originated that facilitated the early evolution of the flower. Expression studies of ABC genes in basally diverging angiosperm lineages, monocots and basal eudicots suggest that the 'classical' ABC system known from core eudicots originated from a more fuzzy system with fading borders of gene expression and gradual transitions in organ identity, by sharpening of ABC gene expression domains and organ borders. Shifting boundaries of ABC gene expression may have contributed to the diversification of the angiosperm flower many times independently, as may have changes in interactions between ABC genes and their target genes.

Fig. 1.

On the evolution of the ABC system of floral organ specification. On the right, different versions of the ABC system are shown. The ABC models differ either by the expression domains of the ABC genes, or by the organs specified by the different gene combinations. For every type of ABC system only one example is shown, even though it may occur in different taxa and may have originated independently several times during evolution. For simplicity, conserved class A genes are presented here even though in most cases class A gene functions might not be separable from functions as floral meristem identity genes. Photographs of cones or flowers of species sculpted by the corresponding ABC system are shown in the middle. The relationships (according to APGII, 2003) between the plant families to which the different species shown belong are indicated by the phylogenetic tree on the left. Note that in some cases (Macleaya, Rumex) the floral structures shown may represent exceptions rather than the rule in the respective plant families. Abbreviations: mo, male organs; fo, female organs; sl, sepal-like tepals; pl, petal-like tepals; sd, staminodes; st, stamens; ca, carpels; te, (petaloid) tepals; pe, petals; pa, palea/lemma; lo, lodicules; se, sepals; sp, sepaloid petals

Fig. 2.

Two models for the specification of male and female organ identity in reproductive cones as a function of floral homeotic protein concentrations. Both models assume that floral homeotic protein expression responds positively to a gradient of the floral meristem identity protein LEAFY, which forms a concentration gradient along the cone axis from bottom (low) to top (high). The graphs represent the concentration of DNA-bound protein complexes determining male (in green) and female (in blue) organ identity, respectively. When reproductive organs are specified by dimers of MADS-domain proteins (we assume that B-protein homodimers and C-protein homodimers and/or B/C-heterodimers specify male organs whereas female organs are specified by C-protein homodimers), the slope with which protein concentration increases and hence target gene activation occurs would be less steep compared with a system where cooperativity due to tetramerization (i.e. male organs are specified by a B/C/E-protein tetramer and female organs by a C/E/C/E-protein tetramer) is taken into account (compare A and B). As a consequences, the ‘zone of unclear organ formation’ (symbolized by a question mark) is narrower when organ identity is specified by tetramers rather then by dimers. Also, although not depicted here for simplicity, the total protein concentration (in contrast to the DNA-bound protein complexes) necessary to occupy a critical threshold of target gene promoters would be higher when dimers specify organ identity. Note, however, that also a system composed of protein dimers can already posses a certain level of cooperativity, and that other factors like feedback regulation that are not entirely taken into account here might also influence the system.

Fig. 3.

Three different scenarios of how SEP-, AP1- and AGL6-like proteins might be phylogenetically related. The phylogenies shown in (A) and (B) are supported by various publications [compare Theissen et al. (2000); Becker and Theißen (2003) and Nam et al. (2003) with Carlsbecker et al. (2003) and Kim et al. (2005)]. The phylogeny shown in (C) is discussed by Becker and Theißen (2003). Dotted lines represent lineages that probably have been lost in the extant gymnosperms. Dimeric and tetrameric complexes bound to DNA are symbolized as in Fig. 2. Asterisks mark the hypothetical origin of higher order complexes. We assume that higher order complex formation was established in the most recent common ancestor of SEP-like and AP1-like proteins.