Review
Leaf shape diversity with an emphasis on leaf contour variation, developmental background, and adaptation

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Abstract

Leaf shape varies markedly. Here I focus on the diversity in leaf contour, which can be considered marginal variation in curvature if we omit detailed marginal structures such as serrations. This curvature can be described by a combination of sigmoids: a curve for the apical half and a curve for the basal half connected with or without an interval. Marginal curvature is determined by the position of the leaf meristem, the acceleration and deceleration of cell proliferation in the leaf meristem, and the angle of directed cell proliferation. Several key factors contributing to this variation have been revealed to date, but the majority of the underlying genetic mechanisms are unclear. Here I provide an overview of current knowledge and propose future directions for the field.

Introduction

Shape is important for organisms to maximize their ability to live in the wild. This is, of course, also the case for plants. Among angiosperms, the major clade of land plants worldwide, leaves are the most diversified organs. Flowers are also highly diversified, but their basic components, the floral organs, are modified leaves. Stems and roots also show species-specific characters, but their diversity is less rich than that of leaves. Branching patterns are also important and diversified characters, but again the diversity is less than that of leaf shape. Leaves are so diversified in shape and form partly because they are the site of photosynthesis. Photosynthesis requires efficient absorption of light energy and the exchange of CO2 for O2, and temperature and water content must be maintained within a certain range. Because the most productive form can differ according to environmental conditions, leaf shape varies among species and can be influenced by biotic or abiotic stresses. For example, flat leaves are metamorphosed into spines in desert plants.

Considering the rich diversity of shape and form in leaves, this review article focuses on leaves, in particular on leaf contour. Although the difference between simple and compound leaves is also an important factor in terms of diversity, it is omitted here because the morphological unit of compound leaves, the leaflet, can be considered a simple leaf in terms of its contour. One difference between compound and simple leaves is whether repetitive morphogenesis occurs; this has been reviewed by others [8], [2]. Determinacy or indeterminacy is also omitted here because it contributes to leaf size but not shape [57], [58], [59] Tsukaya (2014, in press). Finally, variation in marginal structures, namely, the absence or presence of marginal dentations/serrations, is outside the scope of this review, which focuses on leaf contour. I wish to emphasize that the function of marginal serrations in leaves is controversial (see [11], [58]).

Section snippets

Contour variation from the viewpoint of curvature

Most leaf contours can be described by a smooth curve if we omit the absence/presence of digitations/serrations along the margin. This curvature can be described by a combination of sigmoids: a curve for the apical half and a curve for the basal half connected with or without an interval (Fig. 1). Many taxonomic characters of leaf shape can be attributed to the nature of the curvature. The nature of the apical tip, which can be caudate (tailed), acute (pointed), apiculate (tapered to a short

Developmental basis of variation in leaf contour

From the standpoint of developmental biology, variation in leaf contour can be attributed to changes in the acceleration and deceleration of cell proliferation in leaf primordia. This is not pure cell proliferation per se, but rather ‘proliferative growth’ or ‘growth coupled with cell proliferation’. Although genetic controls of polar cell elongation and polar cell distribution/proliferation contribute to an altered leaf index in the model plant Arabidopsis thaliana (hereafter Arabidopsis; [55]

Leaf meristem positioning (1): marginal meristem

We follow the example of [57], [59] in our use of the term meristem. In short, it is defined as actively proliferating tissue, and includes apical meristem, cambium, intercalary meristem, and leaf meristem. Leaf meristem is not always located in the basal part of leaf primordia [57], [59]; however, since the Arabidopsis leaf meristem has been investigated extensively, let us evaluate genetic regulation of leaf meristem positioning in Arabidopsis. In Arabidopsis leaves, two types of meristem

