Question marks signifies a proposed yet unproved function
Question marks signifies a proposed yet unproved function
Blue-light control of the psbD-psbC operon. Contrary to most photosynthetic genes, the rate of transcription of psbD-psbC remains high in mature chloroplasts (Klein and Mullet 1990; Baumgartner et al. 1993; DuBell and Mullet 1995). Responsible is a specific activation of one of the psbD promoters, the blue light-responsive promoter (BLRP; Sexton et al. 1990), which is found upstream of the psbD gene of various species (Fig. 4; Christopher et al. 1992; Wada et al. 1994; Allison and Maliga 1995; Kim and Mullet 1995; To et al. 1996; Hoffer and Christopher 1997; Kim et al. 1999b; Thum et al. 2001). The architecture of the psbD BLRP promoter consists of two conserved upstream elements (PGT-box, AAG-box) and poorly conserved and closely spaced -35/-10-elements. In vivo studies in transplastomic tobacco revealed that deletion of parts of the PGT-box reduced mRNA levels, while subsequent deletion the AAG-box sequences even further reduced transcript levels (Allison and Maliga 1995). In tobacco, therefore, the conserved sequence elements upstream of the psbD promoter core are accountable for light-activated transcript accumulation. In vitro transcription from the psbD promoter in rice, wheat, and barley depends on the -10, but not on the -35 promoter element (To et al. 1996; Satoh et al. 1997; Nakahira et al. 1998; Kim et al. 1999b). The AAG-box of the barley promoter was shown to be the binding site for a nuclear-encoded AAG-binding complex in vitro (AGF; Kim and Mullet 1995). However, binding activity of AGF to the AAG-box is not correlated with tran-scriptional activation of the psbD BLRP (Nakahira et al. 1998). One of the components of AGF of Arabidopsis was cloned and designated plastid transcription factor 1 (PTF1; Baba et al. 2001). Studies on PTF1 -deficient mutants revealed that PTF1 is rather involved in general transcriptional enhancement than in light-dependent activation of psbD transcription. Correspondingly, the PGT-box is the binding site for PGTF, the PGT-binding factor. Its DNA-binding activity is regulated by an ADP-dependent kinase (Kim et al. 1999a). A model based on these in vitro experiments in barley explains that constitutively binding of AGF to the upstream AAG-element may assist promoter recognition by PEP, whereas light-dependent transcriptional activation of psbD transcription is mediated by binding of PGTF to the PGT-box. In the dark, PGTF is phosphorylated and loses its affinity for the PGT element, thereby decreasing transcription. Although the psbD promoter architecture is highly conserved, it is unlikely that PGT is required for light-dependent transcription in various other plants. It was shown for rice (To et al. 1996), wheat (Satoh et al. 1997), and barley in vitro (Kim et al. 1999b) and in transplastomic tobacco in vivo (Thum et al. 2001) that the PGF-box is not required for light-dependent activation in these plants. Therefore, the roles of PGT and PGTF remain largely unknown.
It has been proposed that AthSig5 might act as a mediator of blue-light signaling in activating psbD BLRP transcription in blue light (see Section 4.2.3; Tsunoyama et al. 2002; Nagashima et al. 2004b; Tsunoyama et al. 2004), whereas AGF enhances psbD BLRP transcription by constitutively binding to the AAG-box (Shiina et al. 2005). It is assumed that the signal transduction pathway involves reception of blue light by cryptochromes and PhyA (Thum et al. 2001; Mo-chizuki et al. 2004), further mediation by a protein phosphatase PP7 (Moller et al. 2003), and subsequent induction of Sig5 expression (Mochizuki et al. 2004).
Fig. 7. The role of nuclear-encoded phage-type RNA polymerases in regulation of plastidial gene expression. NEP transcription activity is in part represented by a phage-type RNA po-lymerase encoded by the nuclear located RpoTp gene. NEP transcribes and therefore may regulate expression of the plastidial rpoB operon encoding subunits of the plastid-encoded RNA polymerase (PEP). PEP in turn transcribes genes encoding components of the photo-synthetic complexes (PSI, PSII) that regulate nuclear transcription by generating diverse 'plastid signals' (ROS, reactive oxygen species). The trnE gene encoding trnAGlu which is required for the synthesis of 8-aminolevulinic acid (ALA) is also transcribed by PEP (Hess et al. 1992; Walter et al. 1995). ALA is a precursor of the chlorophyll and heme biosynthesis thought to provide 'plastid signals' which influence nuclear transcription. Furthermore, tRNAGlu is assumed to developmentally inhibit NEP transcription by binding to RpoTp (Hanaoka et al. 2005). In turn, the expression and activity of nuclear-encoded, plastid phage-type RNA polymerase regulates the transcription of plastidial genes and consequently the developmental stage of the plastid (RpoTp; Emanuel et al. 2004). Thus, the regulated network of the nuclear and plastidial transcription machineries may be a key element for a concerted expression of genes located within compartments of the plant cell.
