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(American Journal of Botany. 2009;96:110-128.) doi: 10.3732/ajb.0800182 © 2009 Botanical Society of America, Inc.

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Floral variation and floral genetics in basal angiosperms¹

² Florida Museum of Natural History, University of Florida, Gainesville, Florida 32611 USA ³ Department of Botany, University of Florida, Gainesville, Florida 32611 USA ⁴ Department of Biology, Oberlin College, Oberlin, Ohio 44074 USA

Received for publication 29 May 2008. Accepted for publication 18 November 2008.

ABSTRACT

Recent advances in phylogeny reconstruction and floral genetics set the stage for new investigations of the origin and diversification of the flower. We review the current state of angiosperm phylogeny, with an emphasis on basal lineages. With the surprising inclusion of Hydatellaceae with Nymphaeales, recent studies support the topology of Amborella sister to all other extant angiosperms, with Nymphaeales and then Austrobaileyales as subsequent sisters to all remaining angiosperms. Notable modifications from most recent analyses are the sister relationships of Chloranthaceae with the magnoliids and of Ceratophyllaceae with eudicots. We review "trends" in floral morphology and contrast historical, intuitive interpretations with explicit character-state reconstructions using molecular-based trees, focusing on (1) the size, number, and organization of floral organs; (2) the evolution of the perianth; (3) floral symmetry; and (4) floral synorganization. We provide summaries of those genes known to affect floral features that contribute to much of floral diversity. Although most floral genes have not been investigated outside of a few model systems, sufficient information is emerging to identify candidate genes for testing specific hypotheses in nonmodel plants. We conclude with a set of evo-devo case studies in which floral genetics have been linked to variation in floral morphology.

Key Words: ABC model • basal angiosperms • evo-devo • perianth evolution • symmetry • synorganization

The unifying feature of angiosperms is the flower, with its associated aspects of reproduction. The fossil record clearly indicates that many diverse floral forms were present early in angiosperm evolution (see papers in this issue), so the underlying genetic architecture of the flower must have allowed for apparently early, rapid, and extensive diversification in floral morphology. The genetics of floral traits have long been of interest to angiosperm horticulturalists and evolutionary biologists, and much is known about the genetic control of specific features in a specific study system. Despite this wealth of information, only recently have we begun to understand the fundamental genes that make a flower. Studies of Arabidopsis thaliana (L.) Heynh indicate that thousands of genes are active throughout the development of a flower, and perhaps as many as 20000 genes are expressed at some point in pollen development alone (Zhao et al., 2001). Despite the apparent genetic complexity of the transitions from floral meristem to mature flower, these thousands of genes are themselves governed by a much smaller set of regulators known as transcription factors. Understanding the roles of transcription factors is therefore key to deciphering the genetics of floral diversity. Furthermore, such studies have begun to extend beyond traditional genetic models and in the process have started to provide clues to the genetic control of floral organs early in angiosperm history. In this paper, we review the early evolutionary history of angiosperms, review general patterns of floral diversity and evolution, describe the roles and effects of several key transcription factors, and suggest testable hypotheses for linking morphological diversity with gene expression.

PHYLOGENETIC OVERVIEW

Ultimately, the solution to Darwin’s "abominable mystery" will come from the integration of paleobotany, systematics, and related fields. Here, we consider historical views of the earliest angiosperms and the most recent results from molecular phylogenetics, both based on analyses of extant diversity, and leave detailed discussion of the fossil record to other authors in this issue (see also Crane et al., 2004; Crepet et al., 2004; Crepet, 2008). We do not address the origin of the angiosperms, which has been discussed in several excellent recent reviews (e.g., Doyle, 1994, 1996, 2006; Hilton and Bateman, 2006). Phylogenetic analyses (e.g., Crane, 1985; Doyle and Donoghue, 1986) strongly support the monophyly of angiosperms by identifying many synapomorphies for the angiosperm clade: double fertilization resulting in endosperm formation, the carpel, phloem tissue composed of sieve tubes and companion cells, stamens with two pairs of pollen sacs, and aspects of gametophyte development and structure. Throughout, we will refer to "basal angiosperms" as a group, despite the fact that they do not form a clade; however, this collective term is engrained in the botanical literature and is more convenient than the more precise reference to "nonmonocot, noneudicot angiosperms." With this explanation, we provide an overview of the phylogeny of "basal angiosperms."

Hypotheses surrounding the "most primitive angiosperms" have changed dramatically and repeatedly over the past century. Indeed, the meaning of "most primitive angiosperms" has itself changed. At various times, this label was applied to those genera or families that had retained the largest number of putatively plesiomorphic features, regardless of the actual antiquity of the group as inferred from the fossil record. In other interpretations, the "most primitive angiosperms" were in fact those considered to represent the earliest lineages, regardless of the collective "primitiveness" of their characteristics. Through the application of molecular phylogenetics, the relative branching order and inferences of plesiomorphic characters can be decoupled, permitting reconstruction of both phylogeny and character evolution based on that phylogeny.

Early views of the first angiosperms were based primarily on hypotheses of what constituted the most "primitive" flowers. As described in greater detail later, Cronquist (1968, 1981, 1988), Takhtajan (1991, 1997), and Stebbins (1974) , for example, considered many of the families of Magnoliales (sensu AGP II, 2003) to be the vestiges of the earliest angiosperms, on the basis of their floral morphology. All have some combination of features inferred to be "primitive": an elongate floral axis, a moderate or large number of floral organs, spiral phyllotaxy, and lack of connation and adnation. This view of the earliest angiosperms prevailed throughout most of the latter half of the 20th century and received support from the fossil record with the discovery of Archaeanthus (Dilcher and Crane, 1984), a large, Magnolia-like flower dating to the early Cretaceous.

Despite the longstanding 20th-century view of Magnolia (or something similar) as the prototypical angiosperm, this hypothesis was by no means the only one of the earliest angiosperms. Following the philosophy that classifications should be arranged from simple to complex forms (later interpreted as having evolved from simple to complex), Adrien de Jussieu (1843) placed the Amentiferae (i.e., species with wind-pollinated flowers borne in catkins (aments)) as the first group of angiosperms, and Engler (Melchior, 1964) largely followed suit. The Amentiferae, comprising Platanaceae, Betulaceae, Fagaceae, Juglandaceae, and Salicaceae, are now recognized as being polyphyletic, and their simple flowers are highly reduced rather than ancestrally simple.

Some (e.g., Burger, 1977) have suggested that the monocots were among the "original" angiosperms, but despite their long fossil record (e.g., Araceae date to 115 million years ago [mya]; Friis et al., 2004) and estimated ages for nearly all major lineages of more than 100 million years (Bremer, 2000; Wikström et al., 2001), phylogenetic analyses clearly nest the monocots well within the angiosperms, with strong support in recent analyses for a placement as the sister to the eudicots + Ceratophyllaceae (Moore et al., 2007; Jansen et al., 2007). Other candidates proposed as early lineages of angiosperms were the "paleoherbs" (i.e., ancient lineages of herbaceous plants, such as Nymphaeales and Piperales; Taylor and Hickey, 1992), a result supported by some early molecular studies (e.g., Hamby and Zimmer, 1992).

Despite progress in understanding both phylogeny and character evolution, morphological data sets for basal angiosperms have too few characters, many of which are plagued by homoplasy, to establish relationships with confidence. Likewise, however, single-gene molecular analyses may also be prone to uncertainty and/or error. The landmark rbcL analysis of 499 species (Chase et al., 1993) identified Ceratophyllum as the sister to all other angiosperms (but without support; Chase and Albert, 1998), which fell into either a "uniaperturate pollen" clade or a "triaperturate pollen" clade. Although Ceratophyllum has a long fossil record (Dilcher, 1989), extending back nearly 120–125 mya, few would have argued on any other basis that Ceratophyllum was one of the earliest angiosperm lineages. As additional genes were analyzed (e.g., 18S-26S rDNA, D. Soltis et al., 1997; atpB, Savolainen et al., 2000), it became clear that the placement of Ceratophyllum was an artifact of the initial rbcL analysis; its placement has continued to vary, ranging from sister to the monocots (e.g., Qiu et al., 1999; Zanis et al., 2002) to sister to the eudicots (e.g., D. Soltis et al., 2000; Moore et al., 2007), a position that is relatively strongly supported based on analyses of whole plastid genomes (Jansen et al., 2007; Moore et al., 2007).