Leaf meristem positioning (2): plate meristem

Plate meristem activity is regulated independently of that of the marginal meristem. The roles of AINTEGUMENTA (ANT) and ANGUSTIFOLIA3 (AN3)/At GROWTH REGULATING FACTOR-INTERACTING FACTOR1 (AtGIF1) in leaf development have been analyzed extensively [38], [31], [19], [20]. In both cases, loss-of-function mutations result in smaller, flat leaves and overexpression results in larger, flat leaves. Both are expressed in the plate meristem region; in particular, AN3/AtGIF1 expression is confined to

Leaf meristem positioning (3): third leaf meristem

The third type of meristem important for leaf organogenesis in some plant species is the thickening meristem (Fig. 5). This meristematic activity may correspond to that described in the ‘adaxial meristem’ [23]. Because both the plate and marginal meristems are dependent on the establishment of abaxial/adaxial juxtaposition, unifacial leaf species, which lack the adaxial fate of leaf lamina, cannot use these meristems to generate a flat leaf blade. This may explain why the majority of unifacial

Acceleration and deceleration

Some of the aforementioned key regulators of leaf meristem activity may control not only the position of the meristem but also the rate of acceleration/deceleration of cell proliferation. Changes in this rate can alter leaf contour. In this sense, cell-cycle regulators and ribosome-related genes may also influence leaf contour. Indeed, loss-of-function mutants of ribosomal proteins have leaves with a pointed tip [4], [21], although acceleration or deceleration of cell proliferation in these

Oriented cell division

As is evident in maize leaves, if cell division occurs only perpendicular to the longitudinal axis, clear longitudinal cell files are formed and the leaf contour becomes ribbon like. Even in Arabidopsis leaves, leaf primordia at the earliest phase exhibit cell division perpendicular to the longitudinal axis, enabling the early primordia to protrude like a rod [20]. Thereafter, the direction of cell division is random in the plate meristem because of activation of AN3/AtGIF1 [20], [67]. Although

Oriented cell expansion and others

According to a computer simulation study based on live imaging of Arabidopsis leaf primordia [33], local area growth is directed to the longitudinal axis in the distal part of primordia soon after exiting mitosis (judged from the scale of microscopic images). The direction then changes to become perpendicular to the axis [33]. Such aerial growth must also contribute to leaf contour diversity, and must be mainly due to directional cell expansion, which is regulated by several independent genetic

Adaptive meaning of leaf contour variation: (1) simple cases

An overview of the adaptive meaning of the diversity of leaf contours follows. Some of this variation in contours has been discussed in terms of environmental adaptations, but most has not been reported to have an adaptive meaning. Identifying both the mechanisms and the adaptive meanings of leaf contour variation would enable the design of leaf shapes of useful plants in the future.

A slender leaf base is required to minimize overlap of the leaf surface, which is required for photosynthesis if

Adaptive meaning of leaf contour variation: (2) Unknown functions

Unlike these simple forms, the advantages of most variation in contour are unclear, with a few exceptions. For example, sac-like domatia at the basal part of the leaf blade in some ant plants, such as Callicarpa saccata [39]; Fig. 6D, E), function in symbiosis with ants. The advantages of the pitcher-form leaves of some carnivorous plants are obvious. Moreover, herbivorous insects reportedly avoid an unusual form of leaf contour (Dr. A. Kawakita, Kyoto University, personal communication).

Conclusion

Leaf contour varies markedly among angiosperms, and most variation involves minor differences in leaf curvature. Leaf curvature can be described by a combination of sigmoid curves: a curve for the apical half and a curve for the basal half connected with or without an interval. The nature of marginal curvature depends on the position of the leaf meristem, acceleration and deceleration of cell proliferation in the leaf meristem, and the angle of directed cell proliferation. Of course,

Acknowledgments

This work was supported by the Japan Society for the Promotion of Science (Grant-in-Aid for Scientific Research on Innovative Areas #25113002) and the Bio-Next Project of Okazaki Institute for Integrative Bioscience, National Institutes of Natural Sciences, Japan.

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