Functional Analysis of All AGAMOUS Subfamily Members in Rice Reveals Their Roles in Reproductive Organ Identity Determination and Meristem Determinacy

Dreni, Ludovico; Pilatone, Alessandro; Yun, Dapeng; Erreni, Stefano; Pajoro, Alice; Caporali, Elisabetta; Zhang, Dabing; Kater, Martin M.

doi:10.1105/tpc.111.087007

Cited by 145 publications

(215 citation statements)

References 61 publications

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“…However, unlike PMADS3, FBP6 is also able to interact with FBP26 (Immink et al, 2003), perhaps indicative of the unique function of FBP6 in style and stigma development or in other processes yet to be uncovered. Recently, it was shown that the rice C-function is also redundantly encoded by its two C-clade genes (Dreni et al, 2011). This contrasts with the situation in Arabidopsis and snapdragon, harboring three and two C-clade genes, respectively, where in both cases a single gene has taken up the role of the classical C-function (Bowman et al, 1989;Yanofsky et al, 1990;Bradley et al, 1993).…”

Section: Discussion the C-function In Petunia Is Redundantly Encoded contrasting

confidence: 39%

“…Likewise, the seed development phenotype in our fbp7 fbp11 mutants and in the weaker cosuppression lines (Colombo et al, 1997) indicates a unique function for the petunia D-clade genes during seed development. Thus, MADS13, the rice ortholog of STK and FBP7/11, seems to be so far the only D-clade gene that is absolutely required for ovule identity (Dreni et al, 2011).…”

Section: The Petunia C-and D-clade Genes Redundantly Specify Ovule Idmentioning

confidence: 99%

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Redefining C and D in the Petunia ABC

et al. 2012

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According to the ABC(DE) model for flower development, C-genes are required for stamen and carpel development and floral determinacy, and D-genes were proposed to play a unique role in ovule development. Both C-and D-genes belong to the AGAMOUS (AG) subfamily of MADS box transcription factors. We show that the petunia (Petunia hybrida) C-clade genes PETUNIA MADS BOX GENE3 and FLORAL BINDING PROTEIN6 (FBP6) largely overlap in function, both in floral organ identity specification and floral determinacy, unlike the pronounced subfunctionalization observed in Arabidopsis thaliana and snapdragon (Antirrhinum majus). Some specialization has also evolved, since FBP6 plays a unique role in the development of the style and stigma. Furthermore, we show that the D-genes FBP7 and FBP11 are not essential to confer ovule identity. Instead, this function is redundantly shared among all AG members. In turn, the D-genes also participate in floral determinacy. Gain-of-function analyses suggest the presence of a posttranscriptional C-repression mechanism in petunia, most likely not existing in Arabidopsis. Finally, we show that expression maintenance of the paleoAPETALA3-type B-gene TOMATO MADS BOX GENE6 depends on the activity of C-genes. Taken together, this demonstrates considerable variation in the molecular control of floral development between eudicot species.

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Section: Discussion the C-function In Petunia Is Redundantly Encoded contrasting

confidence: 39%

Section: The Petunia C-and D-clade Genes Redundantly Specify Ovule Idmentioning

confidence: 99%

Redefining C and D in the Petunia ABC

et al. 2012

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“…2D; Yamaguchi et al, 2006;Dreni et al, 2007;Ohmori et al, 2009;Cui et al, 2010). Protein interactions of OsMADS1 with OsMADS13 (a class D gene), OsMADS7, and OsMADS8 (Favaro et al, 2002;Cui et al, 2010) and its genetic interactions with OsMADS6, OsMADS3, OsMADS58, and OsMADS13 (Dreni et al, 2011;Li et al, 2011aLi et al, , 2011bSupplemental Fig. S8) suggest that higher order complexes of these factors may promote meristem termination and ovule development.…”

Section: Interactions Among Mads Factors During Floret Organogenesis mentioning

confidence: 99%

RiceLHS1/OsMADS1Controls Floret Meristem Specification by Coordinated Regulation of Transcription Factors and Hormone Signaling Pathways

