Leaves are initiated by coordinated changes in the polarity of cell division and the growth of a group of founder cells in the peripheral zone of the shoot apical meristem (SAM) (Esau 1977). After leaf initiation, the lamina is formed by the action of the marginal meristem, which is transiently activated at the leaf margin, followed by the action of the plate meristem, both of which contribute to the flattening and expanding of the developing leaf (Avery 1933; Maksymowych 1963; Donnelly et al. 1999). Recent advances in our understanding of the mechanisms of leaf morphogenesis (Tsukaya 2006; Tsukaya and Beemster 2006) have revealed several key regulatory steps. Among these steps, we have recently found two interesting phenomena that might be regulated by long- or short-distance signaling pathways. Here we present an overview of these phenomena.
Although the size, structure, and shape of leaves of a given species are under robust genetic control, these parameters exhibit a certain degree of flexibility, allowing leaves to tailor their growth based on environmental conditions such as light, water, and nutrient availability (Smith and Hake 1992; Kim et al. 2005; Tsukaya 2006). Light is one of the most important envi ronmental factors for leaves. Irradiance is captured by the photosynthetic organelles, chloroplasts, and the captured energy is converted into photo-synthates via a photochemical reaction and the reductive pentose phosphate cycle (Nobel 2005). Because all plant activities require and consume pho-tosynthates, it is crucial that plants produce them in sufficient quantities. Plants can survive under various light conditions by modulating leaf development according to the light environment. Under high-light conditions, leaves thicken and contain large amounts of photosynthetic components per unit leaf area, such as Rubisco and photosystem reaction centers, resulting in high photosynthetic production. High-light-acclimated leaves are called "sun leaves", as compared to "shade leaves", which are formed under low-light conditions. Shade leaves differ from sun leaves in their morphology, which is thinner and broader, and in their physiology, with lower photosynthetic and dark respiration rates, compared to sun leaves. Physiological and ecological studies have revealed details of the differences between these leaf types (for reviews, see Boardman 1977; Bjorkman 1981; Anderson 1986; Terashima et al. 2001). In addition, the developmental aspects of sun and shade leaves are interesting. Recent studies of the development of sun and shade leaves have revealed that the differentiation of new leaf primordia into sun or shade leaves is controlled remotely by mature leaves. In other words, it is controlled by long-distance signaling. In the first half of this review, we present an overview of how leaf type is systematically controlled by long-distance signaling.
In addition to this long-distance pathway, leaf shape and size also appear to be governed locally in each primordium by a shorter-distance signaling pathway. It is noteworthy that cell proliferation and post-mitotic cell expansion occur simultaneously in separate regions of the same developing leaf (Donnelly et al. 1999; White 2006). Finally, both a precise programmed exit from the mitotic cell cycle and the cessation of post-mitotic cell expansion determine leaf size (White 2006). How are these two processes integrated in leaves? The gross size and shape of leaves are not always the simple sum of the behavior of individual cells (Tsukaya 2002, 2003). In fact, a decrease in the cell number due to mutations or genetic manipulations that decrease cell proliferation activity is often associated with an increase in cell size. We named this phenomenon "compensation" (Tsukaya 2002, 2003). A relationship between decreased cell number and increased cell size has been reported in many transgenic plants and loss-of-function mutants of Arabidopsis. For example, a loss-of-function mutation in the AN3/GRF-INTERACTING FAC-TOR1 (GIF1) gene (Kim and Kende 2004), which positively regulates cell proliferation in leaf primordia, causes the typical compensation syndrome (Horiguchi et al. 2005). Similarly, several other mutations that affect cell proliferation have been reported to cause compensation, including aintegumenta (ant), struwwelpeter (swp), swellmap, G protein a-subunit 1, and deformed roots and leaves1 (Mizukami and Fischer 2000; Ullah et al. 2001; Autran et al.
2002; Nelissen et al. 2003; Clay and Nelson 2005). Impaired cell proliferation caused by the reduced activity of cyclin-dependent kinases (CDKs) resulting from the overexpression of either a dominant-negative version of a CDK or a cyclin-dependent kinase inhibitor known as ICK/KRP in tobacco (Nicotiana tabacum), Arabidopsis, and rice also induces compensation (Hemerly et al. 1995; Wang et al. 2000; De Veylder et al. 2001; Boudolf et al. 2004; Barroco et al. 2006). Therefore, compensation is a universal phenomenon in monocot and eudicot species.
In our opinion, this relationship indicates the existence of a short-range signaling within the leaf primordium. In the second half of this review, we will discuss possible mechanisms of leaf-size regulation.
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