An Unknown Long Distance Signaling Mechanism Governs Differentiation Into Sun or Shade Leaves

We will now introduce recent studies that indicate the parts of the plant that recognize light and control the differentiation of new leaves, and discuss candidates for light recognition. Lake et al. (2001) showed that the stomatal index of developing Arabidopsis leaves decreased when mature leaves were shaded.

The authors also showed that the stomatal density and index decreased when mature leaves were exposed to CO2-enriched air, and vice versa. These results indicate that stomatal development in a developing leaf is regulated by long-distance signaling from mature leaves, with leaves sensing the ambient CO2 concentration and light intensity. Yano and Terashima (2001) reported that in Chenopodium album, the leaf thickness, cell-layer number, and cross-sectional area of cells in the palisade tissue increased when mature leaves were exposed to high light, and decreased when mature leaves were exposed to low light. In contrast to the leaf anatomy, chloroplast acclimation was independent of these signals. Therefore, these studies showed that systemic signaling controls leaf development (Fig. 1), although it is unclear whether the information on CO2 and light are transduced by the same signal. Systemic regulation of leaf development has also been reported in tobacco (Thomas et al. 2004) and poplar (Populus trichocarpa x P. deltoides, Miyazawa et al. 2006). In tobacco, the leaf area, size, and degree of undulation of epidermal cells are affected by the light environment of mature leaves, as well as the index and density of the stomata. In addition to the systemic signaling, leaf

Leaf Cell Acclimation Light

Fig. 1 Anatomy of sun and shade leaves and systemic signals involved in their development. Sun and shade leaves of Arabidopsis thaliana and Chenopodium album (A and B, C and D, respectively). Sun leaves of these species have an additional cell layer in the palisade tissue as compared to shade leaves. Sun and shade leaves were grown under PPFD levels of 360-400 or 60-80 |imolm-2 s-1, respectively. The bar represents 100 |im. Information on the light and CO2 stimuli recognized by mature leaves is transferred to new leaves via systemic signal(s) and determines the differentiation fate of new leaves into sun or shade leaves (E)

Fig. 1 Anatomy of sun and shade leaves and systemic signals involved in their development. Sun and shade leaves of Arabidopsis thaliana and Chenopodium album (A and B, C and D, respectively). Sun leaves of these species have an additional cell layer in the palisade tissue as compared to shade leaves. Sun and shade leaves were grown under PPFD levels of 360-400 or 60-80 |imolm-2 s-1, respectively. The bar represents 100 |im. Information on the light and CO2 stimuli recognized by mature leaves is transferred to new leaves via systemic signal(s) and determines the differentiation fate of new leaves into sun or shade leaves (E)

developmental plasticity is maintained for at least several days, since all of these studies analyzed developing leaves, which were already of visible size at the beginning of the treatments.

Why did plants develop systemic signaling? Let us consider a leaf pri-mordium developing on the SAM. The primordium is insulated from severe environments such as xeric air and strong light. Therefore, the primordium itself cannot sense the light or CO2 environments. However, mature leaves are exposed to the actual environment, allowing them to sense reliable information. Therefore, plants gather information from mature leaves rather than from the primordium itself to govern the formation of appropriate leaves (Woodward et al. 2002).

As mentioned above, light quantity is more important than light quality in the formation of sun or shade leaves. The light sensory mechanism and the systemic signal are still hypothetical, but should fulfill the following requirements:

1. Have the ability to monitor direct or indirect light and/or CO2 concentration;

2. Be able to convert environmental information into mobile substance(s) that can be transferred from mature to developing leaves;

3. Be able to induce specific gene expression that regulates cell division and/or cell growth.

Several candidate signals have been considered (Kim et al. 2005; Coupe et al. 2006), including phytohormones, peptides, RNAs (as signals), sugars, and redoxes (as sensors and/or signals). Phytohormones, peptides, and RNAs as signals would require a sensing system, but we are unable to nominate appropriate candidates to date. As mentioned earlier, mutants in major phy-tochromes and cryptochromes and the phot1 mutant show the laminar thickening that is observed in sun leaves. In addition, plant behaviors driven by known photoreceptors differ from sun- and shade-leaf formation in their reaction times. Although the involvement of a photoreceptor cannot be ruled out, the probability that known photoreceptors are involved is low. In contrast, sugars and redoxes are simpler explanations than the above candidates. Since sugars are the products of photosynthesis and the PPFD is a limiting factor in natural environments, plants can indirectly monitor the light environment by monitoring the sugar concentration. In addition, sugars are also transferred from a source (such as a photosynthesizing leaf) to a sink (such as the SAM or leaf primordia). Sugar sensing by hexokinase is well organized in plants (Cho et al. 2006). In addition to these features, sugar regulates gene expression (Koch 2000, 2004; Hanson et al. 2001). Thus, sugar is a likely candidate. Redoxes also fulfill the requirements described above. In high- or low-light conditions, the plastoquinone pool in thylakoid membranes is reduced or oxidized, respectively; hence, the redox state represents the light environment. The redox state controls the transcription levels of photosynthetic genes (Escoubas et al. 1995; Pfannschmidt et al. 1999). Karpinski et al. (1999) reported long-distance signaling mediated by a re-dox system in Arabidopsis. The authors showed that when several parts of rosette leaves were exposed to excess light and their redox state was reduced, the transcription level of pAPX2::LUC, a gene composed of the promoter of an antioxidant defense gene and the luciferase coding region, increased in the remaining parts, especially in young leaves around the SAM. The expression level in the remaining parts did not increase when the plasto-quinone pool was held in an oxidized state using DCMU, an inhibitor of electron transport from PSII to the plastoquinone pool. At present, the many candidates listed above should be verified. Further physiological and developmental analyses as well as global gene expression profiling, which have been considered by Coupe et al. (2006), should explain these interesting phenomena.

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