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, 11, e0163

Leaf Development

Affiliations

Leaf Development

Hirokazu Tsukaya. Arabidopsis Book.

Abstract

Leaves are the most important organs for plants. Without leaves, plants cannot capture light energy or synthesize organic compounds via photosynthesis. Without leaves, plants would be unable perceive diverse environmental conditions, particularly those relating to light quality/quantity. Without leaves, plants would not be able to flower because all floral organs are modified leaves. Arabidopsis thaliana is a good model system for analyzing mechanisms of eudicotyledonous, simple-leaf development. The first section of this review provides a brief history of studies on development in Arabidopsis leaves. This history largely coincides with a general history of advancement in understanding of the genetic mechanisms operating during simple-leaf development in angiosperms. In the second section, I outline events in Arabidopsis leaf development, with emphasis on genetic controls. Current knowledge of six important components in these developmental events is summarized in detail, followed by concluding remarks and perspectives.

Figures

Figure 1.
Figure 1.
Terms used to describe leaf morphology. Left, gross morphology of the fifth rosette leaf of Arabidopsis. Upper right, magnified views of the leaf surface. Lower right, magnified view of cross section of the leaf blade.
Figure 2.
Figure 2.
Meristematic activity in early leaf primordia of Arabidopsis. Development of primordia of eighth foliage leaves (Leaf 8 primordia) monitored with the pCYCB1;1::GUS-DB reporter gene, which acts as a specific marker for the G2/M phase of the cell cycle. Blue color indicates the expression of the reporter gene. Arrows indicate cells at the margins of leaf primordia. (A and B) Scanning electron micrographs of gl1 leaves. Bar, 50 µm. (A) Leaf 8 primordium (indicated by 8) 50 µm in length. Also shown are Leaf 7 (7) and stipules (S) of older leaves. (B) Leaf 8, 0.4 mm long. Arrow indicates enlarged cells at margin. (C) Cross section of Leaf 8 primordium at stage of Leaf 8 primordium (indicated by 8) 50 µm in length. (D) Cross section of Leaf 8 primordium 0.16 mm in length, sectioned at a distance 25% of total length above the base. Bar, 50 µm. (E) Cleared Leaf 8 1.2 mm in length. Bar, 0.5 mm. (F and G) Cross sections of Leaf 8 primordia 1.5 mm in length. Bar, 50 µm. (F) Sections cut at a distance 25% of total length above the leaf base. (G) Section cut at a distance 50% of total length above the leaf base. Modified from Donnelley et al. (1999; Dev. Biol. 215: 407–419 with permission from the authors.
Figure 3.
Figure 3.
Schematic representation of patterns of expression of key genes required for early steps in leaf development in Arabidopsis. Cross sections of a shoot apex with two young leaf primordia and one predicted area of a leaf primordium are shown. Regions in which the indicated genes are expressed are shaded. See text for details.
Figure 4.
Figure 4.
Two-directional cell supply from “leaf meristem” region. Clonal cell files are visualized by a heat-shock-inducible homologous recombination system with a GUS reporter gene. Note extension of a cell file in both directions, to the leaf lamina and to the leaf petiole, from a junction region between them. Note also the presence of five distinct cell files. Figures courtesy of Dr. Y. Ichihashi.
Figure 5.
Figure 5.
Genetic network for adaxial-abaxial polarities of leaf primordia linked to a genetic control system for leaf primordium-SAM boundary formation. See text for details.
Figure 6.
Figure 6.
Cyclic arrest front in Arabidopsis leaves. S-phase nuclei are visualized by EdU incorporation (shown by green spots) to indicate the active region of cell proliferation in the leaf primordia and the shoot apical meristem (SAM) of a Columbia wild-type plant rosette. The border between the EdU positive and negative regions is the arrest front (shown in pink). Three axes around leaf primordia are also indicated by white arrows. Note that the EdU-positive zone in the leaf primordia has a constant size measured as distance from the base of the lamina, as reported by Kazama et al. (2010) from analysis of pCYCB1;1::GUS-DB reporter gene expression (see also Fig. 2). Note also the presence of leaf blade-petiole boundary and leaf primordium-SAM boundary indicated by yellow dots.
Figure 7.
Figure 7.
Patterning of marginal serration.(A,B), Wild-type leaf primordia (A) compared to a cuc23 mutant with a smooth leaf margin (B).(C), Overlay image of (A) and (B) showing that the cuc23 mutant has a defect in serrated margin outgrowth.(D–F) Early development of serration. D, Propidium-iodide stained cell image; (E) auxin maxima visualized by DR5rev::GFP signal; (E), an overlay of (D) and (E). Arrows indicate positions where teeth are predicted to develop.(G–I), Auxin maxima (arrowheads) along the leaf margin seen in the wild-type (G), cuc23 mutant (H), and pin18 mutant (I) leaf primordia expressing DR5rev::GFP. Note that the cuc23 mutant failed to maintain distinct auxin maxima; pin18 has irregularly dense but smaller auxin maxima. Modified from Kawamura et al. (2010).
