Catching a 'hopeful monster': shepherd's purse (Capsella bursa-pastoris) as a model system to study the evolution of flower development

Hintz, Maren; Bartholmes, Conny; Nutt, Pia; Ziermann, Janine M.; Hameister, Steffen; Neuffer, Barbara; Theißen, Günter

doi:10.1093/jxb/erl158

Cited by 47 publications

(39 citation statements)

References 83 publications

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“…The expressed sequence tags (ESTs) encoding the spliced rps16 genes of the chloroplast genomes of Raphanus raphanistrum (a self-incompatible plant; GenBank accession numbers: EY915189 and EY911083; (Sampson, 1967) and Brassica napus (self-compatible plant; GenBank accession number: EV076332; (Okamoto et al, 2007)) are available in the NCBI EST database. B. napus, Barbarea verna (http: //www.pfaf.org/user /Plant.aspx?LatinName= Barbarea verna), C. bursa-pastoris (Hintz et al, 2006), C. lasiocarpa (Tague, 2001), C. wallichii (Hall et al, 2002), L. virginicum (Lemen, 1980), and N. officinale (Manton, 1935) are selfcompatible, and self-compatible plants tend to lose the rps16 from their chloroplast genomes, whereas selfincompatible plants tend to retain the rps16 in their chlo-roplast genomes (Fig. 2).…”

Section: Discussionmentioning

confidence: 99%

Different status of the gene for ribosomal protein S16 in the chloroplast genome during evolution of the genus Arabidopsis and closely related species

et al. 2010

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The ribosomal protein S16 (RPS16), the product of the rps16, is generally encoded in the chloroplast genomes of flowering plants. However, it has been reported that chloroplast-encoded RPS16 in mono-and dicotyledonous plants has been substituted by the product of nuclear-encoded rps16, which was transferred from the mitochondria to the nucleus before the early divergence of angiosperms. Current databases show that the chloroplast-encoded rps16 has become a pseudogene in four species of the Brassicaceae (Aethionema grandiflorum, Arabis hirsuta, Draba nemorosa, and Lobularia maritima). Further analysis of Arabidopsis thaliana and its close relatives has shown that pseudogenization has also occurred via the loss of its splicing capacity (Arabidopsis thaliana and Olimarabidopsis pumila). In contrast, the spliced product of chloroplast-encoded rps16 is observed in close relatives of Arabidopsis thaliana (Arabidopsis arenosa, Arabidopsis lyrata, and Crucihimalaya lasiocarpa). In this study, we identified the different functional status of rps16 in several chloroplast genomes in the genus Arabidopsis and its close relatives. Our results strongly suggest that nuclear-and chloroplastencoded rps16 genes coexisted for at least 126 million years. We raise the possibility of the widespread pseudogenization of rps16 in the angiosperm chloroplast genomes via the loss of its splicing capacity, even when the rps16 encoded in the chloroplast genome is transcriptionally active.

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Section: Discussionmentioning

confidence: 99%

Different status of the gene for ribosomal protein S16 in the chloroplast genome during evolution of the genus Arabidopsis and closely related species

et al. 2010

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“…Changes in homeotic gene expression in the different floral whorls have suggested a role for homeosis in the evolution of flower morphologies (reviewed by Hintz et al, 2006). Heterotopic expression of B-class genes in first whorl floral organs has been implicated in the formation of petaloid tepals instead of sepals in tulips (Kanno et al, 2003), as proposed in the 'shifting boundaries' model (Van Tunen and Angenent, 1993).…”

Section: Reviewmentioning

confidence: 99%

“…The finding that these proteins have the ability to homodimerize in some flowering plant species and in gymnosperms led to the hypothesis that obligate heterodimerization of DEF-and GLO-like proteins arose from homodimerization (several times independently) during flowering plant evolution (Winter et al, 2002), probably owing to a selective advantage (Lenser et al, 2009). Autoregulatory circuits of B-class proteins also partially diverged following more recent gene duplication events and differential gene loss (Lee and Irish, 2011), for example in Solanaceae (Rijpkema et al, 2006;Geuten and Irish, 2010) and the basal eudicot opium poppy (Papaver somniferum) (Drea et al, 2007).Changes in homeotic gene expression in the different floral whorls have suggested a role for homeosis in the evolution of flower morphologies (reviewed by Hintz et al, 2006). Heterotopic expression of B-class genes in first whorl floral organs has been implicated in the formation of petaloid tepals instead of sepals in tulips (Kanno et al, 2003), as proposed in the 'shifting boundaries' model (Van Tunen and Angenent, 1993).…”

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confidence: 99%

Developmental and evolutionary diversity of plant MADS-domain factors: insights from recent studies