During the past decade, Amborella trichopoda Baill. has emerged as the sister to all other extant angiosperms, either alone or with Nymphaeales, in nearly every study that includes adequate taxon sampling (and generally multiple genes) (e.g., D. Soltis et al., 1997, 2000; Mathews and Donoghue, 1999, 2000; Parkinson et al., 1999; Qiu et al., 1999, 2000, 2005; P. Soltis et al., 1999, 2000; Barkman et al., 2000; Graham and Olmstead, 2000; Borsch et al., 2003; Hilu et al., 2003; Leebens-Mack et al., 2005; Jansen et al., 2007; Moore et al., 2007). Until recently, not much was known about this dioecious shrub from the cloud forests of New Caledonia. In recent years, however, that has changed dramatically, with reports of its ecology (Feild et al., 2000, 2004), floral biology, and population structure (Thien, 2003), pollen (Hesse, 2001), anatomy (Carlquist and Schneider, 2001, 2002; Furness and Rudall, 2001), floral development (Posluszny and Tomlinson, 2003; Buzgo et al., 2004), floral genes (e.g., Kim et al., 2004, 2005; Yamada et al., 2004; Albert et al., 2005; Fourquin et al., 2005, 2007; P. Soltis et al., 2006; D. Soltis et al., 2007; Duarte et al., in press), and genome (Soltis et al., 2008). Although Amborella sits at the end of a long branch in most phylogenetic trees (see discussion by Graham et al., 2000; Qiu et al., 2001), its position as sister to all other extant angiosperms seems quite secure based on analyses of genes from all three plant genomes (e.g., Qiu et al., 2005) and extensive analyses of protein-coding genes from the plastid genome (Leebens-Mack et al., 2005; Jansen et al., 2007; Moore et al., 2007). Although in a few analyses, Nymphaeales have appeared as sister to Amborella or all other angiosperms (e.g., Barkman et al., 2000; Graham and Olmstead, 2000; P. Soltis et al., 2000; Kim et al., 2004), these sister-group relationships rarely received substantial support and were often dependent on the method of analysis. Most studies have instead supported Nymphaeales as the subsequent sister to all other extant angiosperms, although see Graham and Iles (2009, pp. 216–227 in this issue) for a note of caution. This early appearance of the water lily lineage is consistent with the recent discovery of a water lily fossil from 115 to 125 mya (Friis et al., 2001).

The surprising recent report of Hydatellaceae—formerly classified in Poales—as sister to extant Nymphaeales (Saarela et al., 2007) has not altered the relative positions of Amborella and Nymphaeales (+ Hydatellaceae) as sisters to all remaining extant angiosperms (e.g., Saarela et al., 2007; Piedrahita et al., unpublished data). To address this issue and to clarify additional relationships among basal angiosperms, we obtained sequences from the inverted repeat (IR) region of the plastid genomes of species of Sarcandra, Austrobaileya, Aristolochia, Canella, Saururus, Tasmannia, Cabomba, Cinnamomum, and Saruma (A. Piedrahita et al., unpublished data) using the amplification, sequencing and annotation of plastomes (ASAP) method (Dhingra and Folta, 2005), along with the IR regions from the complete plastid genomes of Hydatella, Hedyosmum, Musa, Yucca, and Elais (M. Moore et al., unpublished data). The ASAP method is based on 27 overlapping primer pairs that span the typical angiosperm IR, including noncoding regions. We aligned these IR sequences with 25 published sequences using the program MAFFT (Katoh et al., 2002; Katoh and Toh, 2008), followed by manual adjustment, eliminated those intergenic regions that could not be confidently aligned, and analyzed the remaining data (24463 positions) using the program GARLI (Zwickl, 2006) with default parameters ( Fig. 1A; A. Piedrahita et al., unpublished data).

View larger version (35K): [in this window] [in a new window]   Fig. 1. (A) Phylogenetic tree based on maximum likelihood (ML) analysis of the inverted repeat (IR) region of the plastid genome for 39 angiosperms and two gymnosperm outgroups (Pinus and Cycas) (Piedrahita et al., unpublished data). (B) Summary phylogenetic tree of major lineages of angiosperms, based primarily on analyses of the Angiosperm Phylogeny Group (2003), Moore et al. (2007) , and Jansen et al. (2007) , as described in text.

Austrobaileyales, comprising Austrobaileyaceae, Trimeniaceae, Illiciaceae, and Schisandraceae, have emerged as the sister group to all remaining extant angiosperms. This clade is strongly supported in all analyses, as is its placement relative to other clades. It has a long fossil history, with reports of Trimeniaceae and Illiciaceae extending back to the early to late Cretaceous (Frumin and Friis, 1999; Yamada et al., 2008).

All remaining angiosperms form a large clade in the IR tree, the Mesangiospermae sensu Cantino et al. (2007) , comprising monocots, eudicots, Ceratophyllaceae, Chloranthaceae, and magnoliids (Magnoliales, Laurales, Piperales, and Canellales). Although the results of the IR analysis are generally congruent with those recently reported by Jansen et al. (2007) and Moore et al. (2007) for the basal lineages of angiosperms, two major discrepancies exist among the Mesangiospermae. First, in the IR analysis, Ceratophyllum is sister to the monocots, rather than to the eudicots as in Moore et al. (2007). Second, Chloranthaceae are sister to the eudicots + monocots, rather than to the magnoliids, as in Moore et al. (2007) and Jansen et al. (2007). In both cases, the branches in the IR tree are extremely short, and bootstrap support is less than 50%, suggesting a pentachotomy in the IR tree. Relationships among these five lineages have been very difficult to discern, but recent analyses of whole-plastid genome sequences may have resolved this pentachotomy (Moore et al., 2007; Jansen et al., 2007), and see Saarela et al. (2007) and Graham and Iles (2009, pp. 216–227 in this issue). In the whole-plastid trees, Ceratophyllaceae are sister to the eudicots, this clade (Ceratophyllaceae + eudicots) is sister to the monocots, and Chloranthaceae are sister to the magnoliids (although the latter is not strongly supported). The Chloranthaceae-magnoliid clade is sister to the monocots-Ceratophyllaceae-eudicots clade ( Fig. 1B).

Chloranthaceae, with their ancient fossil record (see Couper, 1958; Walker and Walker, 1984; Friis et al., 1986, 2000; Doyle et al., 2003; Eklund et al., 2004), have long been considered basal angiosperms. Their position as sister to magnoliids (Moore et al., 2007) differs from some previous analyses, in which they appeared as sister to a clade of magnoliids + eudicots (Zanis et al., 2002; Davies et al., 2004).

The magnoliids include most of those families typically considered "primitive" or "basal" angiosperms (e.g., Cronquist [1981 and earlier] and Takhtajan [1997 and earlier] Magnoliidae). Despite substantial attention from the systematics community, relationships among these families were not well understood until molecular phylogenetic analyses. In fact, data sets of five or more genes have generally been required to resolve relationships with good support in magnoliids (e.g., Qiu et al., 1999, 2000, 2005; Zanis et al., 2002). Within magnoliids, Magnoliales are sister to Laurales, and Piperales are sister to Canellales.

