Dosage Sensitivity of RPL9 and Concerted Evolution of Ribosomal Protein Genes in Plants
Identifieur interne : 000094 ( Pmc/Corpus ); précédent : 000093; suivant : 000095Dosage Sensitivity of RPL9 and Concerted Evolution of Ribosomal Protein Genes in Plants
Auteurs : Deborah Devis ; Sue M. Firth ; Zhe Liang ; Mary E. ByrneSource :
- Frontiers in Plant Science [ 1664-462X ] ; 2015.
Abstract
The ribosome in higher eukaryotes is a large macromolecular complex composed of four rRNAs and eighty different ribosomal proteins. In plants, each ribosomal protein is encoded by multiple genes. Duplicate genes within a family are often necessary to provide a threshold dose of a ribosomal protein but in some instances appear to have non-redundant functions. Here, we addressed whether divergent members of the
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DOI: 10.3389/fpls.2015.01102
PubMed: 26734020
PubMed Central: 4679983
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<record><TEI><teiHeader><fileDesc><titleStmt><title xml:lang="en">Dosage Sensitivity of RPL9 and Concerted Evolution of Ribosomal Protein Genes in Plants</title><author><name sortKey="Devis, Deborah" sort="Devis, Deborah" uniqKey="Devis D" first="Deborah" last="Devis">Deborah Devis</name></author><author><name sortKey="Firth, Sue M" sort="Firth, Sue M" uniqKey="Firth S" first="Sue M." last="Firth">Sue M. Firth</name></author><author><name sortKey="Liang, Zhe" sort="Liang, Zhe" uniqKey="Liang Z" first="Zhe" last="Liang">Zhe Liang</name></author><author><name sortKey="Byrne, Mary E" sort="Byrne, Mary E" uniqKey="Byrne M" first="Mary E." last="Byrne">Mary E. Byrne</name></author></titleStmt><publicationStmt><idno type="wicri:source">PMC</idno><idno type="pmid">26734020</idno><idno type="pmc">4679983</idno><idno type="url">http://www.ncbi.nlm.nih.gov/pmc/articles/PMC4679983</idno><idno type="RBID">PMC:4679983</idno><idno type="doi">10.3389/fpls.2015.01102</idno><date when="2015">2015</date><idno type="wicri:Area/Pmc/Corpus">000094</idno></publicationStmt><sourceDesc><biblStruct><analytic><title xml:lang="en" level="a" type="main">Dosage Sensitivity of RPL9 and Concerted Evolution of Ribosomal Protein Genes in Plants</title><author><name sortKey="Devis, Deborah" sort="Devis, Deborah" uniqKey="Devis D" first="Deborah" last="Devis">Deborah Devis</name></author><author><name sortKey="Firth, Sue M" sort="Firth, Sue M" uniqKey="Firth S" first="Sue M." last="Firth">Sue M. Firth</name></author><author><name sortKey="Liang, Zhe" sort="Liang, Zhe" uniqKey="Liang Z" first="Zhe" last="Liang">Zhe Liang</name></author><author><name sortKey="Byrne, Mary E" sort="Byrne, Mary E" uniqKey="Byrne M" first="Mary E." last="Byrne">Mary E. Byrne</name></author></analytic><series><title level="j">Frontiers in Plant Science</title><idno type="eISSN">1664-462X</idno><imprint><date when="2015">2015</date></imprint></series></biblStruct></sourceDesc></fileDesc><profileDesc><textClass></textClass></profileDesc></teiHeader><front><div type="abstract" xml:lang="en"><p>The ribosome in higher eukaryotes is a large macromolecular complex composed of four rRNAs and eighty different ribosomal proteins. In plants, each ribosomal protein is encoded by multiple genes. Duplicate genes within a family are often necessary to provide a threshold dose of a ribosomal protein but in some instances appear to have non-redundant functions. Here, we addressed whether divergent members of the <italic>RPL9</italic> gene family are dosage sensitive or whether these genes have non-overlapping functions. The <italic>RPL9</italic> family in <italic>Arabidopsis thaliana</italic> comprises two nearly identical members, <italic>RPL9B</italic> and <italic>RPL9C</italic>, and a more divergent member, <italic>RPL9D</italic>. Mutations in <italic>RPL9C</italic> and <italic>RPL9D</italic> genes lead to delayed growth early in