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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    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.
    Planta 10/2015; DOI:10.1007/s00425-015-2413-2 · 3.26 Impact Factor
    • "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.
    Developmental Dynamics 04/2015; 244(9). DOI:10.1002/dvdy.24280 · 2.38 Impact Factor
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    • "This is expected as AP3 and PI gene products are believed to form a heterodimer that acts in vivo as part of a larger MADS box protein complex, specifying petal as well as stamen identity [8], [9], [11], [30], [31], [32]. In opium poppy, PapsAP3-1 was able to heterodimerize with PapsPI-1 like in Arabidopsis and Antirrhinum [7], [16], [33]. Although PapsPI-1 is required to specify petal as well as stamen identity, PapsAP3-1 functions primarily in the specification of petals and PapsAP3-2 functions primarily in the specification of stamens [16]. "
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    ABSTRACT: The involvement of PISTILLATA (PI) and APETALA (AP) transcription factors in the development of floral organs has previously been elucidated but little is known about their upstream regulation. In this investigation, two novel mutants generated in Papaver somniferum were analyzed - one with partially petaloid sepals and another having sepaloid petals. Progeny from reciprocal crosses of respective mutant parent genotypes showed a good fit to the monogenic Mendelian inheritance model, indicating that the mutant traits are likely controlled by the single, recessive nuclear genes named "Pps-1" and "OM" in the partially petaloid sepal and sepaloid petal phenotypes, respectively. Both paralogs of PISTILLATA (PapsPI-1 and PapsPI-3) were obtained from the sepals and petals of P. somniferum. Ectopic expression of PapsPI-1 in tobacco resulted in a partially petaloid sepal phenotype at a low frequency. Upregulation of PapsPI-1 and PapsAP3-1 in the petal and the petal part of partially petaloid sepal mutant and down-regulation of the same in sepaloid petal mutant indicates a differential pattern of regulation for flowering-related genes in various whorls. Similarly, it was found that the recessive mutation OM in sepaloid petal mutant downregulates PapsPI-1 and PapsAP3-1 transcripts. The recessive nature of the mutations was confirmed by the segregation ratios obtained in this analysis.
    PLoS ONE 06/2014; 9(6):e101272. DOI:10.1371/journal.pone.0101272 · 3.23 Impact Factor
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