Magnoliales comprise Myristicaceae, Degeneriaceae, Himantandraceae, Magnoliaceae, Eupomatiaceae, and Annonaceae, and relationships among these families are now clear (Sauquet et al., 2003). Laurales (sensu APG II, 2003; see Renner, 1999) comprise Calycanthaceae (including Idiospermaceae), Monimiaceae, Gomortegaceae, Atherospermataceae, Lauraceae, Sipurunaceae, and Hernandiaceae. Although Amborellaceae, Trimeniaceae, and Chloranthaceae have occasionally been placed in Laurales (e.g., Perkins, 1925; Thorne, 1974; Cronquist, 1981, 1988; Takhtajan, 1987, 1997), they clearly are not part of this clade. Recent phylogenetic studies unite Aristolochiaceae, Lactoridaceae, Piperaceae, Saururaceae, and Hydnoraceae as Piperales (e.g., Qiu et al., 1999, 2005; P. Soltis et al., 1999; Barkman et al., 2000; D. Soltis et al., 2000; Nickrent et al., 2002; Zanis et al., 2002). While not considered closely related on morphological grounds, Canellaceae and Winteraceae form a well-supported sister group in all multigene analyses (e.g., Qiu et al., 1999; P. Soltis et al., 1999; D. Soltis et al., 2000; Zanis et al., 2002, 2003), as well as in the nonmolecular analysis of Doyle and Endress (2000). Canellales are strongly supported as sister to Piperales, although neither Canellaceae nor Winteraceae have been proposed as closely related to any members of Piperales. Putative synapomorphies for all four major clades of magnoliids are given in Doyle and Endress (2000) , Stevens (2001 onward), and Soltis and Soltis (2004).

The remaining 97% of angiosperm species diversity (Drinnan et al., 1994) falls primarily into the monocot (22%) and eudicot (75%) clades, with Ceratophyllaceae as sister to eudicots (Moore et al., 2007). Relationships among most major lineages of monocots and eudicots are now clear ( Fig. 1; see Chase et al., 2006 , and D. Soltis et al., 2005, respectively, for summaries). Because this paper focuses primarily on floral evolution in early lineages of angiosperms, we will not address these relationships further here, but refer the reader to Fig. 1 and the reviews cited. However, early evolutionary splits within the monocots and eudicots (e.g., Ranunculales) are potentially informative for reconstructions of early angiosperm evolution (e.g., Endress and Doyle, 2009, pp. 22–66 in this issue). Therefore, consideration of floral morphology and floral genetics in eudicots in particular may be relevant for understanding the early diversification of the flower, and the discussion that follows consequently includes information on eudicots, where appropriate.

PATTERNS OF FLORAL EVOLUTION

Historical intuitive interpretations
Throughout most of the 20th century, floral evolution was discussed as "trends"—for example, Armen Takhtajan’s (1991) book Evolutionary Trends in Flowering Plants. Perhaps the best-known "trends" are those referred to as "Bessey’s Dicta" (Bessey, 1915), which, either directly or indirectly, had a profound impact on views of floral diversification for much of the 20th century. Most prominent for considering patterns of floral evolution are the following abbreviated statements: polymery to oligomery, petaly to apetaly, actinomorphy to zygomorphy, hypogyny to epigyny, apocarpy to syncarpy, polycarpy to oligocarpy, polystemony to oligostemony, apostemony to synstemony, and monocliny to dicliny. Bessey also stressed that evolution is not always "upward" and that evolutionary rates may differ among organs/structures, such that a given plant may be a mosaic of ancestral and derived features. Bessey’s views influenced many generations of systematists, particularly in North America. Although explicit reconstructions of specific features across phylogenetic trees show generally complex patterns of floral evolution (discussed later), the "trends" suggested by Bessey are in many cases largely supported (see e.g., Ronse De Craene et al., 2003; D. Soltis et al., 2005).

Although Bessey’s hypotheses are in one sense "phylogenetic"—that is, they describe putative changes through time—they followed neither an explicitly derived phylogenetic tree nor an explicit method for inferring evolutionary transformations in individual characters. Likewise, many other prevailing views of floral evolution lack explicit methodology and emphasize the particular interests of their authors. Despite these shortcomings, the views of floral change on a macroevolutionary scale put forward by Bessey in the early 20th century and by Cronquist, Takhtajan, and Stebbins in the latter half of the 1900s, have contributed many hypotheses that are testable given current understanding of angiosperm phylogeny.

Historical intuitive interpretations vs. phylogenetic reconstruction
Using explicit hypotheses of phylogeny, several recent studies have addressed the evolution of specific floral characters in light of reconstructions of the ancestral flower. Here, we review both the ancestral reconstruction of the flower and patterns of evolution, based in large part on the phylogenetic trees of the Angiosperm Phylogeny Group (2003; Mathews and Donoghue, 1999; Parkinson et al., 1999; Qiu et al., 1999, 2000; P. Soltis et al., 1999; Barkman et al., 2000; D. Soltis et al., 2000; Zanis et al., 2002; Hilu et al., 2003; reviewed in D. Soltis et al., 2005) and compare and contrast these findings with the historical intuitive approach of Bessey, Cronquist, Tahktajan, Stebbins, and others. We limit this discussion to "trends" in overall floral organization because it is floral organ identity and orientation that are best understood from a genetic perspective (see later). We focus on four central features of the flower: (1) the size, number, and organization of floral organs; (2) the evolution of the perianth; (3) floral symmetry; and (4) floral synorganization.

Trends in flower size, organ number, and phyllotaxy
De Jussieu (1843) considered that wind-pollinated flowers borne in catkins (aments) represented the first flowers, with more complex forms arising later. This view of the Amentiferae as the "model" for the earliest angiosperms was followed by Engler (Melchior, 1964). Of course, we now recognize that wind pollination has evolved multiple times in the angiosperms, each time accompanied by a reduction in floral size and complexity (e.g., Stebbins, 1970; Culley et al., 2002).

Takhtajan (1991) viewed the ancestral flower as being of moderate size, with subsequent evolution toward both larger and smaller sizes. The earliest flowers had an indefinite (but moderate) number of separate organs, spirally arranged on a somewhat elongate receptacle (e.g., like those of Degeneria [Degeneriaceae], many Magnoliaceae, Galbulimima [Himantandraceae], Eupomatia [Eupomatiaceae], and Winteraceae). Per Takhtajan (1991) , through time, the receptacle shortened, bringing stamens and carpels into close proximity. "Cyclic" flowers (i.e., those with whorled, rather than spirally arranged, organs) arose early in angiosperm evolution in multiple lineages. The transitions from spiral to cyclic flowers proceeded from the perianth inward or from the carpels outward. Furthermore, Takhtajan (1991) viewed this transformation, especially between spiral phyllotaxy and trimery, as reversible (see also Endress, 1987), generating further diversity in combinations of spiral vs. whorled organ arrangements. A further trend noted by Takhtajan is the reduction in the number of homologous floral organs through time—i.e., "oligomerization"—and a concomitant fixation of the number of parts. Takhtajan viewed these smaller flowers with fixed numbers of parts as more "integrated than archaic, less oligomerized flowers"—a concept similar to Endress’s (1990a) synorganization. On occasion, as in Magnoliaceae, Cactaceae, and Aizoaceae, polymerization led to secondarily derived, large flowers, with many parts.

Consideration of these observations in light of the current phylogeny suggests that the ancestral condition is rather more uncertain (and see Endress and Doyle, 2009, in this issue). Although both Amborella and Austrobaileyales have spiral phyllotaxy, consistent with the model of Cronquist (1988), Takhtajan (1991) , and others, Nymphaeales have whorled phyllotaxy, making the ancestral state equivocal; the fossil record is likewise equivocal, as both spiral and whorled phyllotaxy are present in many early angiosperms. Likewise, reconstructions of the number of parts of the ancestral perianth are equivocal; Amborella and Austrobaileyales again share a state—an indeterminate number of parts. However, trimery, present in Nymphaeales and reconstructed as the ancestral state for all angiosperms except Amborella, Nymphaeales, and Austrobaileyales, evolved early and characterizes many lineages of basal angiosperms ( D. Soltis et al., 2005 ).