After import into plastids, Sig5 associates with AGF (PTF1) and initiates psbD transcription. Furthermore, psbD BLRP activity is also regulated in a developmental and tissue-specific manner, since the Arabidopsis DET1 gene product down-regulates the activity of psbD BLRP in young seedlings (Christopher and Hoffer 1998).
Plastid-to-nucleus signaling. Environmental control of plastidial gene expression is most intense in differentiation from proplastids to either etioplasts (dark) or chloroplasts (light). Analyses of photomorphogenic mutants established the existence of different pathways to communicate light perception to plastids in order to control their development (Leon et al. 1998; Rodermel 2001; Gray et al. 2003; Lopez-Juez and Pyke 2005). However, these analyses also showed that retrograde or 'plastid signals' are controlling nuclear gene expression depending on the developmental status of the plastid (Fig. 7; see Chapter 13; Rodermel 2001; Gray 2003; Beck 2005; Leister 2005; Nott et al. 2006). Both plastid transcription and translation are necessary for the production of a 'plastid signal'. However, it is not an immediate translational product of a plastid gene (Oelmüller et al. 1986; Lukens et al. 1987), but rather part(s) of signal transduction pathways in plastids.
The barley mutant albostrians, with alternating stripes of white and green tissue, contains no detectable ribosomes in plastids of white tissue cells (Siemenroth et al. 1981; Hess et al. 1993). Transcript levels of some photosynthesis-related plastidial and nuclear genes are reduced or missing suggesting the existence of 'plastid signals' controlling nuclear gene expression (Bradbeer et al. 1979; Hess et al. 1994). Recently, transcript levels of the nuclear-encoded RpoTp, which is likely to represent NEP activity, and its plastidial target genes were analyzed throughout the developmental gradient of albostrians leaves (Emanuel et al. 2004). The results revealed a significant influence of the developmental stage of plastids on expression and activity of RpoTp, indicating a plastid-to-nucleus signaling to coordinate expression of plastidial and nuclear-encoded RNA poly-merases as a prerequisite of a concerted gene expression in both plastids and nucleus (Fig. 7).
Redox control of plastid gene expression. Light is not only the energy source for photosynthesis, but also an environmental signal to regulate plant biogenesis and environmental adaptation. Apart from blue/UVA-light, illumination has been early hypothesized to control plastid gene expression via the physiological status of the plastid, e.g., redox conditions (Link 2003; Pfannschmidt and Liere 2005). Redox control of plastidial gene expression has been interpreted as a selection force throughout evolution to retaining their genomes (Allen 1993). First confirmation for such a redox control was obtained by demonstrating that light supported incorporation of radioactive-labeled NADH into the RNA fraction of lettuce plastids (Pearson et al. 1993). Plastidial gene expression is controlled at different levels by photosynthetic activity such as RNA maturation (Deshpande et al. 1997; Liere and Link 1997; Salvador and Klein 1999) and translation (Danon and Mayfield 1994; Bruick and Mayfield 1999; Trebitsh et al. 2000; Zhang et al. 2000). Effects of the redox state on plastidial gene transcription were furthermore demonstrated by growing plants under light conditions generating an imbalance in excitation energy distribution between photosystems (PSII- and PSI-light, 680 and 700 nm, respectively; Pfannschmidt et al. 1999a, 1999b; Fey et al. 2005). Preferential excitation of PSII results in a reduction of the electron transport chain while a preferential excitation of PSI results in its oxidation. The change in photosystem stoichiometry correlated with respective changes in the transcriptional rates and transcript amounts of the plastidial genes for the reaction centre proteins of PSII and PSI, psbA and psaAB. Indeed, the redox state of the plastoquinone pool (PQ) is the major determinant for the changes in gene expression. A reduced PQ pool promotes transcription of the psaAB operon. In reverse, an oxidized PQ pool increases psbA transcription. Opposite regulation of these genes has been recently found also in pea (Tullberg et al. 2000), Chlamydobotrys stellata (Kovacs et al. 2000) and Synechocystis PCC 6803 (Li and Sherman 2000; El Bissati and Kirilovsky 2001) suggesting that this mechanism represents an evolutionary