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First published online 30 June 2004
doi: 10.1242/dev.01205

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Molecular and genetic interactions between STYLOSA and GRAMINIFOLIA in the control of Antirrhinum vegetative and reproductive development

Cristina Navarro^1,*, Nadia Efremova^1,*, John F. Golz², Roger Rubiera¹, Markus Kuckenberg¹, Rosa Castillo¹, Olaf Tietz³, Heinz Saedler¹ and Zsuzsanna Schwarz-Sommer^1,

¹ Abteilung für Molekulare Pflanzengenetik, Max-Planck-Institut für Züchtungsforschung, 50829 Köln, Germany
² School of Biological Sciences, Monash University, Clayton, VIC 3800, Australia
³ Institut für Biologie II, Zellbiologie, Universität Freiburg, 79104 Freiburg, Germany

View larger version (14K): [in a new window]   Fig. 1. Domain structure of GRO/TUP1-like co-repressors in Arabidopsis (LUG and LUH) and Antirrhinum (STY and STY-L). Individual domains are shown in boxes with different shading and domain designations are indicated for the LUG protein (Conner and Liu, 2000). Numbers show the position of amino acids within the proteins. Italic numbers indicate the percentage similarities relative to LUG domains (percentage similarity between LUH and STY-L in brackets). Asterisk indicates the position of the mutation in the sty allele. The sizes of domains are approximately to the scale.

View larger version (67K): [in a new window]   Fig. 2. Morphology of wild-type (A,D), gram (B,E), sty (C,F) and sty gram (G-I) flowers. In A-C the flowers are shown from the top revealing the structure of petals in the second whorl, flowers in E-I are in a side view and the lower part of the wild-type flower in D has been removed to show the stamens and the carpels (front view). The genetic background in A-C and G-I is Sippe 50 and JI75 in E-F. Notice enhanced severity of the mutant phenotypes in E-F compared to B,C. The arrowhead in C points to a stamenoid petal and the arrowheads in E and F point to petaloid sepals. Whorls with homeotically altered organs are numbered in G. In H whorled organisation is disrupted and filamentous organs are indicated by an asterisk. Severe reduction in organ number is illustrated in I. Scale bars: 5 mm.

View larger version (74K): [in a new window]   Fig. 3. Vegetative phenotypes observed with the sty gram double mutant. For comparison the gram mutant is shown in A, F and at the left in D. (A-C) 5- to 6-week-old seedlings. Notice irregular phyllotaxis in B and fused cotyledons above a `bulge' wrapping the arrested shoot tip in C. (D) Comparison of leaves from the fourth node of 10-week-old plants. (E) Detail of a 10-week-old plant with needle-like (arrow) and filamentous leaves (*). (F,G) SE micrographs of freeze-fractured needle-like leaves. The sub-epidermal cell layer is highlighted by false green colour. (H) Histological section of the central vein in a radialised sty gram leaf. p and x indicate phloem and xylem elements, respectively. The mutants in E-H are in the JI75 genetic background. Scale bars: 5 mm (A-E); 50 µm (F,G) and 25 µm (H).

View larger version (55K): [in a new window]   Fig. 4. Vascular skeletons revealing venation patterns in leaves. (A) A wild-type leaf with boxes indicating the approximate position in B-E (tip) and F-I (middle). The insets in F and G show additional five-fold magnifications of a midvein. Genotypes are given under the panels. Scale bars: 1 cm (A): 1 mm (B-I).

View larger version (98K): [in a new window]   Fig. 5. In situ STY (left panel) and GRAM expression patterns (right panel) during wild-type vegetative development. Photographs in a row are from consecutive sections. Cross sections were prepared from the apex of 7- to 8-week-old plants. Because of floral induction the leaf primordia are arranged in a spiral order. This allows more developmental stages to be observed in one section (numbered in B and D), compared to the two to four primordia arranged in decussate phyllotaxis in apices prior to induction. (A,B) In situ mRNA expression patterns. The sections were taken from the top of a shoot and do not reveal the shoot apical meristem. (C,D) The sections for immunolocalisation show the apical meristem and very young initiating primordia. (Arrowhead in C indicates the margin region expressing STY that expands in the gram mutant shown in Fig. 7A) (Insets) Magnification of a small region of a P3 primordium reveals largely nuclear localisation of STY in C and additional cytoplasmic staining for GRAM in D. (E,F) DAPI counter-staining of the sections shown in C,D. Notice dark regions that do not reveal the nuclear DAPI signal due to quenching by the immunological stain. Scale bars: 100 µm.

View larger version (104K): [in a new window]   Fig. 6. In situ STY (A,C,E,G) and GRAM expression patterns (B,D,F,H) in wild-type inflorescences. The longitudinal sections are consecutive in B-F and G-H. (A,B) mRNA expression patterns. (CH) Protein expression revealed by immunolocalisation. P0 indicates the youngest bract (b) primordium and numbers indicate floral developmental stages (Carpenter et al., 1995). The complementary pattern of STY and GRAM expression is illustrated in G,H. stg, stigma; st, style; cw, carpel wall; o, ovules. Scale bars: 200 µm (A,B,E-H); 100 µm (C,D).

View larger version (129K): [in a new window]   Fig. 7. STY protein expression in mutants affecting leaf abaxial-adaxial asymmetry. (A,B) Consecutive cross sections from the apex of a gram-3 plant probed with antibody directed against STY (A) and GRAM (B). The arrowhead in A points to extended STY expression as compared to a wild-type primordium at a similar developmental stage (arrowhead in Fig. 5C). Notice lack of signal in B confirming specificity of the antibody directed against GRAM. (C,D) Immunolocalisation of STY in cross sections of phan mutant apices (main shoot in C and axillary shoot in D) from plants grown at low and at intermediate temperatures. Notice adaxial localisation of the protein in partially or almost fully abaxialised leaf primordia (white arrowheads). Scale bars: 100 µm.

View larger version (58K): [in a new window]   Fig. 8. Hypersensitivity of sty to auxins and auxin transport inhibitors. (A-C) Wild-type and (D-F) sty mutant seedlings after 2 weeks of growth on in vitro culture media supplemented as indicated under the panels. Scale bars: 1 cm.

View larger version (12K): [in a new window]   Fig. 9. Polar auxin transport in inflorescence stem sections. Average and standard deviation in a representative experiment with 20 segments are shown. The difference between wild type and sty mutant is significant at a confidence level >99.9%. *Physiological direction (see Materials and methods).