Lack of conservation of bacterial type promoters in plastids of Streptophyta
© Lyubetsky et al; licensee BioMed Central Ltd. 2010
Received: 20 April 2010
Accepted: 10 May 2010
Published: 10 May 2010
We demonstrate the scarcity of conserved bacterial-type promoters in plastids of Streptophyta and report widely conserved promoters only for genes psaA, psbA, psbB, psbE, rbcL. Among the reasonable explanations are: evolutionary changes of sigma subunit paralogs and phage-type RNA polymerases possibly entailing the loss of corresponding nuclear genes, de novo emergence of the promoters, their loss together with plastome genes; functional substitution of the promoter boxes by transcription activation factor binding sites.
This article was reviewed by Dr. Arcady Mushegian, and by Dr. Alexander Bolshoy and Dr. Yuri Wolf (both nominated by Dr. Purificación López-García).
Genes evolve at different rates. Various hypotheses try to explain, or at least to correlate, the evolutionary rate (sequence conservation) and the functional properties of the protein-coding gene. As far as we know, there is no published evidence on searching for the plastid promoters at the genome scale. This problem should probably be addressed separately for nuclear, plastome and mitochondrial genomes, different taxonomic lineages and different RNA polymerase types. In particular, multisubunit RNA polymerase (PEP), which has the core enzyme encoded in plastome and the sigma subunit in nucleome, binds bacterial type promoters (PEP-promoters); and monosubunit RNA polymerases (NEP), which is nucleome-encoded, binds NEP-promoters. Here we report a study of PEP-promoters of plastome genes in representatives of the green line (Viridiplantae, including Chlorophyta and Streptophyta; Euglenozoa, Rhizaria, in particular Cercozoa; Glaucocystophyceae) and the red line (Rhodophyta, stramenopiles, including Bacillariophyta, Pelagophyceae, Raphidophyceae, Xanthophyceae; Cryptophyta, Haptophyceae, Apicomplexa). Add. file 1 describes the complete list of studied species with plastids, organized according to the NCBI Taxonomy. Plastid genes are believed to be evolutionarily conserved across large taxonomic lineages [, section 9.7c], although the authors are unaware of systematic studies on their promoters conservation. Instead, there is ample published research on the promoter comparisons within small lineages, largely the studies of the promoters and their transcription factors in gamma- and alpha-proteobacteria . Further, some pairs of closely related species have been shown to possess largely diverged promoters [3, 4]. We have reported an evolutionary labile promoter for the ndhF gene in a narrow lineage of dicotyledonous angiosperm plants and described four different promoter types, which are likely to have replaced each other during evolution .
In this study we aimed at searching for widely conserved PEP-promoters in plastomes of the above mentioned taxa. By "widely conserved" we mean the cases when the regions upstream of orthologous genes across the high-level taxonomic divisions can be aligned. The promoters confined to only vascular plants or the red line lineages are not examined here (e.g., the NEP-promoter of gene clpP in vascular plants). In our analyses using the fixed consensus as a query produced massive under-predictions, or, alternatively, massive over-predictions, which suggests that querying without taking into account the alignment of 5'-leader regions is obviously misleading.
Materials and methods
The regions of up to 1000 bp length upstream from all protein-coding genes (90 genes per species at average) in plastomes of species listed in Additional file 1 were extracted from GenBank, and multiple alignments of the regions were constructed. Searches of promoters were conducted using two original algorithms: the first to pre-select leader regions with candidate PEP-promoters (several candidates were found per region), and the second to build a multiple alignment keeping one of the candidate promoters in each of the regions. The alignment was constructed to reveal the two bacterial type boxes and cover the taxonomic diversity of the above mentioned lineages as wide as possible. In a positive prediction, the alignment of the boxes, linker and some flanking regions was required to have a good quality (see below). Otherwise, a negative prediction is produced and a PEP-promoter is not detected with our method. Evidently "positive prediction" means the prediction of a PEP-promoter and "negative prediction" means the lack of positive prediction. Notably, the positive predictions contained experimentally proved PEP-promoters and often their TG-extensions, which indicates that these are not false positives. Also, in all negative predictions the alignment had a considerably lower quality compared to the minimal quality among all positive predictions. All predicted PEP-promoters were located within approximately 40 bp-long highly conserved regions flanked by less conserved 3'-areas and highly variable 5'-areas.
