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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    • "Additionally, seventeen point mutations were also detected in PapsPI-3 as compared to PapsPI-1, of which, nine were before the stop codon in PapsPI-3. In phylogenetic analysis the PapsPI-1 sequence of this investigation (KF550916) and the one reported earlier (ABO13927) [16] clustered together but the sequence of PapsPI-2 reported earlier (nucleotide EF071995, amino acid ABO13928) [16] was different from that of PapsPI-3 reported in this investigation (KF550917; Figure 4). "
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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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    • "A detailed analysis of these possibilities would require downregulation or knockout of DEFand GLO-like genes in species in which DEF-or GLO-like proteins homodimerize. Respective data are only available from very few species, including O. sativa (Nagasawa et al., 2003; Ronai et al., 2003; Yao et al., 2008), Aquilegia vulgaris (Kramer et al., 2007) and P. somniferum (Drea et al., 2007). In these cases, downregulation of the complete set of DEF-like genes resulted in homeotic transformations that very much resembled or were identical to those obtained when the concomitant GLO-like genes were downregulated. "
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    ABSTRACT: Background and Aims DEFICIENS (DEF)- and GLOBOSA (GLO)-like proteins constitute two sister clades of floral homeotic transcription factors that were already present in the most recent common ancestor (MRCA) of extant angiosperms. Together they specify the identity of petals and stamens in flowering plants. In core eudicots, DEF- and GLO-like proteins are functional in the cell only as heterodimers with each other. There is evidence that this obligate heterodimerization contributed to the canalization of the flower structure of core eudicots during evolution. It remains unknown as to whether this strict heterodimerization is an ancient feature that can be traced back to the MRCA of extant flowering plants or if it evolved later during the evolution of the crown group angiosperms.
    Annals of Botany 06/2014; 114(7). DOI:10.1093/aob/mcu094 · 3.65 Impact Factor
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    • "A 194 bp fragment of the petal pigment gene CHALCONE SYNTHASE (CHS) was also amplified, cloned, and ligated into TRV2 for use as an experimental control as previously described [21]. Bacterial growth and plant infiltration methods followed Drea et al. (2007) and Hileman et al. (2005) [22], [23]. Twenty plants at the four-leaf pair stage for each silencing target were infiltrated in half their leaves with a 1∶1 ratio of TRV1 and TRV2 using a needleless syringe for a total of 60 plants (CHS-, FBP21-, and FBP28-TRV2). "
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    ABSTRACT: Flowering time is strictly controlled by a combination of internal and external signals that match seed set with favorable environmental conditions. In the model plant species Arabidopsis thaliana (Brassicaceae), many of the genes underlying development and evolution of flowering have been discovered. However, much remains unknown about how conserved the flowering gene networks are in plants with different growth habits, gene duplication histories, and distributions. Here we functionally characterize three homologs of the flowering gene SUPPRESSOR OF OVEREXPRESSION OF CONSTANS 1 (SOC1) in the short-lived perennial Petunia hybrida (petunia, Solanaceae). Similar to A. thaliana soc1 mutants, co-silencing of duplicated petunia SOC1-like genes results in late flowering. This phenotype is most severe when all three SOC1-like genes are silenced. Furthermore, expression levels of the SOC1-like genes UNSHAVEN (UNS) and FLORAL BINDING PROTEIN 21 (FBP21), but not FBP28, are positively correlated with developmental age. In contrast to A. thaliana, petunia SOC1-like gene expression did not increase with longer photoperiods, and FBP28 transcripts were actually more abundant under short days. Despite evidence of functional redundancy, differential spatio-temporal expression data suggest that SOC1-like genes might fine-tune petunia flowering in response to photoperiod and developmental stage. This likely resulted from modification of SOC1-like gene regulatory elements following recent duplication, and is a possible mechanism to ensure flowering under both inductive and non-inductive photoperiods.
    PLoS ONE 05/2014; 9(5):e96108. DOI:10.1371/journal.pone.0096108 · 3.23 Impact Factor
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