title: Unique role for translation initiation factor 3 in the light color regulation of photosynthetic gene expression.
abstract: Light-harvesting antennae are critical for collecting energy from sunlight and providing it to photosynthetic reaction centers. Their abundance and composition are tightly regulated to maintain efficient photosynthesis in changing light conditions. Many cyanobacteria alter their light-harvesting antennae in response to changes in ambient light-color conditions through the process of chromatic acclimation. The control of green light induction (Cgi) pathway is a light-color-sensing system that controls the expression of photosynthetic genes during chromatic acclimation, and while some evidence suggests that it operates via transcription attenuation, the components of this pathway have not been identified. We provide evidence that translation initiation factor 3 (IF3), an essential component of the prokaryotic translation initiation machinery that binds the 30S subunit and blocks premature association with the 50S subunit, is part of the control of green light induction pathway. Light regulation of gene expression has not been previously described for any translation initiation factor. Surprisingly, deletion of the IF3-encoding gene infCa was not lethal in the filamentous cyanobacterium Fremyella diplosiphon, and its genome was found to contain a second, redundant, highly divergent infC gene which, when deleted, had no effect on photosynthetic gene expression. Either gene could complement an Escherichia coli infC mutant and thus both encode bona fide IF3s. Analysis of prokaryotic and eukaryotic genome databases established that multiple infC genes are present in the genomes of diverse groups of bacteria and land plants, most of which do not undergo chromatic acclimation. This suggests that IF3 may have repeatedly evolved important roles in the regulation of gene expression in both prokaryotes and eukaryotes.
authors.affiliation: Department of Biology and Indiana Molecular Biology Institute, Indiana University, Bloomington, IN, 47405.
authors.forename: Andrian
authors.initials: A
authors.lastname: Gutu
authors.forename: April D
authors.initials: AD
authors.lastname: Nesbit
authors.forename: Andrew J
authors.initials: AJ
authors.lastname: Alverson
authors.forename: Jeffrey D
authors.initials: JD
authors.lastname: Palmer
authors.forename: David M
authors.initials: DM
authors.lastname: Kehoe
mesh_terms: D001483:Base Sequence; D019295:Computational Biology; D000458:Cyanobacteria / Q000502:physiology*; D017931:DNA Primers / Q000235:genetics; D004926:Escherichia coli; D015964:Gene Expression Regulation, Bacterial / Q000502:physiology* / Q000528:radiation effects; D008027:Light; D055537:Light Signal Transduction / Q000235:genetics / Q000502:physiology*; D016013:Likelihood Functions; D008957:Models, Genetic; D008969:Molecular Sequence Data; D005810:Multigene Family / Q000235:genetics*; D010788:Photosynthesis / Q000502:physiology*; D010802:Phylogeny; D039665:Prokaryotic Initiation Factor-3 / Q000235:genetics / Q000378:metabolism*; D017422:Sequence Analysis, DNA; D013045:Species Specificity
chemical_list: D017931:DNA Primers; D039665:Prokaryotic Initiation Factor-3
keywords: phycobilisome; phycocyanin; phycoerythrin; signal transduction
references.citation: J Bacteriol. 1997 Feb;179(4):998-1006
references.pmid: 9023176
references.citation: J Struct Biol. 1998 Dec 15;124(2-3):311-34
references.pmid: 10049814
references.citation: Eur J Biochem. 1997 Oct 15;249(2):564-75
references.pmid: 9370368