The idea of the first algorithm. Given is a set of n leader regions. The goal is to find a subset of the set with one potential promoter in each region such that their total pair-wise similarity is maximal comparing to any other collection of potential promoters in that subset; the subset size is simultaneously maximized. In order to increase search speed, randomly selected regions are set as "linked" and the promoter similarity is estimated only within the linked pairs of regions. It formally means that we consider a graph with n vertices, each assigned a leader region, but only linked regions are connected by an edge in the graph. As a result, the complexity of comparing all pairs of candidate promoters to determine their total similarity is reduced in our algorithm by means of considering a large number of randomly defined sets of edges, i.e. randomly constructed graphs with n vertices assigned the same regions but connected by different edges. By doing so, the computing time becomes square to number n of the regions and cubic to their average length. The algorithm is designed for effective parallelization to enable mass processing of large amounts of long regions in feasible time. The enhanced performance of the parallel implementation allows to compute a solution closer to the maximum quality of the alignment. The algorithm is highly scalable and provides for the approximately linear growth of performance with the number of available processors up to 2000.
The idea of the second algorithm. Along a fixed phylogenetic species tree, the algorithm aligns leader regions with respect to one of the candidate promoters selected by the first algorithm, from the promoter start up to the start codon. It uses a common observation that promoters, as well as transcribed regions, can be well aligned, in contrast to the region upstream of the promoter. The algorithm takes a non-binary (which is often the case) species tree and during the run reduces it to a binary tree in a variety (or even all) possible ways. Each leaf of the tree bears an orthologous gene leader region from the corresponding species. The alignment is constructed as follows. First, each leaf is assigned a nucleotide frequency distribution at each position of the sequence: the distribution contains a unity for the observed nucleotide type and three zeros for the unobserved. A zero distribution contains four zeros. Then, at each inner node, two distribution sequences at its descendant nodes are aligned by any applicable algorithm, with an award for matching two distributions not pre-defined, but calculated anew at each position j taking into account the length of each descendant branch. The award is estimated as a scalar square of the difference between two nonzero distributions weighted for different nucleotide types. The penalty for inserting a gap symbol (i.e., for the alignment of zero and nonzero distributions) is a decreasing function of the number of contiguous gaps: the longer the gap region, the lower the penalty. Two zero distributions are forbidden to align. At each position of the alignment, the distribution in the ancestral sequence is a half-sum of the two distributions in the descendants. When the root distribution sequence is constructed, the algorithm projects the gaps along the tree to its leaves onto the extant sequences, thus obtaining the final multiple alignment. The complexity is linear to the number of leaves. Different binary tree resolutions are compared on the basis of the corresponding alignment quality, which is estimated as follows: , where N a is the number of totally conserved (containing the same character) single columns, N s - the number of totally conserved regions (two or more contiguous totally conserved columns, l i is the number of columns), N b - the number of "nearly" conserved columns (with one non-matching character); b, c and s are parameters. Computing an alignment of 16 sequences with the length of 120-223 bases requires less than one second on a 3 GHz Pentium-4 PC. The automatically computed alignments were manually checked and minor corrections were introduced if so required. Both algorithms are implemented as 32-bit command line utilities written in ANSI C, which can be compiled with many popular compilers and run under Windows or Linux. The algorithms and their detailed descriptions are available from [6, 7].
Estimated coordinates of the transcription initiation sites of the predicted PEP-promoters
Gene psbE(photosystem II cytochrome b559 protein alpha subunit) in plastomes of Streptophyta. Promoters were predicted in most land plants and the algae Chaetosphaeridium globosum, Staurastrum punctulatum, Zygnema circumcarinatum, ref. to Fig. 1, psbE. Negative predictions were obtained for the algae Chara vulgaris, Chlorokybus atmophyticus and Mesostigma viride, even though the region is conserved in their closer relatives. This gene is a pseudogene in the Aneura mirabilis plastome.
