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First published online 13 September 2006
doi: 10.1242/dev.02545

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ASYMMETRIC LEAVES1 and auxin activities converge to repress BREVIPEDICELLUS expression and promote leaf development in Arabidopsis

Angela Hay^*, Michalis Barkoulas^* and Miltos Tsiantis

Department of Plant Sciences, University of Oxford, South Parks Road, Oxford OX1 3RB, UK.

View larger version (59K): [in a new window]   Fig. 1. AXR1 acts redundantly with AS1 to exclude BP expression from leaves. (A-H) Fourth rosette leaf (A,C,E,G) and scanning electron micrographs of the sinus region (B,D,F,H) of (A,B) Col, (C,D) axr1-12, (E,F) as1-1 and (G,H) as1-1;axr1-12 plants; arrowheads indicate lobe (G) and ectopic stipules (H). (I-L) Rosette leaves 1-7 of (I) Col, (J) axr1-12, (K) as1-1 and (L) as1-1;axr1-12. (M) Quantitative RT-PCR analysis of BP, STM and AS1 expression in mature leaves of Col (white bars), axr1-3 (black bars) and as1-1 (grey bars). Error bars indicate s.e.m. (N,O) Fourth rosette leaf of (N) axr1-12;bp-9 double and (O) as1-1;axr1-12;bp-9 triple mutants. (P,Q) Leaves 1-7 of (P) axr1-12;bp-9 and (Q) as1-1;axr1-12;bp-9.(R-V) Leaves stained for BP::GUS expression in (R) Col, (S) axr1-3, (T) as1-1 and (U,V) axr1-3;as1-1; arrows indicate staining in sinus regions. (R-U) Fourth leaves and (V) eighth leaf dissected from 14-day old plants. (W-Y) Scanning electron micrographs of the sinus region of (W) as1-1, (X) as1-1;axr1-12 and (Y) as1-1;axr1-12;bp-9 cauline leaves. Scale bars: 0.5 cm in A,C,E,G,N,O; 25 µm in B,D,F,H,W-Y; 1 cm in I-L,P,Q; 200 µm in R-V.

View larger version (72K): [in a new window]   Fig. 2. PIN1 acts redundantly with AS1 to exclude BP expression from leaves and promote lateral organ initiation. (A-D) Rosettes just before bolting of (A) Col, (B) pin1-6, (C) as1-1 and (D) pin1-6;as1-1. c, cotyledon. (E,F) The number of rosette leaves in (E) Col (n=68), as1-1 (n=56), pin1-En134 (n=30) and pin1-En134;as1-1 (n=19; note, pin1;as1 double mutants were never observed to flower earlier than pin1 or as1 single mutants), and (F) Col (n=68), bp-9 (n=17), pin1-En134 (n=30) and pin1-En134;bp-9 (n=5) plants. (G-L) Inflorescences of (G) Col, (H) bp-9, (I) blr-126, (J) pin1-6, (K) pin1-6;bp-9 and (L) pin1-6;blr-126. (M) The number of naked branches lacking flowers as a fraction of the total number of branches counted for pid (n=28) and bp;pid (n=29) mutants. (N) Quantitative RT-PCR analysis of BP and AS1 expression in mature leaves of Col (white bars) and pin1-En134 (black bars) plants. Error bars indicate s.e.m. (O-R) GUS-stained seedlings of BP::GUS grown on (O) MS media and (P) MS media supplemented with 20 µM TIBA (arrowheads indicate ectopic expression of BP::GUS in leaves), and STM::GUS grown on (Q) MS medium and (R) MS medium supplemented with 20 µM TIBA. Scale bars: 1 cm in A-D,G-L; 200 µm in O-R.

View larger version (51K): [in a new window]   Fig. 3. PIN1 regulates leaf margin development. (A,B) Half-leaf silhouettes of the seventh rosette leaf of (A) wild type and (B) pin1-En134. (C,D) Confocal micrographs of GFP expression (green) in wild-type developing leaf margins. (C) DR5rev::GFP expression maximum at the tip of a serration, and (D) PIN1:GFP localisation indicates the direction of auxin flux (arrowheads) towards the serration tip. (E,F) Whole-leaf silhouettes of the seventh rosette leaf of wild-type (Col) plants grown on (E) MS medium and (F) MS medium supplemented with 5 µM NPA. (G-I) Confocal micrographs of GFP expression (green) in developing leaf margins indicated by boxes in E,F. (G) PIN1:GFP localisation indicates the direction of auxin flux (arrows) towards the serration tip in plants gown on MS (box in E), whereas, in the margin of NPA-treated plants (box in F), PIN1:GFP localisation is non-polar (H) and DR5rev::GFP expression is diffuse (I). Red indicates chlorophyll autofluorescence. Scale bars: 0.5 cm in A,B,E,F; 20 µm in C,D; 10 µm in G-I.

View larger version (69K): [in a new window]   Fig. 4. Prolonged expression of PIN1 at the margin accompanies leaflet initiation in FIL>>BP leaves. (A-D) Young rosette leaves stained for GUS expression of (A,B) PIN1::GUS in wild type (A) and 35S::BP (B), and (C,D) DR5::GUS in wild type (C) and 35S::BP (D). (E-J) Confocal micrographs of GFP expression (green) in developing leaf margins, 7 (E,H), 10 (F,I) and 12 (G,J) days after germination. (E-G) PIN1:GFP in (E) wild-type (arrow indicates GFP expression in initiating serration), (F) wild-type (arrow indicates a basal shift in GFP expression as a second serration initiates), and (G) FIL>>BP (arrows indicate prolonged GFP expression in developing lobes; inset shows a magnification of one of these lobes). (H-J) ANT::GFP is expressed in a similar manner in (H) wild type (arrows indicate GFP expression in initiating serrations), (I) wild-type (arrow indicates a basal shift in GFP expression as a second serration initiates), and (J) FIL>>BP (arrows indicate prolonged GFP expression in developing lobes). (K,L) Rosette leaves of FIL>>BP plants grown on (K) MS medium and (L) MS medium supplemented with 10 µM NPA. (M) Confocal micrograph of PIN1:GFP expression in a developing leaf margin of FIL>>BP plants grown on MS medium supplemented with 5 µM NPA. (N) Proposed role of auxin in regulating BP activity and leaf shape. AS1 acts in overlapping pathways with PIN1 and AXR1 to repress BP expression in Arabidopsis leaves (solid barred lines), thus contributing to definition of the leaf-meristem boundary and control of leaf development. PIN1 is also required to elaborate margin outgrowths (arrow) in wild-type leaves and in leaves in which BP is ectopically expressed. Such BP-mediated changes in leaf shape may involve restriction of the PIN1 expression domain by BP (dotted barred line). Arrows and barred lines denote genetic and not physical interactions. Red indicates chlorophyll autofluorescence. Scale bars: 200 µm in A-D; 20 µm in E-J; 0.5 cm in K,L; 10 µm in M.