Members of the AGAMOUS (AG ) subfamily of MIKC -type MADS-box genes appear to control the development of reproductive organs in both gymnosperms and angiosperms. To understand the evolution of this subfamily in the flowering plants, we have identified 26 new AG -like genes from 15 diverse angiosperm species. Phylogenetic analyses of these genes within a large data set of AG -like sequences show that ancient gene duplications were critical in shaping the evolution of the subfamily. Before the radiation of extant angiosperms, one event produced the ovule-specific D lineage and the well-characterized C lineage, whose members typically promote stamen and carpel identity as well as floral meristem determinacy. Subsequent duplications in the C lineage resulted in independent instances of paralog subfunctionalization and maintained functional redundancy. Most notably, the functional homologs AG from Arabidopsis and PLENA (PLE ) from Antirrhinum are shown to be representatives of separate paralogous lineages rather than simple genetic orthologs. The multiple subfunctionalization events that have occurred in this subfamily highlight the potential for gene duplication to lead to dissociation among genetic modules, thereby allowing an increase in morphological diversity.
FLOWERING LOCUS C (FLC) is a major regulator of flowering responses to seasonal environmental factors. Here, we document that FLC also regulates another major life-history transition-seed germination, and that natural variation at the FLC locus and in FLC expression is associated with natural variation in temperaturedependent germination. FLC-mediated germination acts through additional genes in the flowering pathway (FT, SOC1, and AP1) before involving the abscisic acid catabolic pathway (via CYP707A2) and gibberellins biosynthetic pathway (via GA20ox1) in seeds. Also, FLC regulation of germination is largely maternally controlled, with FLC peaking and FT, SOC1, and AP1 levels declining at late stages of seed maturation. High FLC expression during seed maturation is associated with altered expression of hormonal genes (CYP707A2 and GA20ox1) in germinating seeds, indicating that gene expression before the physiological independence of seeds can influence gene expression well after any physical connection between maternal plants and seeds exists. The major role of FLC in temperature-dependent germination documented here reveals a much broader adaptive significance of natural variation in FLC. Therefore, pleiotropy between these major life stages likely influences patterns of natural selection on this important gene, making FLC a promising case for examining how pleiotropy influences adaptive evolution.life history ͉ pleiotropy ͉ vernalization ͉ natural variation ͉ FRIGIDA
The basal eudicot Aquilegia (columbine) has an unusual floral structure that includes two morphologically distinct whorls of petaloid organs and a clearly differentiated fifth organ type, the staminodium. In this study, we have sought to determine how Aquilegia homologs of the B class genes APETALA3 (AP3) and PISTILLATA (PI) contribute to these novel forms of organ identity. Detailed expression analyses of the three AP3 paralogs and one PI homolog in wild-type and floral homeotic mutant lines reveal complex patterns that suggest that canonical B class function has been elaborated in Aquilegia. Yeast twohybrid studies demonstrate that the protein products of Aquilegia's AP3 and PI homologs can form heterodimers, much like what has been observed for their core eudicot homologs. Downregulation of AqvPI using virus-induced gene silencing indicates that in addition to petal and stamen identity, this locus is essential to staminodial identity but may not control the identity of the petaloid sepals. Our findings show that preexisting floral organ identity programs can be partitioned and modified to produce additional organ types. In addition, they indicate that some types of petaloid organs are not entirely dependent on AP3/PI homologs for their identity.
It has been proposed that the diversification of the MADS-box gene family of transcription factors has played a major role in the radiation of land plants. This suggestion is based on the critical roles that these genes play in plant development and the apparent coincidence of key duplication events with major radiations, such as the establishment of the B and C lineages concurrent with the evolution of the seed plants. On a more recent scale, it is also possible that subsequent duplication events have contributed to later morphological diversifications. In order to investigate this possibility, we are studying the evolution of homologs of the petal and stamen identity genes APETALA3 (AP3) and PISTILLATA (PI) in the Ranunculaceae. In this family, the AP3 and PI lineages have undergone many duplication events at every phylogenetic level. Early duplications gave rise to three paralogous AP3 lineages, which are found throughout the family. In contrast, numerous duplications have occurred relatively recently in the PI lineage. We outline a hypothesis that these duplications have played a role in the evolution of the unique types of petaloid organs in the Ranunculaceae and present preliminary expression data supporting such a scenario.
