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Developmental Biology and Developmental Genetics |
Department of Botany, University of Wisconsin, 430 Lincoln Drive, Madison, Wisconsin 53706 USA
Received for publication 19 June 2007. Accepted for publication 24 January 2008.
ABSTRACT
Whereas most Brassicaceae produce flowers on an elongated inflorescence, a few lineages produce flowers directly from the vegetative rosette on elongated pedicels. Knowing the extent to which independent origins of rosette flowering involve the same developmental and genetic mechanisms could clarify the constraints acting on plant architectural evolution. Prior work in Idahoa, Ionopsidium, and Leavenworthia suggested that changes in the activity or expression of the flower meristem identity gene, LEAFY (LFY), played a role in all three origins of rosette flowering. Here we studied the developmental morphology of L. crassa and immunolocalization of LFY protein in Leavenworthia and Ionopsidium to further compare independent origins of rosette flowering. Leavenworthia crassa differs from Ionopsidium and Idahoa in producing ebracteate flowers. Flowers are, however, associated with "squamules," here interpreted as stipules of a cryptic bract. LFY was detected in L. crassa flower primordia but not in inflorescence meristems. In contrast, the rosette flowering Io. acaule accumulated LFY protein in the inflorescence meristem, whereas its inflorescence-flowering close relative, Io. prolongoi, did not. Thus, although different cases of rosette flowering likely entailed modifications of the same meristem identity program, distinct developmental genetic mechanisms appear to be involved in each case.
Key Words: Arabidopsis • Brassicaceae • cryptic bract • evolutionary developmental genetics (evo-devo) • inflorescence • Ionopsidium • LEAFY/FLORICAULA • Leavenworthia
The independent evolution of the same or very similar morphological traits (homoplasy) is a pervasive pattern in land plant evolution. What is less clear is how often homoplasy results from the repeated deployment of the same genetic and developmental mechanisms (parallelism) and how often the similarity is merely superficial (convergence). Establishing the relative frequency of parallelism and convergence is important because it would help us better understand the extent of developmental constraints on evolution. For example, in a number of evolutionary developmental studies of morphological homoplasy, the same genes are repeatedly involved (Bharathan et al., 2002
; Colosimo et al., 2005; Sucena et al., 2005; Prud'homme et al., 2006), implying that morphological evolution may be subject to considerable developmental constraint such that evolution is limited to a few "lines of least resistance." However, while there is evidence that the same genetic players may be involved repeatedly, studies in plants have yet to document the degree of similarity in the genetic changes that have caused homoplastic evolution. It remains plausible that relatively few genes are targets of morphological evolution, but that these genes can be modulated in a diversity of different ways to achieve the same phenotypic outcomes (see Wittkopp et al., 2003). Further studies of homoplasy in plants are needed, especially in tractable systems with the potential to identify the genetic basis of multiple instances of the "same" trait.
Brassicaceae, currently circumscribed to include 338 genera and over 3700 species (Warwick et al., 2006), is a clade that manifests extensive homoplasy as indicated, for example, by the historical failure of morphological systematics to identify natural groups. Furthermore, because Brassicaceae includes the premier plant genetic model system, Arabidopsis thaliana, it provides the ideal venue for studying the developmental genetic basis of parallel evolution.
A great majority of species in Brassicaceae, including such well-known exemplars as Arabidopsis and Brassica, possess the ancestral plant architecture, inflorescence flowering. Plants begin in a vegetative phase, producing leaves from the shoot apical meristem (SAM) with little stem elongation. These leaves generally form a rosette close to the ground. When induced by environmental stimuli, the plant switches to a reproductive phase, whereupon the SAM begins to produce flowers (Hempel and Feldman, 1994). In parallel with flower production, the internodes in the stem rapidly elongate (bolt), and in most cases, the leaves that would otherwise subtend flowers (i.e., bracts) are suppressed. The resulting elongated portion of the stem bearing flowers is defined as an inflorescence (see Weberling, 1989 for more details). Axillary meristems recapitulate this same developmental progression and produce secondary inflorescences (paraclades).
Despite the preponderance of inflorescence flowering in Brassicaceae, some derived forms of flowering architecture have evolved. Rosette flowering (also called solitary flowering), the focus of this study, is distinguished by a lack of internode elongation along the main stem once flowering has commenced, coupled with flowers emerging on long pedicels from the rosette (Shu et al., 2000; Yoon and Baum, 2004). Rosette flowering has arisen independently in multiple lineages and is reported from at least one species in 29 different Brassicaceae genera (Appel and Al-Shehbaz, 2003).
