The regulation of expression of the genes encoding the large subunit (LSU) and small subunit (SSU) of ribulose 1,5-bisphosphate carboxylase (RuBPCase) was examined in 1-through 8-day-old, dark-grown (etiolated) and light-grown amaranth cotyledons. RuBPCase specific activity in light-grown cotyledons increased during this 8-day period to a level 15-fold higher than in dark-grown cotyledons. Under both growth conditions, the accumulation of the LSU and SSU polypeptides was not coordinated. Initial detection of the SSU occurred 1 and 2 days after the appearance of the LSU in light-and dark-grown cotyledons, respectively. Furthermore, although the levels of the LSU were similar in both light-and dark-grown seedlings, the amount of the SSU followed clearly the changes in enzyme activity. Synthesis of these two polypeptides was dramatically different in etiolated versus light-grown cotyledons. In light the synthesis of both subunits was first observed on day 2 and continued throughout the growth of the cotyledons. In darkness the rate of synthesis of both subunits was much lower than in light and occurred only as a burst between days 2 and 5 after planting. However, mRNAs for both subunits were present in etiolated cotyledons at similar levels on days 4 through 7 (by Northern analysis) and were functional in vitro, despite their apparent inactivity in vivo after day 5. In addition, since both LSU and SSU mRNA levels were lower in dark-than in light-grown seedlings, our results indicate that both transcriptional and post-transcriptional controls modulate RuBPCase production in developing amaranth cotyledons.Ribulose 1,5-bisphosphate carboxylase (RuBPCase) is located in the chloroplasts of all higher plants and is the primary enzyme of photosynthetic carbon fixation. This enzyme has a molecular weight of about 550,000 and consists of eight large (51-to 58-kilodalton [kDa]) and eight small (12-to 18-kDa) subunits (46
Within the chloroplasts of higher plants and algae, photosynthesis converts light into biological energy, fueling the assimilation of atmospheric carbon dioxide into biologically useful molecules. Two major steps, photosynthetic electron transport and the Calvin-Benson cycle, require many gene products encoded from chloroplast as well as nuclear genomes. The expression of genes in both cellular compartments is highly dynamic and influenced by a diverse range of factors. Light is the primary environmental determinant of photosynthetic gene expression. Working through photoreceptors such as phytochrome, light regulates photosynthetic genes at transcriptional and posttranscriptional levels. Other processes that affect photosynthetic gene expression include photosynthetic activity, development, and biotic and abiotic stress. Anterograde (from nucleus to chloroplast) and retrograde (from chloroplast to nucleus) signaling insures the highly coordinated expression of the many photosynthetic genes between these different compartments. Anterograde signaling incorporates nuclear-encoded transcriptional and posttranscriptional regulators, such as sigma factors and RNA-binding proteins, respectively. Retrograde signaling utilizes photosynthetic processes such as photosynthetic electron transport and redox signaling to influence the expression of photosynthetic genes in the nucleus. The basic C3 photosynthetic pathway serves as the default form used by most of the plant species on earth. High temperature and water stress associated with arid environments have led to the development of specialized C4 and CAM photosynthesis, which evolved as modifications of the basic default expression program. The goal of this article is to explain and summarize the many gene expression and regulatory processes that work together to support photosynthetic function in plants.
All living cells possess adaptive responses to environmental stress that are essential to ensuring cell survival. For motile organisms, this can culminate in avoidance or attractile behavior, but for sessile organisms such as plants, stress adaptation is a process of success or failure within the confines of a given environment. Nearly all bacterial species possess a highly evolved system for stress adaptation, known as the "stringent response." This ancient and ubiquitous regulatory response is mediated by production of a second messenger of general stress, the nucleotide guanosine-3 ,5 -(bis)pyrophosphate (ppGpp), which mediates reprogramming of the global transcriptional output of the cell. Accumulation of ppGpp is stress-induced through the enzymatic activation of the well known bacterial ppGpp synthetases, RelA and SpoT. We have recently discovered homologues of bacterial relA/spoT genes in the model plant Nicotiana tabacum. We hypothesize that these homologues (designated RSH genes for RelA/SpoT homologues) serve a stress-adaptive function in plants analogous with their function in bacteria. In support of this hypothesis, we find 1) inducibility of tobacco RSH gene expression following treatment with jasmonic acid; 2) bona fide ppGpp synthesis activity of purified recombinant Nt-RSH2 protein, and 3) a wide spread distribution of RSH gene expression in the plant kingdom. Phylogenetic analyses identifies a distinct phylogenetic branch for the plant RSH proteins with two subgroups and supports ancient symbiosis and nuclear gene transfer as a possible origin for these stress response genes in plants. In addition, we find that Nt-RSH2 protein co-purifies with chloroplasts in subcellular fractionation experiments. Taken together, our findings implicate a direct mode of action of these ppGpp synthetases with regard to plant physiology, namely regulation of chloroplast gene expression in response to plant defense signals.The relA and spoT genes in bacteria encode enzymes that synthesize the unusual nucleotide guanosine-3Ј,5Ј-(bis)pyrophosphate (ppGpp), 1 which is a second messenger of the socalled "stringent response" to nutrient deprivation and environmental stress. ppGpp is the intracellular effector of the stringent response, which acts by binding directly to and inducing allosteric modification of the bacterial RNA polymerase (RNAP) (1). This results in global reprogramming of the bacterium's transcriptional activity. There is a general inhibition of transcription and halting of the production of components of the protein synthesis apparatus in order to conserve energy. Simultaneously, there is an induction of stress genes to ensure proper cell adaptation and survival (2). Until recently, it was believed that the stringent response was limited to the bacterial domain of the prokaryote kingdom; however, plant homologues to these bacterial stress enzymes were recently identified (3, 4). In Arabidopsis thaliana, a relA/spoT homologue At-RSH1 was discovered in a yeast two-hybrid system using a disease resistance p...