The evolution of floral zygomorphy is an important innovation in flowering plants and is thought to arise principally from specialization on various insect pollinators. Floral morphology of neotropical Malpighiaceae is distinctive and highly conserved, especially with regard to symmetry, and is thought to be caused by selection by its oil-bee pollinators. We sought to characterize the genetic basis of floral zygomorphy in Malpighiaceae by investigating CYCLOIDEA2-like (CYC2-like) genes, which are required for establishing symmetry in diverse core eudicots. We identified two copies of CYC2-like genes in Malpighiaceae, which resulted from a gene duplication in the common ancestor of the family. A likely role for these loci in the development of floral zygomorphy in Malpighiaceae is demonstrated by the conserved pattern of dorsal gene expression in two distantly related neotropical species, Byrsonima crassifolia and Janusia guaranitica. Further evidence for this function is observed in a Malpighiaceae species that has moved to the paleotropics and experienced coincident shifts in pollinators, floral symmetry, and CYC2-like gene expression. The dorsal expression pattern observed in Malpighiaceae contrasts dramatically with their actinomorphic-flowered relatives, Centroplacaceae (Bhesa paniculata) and Elatinaceae (Bergia texana). In particular, B. texana exhibits a previously undescribed pattern of uniform CYC2 expression, suggesting that CYC2 expression among the actinomorphic ancestors of zygomorphic lineages may be much more complex than previously thought. We consider three evolutionary models that may have given rise to this patterning, including the hypothesis that floral zygomorphy in Malpighiaceae arose earlier than standard morphology-based character reconstructions suggest.ost flowers are either bilaterally symmetrical (i.e., zygomorphic) and have a single plane of symmetry or radially symmetrical (i.e., actinomorphic) and have several planes of symmetry (1). Floral zygomorphy has evolved independently at least 38 times (2-4) and is a hallmark feature of the most diverse angiosperm clades, including Asteraceae (23,600 spp.), Orchidaceae (21,950 spp.), Fabaceae (19,400 spp.), and Lamiales (23,275 spp.) (5). Plant evolutionary biologists therefore propose that the origin of floral zygomorphy may have been a key innovation for promoting speciation throughout the course of angiosperm evolution (6). The driving force behind the origin of floral zygomorphy has long been thought to be a consequence of selection by specialization on certain insect pollinators (1, 7), which has recently gained experimental support (8).The tropical plant family Malpighiaceae exhibits a strong association between floral zygomorphy and insect pollinator attraction. The floral morphology of the more than 1,000 New World species of this clade is very distinctive and highly conserved, especially with regard to symmetry and pollinator reward. The single upright/dorsal banner petal is strongly differentiated from other petals in the corolla...
Molecular genetic studies in Arabidopsis thaliana and other higher-eudicot flowering plants have led to the development of the 'ABC' model of the determination of organ identity in flowers, in which three classes of gene, A, B and C, are thought to work together to determine organ identity. According to this model, the B-class genes APETALA3 (AP3) and PISTILLATA (PI) act to specify petal and stamen identity. Here we test whether the roles of these genes are conserved throughout the angiosperms by analysing the expression of AP3 and PI orthologues in the lower eudicot subclass Ranunculidae. We show that, although expression of these orthologues in the stamens is conserved, the expression patterns in the petals differ from those found in the higher eudicots. The differences between these expression patterns suggest that the function of AP3 and PI homologues as B-class organ-identity genes is not rigidly conserved among all angiosperms. These observations have important implications for understanding the evolution of both angiosperm petals and the genetic mechanisms that control the identities of floral organs.
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