Differential Recruitment of<i>WOX</i>Transcription Factors for Lateral Development and Organ Fusion in Petunia and<i>Arabidopsis</i>

Vandenbussche, Michiel; Horstman, Anneke; Zethof, Jan; Koes, Ronald; Rijpkema, Anneke S.; Geräts, Tom

doi:10.1105/tpc.109.065862

Cited by 196 publications

(297 citation statements)

References 63 publications

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“…These genes play important roles in determining the broad appearance of dicot leaves (14)(15)(16). STF modulates blade outgrowth by promoting cell proliferation at the adaxial-abaxial junction of leaf primordia (15), but the mechanism of this action is unknown.…”

Section: Discussionmentioning

confidence: 99%

“…NS1 and NS2 are homologs of the Arabidopsis gene PRS/WOX3 involved in the development of lateral sepals and stipules (11,13). Recent work has identified narrow leaf mutants in the WOX1 homologs maewest (maw) in Petunia x hybrida (14), stenofolia (stf) in Medicago truncatula (15), lam1 in Nicotiana sylvestris (15), and wox1/prs double mutant in Arabidopsis thaliana (14,16). These mutants produce narrow leaf blades owing to defects in lateral cell proliferation affecting leaf width, whereas leaf length is virtually unaffected.…”

mentioning

confidence: 99%

“…These mutants produce narrow leaf blades owing to defects in lateral cell proliferation affecting leaf width, whereas leaf length is virtually unaffected. In leaf primordia, STF/MAW/ WOX1 and PRS/WOX3 are expressed at the adaxial-abaxial boundary layer both in the middle mesophyll and at the leaf margin (14)(15)(16), indicating that this region may be important for blade outgrowth. Arabidopsis WOX1 and PRS are proposed to coordinate adaxial/abaxial patterning through interaction with adaxial and abaxial domain-specific polarity factors (16).…”

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confidence: 99%

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Evolutionarily conserved repressive activity of WOX proteins mediates leaf blade outgrowth and floral organ development in plants

Lin

Niu

McHale

et al. 2012

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

138

180

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The WUSCHEL related homeobox (WOX) genes play key roles in stem cell maintenance, embryonic patterning, and lateral organ development. WOX genes have been categorized into three clades-ancient, intermediate, and modern/WUS-based on phylogenetic analysis, but a functional basis for this classification has not been established. Using the classical bladeless lam1 mutant of Nicotiana sylvestris as a genetic tool, we examined the function of the Medicago truncatula WOX gene, STENOFOLIA (STF), in controlling leaf blade outgrowth. STF and LAM1 are functional orthologs. We found that the introduction of mutations into the WUS-box of STF (STFm1) reduces its ability to complement the lam1 mutant. Fusion of an exogenous repressor domain to STFm1 restores complementation, whereas fusion of an exogenous activator domain to STFm1 enhances the narrow leaf phenotype. These results indicate that transcriptional repressor activity mediated by the WUSbox of STF acts to promote blade outgrowth. With the exception of WOX7, the WUS-box is conserved in the modern clade WOX genes, but is not found in members of the intermediate or ancient clades. Consistent with this, all members of the modern clade except WOX7 can complement the lam1 mutant when expressed using the STF promoter, but members of the intermediate and ancient clades cannot. Furthermore, we found that fusion of either the WUS-box or an exogenous repressor domain to WOX7 or to members of intermediate and ancient WOX clades results in a gain-of-function ability to complement lam1 blade outgrowth. These results suggest that modern clade WOX genes have evolved for repressor activity through acquisition of the WUS-box.T he WUSCHEL related homeobox (WOX) genes form a plantspecific family of the eukaryotic homeobox transcription factor superfamily (1, 2). In Arabidopsis, the WOX family consists of 15 members, including the founding member WUSCHEL (WUS) and WOX1-WOX14 (3), which are involved in the regulation of key developmental processes, including stem cell maintenance in shoot and root meristems, embryo apical-basal polarity patterning, and development of lateral organs (1, 4-7). Based on phylogenetic analysis and their distribution in the plant kingdom, WOX genes have been classified into three clades: modern/WUS (found in seed plants), intermediate (found in vascular plants including lycophytes), and ancient (found in vascular and nonvascular plants, including mosses and green algae) (1,8). WOX genes have been proposed to have a common mechanism of action, as demonstrated by complementation of the wox5 and pressed flower (prs/wox3) mutant phenotypes by WUS, as well as by the partial complementation of prs with WOX4 (5, 9, 10). However, the extent to which the functions of WOX family members are conserved remains unclear.The critical requirement of WOX genes for the development of lateral organs, including leaves and flowers, has become increasingly apparent from the identification of several mutant phenotypes in angiosperms. In maize, the narrowsheath1 and 2 (ns1/ns2) double...

