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doi: 10.1242/10.1242/dev.00290

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Three Brick genes have distinct functions in a common pathway promoting polarized cell division and cell morphogenesis in the maize leaf epidermis

Section of Cell and Developmental Biology, U.C. San Diego, 9500 Gilman Drive, La Jolla, CA 92093-0116, USA

View larger version (130K): [in a new window]   Fig. 1. Phenotypes of wild-type and brk2 mutant leaves. Cyanoacrylate glue impressions of the abaxial surfaces of wild-type (A) and brk2 (B) adult leaf blades. In A black arrowheads indicate stomata; in B black asterisk indicates an abnormal stomatal subsidiary cell. Toluidine-Blue-O-stained cross sections of wild-type (C) and brk2 (D) adult leaf blades. Thickenings in the outer epidermal cell wall at the junctions between adjacent epidermal cells are seen in wild type but not brk mutant leaves (black arrows). In both epidermal impressions and cross sections, the brk3 phenotype (not shown) is indistinguishable from that of brk2. Scale bars: 100 µm.

View larger version (182K): [in a new window]   Fig. 3. Comparison of brk single and double mutant phenotypes. Glue impressions of adult leaf blades are shown for each double mutant and the corresponding single mutants from the same segregating population. (A-C) Single brk3 (A), single brk1 (B) and double brk1;brk3 mutants (C). (D-F) Single brk2 (D), single brk1 (E) and double brk1;brk3 mutants (F). (G-I) Single brk2 (G), single brk3 (H) and double brk2;brk3 mutants (I). Asterisks indicate abnormal subsidiary cells. Scale bar: 100 µm.

View larger version (109K): [in a new window]   Fig. 2. Cytoskeletal organization in expanding epidermal pavement cells of wild-type, brk2 and brk3 maize leaves. (A) In wild-type cells, cortical microtubules form bands focused at lobe sinuses; these bands are also observed in brk2 (B) and brk3 (C) cells (arrows). In the wild type, FITC-phalloidin staining of fixed cells (D) and GFP-talin expression in living cells (G) reveal enrichments of cortical F-actin localized at lobe tips (arrowheads). Such cortical F-actin patches are not observed in brk2 and brk3 cells fixed and stained with FITC-phalloidin (E and F, respectively) or expressing GFP-talin (H and I, respectively). Scale bars: 13 µm.

View larger version (19K): [in a new window]   Fig. 4. Generation of marked brk1, brk2 and brk3 mutant sectors for mosaic analysis. (A) Relative locations of brk and marker loci are illustrated, along with the location of a chromosome-breaking Ds transposon used to generate marked brk2 sectors. (B) Cross-sectional view of a hypothetical white sector in a green leaf illustrating all types of sector boundaries analyzed. Horizontal lines denote upper and lower epidermis; black circles denote veins. Green represents wild-type tissue; white represents mutant tissue. (A) Lateral boundary in the epidermis overlying wild type mesophyll. (B) Transverse boundary with mutant epidermis directly overlying wild-type mesophyll. (C) Lateral boundary in the epidermis coinciding with a lateral boundary in the mesophyll. (D) Lateral boundary in the epidermis overlying mutant mesophyll. (E) Transverse boundary having at least one layer of mutant mesophyll separating mutant epidermis from an underlying wild-type cell layer.

View larger version (149K): [in a new window]   Fig. 5. Mosaic analysis of brk2. (A) DIC image of epidermal peel illustrating sector boundaries of types A and B (Fig. 4B). (B) Same field of view as in A but showing chlorophyll autofluorescence in wild-type guard cells. (A,B) White + signs indicate wild-type guard-cell pairs; black minuses indicate mutant guard-cell pairs in an adjacent cell file. Lobe formation in brk2 mutant epidermal cells is not rescued by adjacent wild-type epidermal cells or underlying wild-type mesophyll. (C) DIC image of a glue impression showing junctions between brk2 and wild-type pavement cells; black arrows indicate areas where the lobes of a wild-type cell appear to have grown over the top of an adjacent, unlobed mutant cell. (D) DIC image of an epidermal peel showing four mosaic stomata, two having a wild-type subsidiary flanking brk2 mutant guard cells (white arrowheads), and two having a brk2 mutant subsidiary flanking wild-type guard cells (black arrowheads); the upper one of these brk2 subsidiary cells is abnormal. Scale bars: A, 100 µm; C, 50 µm.

View larger version (121K): [in a new window]   Fig. 6. Mosaic analysis of brk3. (A) DIC image illustrating sector boundaries of types A and B (see Fig. 4B). (B) Chlorophyll autofluorescence at same boundary shown in A. (A,B) A white plus sign indicates a wild-type guard-cell pair, which is flanked by a mutant subsidiary (black arrowhead in A); a black minus sign indicates a mutant guard-cell pair that is flanked by a wild-type subsidiary cell (white arrowhead in A). (C) DIC image of a glue impression showing junctions between brk3 and wild-type pavement cells; black arrows indicate areas where the lobes of wild-type cells appear to have grown over the tops of adjacent, unlobed mutant cells. Scale bars: A, 100 µm; C, 70 µm.

View larger version (21K): [in a new window]   Fig. 7. Summary of stomatal development in maize (after Stebbins and Shah, 1960). Subsidiary mother cells flanking a guard mother cell become polarized and then divide asymmetrically to form stomatal subsidiary cells.

View larger version (147K): [in a new window]   Fig. 8. Mosaic analysis of brk1. (A) DIC image of an epidermal peel illustrating a type D lateral sector boundary (Fig. 4B), which overlies brk1 mesophyll. Scale bar: 110 µm. (B) Chlorophyll autofluorescence in same field of view shown in A. (A,B) A white plus sign indicates a wild-type stoma; black minus signs indicate brk1 mutant stomata in files with lobed pavement cells. Arrows (A) indicate mutant pavement cells with weak marginal lobes that are separated from wild-type cells by one file of mutant cells. (C) DIC image of an epidermal peel illustrating a type B transverse sector boundary (see Fig. 4B). (D) Chlorophyll autofluorescence in same field as shown in C. Epidermal cells with a brk1 mutation appear mutant where they overlie brk1 mesophyll (left of black arrowhead) but wild type where they directly overlie wild-type mesophyll (right of white arrowhead).