Developmental genetic studies of rosette flowering have focused on exemplar species of Ionopsidium (Io. acaule), Idahoa (Id. scapigera), and Leavenworthia (L. crassa) (Shu et al., 2000; Yoon and Baum, 2004; Sliwinski et al., 2006, 2007). Ionopsidium, which includes two rosette-flowering and four inflorescence-flowering species, is thought to be closely related to Cochlearia (Koch, 2001), Leavenworthia is a member of the cardaminoid "clade E" of Beilstein et al. (2006), whereas the monotypic Idahoa is of uncertain phylogenetic affinities (Beilstein et al. 2006).
Architectural evolution in plants has been hypothesized to often involve changes in the regulation and/or function of meristem identity genes (Bradley et al., 1997; Prusinkiewicz et al., 2007). One important meristem identity gene is LEAFY/FLORICAULA (LFY), which promotes flower identity in diverse species (Coen et al., 1990; Weigel et al., 1992; Weigel and Nilsson, 1995). The conventional wisdom is that LFY is excluded from indeterminate shoot meristems, such as the inflorescence meristem (IM), but must be expressed in flower primordia for them to develop properly. Loss of LFY function disrupts flower development (Coen et al., 1990; Weigel et al., 1992), whereas ectopic expression of LFY in the IM is capable of converting it to a terminal flower (e.g., Weigel and Nilsson, 1995). LFY expression in some rosette-flowering species has been characterized directly by detecting mRNA or the LFY protein or indirectly by analyzing promoter:reporter fusions in an Arabidopsis thaliana genetic background (Shu et al., 2000; Yoon and Baum, 2004; Sliwinski et al., 2006, Sliwinski et al., 2007). However, to build a general picture of the evolution of rosette flowering, a number of outstanding questions need to be answered.
The first aim of this study was to examine the morphology of Leavenworthia crassa to assess whether rosette flowering in this species has a similar developmental basis to that reported previously for Ionopsidium acaule (Shu et al., 2000) and Idahoa scapigera (Sliwinski et al., 2007). Specifically, the hypothesis that rosette flowers in L. crassa are derived from axillary paraclades that have undergone homeotic conversion to flowers (Yoon and Baum, 2004) can be informed by determining whether flowers in this species are associated with a subtending leaf, as is typical for paraclades.
The promoters of the LcrLFY gene from L. crassa and the IscLFY2 gene from Idahoa scapigera drive expression in the IM in an A. thaliana background, and the introduction of the full-length genes into A. thaliana converts the IM into a terminal flower (Yoon and Baum, 2004; Sliwinski et al., 2007). Are these genes also expressed in the IM of their source species In the case of Id. scapigera, LFY protein levels in the IM are low compared to developing flowers, suggesting that a transacting mechanism limits LFY accumulation in the IM (Sliwinski et al., 2007). Whether the LcrLFY protein is likewise excluded from the IM of L. crassa was explored by immunolocalization of the LcrLFY protein in developing L. crassa plants.
Ionopsidium acaule expresses mRNA of its single known LFY homolog, IacLFY, not only in flower primordia, but also in the IM (Shu et al., 2000). Nonetheless, this species does not produce terminal flowers, as might be predicted based on studies in other species (e.g., Weigel and Nilsson, 1995). The lack of terminal flowers could reflect regulation at the translational level, which predicts that the IM would lack expression of the IacLFY protein. Alternatively, if LFY protein expression in the IM is causally related to the production of a rosette flowering architecture, for example, by playing a role in stem internode suppression (Sliwinski et al., 2007), then one might expect that an inflorescence flowering species of Ionopsidium such as Io. prolongoi would lack LFY protein expression in the IM. We tested these predictions using immunolocalization of LFY in Io. acaule and Io. prolongoi.
Our developmental data show that L. crassa differs from other studied rosette species in that the leaves that subtend flowers are suppressed. However, we detected small, paired structures, "squamules," associated with each pedicel and interpret these as the stipules of cryptic bracts. Using immunolocalization, we detected IacLFY in the IM of the rosette flowering Io. acaule but not in its close inflorescence flowering relative Io. prolongoi. In the case of L. crassa we found that, like Id. scapigera, LFY protein is excluded from the inflorescence meristem. LFY expression also provides evidence for the presence of a cryptic bract in L. crassa. Taken together, our data suggest that the LFY gene played a role in each origin of rosette flowering, but that the detailed genetic and developmental mechanisms involved were distinct in each case.
