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First published online November 11, 2004
doi: 10.1242/10.1242/dev.01517

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INCOMPOSITA: a MADS-box gene controlling prophyll development and floral meristem identity in Antirrhinum

Simona Masiero^*, Ming-Ai Li^*,, Isa Will, Ulrike Hartmann, Heinz Saedler, Peter Huijser, Zsuzsanna Schwarz-Sommer and Hans Sommer

Abteilung für Molekulare Pflanzengenetik, Max-Planck-Institut für Züchtungsforschung, 50829 Köln, Germany

View larger version (52K): [in a new window]   Fig. 1. (A) Structure of the INCO gene in the wild-type and in inco mutant alleles. Black boxes represent exons and white boxes are introns. Triangles show the position of transposable elements (Tam) in four mutant inco alleles. (B) Northern blot with mRNA isolated from wild-type and inco inflorescences probed with INCO cDNA and with ACTIN cDNA as loading control.

View larger version (30K): [in a new window]   Fig. 2. The MADS-box protein INCO belongs to the StMADS11 subfamily. (A) The predicted amino acid sequence of INCO (AJ699174) is aligned with other plant MADS-box transcription factors. Identical amino acids are shown in shaded boxes, conservative changes by light shading and non-conserved position in light-grey capitals. (B) Phylogenetic tree generated with the ClustalW program using the first 180 amino acids (M, I and K domains) of the proteins. SVP (Q9FVC1) and AGL24 (CAB79364) are from Arabidopsis; FBP13 (AAK21250) from Petunia; J (Q9FUY6) from tomato; and StMADS11 (AAB94006) and StMADS16 (AAB94005) from potato. The tree was rooted with the Antirrhinum GLO (X68831) sequence (as closely or distantly related to the StMADS11 subfamily as members of any other MADS subfamily (Becker and Theißen, 2003); local bootstrap probabilities are indicated at the branching points.

View larger version (93K): [in a new window]   Fig. 3. In situ expression pattern of INCO in longitudinal sections of wild-type (A-E) and mutant (F,G) plants. (A,C) INCO accumulates in vegetative P0 and P1 primordia and in axillary meristems (AM) in wild-type seedlings. (B) INCO messenger in initiating bracts (P0) and in young floral meristems (FM) of a wild-type inflorescence. Signal is absent from the apical dome of vegetative (SAM) and inflorescence (IM) meristems. (D) Stage 2 floral meristem with emerging sepal primordia (sep). (E) Floral meristem at late stage 3. (F) INCO expression is not affected by the flo-662 mutation. (G) Reduced INCO expression in squa mutant inflorescences. Serial sections probed with FLO revealed signals as in wild type, proving that decreased INCO expression is not an artefact (not shown). IM* is an axillary inflorescence meristem. (H,I) In inco inflorescences, expression of the floral meristem identity controlling genes FLO and SQUA is comparable with wild type (not shown). Scale bars: 200 µm in A,B,F-I; 100 µm in C-E.

View larger version (49K): [in a new window]   Fig. 4. Phenotypes of wild type (A) and inco-1 mutant flowers (B-F). The bottom regions of flowers in B-C are magnified on the right to show prophylls (indicated by asterisks) and fusion of petals and sepals (arrows in B,C). inco buds with large prophylls are depicted in D. Globular glands (circled) are present at the tip of prophylls and bracts, but not in sepals. The diagrams on the right schematically show the morphological changes. The positions of sepals in the wild type are designated by d (dorsal, i.e. adaxial), l (lateral) and v (ventral, i.e. abaxial). Size alteration and displacement of lateral inco sepals is highlighted in blue. (E,F) Vascular skeletons show that secondary veins develop parallel to (instead of branching from) the midvein in inco prophylls and sepals (parallel venation), and the glandular structure (circled) at the tip of prophylls. b, bract; s, sepal. Scale bars: 5 mm in A-D; 0.5 mm in E,F.

View larger version (103K): [in a new window]   Fig. 5. SEM analysis of the ontogeny of wild-type (A,C,E) and inco floral meristems (B,D,F). The flowers shown in B are at late stage 2 and at early stage 3 in A, at stage 4 in C,D and at stage 5 in E-H [stages from Carpenter et al. (Carpenter et al., 1995)]. In def (G), second whorl organs are homeotically transformed to sepals and are smaller than in the wild type (see Fig. 6A,B), therefore size and position of sepals is less affected in def inco flowers (H). Prophylls are shown by an asterisk and numbers indicate the sequential order of appearance of sepal primordia. Scale bars: 50 µm in A,B; 100 µm in C-H.

View larger version (69K): [in a new window]   Fig. 6. Double mutant analyses with inco-1. (A) def flower with petals replaced by sepals. (B) inco def flower. In contrast to inco flowers (Fig. 4), lateral sepal size is hardly affected and no fusions occur to second whorl organs. d, dorsal sepal (C) Inflorescence of the strong flo-640 mutant compared with the weak flo-662 allele shown in D. (E) inco flo-662 inflorescence with axillary inflorescences instead of flowers (arrow). (G,H) Flower formation is enhanced in inco squa double mutants compared with squa (F) grown under identical conditions in segregating populations. Asterisks indicate prophylls. Scale bars: 1 cm.

View larger version (78K): [in a new window]   Fig. 7. Phenotypes of transgenic Arabidopsis plants overexpressing INCO and SVP. (A) Delay of flowering in 35S::INCO and 35S::SVP plants (about 27 rosette leaves when bolting after 32 days of growth) compared with wild type (WT, about 17 rosette leaves when bolting after 22 days of growth). 35S::INCO (B) and 35S::SVP (D) flowers with vegetative characters such as branched trichomes on sepals, petals, carpels (arrowheads) and sepaloid (green) petals compared to wild type (C). A more aberrant early flower is shown in D and a less affected later arising one in B. Scale bars: 1 mm.

View larger version (20K): [in a new window]   Fig. 8. Genetic control of Antirrhinum floral meristem identity and prophyll initiation by INCO and SQUA. Arrows indicate promoting functions and bars show negative effects; neither of these is meant to be direct. Proteins are shown as ovals. For simplicity, we neglect the option that INCO and SQUA are likely to interact with other MADS-domain proteins. The control of prophyll development by SQUA and INCO is highlighted by grey on the left. The arrows merging in the FLO control show convergence of processes promoting flower formation. Green shows potential activation by preference for heterodimerisation of INCO with SQUA. Red (and thin lines) suggests a possible mechanism that can counteract the negative influence of the INCO homodimer on flowering in the wild type. Reinforced heterodimerisation of INCO with SQUA supersedes repression of flowering by INCO. This negative influence, therefore, is relevant only in the squa mutant background.

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