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Ribosomal Protein L10 Is Encoded in the Mitochondrial Genome of Many Land Plants and Green Algae

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Ribosomal Protein L10 Is Encoded in the Mitochondrial Genome of Many Land Plants and Green Algae University of Nebraska - Lincoln DigitalCommons@University of Nebraska - Lincoln Faculty Publications from the Center for Plant Science Innovation Plant Science Innovation, Center for 11-2009 Ribosomal protein L10 is encoded in the mitochondrial genome of many land plants and green algae Jeffrey P. Mower University of Nebraska-Lincoln, [email protected] Linda Bonen University of Ottawa, [email protected] Follow this and additional works at: https://digitalcommons.unl.edu/plantscifacpub Part of the Plant Sciences Commons Mower, Jeffrey P. and Bonen, Linda, "Ribosomal protein L10 is encoded in the mitochondrial genome of many land plants and green algae" (2009). Faculty Publications from the Center for Plant Science Innovation. 47. https://digitalcommons.unl.edu/plantscifacpub/47 This Article is brought to you for free and open access by the Plant Science Innovation, Center for at DigitalCommons@University of Nebraska - Lincoln. It has been accepted for inclusion in Faculty Publications from the Center for Plant Science Innovation by an authorized administrator of DigitalCommons@University of Nebraska - Lincoln. BMC Evolutionary Biology BioMed Central Research article Open Access Ribosomal protein L10 is encoded in the mitochondrial genome of many land plants and green algae Jeffrey P Mower*1 and Linda Bonen2 Address: 1Center for Plant Science Innovation and Department of Agronomy and Horticulture, University of Nebraska, Lincoln, NE, USA and 2Department of Biology, University of Ottawa, Ottawa, Canada Email: Jeffrey P Mower* - [email protected]; Linda Bonen - [email protected] * Corresponding author Published: 16 November 2009 Received: 3 August 2009 Accepted: 16 November 2009 BMC Evolutionary Biology 2009, 9:265 doi:10.1186/1471-2148-9-265 This article is available from: http://www.biomedcentral.com/1471-2148/9/265 © 2009 Mower and Bonen; licensee 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. Abstract Background: The mitochondrial genomes of plants generally encode 30-40 identified protein- coding genes and a large number of lineage-specific ORFs. The lack of wide conservation for most ORFs suggests they are unlikely to be functional. However, an ORF, termed orf-bryo1, was recently found to be conserved among bryophytes suggesting that it might indeed encode a functional mitochondrial protein. Results: From a broad survey of land plants, we have found that the orf-bryo1 gene is also conserved in the mitochondria of vascular plants and charophycean green algae. This gene is actively transcribed and RNA edited in many flowering plants. Comparative sequence analysis and distribution of editing suggests that it encodes ribosomal protein L10 of the large subunit of the ribosome. In several lineages, such as crucifers and grasses, where the rpl10 gene has been lost from the mitochondrion, we suggest that a copy of the nucleus-encoded chloroplast-derived rpl10 gene may serve as a functional replacement. Conclusion: Despite the fact that there are now over 20 mitochondrial genome sequences for land plants and green algae, this gene has remained unidentified and largely undetected until now because of the unlikely coincidence that most of the earlier sequences were from the few lineages that lack the intact gene. These results illustrate the power of comparative sequencing to identify novel genomic features. Background from 67 in the jakobid Reclinomonas americana [1] to only The mitochondrial proteome consists of at least 1000 dif- 3 in apicomplexans such as Plasmodium falciparum [2]. ferent proteins. The genes encoding many of these pro- Genes retained in the mitochondrion encode proteins teins were initially encoded within the original respiring involved in fundamental mitochondrial processes such as endosymbiont but have undergone intracellular transfer electron transport, ATP synthesis, gene expression, and to the nucleus over evolutionary time, so that the proteins protein maturation/import. In Reclinomonas mitochon- must be targeted back to the mitochondrion to perform dria, genes for the translational machinery comprise the their function. The number of retained mitochondrial largest single category, with 27 ribosomal protein genes protein-coding genes varies widely among eukaryotes, [1]. Page 1 of 10 (page number not for citation purposes) BMC Evolutionary Biology 2009, 9:265 http://www.biomedcentral.com/1471-2148/9/265 In streptophytes (vascular plants, bryophytes, and charo- unnamed predicted protein from cDNA analysis phycean green algae), the mitochondrial genome