MATERIALS AND METHODS
Plant material
Wild-type and lfy-6 A. thaliana (Ler ecotype) seeds were obtained from the Arabidopsis Biological Resource Center (Ohio State University, Columbus, Ohio, USA). Leavenworthia crassa seeds were obtained from a cultivated source (Baum 379, Wisconsin State Herbarium, Madison, USA). Both species were grown under the same growth conditions as Sliwinski et al. (2006), 22–25°C in long days (16 h light/8 h dark) under fluorescent lights (
90–120 µ E•m–2•s–1). To increase L. crassa germination rates, seeds were soaked in GA3 (350 ppm) for 1 h, planted in soil, and stratified for 2 weeks at 4°C.
Ionopsidium acaule was grown from seeds retained from the plants studied by Shu et al. (2000). Ionpsidium prolongoi plants were derived from seed obtained from the Crucifer Germplasm Collection (c/o C. Gómez-Pampo, Biología Vegetal, Universidad Politécnica, 28040 Madrid, Spain; accession number: 428-2234-73).
Immunolocalization
Fresh plant tissue was dissected and fixed in 4% paraformaldehyde under vacuum for 4 h. Tissue was dehydrated in an ethanol series, moved to Hemo-De (Fisher, Hampton, New Hampshire, USA), and embedded in paraffin (Paraplast Plus, Fisher). Embedded tissue was sectioned longitudinally with a microtome (RM2145, Leica Microsystems, Wetzlar, Germany). Sections were cut at 8 µm and affixed to Probe-On Plus slides (Fisher). Slides were deparaffinized in Hemo-De, rehydrated in an ethanol series, and treated in coplin jars as follows: 10 min in 20 µg/mL proteinase K at 37°C (diluted in 100 mM Tris/50 mM EDTA pH 8.0), 2 x 5 min in phosphate-buffered saline, 30 min in BTX (100 mM Tris-HCl pH 7.5, 400 mM NaCl, 1% BSA w/v, 0.3% Triton X-100 v/v). Slides were moved into a humid box at room temperature and treated as follows: 3 h blocking solution (10% goat serum v/v in BTX; Sigma, St. Louis, Missouri, USA), 90 min 1:300 dilution of LFY antibody (Sessions et al., 2000), 3 x 15 min BTX in coplin jars, 60 min 1:1500 dilution of goat antirabbit alkaline phosphatase-conjugated secondary antibody (Promega, Madison, Wisconsin, USA), 3 x 15 min BTX, 20 min in detection buffer (100 mM Tris-HCl pH 9.5, 100 mM NaCl, 50 mM MgCl2). Nitroblue tetrazolium (NBT)/bromochloroindolyl phosphate (BCIP) stock solution (Roche, Indianapolis, Indiana, USA) was diluted in the detection buffer for final concentrations of 0.15 mg NBT/mL, 0.075 mg BCIP/mL, then added to slides in a foil-wrapped coplin jar. Staining times varied between 45 min and 2.5 h. The staining reaction was stopped in 10 mM Tris-Cl, 1 mM EDTA, pH 8.0, dehydrated in an ethanol series, incubated in Hemo-De, and mounted with Permount and glass coverslips. Sections were imaged using an Olympus (Allentown, Pennsylvania, USA) BX60 optical microscope and Olympus DP70 digital camera. Images were cropped, reoriented, and contrast was adjusted using Photoshop 7 (Adobe Systems, San Jose, California, USA). Immunolocalization experiments were replicated three times for A. thaliana and L crassa and two times for Ionopsidium.
Scanning electron microscopy
Inflorescences of different developmental stages were collected from living plants and immediately fixed in FAA (5% formalin, 5% acetic acid, 47.5% ethanol). Fixed materials were dehydrated to 70% ethanol and dissected under a stereomicroscope. Then, they were further dehydrated to 100% by a gradient series of ethanol concentrations. After dehydration, materials were critical-point dried, sputter-coated with gold, and photographed with a Quanta 200 scanning electron microscope (SEM) at 15 kV (FEI Co., Hillsboro, Oregon, USA). Approximately eight individuals of L. crassa were examined to confirm the consistency of the developmental patterns.