Gene rbcL(the large subunit of ribulose-1,5-bisphosphate carboxylase) in plastomes of Streptophyta. The promoter was experimentally characterized in spinach (S. oleracea) , and mustard (Sinapis alba) . It was predicted in all land plants and in the streptophyte algae Chaetosphaeridium globosum, Chara vulgaris, Staurastrum punctulatum, Zygnema circumcarinatum, ref. to Fig. 1, rbcL.
Gene psaA(apoprotein A1 of photosystem I P700) in plastomes of Streptophyta. Promoter and the transcription initiation site for this gene were experimentally characterized in Arabidopsis thaliana . In Aneura mirabilis it is a pseudogene. The promoter was predicted in almost all land plants and streptophyte algae, except for Chlorokybus atmophyticus and Mesostigma viride, see Fig. 1, psaA. This promoter differs from all other predictions and the bacterial σ-70 promoter. Its "-10" box consensus is CATAAT, which differs from the bacterial type at the first position. At the 5'-end of the box a conserved putative extension is found with the consensus TrTGT. The predicted "-35" box is even more divergent from its counterparts, despite being located within a long conserved region.
Although the alignments shown Fig. 1 are unambiguous within the lineages, neither can be extended onto the Euglenozoa, Chlorophyta, Rhodophyta, Cryptophyta, diatom and other algae with plastids similar to those of the Rhodophyta, see add. file 1.
Normally, the entire promoter region, not only the boxes, is more conserved comparing to the rest of the leader region, which hampers distinguishing between regulated and non-regulated promoters.
We illustrate the comparison between wide and local conservations on the PEP-promoters of genes ycf1, rps4 and psaJ. The promoters were experimentally identified in Arabidopsis thaliana. These genes are among the 85 protein-coding genes in the plastome of A. thaliana. They are not widely conserved.
The ycf1 gene encodes an unknown function protein and has PEP-promoter ycf1-34 with a smaller distance between the "-35" and "-10" boxes than normally . This promoter overlaps with NEP-promoter ycf1-39. PEP-promoters very similar to ycf1-34 with unambiguous multiple alignments of the 5'-UTR regions are found in most eudicotyledonous, magnoliid and basal magnoliophyte plants. Some species (including Cucumis sativus) possess a much longer 5'-UTR region, while in others (including Ranunculus macranthus) the ycf1 PEP-promoter is not found. In monocotyledonous (Liliopsida), gymnosperm and pteridophyte plants possessing the ycf1 gene, its putative PEP-promoters are found but differ considerably from those in eudicotyledons, magnoliids and the basal Magnoliophyta. The promoter in A. thaliana is most similar to that from the cycadophyte Cycas taitungensis.
In A. thaliana the gene rps4 encoding ribosomal protein S4 has PEP-promotor rps4-123 . Similar promoters with unambiguous 5'-UTR multiple alignment are found only in selected species of Brassicaceae: Arabis hirsuta, Barbarea verna, Crucihimalaya wallichii, Draba nemorosa, Lepidium virginicum, Lobularia maritima, Nasturtium officinale and Olimarabidopsis pumila. The plastomes of B. verna, D. nemorosa, L. maritima and O. pumila contain single nucleotide insertions in between the boxes;Arabis hirsute has a single nucleotide deletion. The promoter region is variable even across close species (Aethionema cordifolium, A. grandiflorum, Carica papaya, Citrus sinensis) but their 5'-UTR regions can still be well aligned.
A. thaliana was experimentally found to possess a Sig2-dependent promoter upstream of gene psaJ encoding photosystem I active center subunit IX, with a 37 nucleotide-long 5'-UTR . Although well aligned across all eurosids II, its 5'-UTR regions are conserved only within Brassicaceae and diverge already in C. papaya.
Conserved promoters are found in the monophyletic Streptophyta and in two distant species, B. natans and C. paradoxa. Notably, even though B. natans belongs to the Cercozoa, its plastome is similar to that of green algae . On the contrary, the plastome of C. paradoxa is different in many respects [19, 20].
