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WIREs Dev Biol
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The complex of ASYMMETRIC LEAVES (AS) proteins plays a central role in antagonistic interactions of genes for leaf polarity specification in Arabidopsis

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Leaf primordia are born around meristem‐containing stem cells at shoot apices, grow along three axes (proximal–distal, adaxial–abaxial, medial–lateral), and develop into flat symmetric leaves with adaxial–abaxial polarity. Axis development and polarity specification of Arabidopsis leaves require a network of genes for transcription factor‐like proteins and small RNAs. Here, we summarize present understandings of adaxial‐specific genes, ASYMMETRIC LEAVES1 (AS1) and AS2. Their complex (AS1–AS2) functions in the regulation of the proximal–distal leaf length by directly repressing class 1 KNOX homeobox genes (BP, KNAT2) that are expressed in the meristem periphery below leaf primordia. Adaxial–abaxial polarity specification involves antagonistic interaction of adaxial and abaxial genes including AS1 and AS2 for the development of two respective domains. AS1–AS2 directly represses the abaxial gene ETTIN/AUXIN RESPONSE FACTOR3 (ETT/ARF3) and indirectly represses ETT/ARF3 and ARF4 through tasiR‐ARF. Modifier mutations have been identified that abolish adaxialization and enhance the defect in the proximal–distal patterning in as1 and as2. AS1–AS2 and its modifiers synergistically repress both ARFs and class 1 KNOXs. Repression of ARFs is critical for establishing adaxial–abaxial polarity. On the other hand, abaxial factors KANADI1 (KAN1) and KAN2 directly repress AS2 expression. These data delineate a molecular framework for antagonistic gene interactions among adaxial factors, AS1, AS2, and their modifiers, and the abaxial factors ARFs as key regulators in the establishment of adaxial–abaxial polarity. Possible AS1–AS2 epigenetic repression and activities downstream of ARFs are discussed. WIREs Dev Biol 2015, 4:655–671. doi: 10.1002/wdev.196 This article is categorized under: Gene Expression and Transcriptional Hierarchies > Regulatory Mechanisms Plant Development > Vegetative Development Plant Development > Cell Growth and Differentiation
The leaf structure develops along three axes. Developmental compartments in the shoot apex around the apical meristem and the three structural leaf axes are schematically shown on the left‐hand side and in the middle, respectively (see details in text). CZ, central zone; PZ, peripheral zone; p0, primordium 0; p1, primordium 1; p2, primordium 2.
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AS1–AS2 plays a central role in the antagonistic interaction of genes for adaxial–abaxial polarity specification. Solid lines indicate direct regulation and dashed lines indicate indirect regulation or unconfirmed interactions. Faded names of genes indicate those to be repressed.
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Model for repression of ETT/ARF3 and ARF4 by the AS1–AS2 complex and modifiers in the early stage of leaf primordia in Arabidopsis thaliana. Such repression events are crucial for the establishment of adaxial–abaxial polarity and then cell division and growth along the medial–lateral axis. Class 1 KNOX genes are similarly repressed by AS1–AS2 together with modifier genes, although that is not depicted in this figure.
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(a) The ett and arf4 mutations suppressed major leaf phenotypes of as1‐1 and as2‐1. Representative gross morphology of 40‐day plants and magnified views of their leaves. Gross morphology of Col‐0 (wild type), as1‐1, as1‐1 ett‐13 arf4‐1, as2‐1, and as2‐1 ett‐13 arf4‐1 plants is shown. The genotype of each plant is indicated. Red arrowheads indicate leaf lobes and the arrow indicates a leaflet‐like structure. The introduction of ett arf4 double mutations into as1‐1 or as2‐1 efficiently suppressed the phenotypes of asymmetrically curled leaf blades, asymmetric lobes, and plump and swelled leaf laminas in both mutants in Figure (b). Scale bars: 5 mm (upper) and 2 mm (lower). (b) Gross morphology of typical double mutants (as2‐1 elo3‐27 and as2‐1 eal‐1/bob1). Introduction of ett and arf4 mutations into the double mutants efficiently suppressed the abaxialized leaf phenotypes to form flat symmetric leaves. See details of modifier mutations in Table . Scale bars: 5 mm. Plants were photographed at 28 days after sowing. White arrowheads indicate filamentous leaves. Scale bars: 5 mm. Higher magnification views of filamentous leaves are shown. Scale bars: 1 mm in higher magnification views. Photographs (a) and (b) are reproduced and modified from Ref 34 (Development 2013, 140:1958–1969) and Ref 69 (Plant Cell Physiol 2013, 54:418–431), respectively.
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Dual regulation of ETT/ARF3 gene expression, including by the possibly epigenetic system of AS1–AS2. The AS1–AS2 complex represses ETT/ARF3 directly, and ETT/ARF3 and ARF4 indirectly, via stimulating the miR390 and tasiR‐ARF pathway. In addition, AS1 and AS2 maintain gene‐body DNA methylation of the ETT/ARF3 gene. Solid lines indicate direct regulation and dashed black lines indicate indirect regulation.
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(a) Domain organization of AS1 and AS2 proteins. Both are nuclear proteins. AS2 belongs to the AS2/LOB plant‐specific protein family (42 members are designated as AS2 and ASL1–ASL41). (b) Phenotypes of as1 and as2 leaves. Both as1 and as2 show pleiotropic phenotypes including asymmetrically curled leaf blades, asymmetric lobes, asymmetric secondary vein patterns, less prominent midveins, plump and swelled leaf laminas, and shorter petioles than seen in wild type leaves. Asymmetric leaflet‐like structures are formed in as2. Photograph (as2) is reproduced from Ref 5 (Development 2001, 128:1771–1783).
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Roles of the AS1–AS2 complex in the regulation of class 1 KNOX, ETT/ARF3 and ARF4 genes in early stages of leaf primordia in Arabidopsis thaliana. The introduction of bp knat2 knat6 triple mutations into as1‐1 or as2‐1 efficiently suppressed the phenotypes of short petiole and leaf blade seen in Figure (b).
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