Evolution of the perianth
The origin and diversification of the perianth were central to Takhtajan’s views of floral evolution. He proposed that the first perianth originated from protective bracts ("bracteopetals"; Kozo-Poljanski, 1922). Bracteal perianths are purportedly found in Degeneriaceae, Magnoliaceae, Annonaceae, Canellaceae, Winteraceae, Illiciaceae, Schisandraceae, Austrobaileyaceae, Lauraceae, and Calycanthaceae (see also Smith, 1928; Eames, 1961; Hiepko, 1965). Traditionally, petals of monocots and most "Magnoliopsida" sensu Takhtajan (i.e., essentially all eudicots) have been considered "andropetals," having originated through sterilization and modification of stamens. A staminal origin of petals has been recognized for over a century (e.g., Celakovsky, 1896; Worsdell, 1903; Arber and Parkin, 1907; Kozo-Poljanski, 1922; Troll, 1927, 1928; Eames, 1931, 1961; Hiepko, 1965). More recently, Ronse De Craene (2007) has questioned the accepted staminal origin of petals in eudicots and suggested that at least some eudicots have petals of bracteal origin.

Takhtajan considered the evolutionary replacement of bracteopetals by andropetals unlikely and proposed a sequence by which andropetals may have originated within flowers that bore a perianth of bract-like sepals. Following the view that petals are essentially stamens with arrested development (Goebel, 1933), Takhtajan proposed a two-step origin of the perianth involving a bracteal origin of sepals and an andropetaloid origin of petals.

Character reconstructions based on molecular phylogenetic analyses have identified many examples of independent derivation of a differentiated perianth (e.g., Ronse De Craene et al., 2003; D. Soltis et al., 2005). The ancestral perianth was likely undifferentiated, without distinct sepals and petals, and both the derivation of a differentiated perianth and the loss of perianth appear to have arisen multiple times independently throughout the course of angiosperm evolution (Ronse De Craene et al., 2003; D. Soltis et al., 2005). Explicit models of perianth origin have recently been proposed (e.g., Baum, 1998; Albert et al., 1998, 2002; Frohlich and Parker, 2000; Frohlich, 2006).

An outstanding example of a clade in which multiple derivations of a differentiated perianth have occurred is the Caryophyllales. Although a clade of core eudicots rather than an older group, Caryophyllales can provide excellent information on transitions of perianth form. Recent phylogenetic analysis of the order, together with a parsimony reconstruction analysis of perianth features (Brockington et al., in press), suggests that a simple uniseriate perianth was the ancestral condition within the Caryophyllales; subsequently, there have been a minimum of six independent origins of a differentiated perianth.

Floral symmetry
Shifts between radially symmetric (actinomorphic) and bilaterally symmetric (zygomorphic) flowers have occurred multiple times throughout the history of angiosperms (e.g., Stebbins, 1974; Endress, 1996, 1999; Donoghue et al., 1998; Ree and Donoghue, 1999; Endress and Matthews, 2006). Zygomorphy is evident in the fossil record in the early Tertiary (Crepet et al., 1991; Dilcher, 2000; Crepet, 2008) and among extant plants is generally restricted to the monocots (Orchidaceae and some Zingiberales) and a few clades of core eudicots (the rosid family Fabaceae and the asterids Lamiales and Asteraceae) (Stevens, 2001 onward). However, zygomorphy also occurs in the basal angiosperm Aristolochia (Aristolochiaceae). A general "trend" toward zygomorphy has been observed within many clades of asterids, with shifts to zygomorphy viewed as having important implications for pollination ecology (e.g., Crepet et al., 1991; Crepet, 1996, 2008; Neal et al., 1998; Dilcher, 2000). Multiple gains and losses of zygomorphy in the asterids (e.g., Donoghue et al., 1998; Ree and Donoghue, 1999; Cubas, 2004) suggest a relatively simple genetic switch between actinomorphy and zygomorphy. Furthermore, zygomorphic flowers across the asterids are not homologous, and thus switches both from and to actinomorphy may occur by different genetic mechanisms (Donoghue et al., 1998). Finally, changes in symmetry may occur during development, for example, from zygomorphy early in development to actinomorphy in mature flowers (Endress, 1999; Tucker, 1999).

Floral synorganization
One of the few major trends in floral evolution is that of increasing synorganization of the structural components of the flower (Endress, 1990a). Synorganization (Remane, 1956; Vogel, 1959, 1969; Endress, 1990a) is the connection of two or more structural elements to form a functional system. In flowers, synorganization results generally from congenital or postgenital fusion of parts (sepals, petals, stamens, or carpels) or occasionally from an otherwise close association of parts. Despite the widespread occurrence of floral synorganization, particularly in eudicots, little or nothing is known about the potential genetic control of synorganization, whether associations are among like or unlike floral parts. A prerequisite for experiments designed to address the genetic control of synorganizational associations is a thorough understanding of morphological evolutionary patterns, from both broad and narrow phylogenetic perspectives. Plant families of relatively recent derivation (e.g., the asterids) generally have more highly synorganized flowers than those families that represent more ancient lineages (e.g., magnoliids and other basal angiosperms) (e.g., Endress, 1990b). Although synorganization takes many forms, it is most commonly expressed as the fusion of carpels to form a syncarpous gynoecium, a condition that characterizes 80% of the estimated 260000-plus (Takhtajan, 1997) species of angiosperms (Endress, 1982). Syncarpy is considered evolutionarily successful (Endress, 1990b) because it provides for centralized selection of pollen tubes (Endress, 1982; Endress et al., 1983).

Although more ancient groups of angiosperms exhibit less synorganization than more derived groups, the evolutionary origins of synorganization are unclear. Synorganized flowers characterize most eudicots, but several basal lineages of eudicots lack synorganized flowers (e.g., most Ranunculaceae, Trochodendron, Nelumbo). Among magnoliids, Eupomatia (Magnoliales) exhibits synorganization of stamens to form a synandrium, demonstrating that synorganized flowers have evolved repeatedly. Many groups of monocots also have synorganized flowers (e.g., irises, orchids, gingers, bromeliads), which likely represent parallels to conditions in the eudicots. Apparent losses of synorganization have also occurred in some genera (e.g., Paeonia, in Saxifragales). The phylogenetic distribution of synorganized flowers is a key to understanding floral diversity and the constraints under which floral evolution has proceeded (Endress, 1999).

Synorganization is lacking or limited in those flowers with spiral (or irregular) phyllotaxy (Endress, 1990a, 1990b), in which the structural elements of the flower are arranged along a spiral on the floral apex. Increased synorganization is observed in those flowers with whorled phyllotaxy, wherein identical structural elements are arranged in rings on the floral apex. Apparently correlated with spiral phyllotaxy and a low potential for synorganization are the variability in the number of structural elements of the flower and a high frequency of deviations from the most common floral pattern (Endress, 1990a). For example, many magnoliids and other basal lineages have spiral phyllotaxy and variable numbers of parts (e.g., Friis and Endress, 1990; Takhtajan, 1991), and little or no synorganization of structural elements, although even phyllotaxy appears highly labile in these plants (e.g., Endress, 1987, 1990b, 1994); most fossil flowers from the early Cretaceous have spiral phyllotaxy, but whorled phyllotaxy was also present at that time (see Friis and Endress, 1990). More recent lineages, such as those of the asterid clade, show whorled phyllotaxy, fixed (or nearly so) merosity, and synorganization both among elements of a whorl and between whorls (as in Apocynaceae; Endress, 1990a). In fact, Endress (1990a) considered whorled arrangement, radial symmetry, and a small, fixed number of floral organs prerequisites for the evolution of complex synorganizations. The stability of these associations and the possible preconditions needed for the development of synorganized flowers is supported by mapping several of these characters onto a phylogenetic tree for angiosperms (e.g., Soltis et al., 2005).