2013

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SEPALLATA (SEP) MADS box transcription factors mediate floral development in association with other regulators. Mutants in five rice (Oryza sativa) SEP genes suggest both redundant and unique functions in panicle branching and floret development. LEAFY HULL STERILE1/OsMADS1, from a grass-specific subgroup of LOFSEP genes, is required for specifying a single floret on the spikelet meristem and for floret organ development, but its downstream mechanisms are unknown. Here, key pathways and directly modulated targets of OsMADS1 were deduced from expression analysis after its knockdown and induction in developing florets and by studying its chromatin occupancy at downstream genes. The negative regulation of OsMADS34, another LOFSEP gene, and activation of OsMADS55, a SHORT VEGETATIVE PHASE-like floret meristem identity gene, show its role in facilitating the spikelet-to-floret meristem transition. Direct regulation of other transcription factor genes like OsHB4 (a class III homeodomain Leu zipper member), OsBLH1 (a BEL1-like homeodomain member), OsKANADI2, OsKANADI4, and OsETTIN2 show its role in meristem maintenance, determinacy, and lateral organ development. We found that the OsMADS1 targets OsETTIN1 and OsETTIN2 redundantly ensure carpel differentiation. The multiple effects of OsMADS1 in promoting auxin transport, signaling, and auxin-dependent expression and its direct repression of three cytokinin A-type response regulators show its role in balancing meristem growth, lateral organ differentiation, and determinacy. Overall, we show that OsMADS1 integrates transcriptional and signaling pathways to promote rice floret specification and development.Patterning an angiosperm flower requires the combined and individual functions of class A, B, C, D, and E MADS box transcription factors (Krizek and Fletcher, 2005;Thompson and Hake, 2009). In Arabidopsis (Arabidopsis thaliana), the class E activity is conferred by four redundant proteins, SEPALLATA1 (SEP1), SEP2, SEP3, and SEP4, that are cofactors in complexes with other MADS box factors that determine floral organ identities and meristem determinacy (Pelaz et al., 2000). Studies on loss-and gain-of-function mutants in SEP genes together with protein interaction analyses point to their pivotal role in mediating interactions among other floral organ-patterning genes (Honma and Goto, 2001;Ditta et al., 2004;Immink et al., 2009). The largely shared functions of Arabidopsis SEP genes differ from observations that homologs in other plants often have discrete roles in floral development (Malcomber and Kellogg, 2005), but the molecular mechanism underlying their species-specific roles is not well studied. In addition to the ABCDE class of organ fate regulators, a number of hormone signaling pathways influence floral transition, organ numbers, fertility, and floral meristem (FM) determinacy. Dynamic interactions are reported between transcription factors and specific hormone signaling factors during the establishment of Arabidopsis FMs (Sessions et al., 1997;Leibfried et al., ...

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“…In situ hybridization experiments were performed as described previously by Dreni et al (2011) using as probe STK antisense RNA, which corresponds to nucleotides 455 to 818 (Brambilla et al, 2007).…”

Section: Gus Staining and In Situ Hybridizationmentioning

confidence: 99%

BASIC PENTACYSTEINE Proteins Mediate MADS Domain Complex Binding to the DNA for Tissue-Specific Expression of Target Genes in Arabidopsis

et al. 2012

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BASIC PENTACYSTEINE (BPC) transcription factors have been identified in a large variety of plant species. In Arabidopsis thaliana there are seven BPC genes, which, except for BPC5, are expressed ubiquitously. BPC genes are functionally redundant in a wide range of developmental processes. Recently, we reported that BPC1 binds to guanine and adenine (GA)-rich consensus sequences in the SEEDSTICK (STK) promoter in vitro and induces conformational changes. Here we show by chromatin immunoprecipitation experiments that in vivo BPCs also bind to the consensus boxes, and when these were mutated, expression from the STK promoter was derepressed, resulting in ectopic expression in the inflorescence. We also reveal that SHORT VEGETATIVE PHASE (SVP) is a direct regulator of STK. SVP is a floral meristem identity gene belonging to the MADS box gene family. The SVP-APETALA1 (AP1) dimer recruits the SEUSS (SEU)-LEUNIG (LUG) transcriptional cosuppressor to repress floral homeotic gene expression in the floral meristem. Interestingly, we found that GA consensus sequences in the STK promoter to which BPCs bind are essential for recruitment of the corepressor complex to this promoter. Our data suggest that we have identified a new regulatory mechanism controlling plant gene expression that is probably generally used, when considering BPCs' wide expression profile and the frequent presence of consensus binding sites in plant promoters.

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Functional Analysis of All AGAMOUS Subfamily Members in Rice Reveals Their Roles in Reproductive Organ Identity Determination and Meristem Determinacy

Cited by 145 publications

References 61 publications

Redefining C and D in the Petunia ABC

Redefining C and D in the Petunia ABC

RiceLHS1/OsMADS1Controls Floret Meristem Specification by Coordinated Regulation of Transcription Factors and Hormone Signaling Pathways

BASIC PENTACYSTEINE Proteins Mediate MADS Domain Complex Binding to the DNA for Tissue-Specific Expression of Target Genes in Arabidopsis

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