Functional analyses of genetic pathways controlling petal specification in poppy

Department of Ecology and Evolutionary Biology, Yale University, New Haven, Connecticut, United States
Development (Impact Factor: 6.46). 01/2008; 134(23):4157-66. DOI: 10.1242/dev.013136
Source: PubMed


MADS-box genes are crucial regulators of floral development, yet how their functions have evolved to control different aspects of floral patterning is unclear. To understand the extent to which MADS-box gene functions are conserved or have diversified in different angiosperm lineages, we have exploited the capability for functional analyses in a new model system, Papaver somniferum (opium poppy). P. somniferum is a member of the order Ranunculales, and so represents a clade that is evolutionarily distant from those containing traditional model systems such as Arabidopsis, Petunia, maize or rice. We have identified and characterized the roles of several candidate MADS-box genes in petal specification in poppy. In Arabidopsis, the APETALA3 (AP3) MADS-box gene is required for both petal and stamen identity specification. By contrast, we show that the AP3 lineage has undergone gene duplication and subfunctionalization in poppy, with one gene copy required for petal development and the other responsible for stamen development. These differences in gene function are due to differences both in expression patterns and co-factor interactions. Furthermore, the genetic hierarchy controlling petal development in poppy has diverged as compared with that of Arabidopsis. As these are the first functional analyses of AP3 genes in this evolutionarily divergent clade, our results provide new information on the similarities and differences in petal developmental programs across angiosperms. Based on these observations, we discuss a model for how the petal developmental program has evolved.