typically (XP_002332837) was also identified from Populus tri- contains about 30 to 40 protein-coding genes of identified chocarpa. Interestingly, the moss orf187 shows weak simi- function. Approximately 20 of these genes are universally larity to ribosomal protein L10 from several bacteria, present, whereas the others (or a subset thereof) have including Rickettsia prowazekii and other members of the been lost from various plant groups [3]. Genes encoding alpha-proteobacteria, the lineage from which mitochon- ribosomal proteins and subunits of the succinate dehy- dria originated [25], as well as to mitochondrial L10 from drogenase complex are most commonly absent [3], the jakobid Reclinomonas americana, a protist that pos- although loss or pseudogenization of other genes, such as sesses the most "primitive" and gene-rich of all mitochon- cox2 [4,5], nad7 [6,7], atp8 [7], and cytochrome c biogen- drial genomes [1]. These observations suggested that the esis subunits [7,8] has occurred as well. Typically, a gene moss orf187 (and its homologs) might encode mitochon- is deleted from the plant mitochondrial genome only after drial L10 in plants. Indeed, annotated L10 domains can successful transfer of a copy to the nucleus, although be found in the GenPept records for Physcomitrella orf187 examples exist where loss is correlated with functional (BAE93086) and Chlorokybus orf295 (ABO15139). replacement of a "native" mitochondrial ribosomal pro- tein by a nucleus-encoded plastid or cytosolic homolog A variety of computational and experimental approaches [9,10]. The timing of migration of mitochondrial ribos- were used to determine the distribution of mitochondrial omal protein genes to the nucleus during eukaryotic evo- rpl10-like sequences among streptophytes, and the results lution can be followed by comparative analysis [11,12]. are summarized in Figure 1. To extend the database search, tblastn queries were conducted against the nucle- The mitochondrial genomes of seed plants are particularly otide nr and EST-others databases at GenBank. Indeed, large and recombinogenic. They contain many potential homologous unannotated ORFs are present within the unknown open reading frames (ORFs) which have often complete mitochondrial genomes of the charophyte been annotated as such in genomic sequencing projects Chara vulgaris, [26], the gymnosperm Cycas taitungensis when longer than 100 codons. However, most of these [27], and the angiosperm Carica papaya (EU431224) as ORFs are not broadly conserved, which has brought into well as in partial mitochondrial genome entries for the question their potential functionality. Moreover, it is not angiosperms Solanum lycopersicum and Helianthus annuus. uncommon for plant mitochondrial DNA rearrangements In addition, several truncated and/or frameshifted to give rise to novel chimeric ORFs in specific lineages, sequences were identified in the mitochondrial genomes and in certain instances such ORFs are correlated with of Brassica napus, Oryza sativa, and Bambusa oldhamii, sug- mitochondrial dysfunction in the form of cytoplasmic gestive of recent erosion of the rpl10-like gene. Searches of male sterility [13]. On the other hand, a few ORFs have the EST-others database also revealed numerous shown conservation among plants, and over recent years homologs from a wide range of angiosperms as well as these have been upgraded to known mitochondrial genes. two gymnosperms, Picea glauca and Welwitschia mirabilis. This list includes atp4 [14,15], atp8 [15-17] and mttB (or Their high nucleotide similarity to counterparts identified tatC) [18,19], which previously were denoted as orf25, in completely sequenced mitochondrial genomes of other orfB, and orfX, respectively. Within the three complete seed plants suggests that these are in fact encoded in the non-vascular plant mitochondrial genomes, there is mitochondrial genome, unless there has been extremely another unidentified conserved ORF, named orf-bryo1 in recent gene transfer to the nucleus. One exception is a the hornwort Megaceros aenigmaticus [7], orf187 in the divergent rpl10-like sequence from the fern Adiantum moss Physcomitrella patens [20], and orf168 in the liverwort capillus-veneris (DK949045) that has an amino-terminal Marchantia polymorpha [21], suggesting that it may in fact extension of 25 residues with a weak predicted mitochon- code for a functional mitochondrial product in plants. drial targeting signal, and might therefore be nuclear- located. Results and Discussion Mitochondrial orf-bryo1 is conserved across streptophytes To determine how widely this mitochondrial rpl10-like To determine whether this bryophyte mitochondrial ORF gene is represented in seed plants and to gain more insight might be more widespread among plants, blastp
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