There are many reasons why PEP-promoters upstream of the protein-coding plastome genes are scarce. Their loss may be related to the evolutionary changes of sigma subunit paralogs and phage-type RNA polymerases that lead to rapid replacements of the PEP-promoter. Indeed, the PEP sigma subunits vary already between maize, poplar and thale cress: e.g., maize possesses two Sig2 paralogs and lacks Sig4, while in poplar sig4 is a pseudogene, and thale cress possesses a Sig4 and only one Sig2, . Also, promoters can be lost with their nuclear sigma subunit-encoding genes, such as the Sig4-dependent ndhF promoter in poplar . Some dicotyledonous plants, including Arabidopsis and Nicotiana, have gained the additional phage-type RNA polymerase RpoTmp, which is active in chloroplasts and mitochondria of these plants but is missing from monocotyledonous plants (unpublished dissertation by K. Kühn, 2006). Only one phage-type RNA polymerase, RpoTp, is known from plastids of monocots (Zea, Triticum), two phage-type RNA polymerases - from plastids of dicots (Arabidopsis, Nicotiana): RpoTp in chloroplasts and RpoTmp in both chloroplasts and mitochondria. The moss Physcomitrella patens also has two phage-type polymerases, RpoT1 and RpoT2, which target both chloroplasts and mitochondria . Promoters can emerge de novo, as has been shown, e.g., for the ndhF promoter . Others are lost together with plastome genes, e.g., the chlL promoter in flowering and some other plants (according to the GenBank records). Another possible factor in rapid promoter turnover in plastids may be tissue-specific differentiation of plastid types, especially in vascular and, particularly, flowering plants, which evolved a rich diversity of sigma subunits  and phage type RNA polymerases. Often the promoter boxes are functionally substituted by the transcription activation factor binding sites .
In parasitic, non-photosynthesizing plants, such as dicotyledonous dodder (Cuscuta spp.) and liverwort Aneura mirabilis, many chloroplast genes are pseudogenes  and promoters of these genes are lost too. The promoter conservation might become lower in the presence of alternative promoters. The promoter might have undergone rapid evolution [3, 5] and become unrecognizable. It also might be located beyond the 1000 bp distance from the start codon and thus be overlooked in our analyses.
Given these multiple reasons to expect fast evolution and rapid turnover of the chloroplast promoters, one may ask why some of them, such as the five promoters described above, are so widely conserved? One possible explanation is that three of the conserved promoters regulate the expression of the photosystem components and that the stability of the promoter structure is important to maintain high expression of genes psbA, psbB, psaA; due to the light-dependent translation regulation of psbA, a high amount of mRNA is built up in the dark and translated under light . Conserved promoters upstream of psbA and psaA may also be required to form polycistronic mRNAs, which encode, along with the photosystem components, tRNA and proteins involved in translation that also have to be expressed at high levels: psbA appears to belong to the same operon as histidine tRNA, while psaAB and rps14 are in an operon with methionine tRNA. The psbEFLJ operon and psbBTHpetBD operon might be formed likewise. The other conserved promoter regulates rbcL, the large subunit of a key enzyme involved in the carbon dioxide fixation during the Calvin cycle, the most abundant enzyme in the biosphere, whose gene also must be highly expressed. When a gene is highly transcribed and regulated by a single promoter, the selection pressure prevents any considerable change in the promoter's structure to provide for its effective binding to the polymerase.
Relatively lower conservation of the PEP-promoters of housekeeping genes (viz., tRNA, rRNA, ribosomal protein and PEP subunit-encoding genes, etc.) might be explained by the presence of NEP transcription: e.g., the rpoB transcription is entirely NEP-mediated, although most genes possess both PEP and NEP-promoters. This is the case of the ycf1 and clpP genes, which were experimentally shown in Arabidopsis thaliana to be under several promoters recognized by PEP with different subunits and two NEP, RpoTp and RpoTmp, .
Operonic organization and RNA polymerase competition are important factors explaining the effect of genome rearrangements on the evolution of promoters. Thus, the loss of the common ndhF promoter and the emergence of a new one upstream of gene ndhF in poplar (Populus alba, P. trichocarpa) concur with the deletion of a neighboring gene .
Some conserved promoters might be overlooked. For instance, the well studied psbC promoter is located within a coding region of other gene (according to the GenBank records) and its conservation cannot be assessed without estimating the synonymous vs. non-synonymous substitutions ratio, which is yet to be incorporated in our approach. Similar promoter-like regions were observed within other coding areas (unpublished data), but their role awaits explanation.
