Abstract
The transcription of photosynthesis genes encoded by the plastid genome is mainly mediated by a prokaryotic-type RNA polymerase called plastid-encoded plastid RNA polymerase (PEP). Standard PEP-dependent promoters resemble bacterial sigma-70-type promoters containing the so-called -10 and -35 elements. On the other hand, an unusual light- and stress-responsive promoter (psbD LRP) that is regulated by a 19-bp AAG-box immediately upstream of the -35 element has been mapped upstream of the psbD-psbC operon in some angiosperms. However, the occurrence of the AAG-box containing psbD LRP in plant evolution remains elusive. We have mapped the psbD promoters in eleven embryophytes at different evolutionary stages from liverworts to angiosperms. The psbD promoters were mostly mapped around 500–900 bp upstream of the psbD translational start sites, indicating that the psbD mRNAs have unusually long 5′-UTR extensions in common. The -10 elements of the psbD promoter are well-conserved in all embryophytes, but not the -35 elements. We found that the AAG-box sequences are highly conserved in angiosperms and gymnosperms except for gnetaceae plants. Furthermore, partial AAG-box-like sequences have been identified in the psbD promoters of some basal embryophytes such as moss, hornwort, and lycophyte, whereas liverwort has the standard PEP promoter without the AAG-box. These results suggest that the AAG-box sequences of the psbD LRP may have evolved from a primitive type of AAG-box of basal embryophytes. On the other hand, monilophytes (ferns) use another type of psbD promoter composed of a distinct cis-element upstream of the potential -35 element. Furthermore, we found that psbD expression is not regulated by light in gymnosperms or basal angiosperms, although they have the well-conserved AAG-box sequences. Thus, it is unlikely that acquisition of the AAG-box containing psbD promoter is directly associated with light-induced transcription of the psbD-psbC operon. Light- and stress-induced transcription may have evolved independently and multiple times during terrestrial plant evolution.
Highlights
Chloroplasts in plant and algal cells are semiautonomous organelles that have their own genome and gene expression system, reflecting their cyanobacterial origin
Unlike standard PEP-dependent promoters composed of sigma-70 type −10 (TATAAT) and −35 (TTGACA) elements, it has been shown that psbD LRP activity is dependent on the upstream AAG-box in tobacco (Allison and Maliga, 1995), barley (Kim and Mullet, 1995), rice (To et al, 1996), and wheat (Nakahira et al, 1998; Figure 1A)
The −35 element of the psbD LRP is not essential for transcription activity (To et al, 1996; Nakahira et al, 1998; Kim et al, 1999; Thum et al, 2001b). These findings suggest that the upstream AAG-box may take over the role of the pseudo −35 element in the psbD LRP
Summary
Chloroplasts in plant and algal cells are semiautonomous organelles that have their own genome and gene expression system, reflecting their cyanobacterial origin. Chloroplast transcription is mediated by two distinct RNA polymerase systems, a prokaryotic multi-subunit RNA polymerase (PEP) whose core subunits are encoded by chloroplast genomes and single-subunit. The PEP core enzyme consists of four major subunits, designated as α, β, β , and β ” subunits, which are homologous to bacterial subunits. Another dissociable subunit called a sigma factor allows the core enzyme to initiate transcription from the specific promoters. The functional coordination of PEP and NEP plays a critical role in plastid differentiation in angiosperms
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