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    • "For instance, AP3 gene duplications in core eudicots, resulting in the AP3 and TM6 gene clades, have led to sub-functionalization with AP3 paralogs contributing to the perianth, and TM6 paralogs functioning in stamen identity (Jack et al., 1994; Liu et al., 2004; Vandenbussche et al., 2004; deMartino et al., 2006; Rijpkema et al., 2006). Independent gene duplication in Ranunculales, have also led to sub-functionalization of AP3-III homologs exclusively providing petal identity, and their paralogs AP3-I and AP3-II controlling stamen identity (Drea et al., 2007; Kramer et al., 2007; Sharma et al., 2011; Sharma and Kramer, 2012; Zhang et al., 2013). Gene expression patterns and functional analyses of AP3 homologs have also been used in an attempt to assess homology of atypical floral structures occurring in the second whorl, which are likely modified petals. "
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    ABSTRACT: Aristolochia fimbriata (Aristolochiaceae: Piperales) exhibits highly synorganized flowers with a single convoluted structure forming a petaloid perianth that surrounds the gynostemium, putatively formed by the congenital fusion between stamens and the upper portion of the carpels. Here we present the flower development and morphology of A. fimbriata, together with the expression of the key regulatory genes that participate in flower development, particularly those likely controlling perianth identity. A. fimbriata is a member of the magnoliids, and thus gene expression detected for all ABCE MADS-box genes in this taxon, can also help to elucidate patterns of gene expression prior the independent duplications of these genes in eudicots and monocots. Using both floral development and anatomy in combination with the isolation of MADS-box gene homologs, gene phylogenetic analyses and expression studies (both by reverse transcription PCR and in situ hybridization), we present hypotheses on floral organ identity genes involved in the formation of this bizarre flower. We found that most MADS-box genes were expressed in vegetative and reproductive tissues with the exception of AfimSEP2, AfimAGL6, and AfimSTK transcripts that are only found in flowers and capsules but are not detected in leaves. Two genes show ubiquitous expression; AfimFUL that is found in all floral organs at all developmental stages as well as in leaves and capsules, and AfimAG that has low expression in leaves and is found in all floral organs at all stages with a considerable reduction of expression in the limb of anthetic flowers. Our results indicate that expression of AfimFUL is indicative of pleiotropic roles and not of a perianth identity specific function. On the other hand, expression of B-class genes, AfimAP3 and AfimPI, suggests their conserved role in stamen identity and corroborates that the perianth is sepal and not petal-derived. Our data also postulates an AGL6 ortholog as a candidate gene for sepal identity in the Aristolochiaceae and provides testable hypothesis for a modified ABCE model in synorganized magnoliid flowers.
    Full-text · Article · Dec 2015 · Frontiers in Plant Science
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    • "Agrobacterium growth and plant infiltration methods followed Hileman et al. (2005) and Drea et al. (2007). Batches of 25 plants at the 4–6 leaf stage were infiltrated in half their leaves with a 1:1 ratio of TRV1:TRV2 using a needleless syringe, with at least three experimental replicates for each construct conducted at different times of the year. "
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    ABSTRACT: Main conclusion: Duplicated petunia clade-VI SPL genes differentially promote the timing of inflorescence and flower development, and leaf initiation rate. The timing of plant reproduction relative to favorable environmental conditions is a critical component of plant fitness, and is often associated with variation in plant architecture and habit. Recent studies have shown that overexpression of the microRNA miR156 in distantly related annual species results in plants with perennial characteristics, including late flowering, weak apical dominance, and abundant leaf production. These phenotypes are largely mediated through the negative regulation of a subset of genes belonging to the SQUAMOSA PROMOTER BINDING PROTEIN-LIKE (SPL) family of transcription factors. In order to determine how and to what extent paralogous SPL genes have partitioned their roles in plant growth and development, we functionally characterized petunia clade-VI SPL genes under different environmental conditions. Our results demonstrate that PhSBP1and PhSBP2 differentially promote discrete stages of the reproductive transition, and that PhSBP1, and possibly PhCNR, accelerates leaf initiation rate. In contrast to the closest homologs in annual Arabidopsis thaliana and Mimulus guttatus, PhSBP1 and PhSBP2 transcription is not mediated by the gibberellic acid pathway, but is positively correlated with photoperiod and developmental age. The developmental functions of clade-VI SPL genes have, thus, evolved following both gene duplication and speciation within the core eudicots, likely through differential regulation and incomplete sub-functionalization.
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    • "The long established association between B-class gene expression and 2 nd whorl organ identity, although conserved in many angiosperm lineages such as Solanaceae (Liu et al., 2004; de Martino et al., 2006; Rijpkema et al., 2006), and Papaveraceae (Drea et al., 2007), or in lodicule specification in grasses (Ambrose et al., 2000; Prasad and Vijayraghavan, 2003; Whipple et al., 2004), does not hold true for other lineages, even within the core eudicots (Brockington et al., 2012). It has recently been shown that neither sepal-derived nor stamen-derived petaloid organs of the " living stones " (Caryophyllales) exhibit gene expression patterns consistent with the core eudicot petal identity program, providing evidence for petal development that is independent of B-class gene expression, and suggesting that different genetic control of 2 nd whorl identity has evolved within the Aizoaceae. "
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    ABSTRACT: The development of petal-like organs has occurred repetitively throughout angiosperm evolution. Despite homoplasy, it is possible that common underlying molecular mechanisms are repeatedly recruited to drive the development of petaloid organs. In Zingiberales, infertile, petal-like structures replace fertile stamens, resulting in petaloidy in androecial whorls. Assuming that androecial petaloidy is a shared derived characteristic, we expect to find common ultrastructure and molecular mechanisms underlying androecial petaloidy across Zingiberales. We show that petaloidy in Zingiberales is associated with tightly packed, protruding epidermal cells. Expression patterns for candidate genes involved in petal identity differ between the petaloid organs of Costaceae v. Cannaceae, despite similar macro- and microscopic organization. For all candidate gene families analyzed, our data suggest at least one Zingiberales-specific duplication event. Our data suggest that the patterns of B-class gene expression across the Zingiberales do not correlate with the occurrence of petaloidy, indicating that androecial petaloidy might have evolved independently of B-class gene expression in some lineages. It is possible that gene duplication may play a role in the diversity of petaloid structures found throughout the Zingiberales. It is likely that Zingiberales petaloidy may also result from the deployment of genes other than those involved in specification of petal identity. This article is protected by copyright. All rights reserved. © 2015 Wiley Periodicals, Inc.
    No preview · Article · Apr 2015 · Developmental Dynamics
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