development, and loss of both genes is embryo lethal, indicating that these are dosage-sensitive and redundant genes. Phylogenetic analysis of <italic>RPL9</italic> as well as <italic>RPL4</italic>, <italic>RPL5</italic>, <italic>RPL27a</italic>, <italic>RPL36a</italic>, and <italic>RPS6</italic> family genes in the Brassicaceae indicated that multicopy ribosomal protein genes have been largely retained following whole genome duplication. However, these gene families also show instances of tandem duplication, small scale deletion, and evidence of gene conversion. Furthermore, phylogenetic analysis of <italic>RPL9</italic> genes in angiosperm species showed that genes within a species are more closely related to each other than to <italic>RPL9</italic> genes in other species, suggesting ribosomal protein genes undergo convergent evolution. Our analysis indicates that ribosomal protein gene retention following whole genome duplication contributes to the number of genes in a family. However, small scale rearrangements influence copy number and likely drive concerted evolution of these dosage-sensitive genes.</p></div></front><back><div1 type="bibliography"><listBibl><biblStruct><analytic><author><name sortKey="Arguello, J R" uniqKey="Arguello J">J. R. Arguello</name></author><author><name sortKey="Connallon, T" uniqKey="Connallon T">T. 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<front><journal-meta><journal-id journal-id-type="nlm-ta">Front Plant Sci</journal-id><journal-id journal-id-type="iso-abbrev">Front Plant Sci</journal-id><journal-id journal-id-type="publisher-id">Front. Plant Sci.</journal-id><journal-title-group><journal-title>Frontiers in Plant Science</journal-title></journal-title-group><issn pub-type="epub">1664-462X</issn><publisher><publisher-name>Frontiers Media S.A.</publisher-name></publisher></journal-meta><article-meta><article-id pub-id-type="pmid">26734020</article-id><article-id pub-id-type="pmc">4679983</article-id><article-id pub-id-type="doi">10.3389/fpls.2015.01102</article-id><article-categories><subj-group subj-group-type="heading"><subject>Plant Science</subject><subj-group><subject>Original Research</subject></subj-group></subj-group></article-categories><title-group><article-title>Dosage Sensitivity of RPL9 and Concerted Evolution of Ribosomal Protein Genes in Plants</article-title></title-group><contrib-group><contrib contrib-type="author"><name><surname>Devis</surname><given-names>Deborah</given-names></name><uri xlink:type="simple" xlink:href="http://loop.frontiersin.org/people/287781/overview"></uri></contrib><contrib contrib-type="author"><name><surname>Firth</surname><given-names>Sue M.</given-names></name><uri xlink:type="simple" xlink:href="http://loop.frontiersin.org/people/25951/overview"></uri></contrib><contrib contrib-type="author"><name><surname>Liang</surname><given-names>Zhe</given-names></name><uri xlink:type="simple" xlink:href="http://loop.frontiersin.org/people/195927/overview"></uri></contrib><contrib contrib-type="author"><name><surname>Byrne</surname><given-names>Mary E.</given-names></name><xref ref-type="author-notes" rid="fn001"><sup>*</sup></xref><uri xlink:type="simple" xlink:href="http://loop.frontiersin.org/people/27222/overview"></uri></contrib></contrib-group><aff><institution>School of Biological Sciences, The University of Sydney, Sydney</institution><country>NSW, Australia</country></aff><author-notes><fn fn-type="edited-by"><p>Edited by: <italic>Maria Eugenia Zanetti, Consejo Nacional de Investigaciones Científicas y Técnicas, and Universidad Nacional de LA Plata, Argentina</italic></p></fn><fn fn-type="edited-by"><p>Reviewed by: <italic>Paula Casati, Centro de Estudios Fotosinteticos–Consejo Nacional de Investigaciones Científicas y Técnicas, Argentina; Adriana Garay, Universidad Nacional Autónoma de México, Mexico; Abel Rosado, The University of British