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STY1 and STY2 promote the formation of apical tissues during Arabidopsis gynoecium development

Sandra Kuusk^1,, Joel J. Sohlberg¹, Jeff A. Long², Ingela Fridborg^1,* and Eva Sundberg^1,

¹ Department of Physiological Botany, Evolutionary Biology Centre, Uppsala University, Villavägen 6, S-752 36 Uppsala, Sweden
² California Institute of Technology, Division of Biology 156-29, 1200 East California Boulevard, Pasadena, CA 91125, USA
^* Present address: Department of Plant Biology, Genetic Centre, Swedish University of Agricultural Sciences, Box 7080, S-750 07 Uppsala, Sweden

View larger version (13K): [in a new window]   Fig. 1. Gene organization of STY1 and STY2 and locations of the transposon insertions in sty1-1 and sty2-1. Rectangles correspond to translated regions and lines depict transcribed but untranslated regions and introns. The sequence elements encoding the RING and IGGH domains are boxed. Cysteines and histidines that constitute putative zinc ligands are in bold and enlarged. The putative NLS of each encoded protein is underlined. Triangles denote transposon insertions. All lines and boxes are drawn to scale.

View larger version (136K): [in a new window]   Fig. 2. Scanning electron micrographs of gynoecia of wild type, the sty1-1 mutant and the sty1-1 sty2-1 double mutant. (A) Medial view of a stage 13 wild-type gynoecium. Stigma, style, the two valves and the abaxial replum are indicated. (B-D) Medial views of sty1-1 single mutant gynoecia of increasing age: (B) stage 12, (C) stage 13, (D) stage 15. Note the style cells in apical positions (C,D, arrowheads). (E) Top view of a stage 12 sty1-1 sty2-1 double mutant gynoecium. Arrowhead points to misplaced apical and adaxial style cells. (F-G) Stage 13 sty1-1 sty2-1 double mutant gynoecia that have developed short horn-like protrusions and produced clusters of stigmatic tissue (H, arrowhead). Arrowhead in F indicates the adaxially formed style cells. Scale bar: 100 µm.

View larger version (64K): [in a new window]   Fig. 3. Rosette leaf morphology of 35S::STY1, wild type and sty1-1 sty2-1 double mutant plants. Plants overexpressing STY1 or STY2 typically produce narrow, non-serrated, epinastic leaves (left). sty1-1 sty2-1 double mutant plants develop leaves with increased serration (right) compared to wild-type leaves (center).

View larger version (82K): [in a new window]   Fig. 4. Vascular patterning in wild type, sty1-1 and sty1-1 sty2-1 gynoecia at anthesis. In each gynoecium, the points of bifurcation of the medial veins are indicated with arrowheads. Medial views of (A) a wild-type gynoecium showing medial veins bifurcating just below the style and medial xylem fans extending along the medial side of the style; (B) a sty1-1 gynoecium in which the point of bifurcation of the medial veins is basalized and the medial xylem fans are located laterally on the style; (C) a sty1-1 sty2-1 gynoecium in which the point of bifurcation of the medial veins is basalized and medial xylem fan formation is greatly reduced. Note that pollen grains appear as white spots. Scale bar: 100 µm.