RESULTS
Plant development and morphology of L. crassa
Leavenworthia crassa grows in cedar glades on limestone in the southeastern United States. It is a winter annual species, with individuals overwintering as a rosette and producing flowers the following spring (Rollins, 1963). For the experiments in this paper, L. crassa plants were grown under controlled environmental conditions (see Materials and Methods), omitting the natural overwintering cycle. Plants appeared to develop and flower normally, resembling plants observed in the field and in herbarium collections, consistent with evidence that Leavenworthia can flower before winter if mild temperatures persist late in autumn (Baskin and Baskin, 1971). In healthy plants, flowers were first visible 40–80 d after germination, at which time 40 leaves were visible in the rosette (not all on the main axis). The flowering time of plants growing in suboptimal conditions (e.g., insect damage, plant crowding, water stress) was delayed by several weeks, but leaf number was similar to that of healthy plants.
Sectioning and SEM allowed more accurate measurement of reproductive timing: individuals with 10 expanded rosette leaves were always still vegetative, individuals with 20 expanded leaves had recently begun producing flower primordia from the primary meristem, and individuals with 30–40 expanded leaves had produced many (15) young, unopened flowers. Figure 1C illustrates a typical plant at the last stage: the basalmost 17 nodes bear leaves, the next six nodes bear leaves with paraclades in their axils, and all subsequent nodes (40 in the dissected plant) bear flowers without associated leaves. Each paraclade develops 5–6 leaves before producing flowers (also without subtending bracts). Thus, L. crassa has an architecture that is similar to A. thaliana except for the lack of internode elongation in L. crassa.
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. Like A. thaliana, flowers were ebracteate. However, unlike A. thaliana, each pedicel was adorned with two lateral-adaxial stipule-like protrusions (Fig. 2A, C, D). These structures occur in several Brassicaceae (Arber, 1931) and are usually called "squamules," a term we adopt here.
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LcrLFY expression in L. crassa
Polyclonal LFY antibody serum (Levin and Meyerowitz, 1995; Sessions et al., 2000) was used to study production of the LcrLFY protein in the developing primary meristem of L. crassa as compared to that of LFY in A. thaliana. Antibody staining of LFY in A. thaliana shoot apices was strongest in the flower primordia and absent in the IM (Fig. 3A; Levin and Meyerowitz, 1995; Sessions et al., 2000). Antibody staining in L. crassa sections had strongest LcrLFY staining in developing first and second stage flower primordia, and little to no staining in the IM (Fig. 3B). Slightly elevated levels of staining in the IM were observed in some sections, but only when there was also nonspecific staining throughout the tissue section. In such cases, the amount of staining per cell appeared similar in the IM and in other presumably nonexpressing tissues, but the staining was much stronger in flower primordia.
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). LcrLFY staining was very low in the primary meristem before flower production and in early stage leaves (Fig. 3C). However, LcrLFY staining was stronger on the adaxial side of older leaves, especially at sites that appear to correspond to developing lobes (Fig. 3D). LFY was detected throughout early stage flower primordia except for the putative cryptic bract (stages 1 and 2, Fig. 3B). By stage 3, the protein had diminished in the pedicel and the outer parts of the sepals (Fig. 3E), such that by stage 4, LcrLFY was concentrated in the inner (adaxial) half of the sepals and in the androecium and gynoecium (Fig. 3E, F). In stage 6 flowers, LcrLFY was present in developing stamens, gynoecium, and petals, but its staining was reduced in sepals (Fig. 3G). At stage 8, LcrLFY was detected in anther locules and the central region of the gynoecium (Fig. 3H).
Expression of LFY gene in Ionopsidium
Immunolocalization showed staining of protein, inferred to be IacLFY, in the inflorescence meristem of I. acaule (Fig. 4A), in a pattern almost identical to the mRNA in situ hybridization results reported by Shu et al. (2000). In contrast, the pattern observed in the inflorescence flowering species I. prolongoi (Fig. 4B) resembles A. thaliana, rather than I. acaule, in that the IM is largely free of protein cross-reacting with the anti-LFY antibody.
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Architecture of Leavenworthia crassa
Previous descriptions of rosette flowering (e.g., Shu et al., 2000; Yoon and Baum, 2004) have emphasized two main features that distinguish this habit from inflorescence flowering: flowers are elevated by elongation of the pedicels rather than elongation of the primary shoot axis, and flowers are produced in the axils of expanded leaves. Our observations of L. crassa show that while it does produce flowers with elongated pedicels from a compact rosette, it differs from Idahoa (Sliwinski et al., 2007) and Ionopsidium (Shu et al., 2000) in that flower-associated leaves (bracts) are largely suppressed.
