Translation initiation factor 3 families: what are their roles in regulating cyanobacterial and chloroplast gene expression?

Abstract

Initiation is a key control point for the regulation of translation in prokaryotes and prokaryotic-like translation systems such as those in plant chloroplasts. Genome sequencing and biochemical studies are increasingly demonstrating differences in many aspects of translation between well-studied microbes such as Escherichia coli and lesser studied groups such as cyanobacteria. Analyses of chloroplast translation have revealed its prokaryotic origin but also uncovered many unique aspects that do not exist in E. coli. Recently, a novel form of posttranscriptional regulation by light color was discovered in the filamentous cyanobacterium Fremyella diplosiphon that requires a putative stem-loop and involves the use of two different prokaryotic translation initiation factor 3s (IF3s). Multiple (up to five) putative IF3s have now been found to be encoded in 22 % of sequenced cyanobacterial genomes and 26 % of plant nuclear genomes. The lack of similar light-color regulation of gene expression in most of these species suggests that IF3s play roles in regulating gene expression in response to other environmental and developmental cues. In the plant Arabidopsis, two nuclear-encoded IF3s have been shown to localize to the chloroplasts, and the mRNA levels encoding these vary significantly in certain organ and tissue types and during several phases of development. Collectively, the accumulated data suggest that in about one quarter of photosynthetic prokaryotes and eukaryotes, IF3 gene families are used to regulate gene expression in addition to their traditional roles in translation initiation. Models for how this might be accomplished in prokaryotes versus eukaryotic plastids are presented.

Chromatic Acclimation in Cyanobacteria: A Diverse and Widespread Process for Optimizing Photosynthesis

“…The deletion of infCa, but not infCb, resulted in the loss of Cgi regulation of cpeC, suggesting that IF3a plays a role in the Cgi regulation of CA3 (45). The position of IF3 on the 30S subunit of the ribosome may allow interactions with the cpeC 5' leader stem-loop region identified as critical for Cgi system function (84). Interestingly, many plant genomes appear to encode multiple chloroplast-specific IF3s, and two have been confirmed in the model plant Arabidopsis (84).…”

“…The position of IF3 on the 30S subunit of the ribosome may allow interactions with the cpeC 5' leader stem-loop region identified as critical for Cgi system function (84). Interestingly, many plant genomes appear to encode multiple chloroplast-specific IF3s, and two have been confirmed in the model plant Arabidopsis (84). The two genes encoding these IF3s are differentially expressed developmentally and under various environmental conditions.…”

Chloroplast Translation: Structural and Functional Organization, Operational Control, and Regulation

“…Functional chloroplast orthologs were identified for all three IFs (Sijben- Müller et al, 1986;Campos et al, 2001;Miura et al, 2007;Zheng et al, 2016). Interestingly, many plants contain two or more paralogous genes for plastid IF3, whose differential expression was proposed to regulate chloroplast translation initiation (Nesbit et al, 2015). Also similar to the standard bacterial translation initiation, approximately two-thirds of the chloroplast reading frames are preceded by the purine-rich Shine-Dalgarno sequence (SD) (Shine and Dalgarno, 1974;Scharff et al, 2011).…”

Chloroplast translation initiation factors regulate leaf variegation and development

“…In Arabidopsis, two other genes, At4g30690 and At1g34360, also potentially code for prokaryotic IF3-like proteins ( Fig. 4A; Nesbit et al, 2015). Of the three genes, SVR9 and At4g30690 code for putative chloroplast proteins and share the same gene structures, and approximately 78% identities in amino acid sequences ( Fig.…”

“…In contrast, At1g34360 codes for a mitochondrial protein and its gene structure was different from that of SVR9 or At4g30690 ( Fig. 4A; Nesbit et al, 2015). To confirm the chloroplast localizations of SVR9 and SVR9L1, constructs expressing C-terminal GFP fusion proteins SVR9-GFP and SVR9L1-GFP were generated and used to transform Arabidopsis wild-type leaf protoplasts.…”