Columbia, Canada</italic></p></fn><corresp id="fn001">*Correspondence: <italic>Mary E. Byrne, <email xlink:type="simple">mary.byrne@sydney.edu.au</email></italic></corresp><fn fn-type="other" id="fn002"><p>This article was submitted to Plant Genetics and Genomics, a section of the journal Frontiers in Plant Science</p></fn></author-notes><pub-date pub-type="epub"><day>16</day><month>12</month><year>2015</year></pub-date><pub-date pub-type="collection"><year>2015</year></pub-date><volume>6</volume><elocation-id>1102</elocation-id><history><date date-type="received"><day>15</day><month>9</month><year>2015</year></date><date date-type="accepted"><day>22</day><month>11</month><year>2015</year></date></history><permissions><copyright-statement>Copyright © 2015 Devis, Firth, Liang and Byrne.</copyright-statement><copyright-year>2015</copyright-year><copyright-holder>Devis, Firth, Liang and Byrne</copyright-holder><license xlink:href="http://creativecommons.org/licenses/by/4.0/"><license-p>This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) or licensor are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.</license-p></license></permissions><abstract><p>The ribosome in higher eukaryotes is a large macromolecular complex composed of four rRNAs and eighty different ribosomal proteins. In plants, each ribosomal protein is encoded by multiple genes. Duplicate genes within a family are often necessary to provide a threshold dose of a ribosomal protein but in some instances appear to have non-redundant functions. Here, we addressed whether divergent members of the <italic>RPL9</italic> gene family are dosage sensitive or whether these genes have non-overlapping functions. The <italic>RPL9</italic> family in <italic>Arabidopsis thaliana</italic> comprises two nearly identical members, <italic>RPL9B</italic> and <italic>RPL9C</italic>, and a more divergent member, <italic>RPL9D</italic>. Mutations in <italic>RPL9C</italic> and <italic>RPL9D</italic> genes lead to delayed growth early in development, and loss of both genes is embryo lethal, indicating that these are dosage-sensitive and redundant genes. Phylogenetic analysis of <italic>RPL9</italic> as well as <italic>RPL4</italic>, <italic>RPL5</italic>, <italic>RPL27a</italic>, <italic>RPL36a</italic>, and <italic>RPS6</italic> family genes in the Brassicaceae indicated that multicopy ribosomal protein genes have been largely retained following whole genome duplication. However, these gene families also show instances of tandem duplication, small scale deletion, and evidence of gene conversion. Furthermore, phylogenetic analysis of <italic>RPL9</italic> genes in angiosperm species showed that genes within a species are more closely related to each other than to <italic>RPL9</italic> genes in other species, suggesting ribosomal protein genes undergo convergent evolution. Our analysis indicates that ribosomal protein gene retention following whole genome duplication contributes to the number of genes in a family. However, small scale rearrangements influence copy number and likely drive concerted evolution of these dosage-sensitive genes.</p></abstract><kwd-group><kwd>concerted evolution</kwd><kwd>dosage sensitive</kwd><kwd>gene redundancy</kwd><kwd>plant</kwd><kwd>ribosomal protein</kwd></kwd-group><funding-group><award-group><funding-source id="cn001">Australian Research Council Discovery Project<named-content content-type="fundref-id">10.13039/501100000923</named-content></funding-source><award-id rid="cn001">DP130101186</award-id></award-group></funding-group><counts><fig-count count="6"></fig-count><table-count count="0"></table-count><equation-count count="0"></equation-count><ref-count count="59"></ref-count><page-count count="12"></page-count><word-count count="0"></word-count></counts></article-meta></front><body><sec><title>Introduction</title><p>The 80S ribosome of