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First published online June 25, 2007
doi: 10.1242/10.1242/dev.02864

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Common regulatory networks in leaf and fruit patterning revealed by mutations in the Arabidopsis ASYMMETRIC LEAVES1 gene

Hugo Alonso-Cantabrana^1,*, Juan José Ripoll^1,, Isabel Ochando^1,, Antonio Vera¹, Cristina Ferrándiz² and Antonio Martínez-Laborda^1,

¹ División de Genética, Universidad Miguel Hernández, Campus de San Juan, Ctra. de Valencia s/n, 03550-San Juan de Alicante, Spain.
² Instituto de Biología Molecular y Celular de Plantas (CSIC-UPV), Avda. de los Naranjos s/n, 46022-Valencia, Spain.

View larger version (101K): [in this window] [in a new window]   Fig. 1. Patterning defects in as mutants and 35S::BP Arabidopsis plants. (A,C,E) Stage 17 fruits of the wild-type Col accession. (A) Bright-field stereomicroscope image; (C) SEM; (E) cross section. (B,D,F) Stage 17 fruits of the as1-1 mutant, which produces bumpy fruits (B) and displays large repla both in SEM (D) and cross sections (F). (G,I,K) Bright-field stereomicroscope image (G) and cross sections (I,K) of stage 17 fruits of the Ler accession. (H,J,L) Bright-field stereomicroscope image (H) and cross sections (J,L) of stage 17 fruits of as1-104. Notice the increased size of repla and the reduced size of valves in as1-104 fruits (I-L). (M,N) Cross sections of stage 17 fruits of as2-1 (M) and the 35S::BP line (N), showing the large replum phenotype also seen in as1-1 (D,F). (O,P) Cross sections of stage 17 fruits of the as1-1 bp-1 (O) and as1-104 bp-1 (P) double mutants that show strong recovery of the wild-type replum phenotype. (Q,R) Lignification pattern of stage 18 fruits of Col (Q) and as1-1 (R) stained with phloroglucinol. (S-U) GUS expression in the valve margin driven by the SHP2 promoter in Col (S,T) and as1-1 (S,U) fruits at stage 15. Fruits in the pictures are in the ER background, with the exception of those in G-L and P, which are in the Ler background. Arrowheads indicate the positions of valve margins. Scale bars: 2 mm in A,B,S; 1 mm in G,H; 500 µm in Q,R; 200 µm in I,J; 100 µm in C-F,K-P,T,U. r, replum; v, valve.

View larger version (20K): [in this window] [in a new window]   Fig. 2. Histograms indicating the number of outer epidermal cells in the valve and replum of several wild-type and mutant Arabidopsis lines. (A) Replum; (B) valve. Numbers inside the bars represent the mean number of cells, and lines on top represent standard deviations. Fruits from at least five plants for each genotype were collected for cell counting. At least 20 valves and 20 repla were counted for each line.

View larger version (77K): [in this window] [in a new window]   Fig. 3. AS1 represses the expression of BP in the Arabidopsis gynoecium. (A) In situ localization of AS1 mRNA in a cross section of a Col pistil (stage 10), showing strong expression in valves and lower levels in replum. (B) A control section of a Col pistil (stage 10) hybridized with a sense probe, showing no signal. (C-G) Staining from the KNAT1::GUS-18 reporter in Col and as1-1. In the wild-type background, staining is restricted to the replum, valve margin and style of stage 12 gynoecia (C,E), and the same staining is seen in a fruit at stage 15 (G). In the as1-1 background, valves of stage 12 gynoecia show ectopic expression of BP (D,F). (H,I) Staining from the KNAT1::GUS-1 reporter allows the detection of variations in expression intensity, and shows that BP expression in the replum of stage 15 fruits is more intense in the as1-1 mutant (I) than in the wild-type (H) background. All gynoecia and fruits are in the ER background. Scale bars: 1 mm in G; 0.5 mm in H,I; 200 µm in C,D; 100 µm in A,B,E,F. r, replum; st, style; v, valve.

View larger version (64K): [in this window] [in a new window]   Fig. 4. Interactions of RPL with BP and AS1. (A,B) Cross sections of stage 13 gynoecia from wild-type and 35S::BP Arabidopsis plants, showing GUS staining from the BLR::GUS transgene, a reporter of RPL. (A) GUS staining is restricted to the replum in the wild type. (B) GUS is detected throughout the ovary, including valves and valve margins, in 35S::BP gynoecia. (C,D) GUS staining from the BLR::GUS transgene in rosettes. In the wild-type background (C), staining is detected in the meristem (hidden by the leaves in the picture), whereas the signal is ectopically seen in cotyledons and leaves of plants that overexpress BP (D). (E,F) Cross sections of stage 17 fruits from several mutants harboring rpl alleles. Fruits from rpl-1 (E) and rpl-2 (F) show narrow repla containing cells that adopt a valve margin identity. (G) The replumless phenotype is even stronger in the bp-9 rpl-2 double mutant. (H-J) The as1-1 allele rescues the replumless phenotype conferred by rpl alleles. The wild-type phenotype is observed in as1-1 rpl-2 (H) and as1-1 rpl-1 (I) fruits. (J) A moderate replumless phenotype is observed in an as1-1 rpl-1 fruit. (K,L) SEMs of stage 17 fruits showing the replumless phenotype of rpl-2 (K) and the wild-type phenotype of an as1-1 rpl-2 fruit (L). The genetic background is ER, with the exception of E, I and J, in which rpl-1 and as1-1 rpl-1 are in the er background. Scale bars: 1 mm in C,D; 100 µm in A,B,E-L.

View larger version (101K): [in this window] [in a new window]   Fig. 5. Synergistic interaction between ful-1 and as1 alleles. (A-D) Bright-field stereomicroscope images (A,B) and SEMs (C,D) of stage 17 fruits. The ful-1 mutant exhibits small valves and enlarged and creased repla (A,C). The as1-104 allele enhances the mutant phenotype of ful-1, so that as1-104 ful-1 double mutants show very small valves and very compressed and distorted repla (B,D). (E-G) GUS staining in cross sections of fruits containing the ful-1 reporter. The reporter is expressed only in the valves of as1-104 (E), ful-1 (F) and as1-104 ful-1 (G) fruits. Note the very reduced width of valves and the large size of repla in the double mutant (G). The as1-104 fruit in E is heterozygous for the ful-1 reporter. (H,I) Stage 17 fruits from the as1-1 ful-1 rpl-1 triple mutant showing a reduced mutant phenotype compared with the as1-104 ful-1 double mutant. SEM (H) and transverse section (I) displaying GUS staining from the ful-1 reporter in the aberrant valves. All fruits are in the er background. Scale bars: 1 mm in A,B; 400 µm in C,D,H; 200 µm in E-G,I.

View larger version (53K): [in this window] [in a new window]   Fig. 6. A model for pattern formation along the mediolateral axis of the ovary in Arabidopsis. Three domains are specified by the opposing gradients of two antagonistic factors: valve factors (FIL/JAG activity; blue) and replum factors (class I KNOX genes; yellow). The FIL/JAG activity specifies valve formation, class I KNOX genes determine the replum, and the valve margin (green) is formed in the region in which both valve factors and replum factors are expressed. The AS function (red), carried out by AS1 and AS2, represses class I KNOX genes, preventing the expression of these genes in valves and maintaining their expression below certain levels in the replum and valve margin.