Synorganization of stamens occurs less frequently than synorganization of carpels or petals, although synorganized stamens do occur in some groups, including the basal angiosperm Eupomatia (Eupomatiaceae) and the core eudicots Fabaceae, Malvaceae, and Asteraceae. Associated with this more limited synorganization is greater variability in both number and arrangement of stamens. Patterns of stamen organization are associated with other floral traits and may depend, to some extent, on the structure and organization of the flower as a whole. In this respect, the degree of synorganization of the entire flower may either constrain or allow the evolution of certain types of stamen organization. Evolutionary and developmental constraints on basic floral structure are generally attributed to physical limitations, such as the size and shape of the receptacle and/or floral apex (e.g., Endress, 1990a, 1990b; Takhtajan, 1991). Polymery (or true polyandry), the spiral arrangement and centripetal development of many stamens, is often associated with spiral phyllotaxy, an undifferentiated perianth, the presence of staminodes, complex floral vasculature, and typically trimery or dimery as the basic merosity of the flower (Ronse De Craene and Smets, 1994, 1995).

The reconstructed ancestral flower of crown angiosperms
In contrast to the paradigm of large, strobiloid flowers as ancestral, both explicit character reconstructions (e.g., Doyle and Endress, 2000; Ronse De Craene et al., 2003; D. Soltis et al., 2005) and the fossil record (e.g., Taylor and Hickey, 1992; Friis et al., 2000) suggest that the earliest flowers were instead of small to moderate size (see also Endress, 2001, 2006). As noted, however, both the phyllotaxy and merosity of the ancestral angiosperm flower are equivocal. The perianth was probably undifferentiated, and the stamens were likely laminar, producing pollen characterized by irregular radial (columellar) elements mixed with granules—and "intermediate" morphology (Doyle and Endress, 2000), in contrast to Cronquist’s (1988) view of granular infratectal pollen structure as ancestral. The earliest carpels appear to have been ascidiate and closed by secretion (Endress and Igersheim, 2000), rather than plicate per Eames (1961) and Cronquist (1968, 1988), although postgenital fusion is also present in the earliest lineages of extant angiosperms (Endress and Igersheim, 2000). Morphological and developmental studies of extant species continue to allow inferences of other features of early angiosperms (e.g., endosperm ploidy, Williams and Friedman [2002 ], Friedman [2008]; endosperm formation, Floyd and Friedman [2000]), as do new reports and interpretation of the fossil record (e.g., Sun et al., 1998, 2002; Friis et al., 2001, 2004; Gandolfo et al., 2004).

DEVELOPMENTAL GENETICS OF THE FLOWER

Overview
Because of its central role in both agricultural and evolutionary studies, the flower has received extensive attention from morphological, developmental, and genetic perspectives, and syntheses of developmental genetics have emerged, based on prominent models and crops (see, e.g., reviews in Davies et al., 2006; Endress, 2006; Frohlich, 2006; Irish, 2006; Rijpkema et al., 2006; D. Soltis et al., 2006; Teeri et al., 2006; Zahn et al., 2006a; Theissen and Melzer, 2007). It may be that small changes in the timing or location of gene expression can lead to large changes in floral phenotype. Developmental genetics is providing a host of candidate genes with which to test hypothesized effects and infer causation of floral diversity. For example, the genetic control of floral organ identity—via the ABC model (Bowman et al., 1991; Coen and Meyerowitz, 1991)—has been thoroughly investigated in Arabidopsis and Antirrhinum and extended, in one form or another, to most other angiosperms (see Irish, 2006; P. Soltis et al., 2006; Theissen and Melzer, 2007 , for reviews). Likewise, knowledge of other gene systems, such as the transcription factors that regulate floral symmetry, allows for testable hypotheses on the shifts between radially and bilaterally symmetrical flowers. Eventually, detailed analyses of the genetics of model organisms will provide further candidates for linking genes with phenotypes. In the sections that follow, we present examples of floral diversity that may be related to specific gene actions. Such studies are in their infancy, in an evolutionary context, particularly for basal angiosperms, and the results presented here are clearly limited to the small sample of plant species investigated to date. Therefore, some of the examples we describe involve eudicots rather than basal angiosperms, simply to illustrate the ways in which developmental genetics and studies of floral evolution can be integrated. However, before presenting these examples, we will review briefly some of the fundamental aspects of floral genetics.

The ABC model
The ABC model describes the activities of transcription factors that regulate floral organ identity ( Fig. 2). This combinatorial model of gene activity posits that A function specifies sepals, the combined activity of A and B functions specifies petals, B and C functions together specify stamens, and C function alone specifies carpels. In Arabidopsis, APETALA1 (AP1) and APETALA2 (AP2) control the A function, APETALA3 (AP3) and PISTILLATA (PI) are B-function genes, and AGAMOUS (AG) is the C-function gene. Recognition of the role of SEPALLATA (SEP) genes in the specification of floral organ identities (E function; Pelaz et al., 2000; Theissen, 2001; Ditta et al., 2004) has led to the revision of the "ABC" model as the "ABCE" model. The D function controls ovule identity, and the D-function gene in Arabidopsis is SEEDSTICK (STK) (Colombo et al., 1995; Pinyopich et al., 2003). All of these genes, except AP2, are MADS-box genes. A major question is, "What regulates the regulators?" This topic has been addressed in detail for the A, B, and C functions by Zahn et al. (2006a) .

View larger version (23K): [in this window] [in a new window]   Fig. 2. (A) ABC(E) model of floral organ identity, illustrating combinatorial action of A-, B-, C-, and E-function genes. (B) Fading borders model, showing gradients in levels of gene products in overlapping regions of gene action (based on gene expression studies of basal angiosperms, especially Kim et al., 2005); note that the E-function has not yet been examined in detail, and the E box is therefore left open.

Where divergent floral morphologies are due to alterations in organ specification, the ABC genes represent excellent candidates for the genetic control of floral differences, although many aspects of floral morphology are likely to be controlled by other means. Much of floral diversity is represented by changes in the number and arrangement of floral organs. Because the activities of the ABC regulators have little to do with expanding and declining numbers of floral organs (with the exception of organ absence, perhaps), other genes and gene systems are needed to explain such differences.

CYCLOIDEA and other genes that control floral symmetry
Floral symmetry in the model Antirrhinum majus L. (snapdragon) is controlled by three transcription factors in two gene families. CYCLOIDEA (CYC), of the TCP family, specifies dorsal floral identity (Luo et al., 1996, 1999; Almeida et al., 1997; reviewed in Howarth and Donoghue, 2006) and is the best studied of the symmetry-controlling genes; DIVARICATA and RADIALIS of the MYB family are also involved in floral symmetry (Almeida et al., 1997; Galego and Almeida, 2002; Corley et al., 2005; Costa et al., 2005). In Antirrhinum majus (snapdragon), CYC and its close relative DICHOTOMA (DICH) are partially redundant in function, differing slightly in the timing of expression, but both are required for production of a "normal" bilaterally symmetrical flower with proper dorsiventrality. Mutations lead to radially symmetrical flowers and loss of dorsiventrality. A complex pattern of gene duplication throughout the history of eudicots has produced a set of paralogs (Howarth and Donoghue, 2006), the functions of which are still unknown, but which may contribute in combination with other genes to fundamental shifts in floral morphology. Homologs of CYC are also involved in determining symmetry in the asterid Gerbera (Broholm et al., 2008) and have been recruited, apparently independently, to control floral symmetry in legumes (Fabaceae) and Iberis (Brassicaceae), both rosids (Feng et al., 2006; Busch and Zachgo, 2007; Wang et al., 2008). The control of symmetry in other lineages, including basal angiosperms like Aristolochia and relatives (which have contrasting types of symmetry), is as yet unknown but could involve other genes in new and complex ways.

