Promoter bashing, microRNAs, and Knox genes. New insights, regulators, and targets-of-regulation in the establishment of lateral organ polarity in Arabidopsis.

The bodies of seed plants are comprised of two classes of organs with contrasting growth and symmetry attributes. Stems and roots are indeterminate organs that exhibit apical growth at apical meristems and radial growth at the vascular cambium, a pattern of growth that results in primarily radially symmetric organs. Lateral organs of the shoot, for example cotyledons, leaves, and floral organs, are determinate and exhibit localized planer growth resulting in breaking of radial symmetry and asymmetric development. Localized planer growth in the leaf generates the leaf blade, the principle site of photosynthesis in most plants. The seed plant body may be described with reference to defined axes of symmetry (Fig. 1). The primary axis of the seed plant body is the apical-basal axis. The apical-basal axis is established during embryogenesis and runs from the center of the primary shoot apical meristem to the center of the primary root apical meristem (Fig. 1A, Axis 1). Distinct organ types are generated at specific positions along the apical-basal axis (root meristem, root, hypocotyl, cotyledon, stem-internode, and shoot apical meristem). Radially symmetric organs possess a second axis, the centralperipheral axis, which extends from the apical-basal axis at the center of the organ outward to the organ epidermis (Fig. 1, A and B, Axis 2). Asymmetric development along the central-peripheral axis is evident in the pattern of vascular tissue placement, with xylem developing in closer proximity to the apicalbasal axis relative to phloem (Fig. 1B). Lateral organs of the shoot arise from the flanks of shoot meristems and consequently possess an intrinsic positional relationship with the meristem from which they are derived. Two axes of lateral organs, the proximal-distal (Fig. 1C, Axis 3) and adaxial-abaxial (Fig. 1D, Axis 4) axes, may be readily defined with respect to the position of the lateral organ in relationship to the meristem from which the organ is derived. Both these axes are exploited as references for the regulation of asymmetrical development. The proximal-distal axis runs from the base of the organ (proximal, i.e. nearest to the meristem) to the tip (distal, i.e. furthest from the meristem; Fig. 1C). Asymmetric development along the proximal-distal axis is most evident in leaves, in that the amount of lateral growth frequently correlates with location along the proximal-distal axis in a manner that is highly predictable for a given species. The adaxialabaxial axis runs from the surface of the lateral organ closest to the meristem (ad-adjacent) to the surface of the organ furthest from the meristem (ab-away; Fig. 1D). Asymmetric development in the adaxial-abaxial axis is most evident in many species in the leaf blade, where the adaxial epidermis and underlying mesophyll differentiate to develop characteristics specialized for efficient light capture, while the abaxial epidermis and mesophyll develop characteristics specialized for efficient gas exchange (Fig. 1E). Proper asymmetric development along the adaxial-abaxial axis is therefore often critical for development of a leaf architecture optimized for photosynthesis. It should be noted that the central-peripheral axis of radially symmetric organs and the adaxial-abaxial axis of shoot lateral organs are equivalent. Both axes are defined with respect to the same reference, the apicalbasal axis at the center of the shoot meristem. Moreover, the pattern of vascular tissue placement in lateral organs (xylem-adaxial, phloem-abaxial; Fig. 1E) is equivalent to that in radially symmetric organs (xylemcentral, phloem-peripheral; Fig. 1B). The ultimate basis of asymmetrical development in all multicellular organisms is the ability of cells to interpret their position with respect to an external reference and transduce this information into asymmetric patterns of cellular differentiation, a process termed polarity establishment. The positional relationship of lateral organs to the meristem from which they are derived indicates that the meristem could in principle serve as the reference for polarity establishment in lateral organs. That this is in fact the case is demonstrated by surgical experiments performed roughly 50 years ago (Warlaw, 1949; Sussex, 1955; Snow and Snow, 1959). When an incision is placed between the meristem and the site where a lateral organ primordiawill next emerge (the P0 site), a lateral organ primordia emerges but develops as a radially symmetrical structure with apparently abaxial characteristics. Several tentative conclusions may be drawn 1 This work was supported by the NSF (grant nos. IBN 9986054 and IBN 0077984 to J.L.B.), by the NRICGP (project no. CALR–2003– 02600 to E.M.E.), and by BARD (postdoctoral fellowship no. FI–314– 2001 to A.I.). * Corresponding author; e-mail [email protected]; fax 530– 752–5410. www.plantphysiol.org/cgi/doi/10.1104/pp.104.040394.