references.citation: Science. 1996 Sep 6;273(5280):1409-12
references.pmid: 8703080
references.citation: J Bacteriol. 1994 Mar;176(5):1434-42
references.pmid: 8113185
references.citation: Mol Cell. 1999 May;3(5):601-9
references.pmid: 10360176
references.citation: J Bacteriol. 1989 Jul;171(7):3727-31
references.pmid: 2544553
references.citation: Bioessays. 2002 Aug;24(8):700-7
references.pmid: 12210530
references.citation: Mol Biol Evol. 2011 Nov;28(11):3019-32
references.pmid: 21652613
references.citation: J Bacteriol. 1997 Jun;179(12):3914-21
references.pmid: 9190806
references.citation: Appl Environ Microbiol. 2001 Feb;67(2):991-4
references.pmid: 11157276
references.citation: J Mol Biol. 1975 May 25;94(3):461-78
references.pmid: 1100842
references.citation: Mol Plant. 2012 Jan;5(1):1-13
references.pmid: 21772031
references.citation: Biochemistry. 1975 Apr 22;14(8):1553-9
references.pmid: 1092339
references.citation: Mol Microbiol. 2007 Apr;64(2):319-32
references.pmid: 17381552
references.citation: Mol Gen Genet. 1977 Feb 28;151(1):17-26
references.pmid: 325363
references.citation: Mol Microbiol. 2002 Feb;43(3):749-62
references.pmid: 11929529
references.citation: Biochim Biophys Acta. 2002 Sep 13;1577(2):240-50
references.pmid: 12213655
references.citation: Annu Rev Plant Biol. 2006;57:127-50
references.pmid: 16669758
references.citation: Photosynth Res. 2003;76(1-3):207-15
references.pmid: 16228579
references.citation: J Bacteriol. 2002 Feb;184(4):962-70
references.pmid: 11807056
references.citation: RNA. 2004 Feb;10(2):265-76
references.pmid: 14730025
references.citation: Proc Natl Acad Sci U S A. 2011 Nov 8;108(45):18542-7
references.pmid: 22042852
references.citation: Plant Cell. 2003 Oct;15(10):2448-63
references.pmid: 14508001
references.citation: RNA. 1995 Oct;1(8):772-82
references.pmid: 7493323
references.citation: J Bacteriol. 1977 Apr;130(1):82-91
references.pmid: 856789
references.citation: Nature. 1970 Dec 26;228(5278):1273-5
references.pmid: 4922688
references.citation: J Bacteriol. 1994 Oct;176(20):6362-74
references.pmid: 7929008
references.citation: J Bacteriol. 1994 Mar;176(5):1427-33
references.pmid: 8113184
references.citation: Mol Microbiol. 2005 Mar;55(5):1538-52
references.pmid: 15720559
references.citation: Plasmid. 1983 Sep;10(2):156-63
references.pmid: 6314409
references.citation: Mol Microbiol. 2004 Jan;51(2):567-77
references.pmid: 14756794
references.citation: Plasmid. 1993 Sep;30(2):90-105
references.pmid: 8234495
references.citation: Proc Natl Acad Sci U S A. 2000 Jun 6;97(12):6640-5
references.pmid: 10829079
references.citation: Mol Microbiol. 2008 Apr;68(2):286-97
references.pmid: 18346116
references.citation: BMC Evol Biol. 2011 Jun 30;11:187
references.pmid: 21718514
references.citation: Mol Cell Biol. 1994 Aug;14(8):5268-77
references.pmid: 8035805
references.citation: J Cell Biol. 1994 Dec;127(6 Pt 1):1537-45
references.pmid: 7798310
references.citation: Nucleic Acids Res. 1997 Sep 1;25(17):3389-402
references.pmid: 9254694
references.citation: RNA. 2007 Aug;13(8):1355-65
references.pmid: 17592046
references.citation: Proc Natl Acad Sci U S A. 1992 Oct 15;89(20):9415-9
references.pmid: 1409650
references.citation: Mol Microbiol. 2002 Jun;44(6):1517-31
references.pmid: 12067341
references.citation: Crit Rev Biochem Mol Biol. 2012 Jul-Aug;47(4):334-48
references.pmid: 22515367
references.citation: Microbiol Mol Biol Rev. 2005 Mar;69(1):101-23
references.pmid: 15755955
references.citation: Nucleic Acids Res. 2004 Mar 19;32(5):1792-7
references.pmid: 15034147