Other genes affecting floral morphology
The ABC model applies only to organ identity and thus can be used only for testing hypotheses of organ homology, ancestry, etc. Changes in the numbers and arrangements of floral organs are controlled by other genes, but data are generally only available for Arabidopsis. Whether the orthologs to the Arabidopsis genes maintain similar functions in other species is not yet known; however, the Arabidopsis genes provide possible candidates for evo-devo study. In Arabidopsis, the homeodomain protein WUSCHEL and the CLAVATA ligand–receptor system control the fate of shoot apical meristems, thereby affecting the number of floral organs. Both WUSCHEL and the CLAVATA genes act by regulating hormone levels in the shoot apical meristem (Leibfried et al., 2005). The CLV/WUS genetic module may cause changes in meristem size and therefore shifts in the number of floral organs. Other candidates are PERIANTHIA (PAN) and ETTIN (ETT). PAN is required for floral organ patterning in Arabidopsis thaliana and acts downstream of genes affecting floral meristem identity and independently of those controlling meristem size; pan mutants show a switch to pentamery in sepals, petals, and stamens in A. thaliana (Running and Meyerowitz, 1996). Also in A. thaliana, ETT specifies regional floral meristem identity and affects perianth organ number, stamen number, and differentiation in stamens and gynoecia (Sessions et al., 1997). Like PAN, ETT acts independently of CLV. More information on the patterns and timing of gene expression is needed for all of these genes in Arabidopsis and other models before they can be fully considered as candidate genes to explain alterations in floral organ number on an evolutionary scale.

Carpel closure, a key event in early angiosperm evolution, has been addressed thoroughly from a morphological perspective (Endress and Igersheim, 2000). The carpels of most of the basal lineages of extant angiosperms (Amborella, Cabomba, Brasenia, Austrobaileya, Trimenia, Kadsura, and Ascarina) are closed by secretion (Endress and Igersheim, 2000; Endress, 2005), suggesting that this was the plesiomorphic state. At least some fusion occurred independently in multiple lineages of basal angiosperms, such as Nymphaea, Illicium, and the magnoliids (Endress and Igersheim, 2000), and eventually carpels closed by fusion were established as the main state in the remainder of the angiosperms. The genes CRABS CLAW and TOUSLED control major facets of carpel development, including carpel fusion in Arabidopsis, and have been shown to have conserved roles in Amborella and Cabomba (Fourquin et al., 2005, 2007). However, the fact that these genes have conserved expression in Arabidopsis, Amborella, and Cabomba indicates that they are not responsible for variation in the degree of carpel fusion among angiosperm lineages, and the gene(s) controlling the extent of fusion have not been identified. Another gene involved in carpel development is YABBY-2, which in Arabidopsis is expressed in the abaxial domains of the leaf, carpel, stamen, and perianth and contributes to dorsiventrality (reviewed in Yamada et al., 2004). The Amborella ortholog of YABBY-2, AmbF1, is expressed instead in the adaxial tissues of carpel and leaf, suggesting a possible shift in the polarity pathway between basal angiosperms and Arabidopsis (Yamada et al., 2004).

USING FLORAL GENES TO TEST HYPOTHESES OF FLORAL EVOLUTION

Correlating variation in organ identity with gene expression patterns
In many basal angiosperms, the perianth is considered "undifferentiated" with no true sepals or petals. However, developmental studies of Amborella suggest that in fact the perianth is differentiated into outer and inner tepals (Buzgo et al., 2004), but with a gradual transition from lateral receptacular bracts to tepals, from outer tepals to inner tepals, and from inner tepals to stamens in male flowers (and from tepals to staminodes and then carpels in female flowers). This gradual transition from outer to inner floral organs also appears to characterize other basal angiosperms such as Austrobaileyales and may therefore represent the ancestral condition (e.g., Ronse De Craene et al., 2003; Soltis et al., 2005).

This view of floral morphology is not consistent with the discrete whorls of morphologically distinct floral organs present in most eudicots and predicted by the ABC model. Neither the ABC model nor the alternative sliding/shifting boundary modification (Bowman, 1997; Kramer et al., 2003) can account for such morphological intergradations. The fading borders model (Buzgo et al., 2004) suggests that gradual transitions in organ morphology result from a gradient in levels of expression of floral regulators across the meristem ( Fig. 2B). Overlapping expression of floral regulators would impose some features of adjacent organs onto each other and thus produce morphologically intergrading rather than distinct floral organs. Expression of B, C, and E homologs in basal angiosperms is often broader than specified by the ABC model, and expression of B-function homologs in particular supports the fading borders model (Kim et al., 2005).

Given the typically broad expression patterns of B and C homologs in most basal angiosperms studied to date, the ABCE model of Arabidopsis and Antirrhinum appears to have been derived from an ancestral genetic program that expressed floral regulators broadly across the floral meristem (see Kim et al., 2005). Although fundamental components of the floral genetic/developmental program have been conserved across the angiosperms, evolutionary diversification of this ancestral program may have occurred through localized expression of different regulators to different regions of the meristem. For example, restricted expression of floral organ regulators resulted in the specification of discrete floral whorls (Kim et al., 2005), as seen in most eudicots and explained by the combinatorial action of the ABCE model of Arabidopsis. In the magnoliid Asimina (Annonaceae) and in the core eudicots, restricted gene expression results in flowers with distinct and differentiated sepals, petals, stamens, and carpels—an obviously independent derivation of the whorled floral structure in these distant lineages (Kim et al., 2005). In the basal eudicots Ranunculus and Aquilegia (Ranunculaceae), shifts in location of B function, directed by duplicate B-function genes, are correlated with changes in perianth morphology (Kramer et al., 2003; Kramer and Zimmer, 2006; Rasmussen et al. [2009], pp. 96–109 in this issue). In general, divergent floral morphologies may be controlled by underlying shifts in the timing and/or location of expression of a key set of floral regulators. Different "attempts" at fine-tuning of the ancestral program may be responsible for having generated much of the floral diversity that exists, or has existed.

Decoupling morphological variation and candidate gene expression
In many cases, morphological variation is correlated with spatiotemporal patterns of gene expression. However, there are also instances in which the evolution of morphological variation does not appear to correlate with patterns of candidate gene expression; these are of equal importance when attempting to understand the extent to which key regulatory genes have influenced the evolution of morphological novelty. An analysis of MADS-box gene expression in Aristolochia (Aristolochiaceae; Jaramillo and Kramer, 2004) revealed that orthologs of the B-function genes APETALA3 and PISTILLATA are expressed in the showy perianth but that their expression is restricted to the nonpetaloid tissue. These AP3 and PI orthologs do not seem to be involved in the production of the petaloid parts of the perianth. Clearly, therefore, the evolution of tissues characteristic of particular floral organs, e.g., petals, can occur independently of proposed candidate genes. AP3 and PI have been shown to be expressed in the showy perianth parts of petaloid monocots such as Tulipa (Liliaceae) but are also expressed in the morphologically distinct and nonpetaloid second-whorl lodicules of derived grasses such as Oryza and Zea (Poaceae; Ambrose et al., 2000; Nagasawa et al., 2003). Whipple et al. (2007) demonstrated that AP3 and PI expression is maintained in the second perianth whorl of basal monocots through derived grasses, irrespective of the degree of morphological change that has occurred in these organs. These results support a conserved role for the B function in the second whorl of perianth across angiosperms, but they argue that this conservation is due to the role of these genes in allowing differentiation of perianth organs rather than specifying petal identity (and characteristics) per se. B-gene expression can perhaps be maintained as a molecular switch even when the downstream morphological pathways that are turned on by this switch have undergone considerable diversification. Additional studies of instances in which floral morphology and patterns of gene expression are not correlated will provide further insight into the evolution of floral development.