higher eukaryotes is a macromolecular complex composed of two subunits, a large 60S subunit and a small 40S subunit. The 60S subunit comprises 28S, 5.8S, and 5S rRNA and 47 ribosomal proteins. The 40S subunit is composed of 18S rRNA and 33 proteins (<xref rid="B33" ref-type="bibr">Melnikov et al., 2012</xref>). Ribosomes are produced through a cascade of events involving coordinated processing of precursor rRNA, progressive association of individual ribosomal proteins with rRNA, export of pre-ribosome particles from the nucleolus to the cytoplasm, and assembly to form mature subunits. The two subunits join at translation initiation to form a ribosome, which carries out protein synthesis.</p><p>In <italic>Arabidopsis thaliana</italic>, each ribosomal protein is encoded by multiple genes (<xref rid="B2" ref-type="bibr">Barakat et al., 2001</xref>). Duplicate ribosomal protein genes may serve to provide a critical dose of a ribosomal protein or may provide distinct functions through differential expression or through diversification of protein function (<xref rid="B25" ref-type="bibr">Horiguchi et al., 2012</xref>; <xref rid="B56" ref-type="bibr">Xue and Barna, 2012</xref>). In <italic>Arabidopsis</italic>, mutations in members of a ribosomal protein family may have different phenotypic outcomes but more often show similar dose-dependent phenotypes (<xref rid="B17" ref-type="bibr">Degenhardt and Bonham-Smith, 2008</xref>; <xref rid="B58" ref-type="bibr">Yao et al., 2008</xref>; <xref rid="B20" ref-type="bibr">Fujikura et al., 2009</xref>; <xref rid="B15" ref-type="bibr">Creff et al., 2010</xref>; <xref rid="B39" ref-type="bibr">Rosado and Raikhel, 2010</xref>; <xref rid="B40" ref-type="bibr">Rosado et al., 2010</xref>; <xref rid="B24" ref-type="bibr">Horiguchi et al., 2011</xref>; <xref rid="B45" ref-type="bibr">Stirnberg et al., 2012</xref>; <xref rid="B10" ref-type="bibr">Casanova-Sáez et al., 2014</xref>; <xref rid="B59" ref-type="bibr">Zsögön et al., 2014</xref>). Mutations in <italic>A. thaliana</italic> ribosomal protein genes are generally recessive, and only two semi-dominant mutants have been described (<xref rid="B8" ref-type="bibr">Byrne, 2009</xref>; <xref rid="B25" ref-type="bibr">Horiguchi et al., 2012</xref>). <italic>Arabidopsis Minute-like1</italic> (<italic>aml1</italic>) has a mutation in the <italic>RPS5B</italic> gene and homozygous mutants arrest during early stages of embryo development. Hemizygous plants are viable and have a range of phenotypes including reduced seedling size and altered organ vascular patterning (<xref rid="B55" ref-type="bibr">Weijers et al., 2001</xref>). <italic>rpl27ac-1d</italic> is a dominant-negative mutation in the <italic>RPL27aC</italic> gene and homozygous plants have abnormal development of embryos and pleiotropic defects in the plant shoot. Heterozygous plants are slow growing with distinct developmental phenotypes, including pointed and serrated leaves (<xref rid="B46" ref-type="bibr">Szakonyi and Byrne, 2011a</xref>,<xref rid="B47" ref-type="bibr">b</xref>). Increasing the ratio of <italic>rpl27ac-1d</italic> relative to wild type results in a progressive increase in the range and severity of phenotypes consistent with plant growth and development being sensitive to the dose of RPL27a (<xref rid="B59" ref-type="bibr">Zsögön et al., 2014</xref>).