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Section: Discussionmentioning

confidence: 99%

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confidence: 99%

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confidence: 99%

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Evolutionarily conserved repressive activity of WOX proteins mediates leaf blade outgrowth and floral organ development in plants

Lin

Niu

McHale

et al. 2012

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

138

180

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“…Samples for cryoscanning electron microscopy were analyzed as described previously (Vandenbussche et al, 2009). Pistils and ovaries shown in Figures 2S, 2T, 2V, and 2W were fixed in Carnoy's solution II 1:3:6 glacial acetic acid:chloroform:ethanol for 12 h at 4°C, dehydrated in ethanol, and embedded in Technovit 7100.…”

Section: Microscopymentioning

confidence: 99%

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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“…PRS is a member of the WOX (for WUSCHEL related homeobox) gene family (Haecker et al, 2004) and is necessary for the establishment of marginal domains in bifacial leaves via specific expression in leaf margins (Matsumoto and Okada, 2001;Vandenbussche et al, 2009), with loss of function in maize resulting in a narrow leaf phenotype (Nardmann et al, 2004). Phylogenetic analysis revealed that, in Juncaceae and Poaceae, the PRS genes consist of two subclasses, which we have designated PRSa and PRSb (see Supplemental Figure 6 and Supplemental Data Set 5 online).…”

Section: Prsb Is Expressed Only In the Flattened Leaf Primordiamentioning

confidence: 99%

Genetic Framework for Flattened Leaf Blade Formation in Unifacial Leaves ofJuncus prismatocarpus

2010

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Angiosperm leaves generally develop as bifacial structures with distinct adaxial and abaxial identities. However, several monocot species, such as iris and leek, develop unifacial leaves, in which leaf blades have only abaxial identity. In bifacial leaves, adaxial-abaxial polarity is required for leaf blade flattening, whereas many unifacial leaves become flattened despite their leaf blades being abaxialized. Here, we investigate the mechanisms underlying the development and evolution of flattened leaf blades in unifacial leaves. We demonstrate that the unifacial leaf blade is abaxialized at the gene expression level and that an ortholog of the DROOPING LEAF (DL) gene may promote flattening of the unifacial leaf blade. In two closely related Juncus species, Juncus prismatocarpus, which has flattened unifacial leaves, and Juncus wallichianus, which has cylindrical unifacial leaves, DL expression levels and patterns correlate with the degree of laminar outgrowth. Genetic and expression studies using interspecific hybrids of the two species reveal that the DL locus from J. prismatocarpus flattens the unifacial leaf blade and expresses higher amounts of DL transcript than does that from J. wallichianus. We also show that leaf blade flattening is a trigger for central-marginal leaf polarity differentiation. We suggest that flattened unifacial leaf blades may have evolved via the recruitment of DL function, which plays a similar cellular but distinct phenotypic role in monocot bifacial leaves.

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Differential Recruitment ofWOXTranscription Factors for Lateral Development and Organ Fusion in Petunia andArabidopsis

Cited by 196 publications

References 63 publications

Evolutionarily conserved repressive activity of WOX proteins mediates leaf blade outgrowth and floral organ development in plants

Evolutionarily conserved repressive activity of WOX proteins mediates leaf blade outgrowth and floral organ development in plants

Redefining C and D in the Petunia ABC

Genetic Framework for Flattened Leaf Blade Formation in Unifacial Leaves ofJuncus prismatocarpus

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