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WIREs Dev Biol
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Morphogenesis of simple leaves: regulation of leaf size and shape

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Abstract Plants produce new organs throughout their life span. Leaves first initiate as rod‐like structures protruding from the shoot apical meristem, while they need to pass through different developmental stages to become the flat organ specialized in photosynthesis. Leaf morphogenesis is an active process regulated by many genes and pathways that can generate organs with a wide variety of sizes and shapes. Important differences in leaf architecture can be seen among different species, but also in single individuals. A key aspect of leaf morphogenesis is the precise control of cell proliferation. Modification or manipulation of this process may lead to leaves with different sizes and shapes, and changes in the organ margins and curvature. Many genes required for leaf development have been identified in Arabidopsis thaliana, and the mechanisms underlying leaf morphogenesis are starting to be unraveled at the molecular level. WIREs Dev Biol 2014, 3:41–57. doi: 10.1002/wdev.115 This article is categorized under: Plant Development > Vegetative Development Plant Development > Cell Growth and Differentiation

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Role of the miR396‐GRFGIF regulatory network in leaf growth. (a) Scheme showing the expression pattern of CYCLINB1;1 (CYCB1;1), miR396, and KLUH. CYCB1;1 indicates dividing cells; miR396 negatively regulates GRF transcription factors and therefore cell proliferation; and KLUH generates an unknown mobile signal that stimulates cell proliferation. (b) GUS staining in developing leaves #5 of transgenic plants harboring CYCB1;1, wtGRF2, rGRF2, and miR396, reporters. The GRF2 reporter is sensitive to the posttranscriptional regulation by miR396, while rGRF2 has mutations in the miRNA‐binding site, so that it is resistant to miR396 action. (c) GRFs and GIFs promote cell proliferation. Silhouette of first leaves of plants overexpressing miR396 (35S:miR396) or GRF2 (rGRF2) and knock‐outs in GRFs or GIF1 (also known as AN3). Palisade parenchyma cell number and size normalized to wild‐type are indicated below each leaf. (Reprinted with permission from Ref . Copyright 2012 PLOS).

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Cell proliferation and expansion during leaf development. (a) Distribution of the cell proliferation and expansion phases in developing leaves of increasing ages. A CYCLINB1;1, (CYCB1;1:GUS) reporter labels cells in the G2‐M phase of the cell cycle. Note that cell proliferation is restricted to the proximal part of the leaf, while cell expansion occurs in the distal part. (b) Magnitude of the cell expansion process during leaf maturation. Outline of adaxial epidermal pavement cells and paradermal view of palisade parenchyma cells in proliferating and mature leaves (Reprinted with permission from Ref 74. Copyright 2010 The Company of Biologists Ltd).

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Early events in leaf development. (a) Scanning electron microscopy of a vegetative shoot apical meristem. Note the spiral phyllotaxy of leaf primordia (LP) around the meristem. (b) Architecture of the vegetative shoot apical meristem. Cells in the S‐phase of the cell cycle are revealed by the expression of HISTONE H4 detected by in situ hybridization in medial‐longitudinal sections. (c) Genes and hormones involved in meristem maintenance and leaf initiation. (d) Expression and activity patterns of genes and small‐RNAs essential for the establishment of leaf polarity.

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Generation of leaf serrations. Scheme showing the interplay between CUC2 and auxin in the formation of leaf serrations in Arabidopsis leaves. CUC2 promotes the establishment of PIN1 convergence points which in turn generate auxin maxima at the tip of serrations. The auxin maximum represses CUC2 at the serration tip and promotes tooth growth. Note that CUC2 is regulated by miR164.

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Dicotyledonous leaves and their variations in size and shape. (a) Arabidopsis thaliana plant showing the three different axes of asymmetries. Bottom left, adult and juvenile leaves. (b) Cross sections of an Arabidopsis leaf blade showing the organization of the different tissues. Two single‐celled layers of epidermis enclose the mesophyll, organized in palisade and spongy parenchyma. (c) Samples for leaf shape and size variations found in nature. The rightmost leaf is a compound or dissected leaf with seven leaflets, while all the others are simple leaves with different shapes, sizes, and margins. From left to right, leaves of Ficus benjamina, Populus nigra, Pyracantha coccinea, Morus nigra, Pelargonium hortorum, Salix babylonica, Hedera helix, and Fraxinus excelsior.

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Variation of leaf shape and size in Arabidopsis natural accessions. (a) Leaf #1 shape and size of 12 Arabidopsis thaliana accessions. The heatmaps represent the leaf area (top) or the length‐to‐width ratio of each accession. (b) A naturally occurring miR164 allele defective in the biogenesis of the miRNA found in the C24 Arabidopsis accession produces deeper serrations when introgressed in Col‐0 plants (Col‐0 × C24 RIL).

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Heteroblasty. (a) Cotyledons, successive true rosette, and cauline leaves in Arabidopsis thaliana. (b) Scheme showing the regulation of vegetative phase change by the miR156‐mediated repression of SPL genes.

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Regulation of leaf curvature. (a) Overexpression of miRNA miR319, which negatively regulates TCP transcription factors as seen in the jaw‐D mutant produces an excess of cells in the margins that causes crinkled leaves. (b) Integration of the miR319/TCP and miR396/GRF regulatory nodes in cell proliferation and differentiation.

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