Bracteopetals vs. andropetals in Lauraceae
The underlying genetic mechanism of floral organ identity provides a means for testing among hypotheses of bracteal and andropetaloid origins of the perianth (e.g., Albert et al., 1998, 2002; Baum, 1998; Chanderbali et al., 2006; discussed later). The perianth in most basal angiosperms is typically composed of morphologically similar tepals, presumably of bracteopetaloid origin (e.g., Takhtajan, 1991; see earlier). However, there may be a bias in studies of bracteopetals vs. andropetals, with many apparent examples of bracteopetals yet to be thoroughly examined by in situ hybridization of MADS-box gene orthologs. One of the few studies to date, in addition to Amborella (Kim et al., 2005) and Aristolochia (Jaramillo and Kramer, 2004), in which the spatial and temporal aspects of gene expression have been examined, is that of Persea americana Mill. (Lauraceae; Chanderbali et al., 2006). The flowers of Lauraceae are trimerous, with three stamen whorls and an inner whorl of staminodes surrounding a single carpel (Rohwer, 1993). The two perianth whorls are morphologically similar and have been considered bracteopetals on the basis of their generally "sepaloid" appearance (Ronse De Craene et al., 2003; Albert et al., 1998). However, homologs of the C-class gene AGAMOUS—typically only expressed in stamens and carpels—are also expressed in the tepals of Persea (avocado), perhaps the vestige of a staminal ancestry of Persea tepals and suggesting andropetaly rather than bracteopetaly in Persea and other Lauraceae (Chanderbali et al., 2006). Although the expression of AG homologs in tepals of Persea may instead reflect expansion of gene expression from the reproductive organs into the perianth, both genetic and morphological data make this interpretation less likely (Chanderbali et al., 2006). The replacement of outer stamen whorls by tepaloid staminodes in several members of Lauraceae suggests a close developmental pathway between stamens and tepals and further supports the andropetaloid origin of tepals in this family. Microarray analysis has identified over 1000 genes with elevated expression in floral tissues (relative to leaves), including homologs of AP3, PI, AG, and SEP3 and many other transcription factors; this approach further supports the interpretation of a staminal origin of the perianth in Persea (Chanderbali et al., 2008). Further study of gene expression and function in Persea, a transformable (Cruz-Hernández et al., 1998; Litz et al., 2005) woody, basal angiosperm, should help to address fundamental questions of homology and the origin of the perianth.

In this case study in Lauraceae, the expression of floral genes has been employed to question traditional concepts of organ homology. To detect differences in gene expression between bracteopetals and andropetals, we need a clear understanding of the homology of the petaloid organ (either to stamens or bracts). As argued by Ronse De Craene (2007) , traditional concepts of bracteopetals and andropetals, particularly in core eudicots, need re-evaluation. Nonetheless, indisputable examples of bracteopetals and andropetals within closely related lineages do exist, for example in the core Caryophyllales (see later; Brockington et al., in press).

Caryophyllales perianth reconstruction
Although a distinct lineage of eudicots rather than one of basal angiosperms, Caryophyllales exhibit patterns of perianth evolution that allow for untangling bracteopetals from andropetals. Molecular phylogenetic analyses have identified many examples of independent derivation of a differentiated perianth (Ronse De Craene et al., 2003; D. Soltis et al., 2005). From an ancestral simple uniseriate perianth in Caryophyllales, there have been between six and 10 independent origins of a differentiated perianth (Brockington et al., in press). Although in Caryophyllales the homology of the perianth parts to petals in other core eudicots is uncertain, it is clear that many lineages (Sesuvioideae of Aizoaceae, Nyctaginaceae, Portulacaceae, Cactaceae) possess petaloid organs that are bracteal in origin. Furthermore, the occurrences of stamen-derived petals within Caryophyllales (Caryophyllaceae, Aizoaceae, and Glinus and Corbichonia in Molluginaceae) are independent events (Ronse De Craene, 2007; Brockington et al., in press). These independent occurrences are valuable as there are very few examples of petals within core eudicots that are unquestionably stamen-derived (Ronse De Craene, 2007). The pattern of perianth evolution in Caryophyllales therefore presents an important opportunity to address questions as to differences and/or similarities in the genetic determination of bracteopetals and andropetals. The genetic and developmental control of both andropetals and bracteopetals within the predominantly andropetaloid core eudicots merits further investigation.

Radial vs. bilateral symmetry
CYCLOIDEA and related genes have been proposed as key elements in the many shifts between actinomorphy and zygomorphy. However, the loss of zygomorphy is much more complex than a simple loss of CYC expression. Furthermore, CYC and its relatives play other roles than simply controlling floral symmetry. In Antirrhinum majus and other Antirrhineae, mutations in both CYC and DICH are required to produce ventralized flowers with radial symmetry. It would seem that CYC/DICH double mutants could arise fairly regularly, resulting in independent losses of zygomorphy within otherwise zygomorphic clades. However, mutations in CYC seem not to be responsible for at least some of the switches from zygomorphy to actinomorphy in the asterids (Donoghue et al., 1998). Changes in symmetry through development also suggest that the classic gene action of CYC cannot fully explain all switches between zygomorphy and actinomorphy. Finally, evidence of extensive gene duplication of the CYC lineage in core eudicots (Howarth and Donoghue, 2006) suggests that the genetic control of bilateral symmetry may be more complex than typically envisioned. For example, in Lonicera morrowii A. Gray (Caprifoliaceae), expression of duplicate copies varies with development and may be partitioned among petals (Howarth and Donoghue, 2006), but additional work is needed to evaluate the generality of this result among species with multiple CYC paralogs.

Mohavea confertiflora A. Heller is a close relative of Antirrhinum majus that differs in corolla symmetry (i.e., it has radial symmetry) and pollination mode, possibly due to changes in expression of CYC and DICH orthologs. Hileman et al. (2003) demonstrated that shifts in the expression of CYC and DICH orthologs are correlated with changes in floral morphology in Mohavea: abortion of the lateral stamen is correlated with expansion of CYC and DICH expression, while a reduction in DICH expression is associated with the symmetry of the adaxial petals. Therefore, differences in levels and location of expression of these key regulators have had a profound effect on floral morphology and consequently on pollination ecology of this species.

Gene duplications and their role in floral diversification
Gene duplications represent the ultimate source for the origin of genetic novelty (Ohno, 1970), and it is reasonable to predict that duplications in genes controlling aspects of floral morphology may be responsible for morphological novelty. This prediction has been best studied in Aquilegia vulgaris L. (Kramer et al., 2007; see Rasmussen et al. 2009, pp. 96–109 in this issue). Duplications of the floral organ identity gene AqvAP3 have produced three paralogs, and each has its own function in specifying the petaloid sepals, petals, and staminodes (Kramer et al., 2007). These paralogs have diverged in expression in space and time. Early in floral development, AqvAP3-1 is expressed in petal, stamen, and staminode primordia but later in development its expression is restricted to staminodes. AqvAP3-2 is expressed early in stamens and staminodes, but then its expression shifts to stamens and petals with some sepal expression very late in development. AqvAP3-3 is restricted to petals throughout most of development, with very low expression in stamens at later stages. Functional analyses of AqvPI, which is expressed in all floral organs except carpels, demonstrates that the Aquilegia B-class genes control petal, stamen, and staminode identity with little contribution to sepal development, despite the petaloid appearance of the sepals (see Rasmussen et al., 2009, pp. 96–109 in this issue).

