title: Nucleus-independent control of the rubisco operon by the plastid-encoded transcription factor Ycf30 in the red alga Cyanidioschyzon merolae.
abstract: Chloroplasts originated from a cyanobacterium, which was engulfed by a primitive eukaryotic host cell. During evolution, chloroplasts have largely lost their autonomy due to the loss of many genes from their own genomes. Consequently, expression of genes encoded in the chloroplast genome is mainly controlled by the factors transferred from the cytosol to chloroplasts. However, chloroplast genomes of glaucophytes and red algae have retained some transcription factors (hypothetical chloroplast open reading frame 27 to 30 [Ycf27-Ycf30]) that are absent from green algae and land plants. Here, we show that the red algal chloroplast up-regulates transcription of the Rubisco operon rbcLS-cbbX via Ycf30 independently of nuclear control. Light-induced transcriptional activation of the Rubisco operon was observed in chloroplasts isolated from the red alga Cyanidioschyzon merolae. The activation was suppressed by 3-(3,4-dichlorophenyl)-1,1-dimethylurea. These results suggest that chloroplast autonomously regulates transcription of the Rubisco operon in response to the activation of photosynthesis driven by the light. Transcriptional activation of the Rubisco operon was specifically repressed by the addition of anti-Ycf30 antibodies. Furthermore, reduced NADP, ribulose-1,5-bisphosphate, and 3-phosphoglyceric acid triggered the up-regulation of Rubisco transcription in the dark, and the activation was dependent on Ycf30. Thus, red algal chloroplasts have retained a nucleus-independent transcriptional regulation of the Rubisco operon to respond to environmental changes. The autonomous system would have been necessary for the initial fixation of cyanobacterial photosynthesis in the ancient nonphotosynthetic eukaryotic host. It has remained functional in the red algal chloroplast over evolutionary time.
authors.affiliation: Initiative Research Program, Advanced Science Institute, RIKEN, Wako, Saitama, Japan.
authors.forename: Ayumi
authors.initials: A
authors.lastname: Minoda
authors.forename: Andreas P M
authors.initials: AP
authors.lastname: Weber
authors.forename: Kan
authors.initials: K
authors.lastname: Tanaka
authors.forename: Shin-ya
authors.initials: SY
authors.lastname: Miyagishima
mesh_terms: D002467:Cell Nucleus / Q000378:metabolism; D002736:Chloroplasts / Q000235:genetics; D018506:Gene Expression Regulation, Plant; D008027:Light; D009876:Operon; D010940:Plant Proteins / Q000235:genetics / Q000378:metabolism*; D011401:Promoter Regions, Genetic; D000461:Rhodophyta / Q000235:genetics* / Q000378:metabolism; D012273:Ribulose-Bisphosphate Carboxylase / Q000235:genetics / Q000378:metabolism*; D014157:Transcription Factors / Q000235:genetics / Q000378:metabolism*; D015533:Transcriptional Activation
chemical_list: D010940:Plant Proteins; D014157:Transcription Factors; D012273:Ribulose-Bisphosphate Carboxylase
references.citation: Plant Cell Physiol. 2010 May;51(5):707-17
references.pmid: 20375110
references.citation: Mol Microbiol. 2008 Apr;68(1):98-109
references.pmid: 18312274
references.citation: Mol Biol Evol. 2008 Apr;25(4):748-61
references.pmid: 18222943
references.citation: J Bacteriol. 2004 Dec;186(23):8026-35
references.pmid: 15547275
references.citation: Plant Cell Physiol. 2004 Jun;45(6):667-71
references.pmid: 15215501
references.citation: Plant J. 2009 Sep;59(5):826-39
references.pmid: 19453453
references.citation: Science. 1995 Jun 16;268(5217):1622-4
references.pmid: 7777861
references.citation: J Biol Chem. 1978 Dec 25;253(24):8949-56
references.pmid: 363713
references.citation: DNA Res. 2005;12(2):151-6
references.pmid: 16303746
references.citation: PLoS Genet. 2010 Feb 26;6(2):e1000827
references.pmid: 20195500
references.citation: Curr Biol. 2005 Jul 26;15(14):1325-30
references.pmid: 16051178
references.citation: Nature. 2004 Apr 8;428(6983):653-7
references.pmid: 15071595
references.citation: Arch Microbiol. 2002 Aug;178(2):85-93
references.pmid: 12115053
references.citation: Plant Cell. 1998 Oct;10(10):1713-22
references.pmid: 9761797
references.citation: Proc Natl Acad Sci U S A. 2008 Jul 22;105(29):10061-6
references.pmid: 18632566
references.citation: Plant Physiol. 2008 Nov;148(3):1487-96
references.pmid: 18799657
references.citation: J Bacteriol. 1998 Aug;180(16):4080-8
references.pmid: 9696753
references.citation: Nature. 1998 May 14;393(6681):162-5
references.pmid: 11560168
references.citation: Proc Biol Sci. 2009 Jun 22;276(1665):2133-45
references.pmid: 19324807
references.citation: Planta. 1999 Sep;209(3):371-5
references.pmid: 10502105
references.citation: Annu Rev Microbiol. 1993;47:597-626
references.pmid: 8257110
references.citation: Mol Biol Evol. 1996 Jul;13(6):873-82
references.pmid: 8754222
references.citation: Mol Microbiol. 2001 Jan;39(2):455-68
references.pmid: 11136465
references.citation: BMC Mol Biol. 2008 Apr 29;9:43
references.pmid: 18442420
references.citation: Plant Physiol. 1979 Nov;64(5):880-3
references.pmid: 16661074
references.citation: Plant Physiol. 1986 Mar;80(3):655-9
references.pmid: 16664680
references.citation: Plant Cell. 1990 Aug;2(8):795-803
references.pmid: 2152128
references.citation: Mol Biol Evol. 2000 Apr;17(4):576-83
references.pmid: 10742049
references.citation: Genes Genet Syst. 2008 Apr;83(2):135-42
references.pmid: 18506097
references.citation: Plant Mol Biol. 2005 Oct;59(3):375-85
references.pmid: 16235106
references.citation: J Bacteriol. 1998 Mar;180(6):1411-7
references.pmid: 9515907
references.citation: Proc Natl Acad Sci U S A. 1993 Feb 15;90(4):1556-60
references.pmid: 8434017
references.citation: J Exp Bot. 2008;59(11):3009-18
references.pmid: 18611912
references.citation: Genes Genet Syst. 2008 Apr;83(2):127-33
references.pmid: 18506096
references.citation: Plant Mol Biol. 1993 Jan;21(1):27-38
references.pmid: 7678762