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Review
, 22 (4), 1019-32

Morphogenesis of Simple and Compound Leaves: A Critical Review

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Review

Morphogenesis of Simple and Compound Leaves: A Critical Review

Idan Efroni et al. Plant Cell.

Abstract

The leaves of seed plants evolved from a primitive shoot system and are generated as determinate dorsiventral appendages at the flanks of radial indeterminate shoots. The remarkable variation of leaves has remained a constant source of fascination, and their developmental versatility has provided an advantageous platform to study genetic regulation of subtle, and sometimes transient, morphological changes. Here, we describe how eudicot plants recruited conserved shoot meristematic factors to regulate growth of the basic simple leaf blade and how subsets of these factors are subsequently re-employed to promote and maintain further organogenic potential. By comparing tractable genetic programs of species with different leaf types and evaluating the pros and cons of phylogenetic experimental procedures, we suggest that simple and compound leaves, and, by the same token, leaflets and serrations, are regulated by distinct ontogenetic programs. Finally, florigen, in its capacity as a general growth regulator, is presented as a new upper-tier systemic modulator in the patterning of compound leaves.

Figures

Figure 1.
Figure 1.
Morphology and Ontogeny of the Leaf. (A) Different types of leaves and their parts. From left: the simple leaf of Arabidopsis, the pinnately compound tomato and pea, and the palmate leaf of Lupinus perennis. All leaves have a basal petiole and a distal domain made of continuous or separated laminae units. (B) SAM of Petunia, showing developing leaf primordia. Arrows mark the three axes of leaf asymmetry. Bar = 50 μm. (C) Stages in the ontogeny of a simple leaf. Color gradient indicates the maturation state of the leaf cells. Rough estimates of size and number of cells are typical of leaves of Arabidopsis and tobacco. Light-green (immature) polygons mark the region of slow maturation associated with the marginal blastozone. (Photograph in [B] courtesy of John Alvarez.)
Figure 2.
Figure 2.
Environmental and Genetic Regulation of Leaf Size. (A) Different branches of a single Epipremnum pinnatum plant. Left branch with small leaves was hanging, while right branch was wrapped around a supporting pole. (B) Wild-type Arabidopsis plants grown under three environmental conditions natural for this species: agar plates (left), pots under long days (middle), and pots under short days (right) photographed together. (C) and (D) The molecularly similar mutations gob-4D and cuc2-1D produce opposite effects on leaf size in tomato (Berger et al., 2009) (C) and Arabidopsis (Larue et al., 2009) (D), respectively. (E) Altering the levels of the CIN-TCP proteins can have dramatic effects on leaf shape and size (Efroni et al., 2008). Shown are leaves overexpressing a miR319-insensitive version of TCP4 (BLS>rTCP4) or overexpressing miR319 that negatively regulate five CIN-TCPs (35S:miR319 and KAN1>miR319). Note the large effect of the microRNA activated with the KAN promoter (right), which is transiently active during early stages of leaf primodium development. Bars = 10 cm in (A), 1 cm in (B), (D), and (E), and 5 cm in (C). (Photographs in [A] and [B] are courtesy of I.E. [C] is reprinted from Berger et al. [2009]. [D] is courtesy of Clayton Larue, and [E] is reprinted from Efroni et al. [2008].)
Figure 3.
Figure 3.
Genetic Regulation of Compound Leaf Patterning. (A) KN1-induced reiterations of a compound pattern of tomato leaves (Hareven et al., 1996). Note the absence of additional primary leaflets, intercalary folioles, or marginal elaborations. tf, trifoliate. (B) Similar marginal lobing response to elevated KNOX of the simple leaves of the tomato mutant La (left; Hareven et al., 1996) and Arabidopsis (right), where the KNOX gene STM is driven by the leaf-specific promoter BLS. (C) A range of reiterations of the pea compound program conditioned by uni, afilia (af), and tendrilless (tl) (Hofer and Ellis, 1996). (D) Compound Cardamine leaves respond to KNOX by initiation of additional leaflets (Hay and Tsiantis, 2006). Bars = 10 cm in (A) and 1 cm in (C) and (D). ([A] and tomato leaf of [B] are reprinted from Hareven et al. [1996], with permission from Elsevier. Arabidopsis leaf of [B] is reprinted from Shani et al. [2009]. Right image in [C] is reprinted from Gourlay et al. [2000]. Other genotypes in [C] are described in Hofer and Ellis [1996], and images were kindly provided by Julie Hofer. [D] is reprinted by permission from Macmillan Publishers Ltd.: Nature Genetics, Hay and Tsiantis [2006], copyright 2006.)
Figure 4.
Figure 4.
Regulation of Leaflet Initiation by Local and Systemic Florigen Levels. (A) and (B) Selected examples of gradual leaflet loss correlated with transition to flowering in the domesticated rose ([A], left; Shalit et al., 2009) or Murraya exotica ([A], right). In tomato, such loss is evident in the sensitive trifoliate self pruning (tf sp) background (B). (C) Simple leaves induced by grafting a tomato trifoliate receptor with florigen-producing donor (35S:SFT//trifoliate; Shalit et al., 2009). Bars = 5 cm. (Images are reprinted from Shalit et al. [2009], except for the M. exotica image that was taken by I.E.)

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