The partitioning of gene function among duplicate copies (i.e., subfunctionalization, Lynch and Conery, 2000) allows for possible functional divergence and the evolution of novelty. It may be that the presence of multiple AqvAP3 paralogs, each with its own function, allowed for the derivation of both petaloid sepals and staminodes in Aquilegia. Taking this line of reasoning further, other floral novelties may also be related to gene duplications and partitioning of gene function among duplicates. For example, many key floral regulators have undergone gene duplication at various points in the phylogenetic history of angiosperms (see also paper by D. Soltis et al., 2009, pp. 336–348 in this issue). The AP3 and PI gene lineages are the products of a gene duplication in the common ancestor of the angiosperms, possibly more than 260 mya (Kim et al., 2004); a single homolog to this gene pair is present in extant gymnosperms. Likewise, the SEP genes, which are required for forming the quartets that carry the AP1, AP2, AP3, and PI protein subunits, were duplicated in the common ancestor of the angiosperms (Zahn et al., 2005). The coincidence of these duplicate genes may have actually led to the development of the floral organ identity program responsible for the origin of the flower (Zahn et al., 2005). Additional duplication of the AP3 gene lineage, along with duplications in the AP1, AG, and SEP gene lineages (Kramer et al., 1998, 2004; Litt and Irish, 2003; Kramer and Hall, 2005; Zahn et al., 2005; reviewed in Kramer and Zimmer, 2006; Irish, 2006), near the origin of the core eudicots suggests that these duplications may also be involved in the "new" floral morphology that emerged in the core eudicots: a synorganized flower based on a pentamerous groundplan ( D. Soltis et al., 2003). Duplications within the AP1 lineage (Litt and Irish, 2003) are associated with shifts in expression patterns and possibly function. The paralogs AP1 and FRUITFULL (FUL), of the euAP1 and euFUL gene lineages, respectively, have different functions (reviewed in Kramer and Hall, 2005). Early in flower development, AP1 contributes to floral meristem identity and later helps to specify sepal and petal identity; FUL also contributes to floral meristem identity early in development and to carpel and fruit development later. However, despite similar expression patterns of euAP1 orthologs across the angiosperms, the AP1 function of Arabidopsis thaliana is not conserved (see Kramer and Hall, 2005); this expression pattern is not observed for euFUL orthologs. Meanwhile, the sister lineage to the euAP1 and euFUL lineage, the FUL-like clade, occurs in basal angiosperms and has different expression patterns and therefore likely different functions from AP1, FUL, and their orthologs. Expression levels of the FUL-like genes in the basal angiosperms Nuphar and Magnolia were greater in leaves and carpels than in perianth or stamens—more like those of euFUL orthologs than euAP1 orthologs, perhaps indicating the ancestral expression pattern of the AP1 lineage (Kim et al., 2005; Yoo et al., unpublished data). However, expression was high in leaves and all floral organs in Cabomba (Yoo et al., unpublished data). An AP1 homolog has not been detected in Amborella (Kim et al., 2005). Finally, duplications in the CYC gene lineage throughout the core eudicots may also be related to changes in floral morphology (Howarth and Donoghue, 2006). Whether these duplications in many floral gene lineages arose via independent duplication events or through polyploidy remains unknown; regardless, however, they supply a rich source of genetic material that may generate floral novelty. Such genes deserve greater attention in comparative studies.

Although the functions of ABC homologs in basal angiosperms have not yet been demonstrated, their expression patterns may serve as proxies for initial inferences of functional divergence of duplicate gene pairs. Duplications of ABC genes have occurred on more local phylogenetic levels (e.g., within a species or genus), and while some duplicates have similar or identical expression patterns (e.g., EScaAG1 and EScaAG2 in Eschscholzia californica Cham., Zahn et al., 2006b; Nyod.AG1–1 and -2 in Nymphaea odorata Aiton, Yoo et al., unpublished data), several duplicate genes have divergent expression patterns and therefore possibly divergent functions ( Table 1). For example, whereas duplicate AP3 homologs in Nuphar advena (Aiton) W. T. Aiton have identical expression patterns across floral organs late in floral development, when analyzed with RT-PCR, early in development Nu.ad.AP3.2 is clearly expressed in inner tepals, and Nu.ad.AP3.1 is not (as detected by in situ hybridization; Kim et al., 2005). Putative alternatively spliced AP3-homolog variants in Nymphaea odorata (class I and class VI) differ dramatically in their expression patterns, with Nyod.AP3 class I expressed at moderate to high levels in leaves, sepals, petals, inner stamens, and carpels, while Nyod.AP3 class VI expression is restricted to inner stamens and carpels (Yoo et al., unpublished data). Likewise, differences in expression occur among AGL2-homolog duplicates and AGL6-homolog duplicates in Cabomba caroliniana A. Gray (Yoo et al., unpublished data). In Illicium floridanum J. Ellis, the expression of AP3 homologs varies, with Il.fl.AP3.2 expressed in outer tepals, inner tepals, and stamens, Il.fl.AP3.1 expression limited to inner tepals and stamens, and Il.fl.AP3.3 expression restricted to inner tepals (Kim et al., 2005). It is tempting to speculate that differences in expression patterns of duplicate AP3 homologs in these basal angiosperms may contribute to morphological variation in sepaloidy vs. petaloidy in perianth organs and stamens; however, functional studies have not yet been conducted.

As with the major duplications of ABC genes described, it is unclear whether the duplications found within the basal angiosperms arose via polyploidy, tandem duplications, or some other mechanism. However, given that many basal angiosperms are ancient polyploids (e.g., Stebbins, 1950; Soltis and Soltis, 1990; Cui et al., 2006; see D. Soltis et al., 2009, pp. 336–348 in this issue), many of these duplicate pairs may have arisen via polyploidy.

PROSPECTUS

Floral variation, particularly in basal angiosperms, is extensive, and its genetic control is only beginning to be understood. Knowledge of the genes controlling floral development and most floral morphology is still in its infancy but is expanding rapidly. With the addition of new models, generalities can be tested, resulting in the eventual identification of candidates to explain morphological differences. For some hypotheses, such as the fading borders model, predictions from morphology and development have been upheld by genetics. For others, such as the homology of the perianth of grass flowers, conservation of gene expression patterns does not maintain a stable morphology. The decoupling of morphology and genetics may be real, or it may reflect errors in homology assessment at the morphological, developmental, and/or genetic level. Opportunities to study this decoupling may arise through identification of morphological convergence.

Convergence in morphological features is evident in several of the characters described by Bessey (1915) as important transformations from ancestral to derived states. In fact, Bessey’s dicta often correspond to patterns of character-state change identified through explicit reconstruction of character evolution, at least as "trends" if not as absolutes. Whereas Bessey’s dicta may suggest a simple transition from ancestral to derived state, the features identified by Bessey have often undergone convergent evolution, with multiple derivations of the "same" characteristic. Comparison of the genetics of these states would indicate whether there are multiple ways of arriving at the same point.

Synorganization is a major theme in discussions of floral evolution, yet it has not been addressed from an evo-devo perspective. A complex set of morphological features is involved in any synorganization—it typically involves more than one organ type, and it may involve the number of organs, floral symmetry, etc., of a flower. Future studies should look to characterize the morphological and developmental features in such a way as to identify key elements of a given synorganization—and then take an evo-devo approach to understanding those elements. Ultimately, an evo-devo perspective on synorganization should help to explain both the evolution of specific floral organs as well as the collective, integrated organ systems that arise via synorganization, one of the major trends/processes in the evolution of floral variation.

FOOTNOTES

¹ This work was supported in part by NSF Plant Genome Grants PGR-0115684 and PGR-0638595. The authors thank three anonymous reviewers for helpful comments on a previous draft of this paper.

⁵ Author for correspondence (e-mail: psoltis{at}flmnh.ufl.edu)

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