Reviewer's report 1
Arcady Mushegian, Stowers Institute
1st paragraph: the authors assert that there is no published evidence on searching for promoters at the genome scale. This is not true and needs to be qualified: there are many papers about eukaryotes and several about either methods to detect or databases of detected promotors in various groups of bacteria, some of which have been obtained using intergenomic conservation as one of the criteria. Citing the research behind J.Collado-Vides databases or RegulonDB might be in order.
Methods: references 4 and 5 are links to the authors' website with the documentation of their software. Why the reliance on the original code instead of the established methods of motif search and sequence alignment? Please explain crucial differences in the algorithms and how the homegrown ones were tested.
A suggestion that may help to provide a more complete picture of the evolutionary trends in chloroplast promoter conservation: A. thaliana chloroplast has 85 protein-coding genes. Can we have a table that shows, for each gene, how broadly its promoter is conserved?
Response: The "Results" section now contains an analysis of PEP-promoter conservation upstream some coding genes in A. thaliana. An analysis of all 85 genes would be a subject for a separate publication. We show (as also noted in ) a typical problem in finding non-widely conserved promoters. Thus, well studied gene ndhF in A. thaliana is found to have only one PEP-promoter out of the four types known in Magnoliophyta, which is conserved across the Brassicaceae and predicted in all sequenced eurosids II and in Vitis vinifera . Chloroplast PEP-promoters are experimentally unidentified for many coding genes in A. thaliana, while for many they are . These promoters are conserved also in the Brassicaceae but already in eurosids II their recognition depends on imposed cut-offs and requires biological validation. For widely conserved promoters over-prediction is much lower than for promoters conserved within a thin lineage where the leader regions did not diverge to a noticeable extent.
Reviewer's report 2
Alexander Bolshoy, University of Haifa (nominated by Purificación López-García, Université Paris-Sud)
In the paper of Lyubetsky et al. conservation and variability of the plastid promoters is studied, and, to the best of my knowledge, for the first time at the whole genome level. Undoubtedly, the problem is important and non-trivial. The authors obtained unexpected result: promoter regions in plastids are less conservative than corresponding coding sequences. To identify promoters the authors proposed an original method of searching short motifs surrounded by certain other motifs. Thus, the proposed article includes an interesting problem, original methods to solve it and non-trivial results of analysis of promoter regions. It makes this article suitable for publication in the Discovery Notes section of Biology Direct.
In Background section you use a term "lower conservation". Can you show how have you compared protein conservation with promoter conservation? Response: Comparing to the PEP-promoters, their regulated proteins are always widely conserved and well aligned. A family present in vascular pants is almost ubiquitous, while known widely conserved PEP-promoters are only five. PEP-promoters might be more abundant than NEP-promoters: the knockout of RpoTp-NEP is not lethal for A. thaliana, while the PEP-promoter loss (e.g. in Epifagus virginiana) entails the loss of numerous genes. The authors are unaware of detailed estimates.
In Background section you use the term "widely" to indicate that the leader region sequences upstream orthologous genes can be aligned across high-level taxonomic divisions. Please, give some details for better understanding of the term "widely conserved"?
In Background section the following phrase "... using the fixed consensus as a query produced massive under-predictions, or, alternatively, massive over-predictions..." needs some explanation.
Materials and methods. Please, give a short description of your algorithms.
Results. Why the authors insist to strengthen differences between plastid REP-promoter of psaA gene and bacterial σ-70 promoters?
Response: The psaA leader regions have a reliable long alignment, which accents the fact that this promoter considerably differs from the bacterial sigma-70 consensus.
Reviewer's report 3
Yuri I. Wolf, National Center for Biotechnology Information (nominated by Purificación López-García, Université Paris-Sud)
p. 2. "Plastid genes and their promoters are believed to be evolutionarily conserved across large taxonomic lineages". This is a strong statement that requires at least a couple of references, indicated who, when and in what form expressed these beliefs.
p.3 and throughout. "The term "widely" is used to indicate...". The authors attempt to clarify the usage of the term "widely", but actually just substitute it by no less vague "across high-level taxonomic divisions". I suggest to specify the "high-level taxonomic divisions" used in the definition of "widely" and avoid the italicized usage of this term further in the text.
pp. 4-6. The gene-specific section of the Results reads like a verbal narration of the content of the Table 1. It is not clear why the authors need such a detailed listing of facts that don't seem to lead to any particular conclusions. I would recommend considering the possibility of removing this part from Results altogether, joining Results and Discussion and use the extra available space to somewhat expand the Methods section.