old means of regulating gene expression. These data provide a first model on how plants adapt to light quality gradients occurring in natural environments under low light intensities. Still, the signal transduction pathway connecting the PQ pool with transcription is yet unknown. However, a long-term response may represent an extended branch of the short-term response (the state transition), which is also regulated by the redox state of the PQ pool (Allen and Forsberg 2001; Pursiheimo et al. 2001). The PQ oxidation site at the cyt b6f complex functions as a sensor for the PQ redox state during state transition (Vener et al. 1997; Zito et al. 1999). A putative DNA-binding protein of PS II, TSP9, is partially released from PSII upon PQ reduction in spinach and may represent such a signal transducer towards transcription (Carlberg et al. 2003; Zer and Ohad 2003). Identification of an additional protein of 31 kDa capable of sequence-specific binding between positions + 64 to +83 (region D) of the light dependent psaAB PEP promoter region (Chen et al. 1993; Cheng et al. 1997a) suggests the existence of yet unidentified transcription factors that transmit redox signals. Furthermore, the Arabidopsis high chlorophyll fluorescence mutant hcf145 shows decreased mRNA stability and transcription of psaA (Lezhneva and Meurer 2004). Thus, HCF145 might be involved in transcrip-tional regulation of the psaA operon. Further analysis of this promoter has yet to be reported.
PEP is not only responsible for the redox regulation at the psbA and psaAB promoters, but apparently is also regulated via redox control. A regulatory impact on steady-state levels of transcripts of genes for PEP components was observed by microarray analyses (Fey et al. 2005): rpoB (plastid-encoded ß-subunit), AthSig5 (nuclear-encoded c-factor), and SibI (nuclear-encoded Sig1-binding protein; Morikawa et al. 2002). Interestingly, rpoB is transcribed by a nuclear-encoded phage-type RNA polymerase (Fig. 7, RpoTp; Liere et al. 2004), suggesting a redox regulation of this enzyme (see Chapter 13).
Developmental switch from NEP to PEP. A regulatory role, which links chlorophyll synthesis and the developmental switch from nucleus-encoded RNA po-lymerases to the plastid-encoded bacterial-type enzyme, has been proposed for the plastid-encoded tRNAGlu in Arabidopsis (Hanaoka et al. 2005). tRNAGlu is not only required for translation, but also for synthesis of 8-aminolevulinic acid, a precursor of chlorophyll (Schön et al. 1986). In gel mobility shift experiments recombinant RpoTp specifically bound this tRNA. Additionally, transcription from a putative plastidial accD NEP promoter sequence was inhibited by addition of tRNAGlu to in vitro transcription reactions with proplastid extracts from Arabidop-sis. Hence, the authors suggested tRNAGlu to developmentally inhibit transcription by RpoTp (Fig. 7).
Bacterial-like stringent control. In bacteria, one of the most important processes to regulate gene expression is the so-called 'stringent control' enabling adaptation to nutrient-limiting conditions (Cashel et al. 1996). The effector molecule is guanosine 5'-diphosphate 3'-diphosphate (ppGpp), which binds to the core RNA polymerase modifying its promoter specificity (Toulokhonov et al. 2001). Stress-
induced synthesis is mediated by ppGpp synthetases, RelA and SpoT, homologues of which were found in Chlamydomonas reinhardtii (Kasai et al. 2002), Arabi-dopsis (van der Biezen et al. 2000), and tobacco (Givens et al. 2004). Plastidial targeting has been demonstrated for some of these RSH termed proteins, suggesting an implication in ppGpp signaling in plastids. RSH expression and plastidial ppGpp levels are clearly elevated by light and various abiotic and biotic stress conditions. Furthermore, PEP activity is inhibited by ppGpp in vitro (Givens et al. 2004; Takahashi et al. 2004). Thus, it is conceivable that PEP might indeed be under control of a bacterial-like stringent response mediated by ppGpp. Interestingly, stress signals specifically induce transcription initiation from the psbD BRLP conferred by a special c-factor, AthSig5 (see Section 3.2.3; Nagashima et al. 2004b; Tsunoyama et al. 2004). However, target genes that are regulated by a plastidial stringent control have yet to be identified, which might help to elucidate the molecular mechanisms of transcriptional responses to plant hormones and environmental stress situations.
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