View larger version (145K): [in a new window]   Fig. 5. Phenotypes associated with 35S::STY1 and 35S::STY2 plants. For simplicity, all illustrations show 35S::STY1 plants. 35S::STY2 plants are identical to 35S::STY1 plants in all aspects shown. (A) Medial view of a stage 13 35S::STY1 gynoecium. Regions with ectopic epidermal style cells are bordered by a white line. (B) Close up of wild-type style cells. (C) 35S::STY1 style cells. Close up of upper section indicated in A. (D) Close up of lower section indicated in A that displays the border between valve cells and ectopic style cells in a 35S::STY1 valve. (E) Poorly developed anthers (arrowheads) and narrow petals of a 35S::STY1 flower. (F) Lateral view of a 35S::STY1 silique. (G) Inner valve epidermal cells. (H) Transverse section of a wild-type valve. (I) Transverse section of a 35S::STY1 valve. Double headed arrow indicates the region of ectopic style cell formation. A mass of overproliferating chlorenchyma cells is seen above the area with ectopic style cells. (J) 35S::STY1 gynoecium with a dehiscing valve still attached to the style along the area where no dehiscence zone is formed (arrow). (K-N; P-R) Transmission electron micrographs of transverse sections of wild-type and 35S::STY1 valves. (K) Wild-type valve. (L) 35S::STY1 valve. (M) Close up of outer epidermal cells of a 35S::STY1 valve. (N) Close up of inner epidermal cells of a 35S::STY1 valve. (O) Medial view of a 35S::STY1 gynoecia with discontinuous lateral xylem strands (arrowheads) and massive medial xylem fans. (P) Close up of wild-type outer epidermal valve cells. (Q) Close up of wild-type style cells. (R) Close up of 35S::STY1 style cells. (S) Medial view of a 35S::STY1 gynoecia with more severe defects than those in (O). Scale bars: 100 µm in A,E,F,J,O,S; 20 µm in B,C,D. sy, style; e sy, ectopic style; r, replum; v, valve; o e, outer epidermis; i e, inner epidermis.

View larger version (92K): [in a new window]   Fig. 6. Expression of STY1 in wild type determined by in situ hybridization (A-I) and STY1::GUS histochemical staining (J-Q). (A,B) Transverse consecutive sections of an inflorescence meristem; (A) most apical section. Floral primordia are numbered according to their relative age from P1 to P5. By stage 2 (B) STY1 expression is localized to sepal analgen (s). (C) Longitudinal section of an inflorescence meristem. Expression is seen in sepal primordia and in abaxial parts of the floral meristem (cryptic bract, cb). (D-F) Expression in the elongating gynoecium. (D) Transverse section of the tip of a stage 8 gynoecium. (E) Longitudinal section of a stage 6 bud. (F) Longitudinal section of a stage 9 flower. Signal is restricted to the apical parts of the gynoecium. (G) Longitudinal section of a stage 12 gynoecium showing expression between the style and the stigma, in outer layers of the septum and in outer integuments. (H) Longitudinal section of young ovules. Expression is seen in outer integuments (o i) and in the tip of the nucellus (n). (I) Longitudinal section of a globular stage embryo. Expression is restricted to cotyledon primordia. Red signals are due to artifacts. (J) Inflorescence. (K) Cauline leaf. (L) 8-day-old seedling. (M) Top view of an inflorescence. Compare with D. (N) Medial view of a stage 12 gynoecium. (O,P) Emerging lateral root primordia. (Q) Root tips. Scale bars: 50 µm in A-F,H; 100 µm in G; 40 µm in I.

View larger version (131K): [in a new window]   Fig. 7. STY2::GUS localization patterns. (A) Inflorescence showing STY2::GUS staining in style and stigmatic tissues and in anthers (arrowheads). (B) 8-day-old seedling. (C) 2-week-old seedling. Note strong GUS staining in trichomes. (D,E) Emerging lateral root primordia.

View larger version (158K): [in a new window]   Fig. 8. Phenotypes of sty1-1 crc-1 and sty1-1 spt-2 double mutants. (A) crc-1 (B) sty1-1 crc-1. The style and stigmatic regions are markedly reduced (arrowhead). (C) Enlargement of the region indicated in B. The cells between the arrowheads show style cell characteristics. (D) A sty1-1 crc-1 double mutant gynoecium that has developed two style-like structures with a few stigmatic papillar cells growing from each structure. (E) Medial view of a sty1-1 crc-1 gynoecium. (F) spt-2. (G) sty1-1 spt-2. (H) sty1-1 spt-2. Mature silique. (I) Medial view of a sty1-1 spt-2 gynoecium. Lateral strands are connected to the medial stylar xylem fans. Arrowhead points to stylar xylem fans produced by both medial and lateral strands. (J) Lateral outgrowth of a sty1-1 spt-2 carpel. Ridged style cells have differentiated at the tip. (K) Apical part of a sty1-1 spt-2 gynoecium. Note the absence of stigmatic papillae. (L) Medial view of a sty1-1 spt-2 gynoecium. Medial and lateral veins enter lobate structures. Scale bars: 100 µm in A,B,D,F,G; 20 µm in J,C; 50 µm in K and 500 µm in H.