et al. 2012

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SummaryMembers of the MADS-box transcription factor family play essential roles in almost every developmental process in plants. Many MADS-box genes have conserved functions across the flowering plants, but some have acquired novel functions in specific species during evolution. The analyses of MADS-domain protein interactions and target genes have provided new insights into their molecular functions. Here, we review recent findings on MADS-box gene functions in Arabidopsis and discuss the evolutionary history and functional diversification of this gene family in plants. We also discuss possible mechanisms of action of MADS-domain proteins based on their interactions with chromatin-associated factors and other transcriptional regulators. Key words: MADS-box genes, Plant development, Evolution, Transcriptional regulationIntroduction MADS-domain transcription factors comprise one of the beststudied gene families in plants and members of this family play prominent roles in plant development. Two decades ago, the first MADS-box genes AGAMOUS (AG) from Arabidopsis thaliana (Yanofsky et al., 1990) and DEFICIENS (DEF) from Antirrhinum majus (Schwarz-Sommer et al., 1990) were discovered as regulators of floral organ identity. The sequence of the ~60 amino acid DNA-binding domains within these proteins showed striking similarities to that of the previously characterized proteins serum response factor (SRF) in Homo sapiens (Norman et al., 1988) and Minichromosome maintenance 1 (Mcm1) in Saccharomyces cerevisiae (Passmore et al., 1988). This shared and conserved domain was named the MADS domain (for MCM1, AG, DEF and SRF) and is present in all MADS-domain transcription factor family members (Schwarz-Sommer et al., 1990). Structural analysis of animal and yeast MADS domains showed that the N-terminal and central parts of the MADS domain make contacts with the DNA, while the C-terminal part of this domain contributes mainly to protein dimerization, resulting in a DNA-binding protein dimer consisting of two interacting MADS monomers (e.g. Pellegrini et al., 1995;Huang et al., 2000). Over the past 22 years, many MADS-box gene functions were uncovered in the model species Arabidopsis thaliana and in other flowering plants. Important model plant species for MADS-box gene research include snapdragon (Antirrhinum majus) (reviewed by Schwarz-Sommer et al., 2003), tomato (Solanum lycopersicum), petunia (Petunia hybrida) (Gerats and Vandenbussche, 2005), gerbera (Gerbera hybrida) (Teeri et al., 2006) and rice (Oryza sativa) (reviewed by Yoshida and Nagato, 2011).Initially, MADS-box genes were found to be major players in floral organ specification, but more recent studies revealed functions for MADS-box genes in the morphogenesis of almost all organs and throughout the plant life cycle, from embryo to gametophyte development. The MADS-box gene family in higher plants is significantly larger than that found in animals or fungi, with more than 100 genes in representative flowering plant Development 139, 3081-3098 (2012) REVIEW Box 1...

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“…Double-flowered cultivars have become popular garden plants because of the attractiveness imparted by the extra petals (e.g., roses, peonies, carnations, and camellias). Moreover, scientists have put similar natural deviations from normal development to good use to help elucidate the genetic basis of normal flower development (32,33). Although morphological, developmental, and/or genetic aspects of double-flower cultivars have been investigated (22,(34)(35)(36)(37)(38)(39)(40)(41)(42)(43)(44), no functional evidence for the underlying molecular mechanism of this familiar phenotype is available to date in a noncore eudicot.…”

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confidence: 99%

Loss of deeply conserved C-class floral homeotic gene function and C- and E-class protein interaction in a double-flowered ranunculid mutant

Galimba

Tolkin

Sullivan

et al. 2012

Proc. Natl. Acad. Sci. U.S.A.

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In the model plant Arabidopsis thaliana, a core eudicot, the floral homeotic C-class gene AGAMOUS (AG) has a dual role specifying reproductive organ identity and floral meristem determinacy. We conduct a functional analysis of the putative AG ortholog ThtAG1 from the ranunculid Thalictrum thalictroides, a representative of the sister lineage to all other eudicots. Down-regulation of ThtAG1 by virus-induced gene silencing resulted in homeotic conversion of stamens and carpels into sepaloid organs and loss of flower determinacy. Moreover, flowers exhibiting strong silencing of ThtAG1 phenocopied the double-flower ornamental cultivar T. thalictroides 'Double White.' Molecular analysis of 'Double White' ThtAG1 alleles revealed the insertion of a retrotransposon causing either nonsense-mediated decay of transcripts or alternative splicing that results in mutant proteins with K-domain deletions. Biochemical analysis demonstrated that the mutation abolishes protein-protein interactions with the putative E-class protein ThtSEP3. C-and E-class protein heterodimerization is predicted by the floral quartet model, but evidence for the functional importance of this interaction is scarce outside the core eudicots. Our findings therefore corroborate the importance and conservation of the interactions between C-and E-class proteins. This study provides a functional description of a full C-class mutant in a noncore ("basal") eudicot, an ornamental double flower, affecting both organ identity and meristem determinacy. Using complementary forward and reverse genetic approaches, this study demonstrates deep conservation of the dual C-class gene function and of the interactions between C-and E-class proteins predicted by the floral quartet model. floral organ identity genes | MADS-box genes | solo long terminal repeats | RNA silencing C urrent understanding of floral patterning has emerged primarily from studies in the core eudicot model plants Arabidopsis thaliana and Antirrhinum majus. In these species, the genetic ABCE model predicts how combinatorial expression of four classes of transcription factors specifies organ identity in the floral meristem (1-4). According to the latest Arabidopsis model, which incorporates the role of the E-class proteins, once flowering has initiated, A-and E-class proteins specify sepals; A-, B-, and E-class proteins specify petals; B-, C-, and E-class proteins specify stamens; and C-and E-class proteins specify carpels and terminate floral meristem development (2, 5, 6). The underlying biochemical mechanism for specifying organ identity has been described by the floral quartet model, which predicts that correct transcription of organ-specific genetic programs requires the formation of hetero-multimeric complexes between these four interacting classes of transcription factors (5,(7)(8)(9). Mutations affecting the class-A, -B, -C, and -E functions are homeotic, resulting in the replacement of one organ type by another. Loss of expression of the Arabidopsis C-class gene AGAMOUS (AG) results in conversi...

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Catching a 'hopeful monster': shepherd's purse (Capsella bursa-pastoris) as a model system to study the evolution of flower development

Cited by 47 publications

References 83 publications

Different status of the gene for ribosomal protein S16 in the chloroplast genome during evolution of the genus Arabidopsis and closely related species

Different status of the gene for ribosomal protein S16 in the chloroplast genome during evolution of the genus Arabidopsis and closely related species

Developmental and evolutionary diversity of plant MADS-domain factors: insights from recent studies

Loss of deeply conserved C-class floral homeotic gene function and C- and E-class protein interaction in a double-flowered ranunculid mutant

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