Given the predominance of inflorescence flowering in Brassicaceae, including close relatives of Leavenworthia such as Cardamine, one might assume that the Leavenworthia lineage evolved rosette flowering from inflorescence flowering by suppression of internode elongation along the main axis. However, the fact that Selenia, the sister group to Leavenworthia, is inflorescence flowering yet produces mainly bracteate flowers (unpublished data), complicates the evolutionary scenario. One could propose either that bract derepression is derived in Selenia or that bracts were suppressed subsequent to the evolution of rosette flowering in Leavenworthia. We favor the latter hypothesis because we consider it relatively likely that the concave structure of the shoot apical meristem, perhaps driven by selection to retain the meristematic tissue close to the ground during the winter, would lead to suppression of bracts because of physical crowding. Under this model, the retention of squamules, the bracts' stipules, can be seen either as an incomplete suppression of the bract or as retention of these structures for some as yet unknown function. Developmental studies of other species of Leavenworthia,Selenia, and close relatives in the cardaminoid clade placed in a phylogenetic framework, could help distinguish these alternatives.
The development of L. crassa can be understood in adaptive terms given the extreme variability in the microenvironment encountered by individual plants in the glade habitat. Plants that establish in small rock crevices or shallow, soil-filled depressions will be faced with a very short growing season in the spring because of the likelihood of drought in the height of summer. In this condition, reproductive assurance may be gained by producing flowers singly, rather than investing in an entire inflorescence before flower maturation. Those plants that establish in deeper soil pockets will initially produce rosette flowers; however, because of the lack of leaf production by the main axis, flowering will come at the cost of photosynthesis. Thus, in larger plants, development shifts to the axillary branches that initially bear leaves. At this point in the season, the plants could have sufficient photosynthate to invest in an inflorescence. Under this model, the production of elongate secondary inflorescences allows for the production of additional seed when conditions are optimal. It will, therefore, be interesting to determine whether L. uniflora, which is sister to the remaining species in the genus (Beck et al., 2006) and differs from other Leavenworthia in the lack of elongated inflorescences (Rollins, 1963), also suppresses bracts on the main axis.
LFY protein and the evolution of rosette flowering in Leavenworthia
Antibody staining in L. crassa shows a similar pattern of LFY protein accumulation to that reported previously for A. thaliana (Weigel et al., 1992; Levin and Meyerowitz, 1995; Sessions et al., 2000; Hepworth et al., 2006): LFY staining is highest in flower primordia and absent or at much lower levels in shoot apical meristems. A similar pattern has been reported for another rosette flowering taxon, Idahoa scapigera (Sliwinski et al., 2007). The LFY gene of L. crassa and one of the two Id. scapigera genes have promoters that drive expression in the shoot apical meristem when placed in an A. thaliana genetic background (Yoon and Baum, 2004; Sliwinski et al., 2007). The fact that these promoters drive expression in the IM of A. thaliana but not in the IM of the source species can be explained by evolutionary divergence in the mechanisms regulating LFY expression. For example, there could be inhibitors of LFY expression that are present in the IM of L. crassa and Id. scapigera but not in the IM of A. thaliana. One plausible candidate for playing a role in downregulating LFY in L. crassa is the homolog of TERMINAL FLOWER1 (TFL1) (Sliwinski et al., 2006).
Yoon and Baum (2004) and Sliwinski et al. (2006) hypothesized that the evolution of rosette flowering in Leavenworthia might have been achieved by homeotic conversion of axillary meristems within the vegetative rosette from an inflorescence to a floral identity. The speculation was that LFY was upregulated in most shoot meristems with the important exception of the primary shoot meristem, which is protected by a suppressor of LFY expression, perhaps TFL1. Our discovery that the rosette flowers of L. crassa are not subtended by expanded leaves tends to undermine this model, favoring instead a model involving suppression of internode elongation in the main axis.
LFY and the evolution of rosette flowering in Ionopsidium
In the case of Io. acaule, the pattern of expression of the LFY homolog is quite distinct from that seen in Idahoa scapigera (Sliwinski et al., 2007) and L. crassa (this study). In Ionopsidium there is strong expression of LFY mRNA (Shu et al., 2000) and LFY protein (this study) in the IM, whereas the other species have reduced expression in the IM. Curiously, whereas the promoters of LFY homologs from Id. scapigera and L. crassa drove expression in the IM in an A. thaliana background and could drive the production of terminal flowers, the IacLFY promoter did not drive expression in the IM in A. thaliana. These expression data implicate trans-regulatory activation of IacLFY expression in the IM of Io. acaule (Yoon and Baum, 2004). The fact that we observed IacLFY expression in the IM of Io. acaule, but that these meristems persist in the indeterminate state and do not form terminal flowers, implies posttranslational mechanisms for suppressing LFY function in the IM (but not in axillary meristems). Candidate mechanisms include protein modification, exclusion of LFY protein from the nucleus (although there is no visual evidence of this in Fig. 4A), or the lack of a necessary coregulator of one or more target genes.