Figure 8.
Figure 8.
Leaves and floral organs of wild-type and phb-1d mutant of Arabidopsis.(A) Wild-type rosette. Bar, 5 mm.(B) Rosette of phb-1d/+ heterozygote. Note that leaves grow upward, with trumpet-like or rod-like shapes. Bar, 5 mm.(C) Rosette of phb-1d /phb-1d homozygote. Foliage leaves (l) and cotyledons (c) are extremely radialized and grow vertically. Bar, 1.25 mm.(D) Adaxial (left) and abaxial (right) side of a wild-type foliage leaf. The adaxial surface is glossy and dark green whereas the abaxial surface is matte, dull or pale green. Bar, 1.75 mm.(E) Severely adaxialized phb-1d leaf. The glossy, dark-green surface characteristic of the adaxial surface extends around the circumference of the radialized leaf. The petiole is highly reduced. Bar, 1 mm.(F) Less severely adaxialized leaf. This trumpet-shaped leaf exhibits adaxial characters on the outside of the cup. The inside of the cup has abaxial characters. Bar, 1 mm.(G) Wild-type inflorescence. Bar, 2 mm.(H) Inflorescence of phb-1d/+ ; sepals fail to enclose the developing flower (p, petal). Bar, 1.25 mm.(I) Cross section of wild-type foliage leaf at midvein; adaxial surface is up (b, leaf blade; m, midrib; v, vascular tissue). Bar, 100 µm.(J) Magnification of wild-type vascular tissue in midrib (x, xylem; p. phloem). Bar, 20 µm.(K) Cross section of extremely radialized leaf of phb-1d/ + heterozygote. Bar, 100 µm.(L) Magnification of vascular tissue in a moderately radialized phb-1d/ + leaf. Note that xylem cells surround phloem cells. Bar, 20 µm. Photographs are reproduced from McConnell and Barton (; Development 125, 2935–2942) with permission.
Figure 9.
Figure 9.
An epiphyllous inflorescence on foliage leaves of the Arabidopsis yab3 fil double mutant. Loss of activity in the leaf-lamina identifier YABBY gives deformed leaves the ectopic identity of a shoot apical meristem. Seeds were a gift from J. Bowman (Monash University, Australia). Bar, 1 mm.
Figure 10.
Figure 10.
Compensation is regulated non-cell autonomously. (A) Leaf morphology and size of a wild-type leaf, an an34 leaf, and a chimera leaf harboring both the an34 mutant and AN3/AtGIF1-overexpressing (marked by GFP expression) cells in the configuration of a spotted chimera. Bar, 5 mm. (B–G) Micrographs of subepidermal palisade cells of the wild type (B), an34 (C), and the chimera (D–G). (F and G) Fluorescent microscopy of the cells in (D) and (E), respectively. Bar, 50 µm. The an34 leaves have much larger cells (C) than do wild-type leaves (B), showing a typical compensation. Note that in the chimera leaf, both an34 cells (D, F) and AN3::GFP-overexpressing cells (E, G) expand to the same extent as the cells in the an34 mutant leaf (C), indicating non-cell-autonomous regulation of compensated cell enlargement. In a chimera harboring both the an3 mutant and AN3/StGIF1-overexpressing (marked by GFP expression) cells, both cells have the same level of compensated cell enlargement as cells of an3 mutant leaves. Figures courtesy of K. Kawade.
Figure 11.
Figure 11.
Genes that control the leaf index value in Arabidopsis. See text for details. Photograph is reproduced from Tsukaya (; Int. J. Dev. Biol. 49: 547–555) with permission.
Figure 12.
Figure 12.
Gross morphology of rosette and flowering plants of the wild type (left) and the phyB-9 mutant (right). Plants were cultivated at 22°C under 12 hours of strong light and 12 hours of darkness daily. Note the altered growth of the leaf lamina and leaf petiole between wild type and the phyB-9 mutant. Bar, 5 mm.
Figure 13.
Figure 13.
Environmental control of the direction of rosette leaf radial positioning in Arabidopsis. A–C, Position of rosette leaves under continuous light illuminated from all sides. Plants were grown on transparent gel in a normal position (A), after a 90° rotation (B), or inversion (C). D, Schematic model of leaf movement in darkness, grown in a normal position (left) or inverted (right). Figures are reproduced and modified from Mano et al. (; Plant Cell Physiol. 47: 217–223) with permission.
Figure 14.
Figure 14.
Heteroblasty in Arabidopsis (Columbia wild type) under continuous light at 22°C. The image shows gradual changes in the shape of leaves. From left: two cotyledons (cot), eight foliage, rosette leaves (rosette leaves), and three cauline leaves. Foliage leaves and cauline leaves are arranged from left as: first foliage leaf; second foliage leaf; third, fourth … eighth foliage leaf; first, second, and third cauline leaf. Bar = 5 mm. Reproduced from Tsukaya et al. (; Planta 210, 536–542) with permission.

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