Molecular mechanisms of RuBisCO biosynthesis in higher plants

Abstract

RuBisCO is a key enzyme catalyzing the CO 2 -fixing reaction in the initial step of the Calvin cycle. However, its enzymatic properties are inadequate for plants because of its small turnover rate of the carboxylase reaction (Harris and Koniger 1997) and its low affinity for CO 2 . Thus, this enzyme limits the rate of carbon assimilation and net photosynthesis (Yokota and Shigeoka 2007). To compensate for its enzymatic inefficiencies, RuBisCO comprises as much as half of leaf total soluble proteins in higher plants, corresponding to 30% of total nitrogen compounds in the leaves. Consequently RuBisCO is regarded as the most abundant protein in the world (Gatenby and Ellis 1990;Makino et al. 2003). Indeed, a decrease in the amount of RuBisCO causes strong inhibition of CO 2 assimilation and subsequent growth retardation (Rodermel et al. 1988;Quick et al. 1991;Hudson et al. 1992;Masle et al. 1993). Therefore, it is important to understand how plants synthesize RuBisCO abundantly and maintain a sufficient amount for growth and development. How is RuBisCO synthesized optimally in plant chloroplasts? Gene expression of nuclear-and chloroplast-encoded subunits of RuBisCORuBisCO functions as an enzyme in the chloroplast stroma with a hexadecameric structure consisting of eight large (LSU) and eight small subunits (SSU). LSUs and SSUs are synthesized through distinct processes as the genes encoding them are individually located on different genomes (Figure 1). SSU is encoded by rbcS in the nuclear genome as a multigene family ranging from 2 to 12 members (Gutteridge and Gatenby 1995). The expression of rbcS is regulated by various endogenous and/or exogenous signals, such as light/dark transition, light quality, circadian rhythm, temperature, atmospheric CO 2 concentration, and nitrogen supply. It is also controlled in an organ-and tissue-specific manner, and by developmental stages (Sugita and Gruissem 1987; Dedondar et al. 1993; Pilgrim and McClung 1993;Gesch et al. 1998;Yoon et al. 2001;Imai et al. 2007). The relationship between rbcS expression and light conditions has been studied well. The signal transduction pathway mediated by phytochrome and the G protein is involved in light-stimulated transcription and light quality-dependent expression pattern of rbcS (Zhou 1999). Dark-induced down-regulation of rbcS expression is regulated by CONSTITUTIVELY MORPHOGENIC/ DE-ETHIOLATED/FUSCA (COP/DET/FUS), which are well known as repressors of photomorphogenesis (Millar et al. 1994). However, cis elements or trans-acting factors involved in the regulation of the rbcS expression response to various endogenous and/or exogenous signals are not well understood.After transcription in the nucleus, rbcS mRNA is translated on 80S ribosomes in the cytosol to synthesize the precursor protein of SSU (PreSSU) with the transit peptide in its N-terminal required for targeting to the chloroplast. The PreSSU is carried to the chloroplast outer membrane by heat shock protein70 (hsp70) and 14- Molecular mechanisms of RuBisCO biosynthesis in hi...

Advancing Our Understanding and Capacity to Engineer Nature’s CO2-Sequestering Enzyme, Rubisco

“…5; Nishimura et al, 2008). In prokaryotes and the plastid genome of nongreen algae, genes for the L-(rbcL) and S-(rbcS) subunits of form I Rubiscos are colocated in an operon.…”

“…A conserved pentatricopeptide repeat protein, MRL1, has recently been identified in Chlamydomonas and Arabidopsis (Arabidopsis thaliana) that specifically binds to the 5# untranslated region of rbcL to stabilize the mRNA and/or ensure correct processing of the transcript (Johnson et al, 2010). The fundamental aspects of rbcL translation and posttranslational processing in chloroplasts also lack detail but appear to show similarities to the bacterial translational machinery (consistent with its prokaryotic ancestry), albeit reliant on nucleus-encoded factors for proper functioning (for review, see Nishimura et al, 2008). Nascent L-subunits are targeted for extensive N-terminal processing (for review, see Houtz et al, 2008) that begins with the deformylation of N-formyl-Met-1 by peptide deformylase and then Met-1 and Ser-2 removal via an uncertain peptidase process, leaving an N-terminal Pro-3 that is acetylated by an unknown a N-acetyltransferase.…”

“…In plastids, it is thought that newly translated L-subunits interact with the general Hsp70 chaperone system (DnaK/DnaJ/GrpE) and the Rubisco-specific chaperone BSDII (for review, see Nishimura et al, 2008). These chaperones prevent misfolding and convey the unfolded L-peptide to the folding cage of the chaperonin-60/21 complexes (plant homologous of the GroEL and GroES Escherichia coli proteins).…”

“…The propensity of plant Rubisco L-subunits to form misfolded, insoluble aggregates in E. coli continues to Nishimura et al (2008). Uncertainties in the biogenesis process are indicated by question marks.…”

Engineering of chimeric eukaryotic/bacterial Rubisco large subunits in <i>Escherichia coli</i>

“…On the other hand, heterologous expression and assembly of cyanobacterial (Synechococcus PCC6301) Rubisco in E. coli is invariably succesful (Goloubinoff et al, 1989;Parikh et al, 2006;Mueller-Cajar and Whitney, 2008). Different but possibly homologous assemblyassisting factors have evolved, which assist with higher plant Rubisco folding and assembly in chloroplasts even though these plastids originated from a cyanobacterial endosymbiont (reviewed in Nishimura et al, 2008).…”