Promoter blocks for different genes seem to be aligned, but all shown sequences have different lengths. This leads to a seemingly paradoxical result - the magenta mark for the experimentally identified transcription initiation site in psbB of Spinacia oleracea highlights an empty space.
Response: The Figure 1 shows a good alignment, which length cannot be amended. If the psbB alignment is appended some columns to the right, its quality will decrease. In magenta is now a character existing in this position in spinach an experimentally proved to be at the transcription start.
The authors are grateful to Leonid Rusin for valuable discussion and help in manuscript preparation. This study was partly supported by the International Science & Technology Center (project no. 3807) and the Federal Agency for Education (grant no. P2370).
- Singer M, Berg P: Genes and Genomes. 1991, Blackwell Scientific Publications Ltd. OxfordGoogle Scholar
- Collado-Vides J, Salgado H, Morett E, Gama-Castro S, Jiménez-Jacinto V, Martínez-Flores I, Medina-Rivera A, Muñiz-Rascado L, Peralta-Gil M, Santos-Zavaleta A: Bioinformatics resources for the study of gene regulation in bacteria. J Bacteriol. 2009, 191 (1): 23-31. 10.1128/JB.01017-08.PubMedPubMed CentralView ArticleGoogle Scholar
- Swiatecka-Hagenbruch M, Liere K, Borner T: High diversity of plastidial promoters in Arabidopsis thaliana. Mol Genet Genomics. 2007, 277: 725-734. 10.1007/s00438-007-0222-4.PubMedView ArticleGoogle Scholar
- Hoffer PH, Christopher DA: Structure and blue-light-responsive transcription of a chloroplast psbD promoter from Arabidopsis thaliana. Plant Physiol. 1997, 115: 213-222. 10.1104/pp.115.1.213.PubMedPubMed CentralView ArticleGoogle Scholar
- Seliverstov AV, Lysenko EA, Lyubetsky VA: Rapid evolution of promoters for the plastome gene ndhF in flowering plants. Russian Journal of Plant Physiology. 2009, 56 (6): 837-844. 10.1134/S1021443709060144.View ArticleGoogle Scholar
- Finding of multi-box regulatory signal in the set of unaligned sequences. [http://lab6.iitp.ru/en/twobox/]
- A tree-based method of sequence alignment. [http://lab6.iitp.ru/en/treeal/]
- Favorov AV, Gelfand MS, Gerasimova AV, Ravcheev DA, Mironov AA, Makeev VYu: A Gibbs sampler for identification of symmetrically structured, spaced DNA motifs with improved estimation of the signal length. Bioinformatics. 2005, 21 (10): 2240-5. 10.1093/bioinformatics/bti336.PubMedView ArticleGoogle Scholar
- Danilova LV, Gorbunov KIu, Gelfand MS, Liubetskiĭ (Lyubetsky) VA: Algorithms for isolating regulatory signals in DNA sequences. Mol Biol (Mosk). 2001, 35 (6): 987-95. 10.1023/A:1013282101105. [Article in Russian].View ArticleGoogle Scholar
- Danilova LV, Lyubetsky VA, Gelfand MS: An algorithm for identification of regulatory signals in unaligned DNA sequences, its testing and parallel implementation. In Silico Biol. 2003, 3 (1-2): 33-47.PubMedGoogle Scholar
- Rubanov L, Seliverstov A, Lyubetsky V: Multiple alignment based on species tree. Abstracts of the Sixth International Conference on Bioinformatics of Genome Regulation and Structure, BGRS'2008: 22-28 June 2008; Novosibirsk. 2008, 212-Google Scholar
- Homann A, Link G: DNA-binding and transcription characteristics of three cloned sigma factors from mustard (Sinapis alba L.) suggest overlapping and distinct roles in plastid gene expression. Eur J Biochem. 2003, 270 (6): 1288-300. 10.1046/j.1432-1033.2003.03494.x.PubMedView ArticleGoogle Scholar