Salicylic acid (SA) treatment has recently been reported to inhibit replication of tobacco mosaic virus (TMV) in inoculated tissue. Furthermore, resistance is induced via a novel defensive signal transduction pathway sensitive to inhibition by salicylhydroxamic acid (SHAM; S. Chivasa, A. M. Murphy, M. Naylor, and J. P. Carr, Plant Cell 9: 547–557, 1997). The goals of this study were to determine if replication of viruses other than TMV could be inhibited by SA and, if so, whether the resistance to other viruses could also be prevented by SHAM. Potato virus X (PVX) RNA accumulation in inoculated tobacco leaf tissue was reduced by SA treatment and resistance was dependent on the SHAM-sensitive signaling pathway. However, although symptoms of cucumber mosaic virus (CMV) infection were delayed in SA-treated tobacco plants, this was not due to inhibition of replication but rather to inhibition of systemic movement of the virus. 14CO2-feeding experiments indicated that SA-induced interference with long-distance virus movement is not a by-product of disrupted photosynthate translocation. Significantly, SA-induced resistance to CMV was abolished by SHAM. Thus, the SHAM-sensitive signaling pathway activates both resistance mechanisms: inhibition of long-distance CMV movement and inhibition of TMV and PVX replication.
Communicated by C. S. Levings III, February 19, 1988 ABSTRACT When light-grown seedlings of amaranth are transferred to total darkness, synthesis of the large subunit (LS) and small subunit (SS) of ribulose-1,5-bisphosphate carboxylase [RbuP2Case; 3-phospho-D-glycerate carboxylase (dimerizing), EC 4.1.1.39] is rapidly depressed. This reduction in RbuP2Case synthesis occurs in the absence of any corresponding changes in levels of functional mRNA for either subunit. Four hours after light-to-dark transition little, if any, changes in the distribution of LS and SS mRNAs on polysomes could be detected. The association of these mRNAs with polysomes was authenticated by treatment with RNase A or puromycin. Furthermore, polysomes were able to synthesize LS and SS precursor in cell-free translation systems supplemented with inhibitors of 'initiation. Therefore, during a light-to-dark transition LS and SS mRNAs remained bound to polysomes but were not translated in vivo, suggesting that control is exercised, in part, at the translational elongation step.Ribulose-1,5-bisphosphate carboxylase [RbuP2Case; 3-phospho-D-glycerate carboxylase (dimerizing), EC 4.1.1.39] is found in the chloroplasts of all higher plants and is a principal enzyme in photosynthetic carbon fixation. This enzyme has a molecular mass of -555,000 and consists of eight large (51-58 kDa) and eight small (12-18 kDa) subunits (LS and SS, respectively) (1), with the active site located on the LS (2, 3). The LS is encoded on the chloroplast genome and translated on 70S chloroplast ribosomes (4, 5). The SS is encoded in the nucleus and translated on free, cytoplasmic ribosomes as a 20-kDa precursor (6-8). The precursor is processed to its final size during transport into the chloroplast, where it assembles with LS polypeptides to form the active holoenzyme.The control of RbuP2Case production and activity in a number of plant species is very complex, with regulation occurring at many levels. Control at the level of LS or SS mRNA accumulation has been well documented (9). In several cases alterations in transcriptional activity have been shown to be responsible for these changes in mRNA levels (9). At the other end of the spectrum, regulation at the posttranslational level via turnover of the protein (10) as well as by activation (1, 11) or inhibition (12) of the enzyme's activity has also been reported.We have previously described the effects of environmental (light) (13,14) or developmental (13, 15) signals on the expression of LS and SS genes in the C4 dicotyledonous plant Amaranthus hypochondriacus. The expression of these genes is regulated not only at the level of mRNA accumulation but also posttranscriptionally. In amaranth cotyledons rapid and dramatic alterations in the synthesis of the LS and SS polypeptides occur in response to changes in illumination without corresponding changes in mRNA levels. Because the stability of these polypeptides and the functionality in vitro of their respective mRNAs were not affected by alterations in illumination, th...
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