Overrepresentation of elements recognized by TCP-domain transcription factors in the upstream regions of nuclear genes encoding components of the mitochondrial oxidative phosphorylation Machinery.

We have observed that a cis-acting regulatory element, known as site II, is overrepresented in the promoters of nuclear genes encoding components of the oxidative phosphorylation (OxPhos) machinery from both Arabidopsis (Arabidopsis thaliana) and rice (Oryza sativa). Site II elements have been described in promoters of rice and Arabidopsis proliferating cell nuclear antigen (PCNA) genes (Kosugi et al., 1995; Trémousaygue et al., 2003) and are also present in the majority of Arabidopsis genes encoding ribosomal proteins (Trémousaygue et al., 2003). Loss-of-function analysis has determined that a pair of site II elements present in the rice PCNA promoter is essential for the expression of a reporter gene in the shoot and root meristems of transgenic tobacco (Nicotiana tabacum; Kosugi et al., 1991, 1995). In fact, a promoter region containing these elements is enough to confer expression in tobacco protoplasts when fused to a minimal promoter (Kosugi et al., 1995). Similar elements in Arabidopsis PCNA-2 produce expression in root primordia and young leaves (Trémousaygue et al., 2003). Accordingly, these elements have been implicated in the expression of genes in meristematic tissues and/or proliferating cells. Site II elements are frequently present in more than one copy and found in combination with another motif, known as telo box or internal telomeric repeat due to its similarity to the repeated unit of plant telomeres (Trémousaygue et al., 2003). The generation of new mitochondria, which occurs by fission of preexisting ones, is not necessarily linked to cell division. In fact, the number of mitochondria present in a cell is not constant and depends on the tissue and developmental stage and on external conditions (Huang et al., 1994; Griffin et al., 2001). A wellknown example in plants is the increase in the number of mitochondria per cell that occurs in anthers during sporogenesis (Lee and Warmke, 1979). It can be postulated, however, that proliferating tissues would require active mitochondrial biogenesis to maintain the mitochondrial population of newly formed cells. In addition, it can be envisaged that active cell division may require additional energy input derived from mitochondrial OxPhos, and that this may require an increase in the amount of proteins involved in this and related processes. Biogenesis of the OxPhos complexes requires the expression of two separate genomes within one cell. This is because some of the proteins that compose these complexes are encoded within the organelle genome, while the rest are encoded in the nucleus (Mackenzie and McIntosh, 1999). It is generally assumed that the expression of genes encoded in these genomes must be somehow coordinated to ensure correct complex assembly. A recent study suggests that coordination of the expression of genes encoded in the nuclear and the mitochondrial compartments occurs at the posttranslational level (Giegé et al., 2005). Regarding the coordination of nuclear genes themselves, it is more likely that regulation takes place at the transcriptional level, perhaps through the interaction of common sets of transcription factors with cognate binding sites present in the respective promoters. Studies of promoter elements required for the expression of one of the two genes encoding mitochondrial cytochrome c (Cytc-1) in Arabidopsis revealed the existence of a couple of site II motifs linked to a downstream-located telo box that were required for expression in root and shoot meristems, nascent leaves, and anthers (Welchen and Gonzalez, 2005). Since cytochrome c participates as a shuttle of electrons between complexes III and IV, we analyzed the existence of similar elements in the putative promoters of nuclear genes encoding components of these complexes and found that a high proportion of them 1 This work was supported by Consejo Nacional de Investigaciones Cientı́ficas y Técnicas, by Agencia Nacional de Promoción Cientı́fica y Tecnológica, by Fundación Antorchas, and by Universidad Nacional del Litoral. * Corresponding author; e-mail [email protected]; fax 54– 342–4575219. The author responsible for distribution of materials integral to the findings presented in this article in accordance with the policy described in the Instructions for Authors (www.plantphysiol.org) is: Daniel H. Gonzalez ([email protected]). [W] The online version of this article contains Web-only data. www.plantphysiol.org/cgi/doi/10.1104/pp.105.075366.