- Gruissem W, Zurawski G: Analysis of promoter regions for the spinach chloroplast rbcL, atpB and psbA genes. The EMBO Journal. 1985, 4 (13A): 3375-3383.PubMedPubMed CentralGoogle Scholar
- Crooks GE, Hon G, Chandonia JM, Brenner SE: WebLogo: A sequence logo generator. Genome Research. 2004, 14: 1188-1190. 10.1101/gr.849004.PubMedPubMed CentralView ArticleGoogle Scholar
- Westhoff P, Herrmann RG: Complex RNA maturation in chloroplasts. The psbB operon from spinach. Eur J Biochem. 1988, 171: 551-564. 10.1111/j.1432-1033.1988.tb13824.x.PubMedView ArticleGoogle Scholar
- Fey V, Wagner R, Braütigam K, Wirtz M, Hell R, Dietzmann A, Leister D, Oelmüller R, Pfannschmidt T: Retrograde plastid redox signals in the expression of nuclear genes for chloroplast proteins of Arabidopsis thaliana. The Journal of Biological Chemistry. 2005, 280: 5318-5328. 10.1074/jbc.M406358200. Additions and Corrections, ibid, 280(17): 17572PubMedView ArticleGoogle Scholar
- Nagashima A, Hanaoka M, Motohashi R, Seki M, Shinozaki K, Kanamaru K, Takahashi H, Tanaka K: DNA microarray analysis of plastid gene expression in Arabidopsis mutant deficient in a plastid transcription factor sigma, SIG2. Biosci Biotechnol Biochem. 2004, 68 (3): 694-704. 10.1271/bbb.68.694.PubMedView ArticleGoogle Scholar
- Rogers MB, Gilson PR, Su V, McFadden GI, Keeling PJ: The complete chloroplast genome of the chlorarachniophyte Bigelowiella natans: evidence for independent origins of Chlorarachniophyte and Euglenid secondary endosymbionts. Mol Biol Evol. 2007, 24 (1): 54-62. 10.1093/molbev/msl129.PubMedView ArticleGoogle Scholar
- Lemieux C, Otis C, Turmel M: A clade uniting the green algae Mesostigma viride and Chlorokybus atmophyticus represents the deepest branch of the Streptophyta in chloroplast genome-based phylogenies. BMC Biology. 2007, 5 (2): 1-17.Google Scholar
- Li S, Nosenko T, Hackett JD, Bhattacharya D: Phylogenomic analysis identifies red algal genes of endosymbiotic origin in the Chromalveolates. Mol Biol Evol. 2006, 23 (3): 663-674. 10.1093/molbev/msj075.PubMedView ArticleGoogle Scholar
- Lysenko EA: Plant sigma factors and their role in plastid transcription. Plant Cell Rep. 2007, 26: 845-859. 10.1007/s00299-007-0318-7.PubMedView ArticleGoogle Scholar
- Swiatecka-Hagenbruch M, Emanuel C, Hedtke B, Liere K, Borner T: Impaired function of the phage-type RNA polymerase RpoTp in transcription of chloroplast genes is compensated by a second phage-type RNA polymerase. Nucleic Acids Research. 2008, 36 (3): 785-792. 10.1093/nar/gkm1111.PubMedPubMed CentralView ArticleGoogle Scholar
- Wickett NJ, Zhang Y, Hansen SK, Roper JM, Kuehl JV, Plock SA, Wolf PG, Depamphilis CW, Boore JL, Goffinet B: Functional Gene Losses Occur with Minimal Size Reduction in the Plastid Genome of the Parasitic Liverwort Aneura mirabilis. Mol Biol Evol. 2008, 25 (2): 393-401. 10.1093/molbev/msm267.PubMedView ArticleGoogle Scholar
- Seliverstov AV, Lyubetsky VA: Translation regulation of intron containing genes in chloroplasts. Journal of Bioinformatics and Computational Biology. 2006, 4 (4): 783-793. 10.1142/S0219720006002235.PubMedView ArticleGoogle Scholar
This article is published under license to BioMed Central Ltd. This is an Open Access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/2.0), which permits unrestricted use, distribution, and reproduction in any medium, provided the original work is properly cited.