The IM expression of LFY could plausibly explain the origin of rosette flowering within Ionopsidium (Shu et al., 2000). If this hypothesis is correct, then one would predict that the evolution of LFY expression in the IM would coincide with the origin of rosette flowering. Conversely, if expression in the IM were due simply to changes in the regulation of LFY in a broader clade that included Io. acaule, then one should observe expression in the IM of inflorescence-flowering species of Ionopsidium. Our observations of the inflorescence-flowering Io. prolongoi support the former hypotheses: LFY expression is restricted to the flower primordia and is absent from the IM. Thus, there appears to be a correlation between the origin of rosette flowering and the shift toward LFY expression in the IM of Io. acaule. This result implies that changes in IacLFY expression, though not changes at the IacLFY locus, contributed to the evolution of rosette flowering.
Ectopic expression of LFY in A. thaliana can cause the compression of internodes in the inflorescence (Sliwinski et al., 2007). While there is much about this phenomenon that needs further study, we may hypothesize that IaLFY production in the Io. acaule shoot apex causes this species, unlike Io. prolongoi, to suppress elongation of the inflorescence axis. Considering that inflorescence-flowering species of Ionopsidium produce bracteate flowers, suppression of internodes would be sufficient to convert an inflorescence-flowering ancestor into a plant with an architecture like that found in Io. acaule.
Similarities among the three origins of rosette flowering
Data collected in this and other studies (Table 1) implicate the meristem identity pathway, which includes LFY, in the three independent origins of rosette flowering in Idahoa, Ionopsidium, and Leavenworthia. In Idahoa and Leavenworthia, the LFY homologs cause phenotypes in an A. thaliana genetic background that are suggestive of a role in rosette flowering (Yoon and Baum, 2004; Sliwinski et al., 2006, Sliwinski et al., 2007), and in both species the LFY locus shows anomalous patterns of molecular evolution suggestive of directional selection or altered selective constraints on LFY function (Baum et al., 2005). In Ionopsidium the protein and mRNA expression patterns determined for the LFY homolog suggest a possible role in the evolution of rosette flowering.
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). These results contrast with the few previous studies of the genetic basis of morphological homoplasy, which have often found evidence for the repeated cooption of the same genetic mechanisms (e.g., Colosimo et al., 2005; Sucena et al., 2005; Prud'homme et al., 2006). However, as our study shows, it is possible for the same gene to play a role in multiple origins of the "same" trait, but nonetheless for there to be differences in the detailed mechanisms. If this pattern is corroborated by future work, then the relative lack of developmental constraint implied may go some way to explaining the amazing architectural diversity seen in extant angiosperms.
FOOTNOTES
1 The authors would like to thank D. Weigel and J. Lohmann for the generous donation of anti-LFY antibody; E. Spalding, G. Prenner, and the UW-Madison Plant Imaging Center for SEM assistance; M. Otegui and I. Cacho for help with immunolocalization methods; K. Elliot for help with figures; and N. Van Abel and C. Barnes for laboratory assistance. I. Al-Shehbaz provided valued guidance, and two anonymous reviewers and the associate editor gave helpful input. Funding was provided by the National Science Foundation (IOB-0234118) and a UW-Madison Hilldale Undergraduate/Faculty Research Fellowship. 
2 Present address: Department of Biochemistry and Biophysics, University of California–San Francisco, 1550 Fourth St., San Francisco CA 94158-2324 USA
3 Present address: Division of Applied Plant Sciences, Kangwon National University, Chuncheon 200-701, South Korea
4 Present address: Department of Biology, Denison University, 350 Ridge Rd., Granville OH 43023 USA
5 Author for correspondence (e-mail: dbaum{at}wisc.edu)
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  Compiled by, F. Tooke, T. Chiurugwi, and N. Battey Flowering Newsletter bibliography for 2008 J. Exp. Bot., June 23, 2009; (2009) erp154v1. [Full Text] [PDF]
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