</p><p>RPL27a is encoded by two redundant genes. Loss-of-function mutations in <italic>RPL27aC</italic> and <italic>RPL27aB</italic> have mild and no leaf phenotype, respectively, whereas double heterozygote plants have a pointed and serrated leaf shape phenotype (<xref rid="B59" ref-type="bibr">Zsögön et al., 2014</xref>). Mutations in both <italic>RPL27aB</italic> and <italic>RPL27aC</italic> genes are not transmitted through gametes indicating dramatically reduced levels of RPL27a is haploid lethal (<xref rid="B59" ref-type="bibr">Zsögön et al., 2014</xref>). Likewise ribosomal proteins RPL4, RPL5, RPL36a, and RPS6, are each encoded by two functional genes. For each of these duplicate genes, single mutants are viable and plants display a pointed and serrated leaf phenotype that is characteristic of mutations in <italic>A. thaliana</italic> ribosomal protein genes. Double heterozygous mutants for both genes within a family also display these leaf phenotypes and mutant alleles in duplicate genes are not transmitted through gametes (<xref rid="B58" ref-type="bibr">Yao et al., 2008</xref>; <xref rid="B20" ref-type="bibr">Fujikura et al., 2009</xref>; <xref rid="B15" ref-type="bibr">Creff et al., 2010</xref>; <xref rid="B40" ref-type="bibr">Rosado et al., 2010</xref>; <xref rid="B10" ref-type="bibr">Casanova-Sáez et al., 2014</xref>). These phenotypes indicate that members of these ribosomal protein families are redundant and that the duplicate genes in a family are required for production of sufficient levels of a ribosomal protein for viability of haploid gametes and for plant growth.</p><p>Duplicate genes may arise through whole or partial genome duplication, or through tandem gene duplication. Many flowering plants are ancient polyploids and retain evidence of past genome duplications (<xref rid="B52" ref-type="bibr">Van de Peer et al., 2009</xref>). Duplicate genes created through genome duplication either diverge in function or one duplicate is lost from the genome. However, gene loss is biased and dosage sensitive genes appear to be preferentially retained following genome duplication. According to the gene balance hypothesis, following whole genome duplication, an unfavorable imbalance in the optimum ratio of proteins may arise from loss of genes that code for components of a protein complex or components in a molecular pathway. As such dosage-sensitive genes may be retained following whole genome duplication in order to maintain a balance in the concentration of proteins in complex or in a molecular pathway (<xref rid="B53" ref-type="bibr">Veitia, 2002</xref>; <xref rid="B34" ref-type="bibr">Papp et al., 2003</xref>; <xref rid="B3" ref-type="bibr">Birchler and Veitia, 2012</xref>). Consistent with the gene balance hypothesis, multiple plant species display evidence of over-retention of genes within the ontology category of “ribosome” following genome duplication (<xref rid="B5" ref-type="bibr">Blanc and Wolfe, 2004</xref>; <xref rid="B31" ref-type="bibr">Maere et al., 2005</xref>; <xref rid="B37" ref-type="bibr">Rizzon et al., 2006</xref>; <xref rid="B49" ref-type="bibr">Thomas et al., 2006</xref>; <xref rid="B54" ref-type="bibr">Wang et al., 2011</xref>; <xref rid="B27" ref-type="bibr">Jiang et al., 2013</xref>).</p><p>Although there is an overall trend toward retention of ribosomal protein genes post-genome duplication, there has been limited analysis of the evolution of specific cytoplasmic ribosomal protein gene families within plants. Here we demonstrate that two divergent members of the ribosomal protein family <italic>RPL9</italic>, <italic>RPL9C</italic>, and <italic>RPL9D</italic>, are dosage-sensitive and redundant, indicating that these duplicate ribosomal protein genes serve to maintain adequate levels of a ribosomal protein for sufficient ribosome production. Analysis of <italic>RPL9</italic> family genes in Brassicaceae species, and more broadly within eudicots and monocots revealed limited <italic>RPL9</italic> copy number variation between species. In the Brassicaceae, <italic>RPL9</italic> copy number appears to be the outcome of multiple genome rearrangements including whole genome duplication, tandem duplication and gene loss. Furthermore nucleotide sequence variation between <italic>RPL9</italic> genes within a species appears to be driven toward homogenization, likely through gene conversion. Analysis of <italic>RPL4</italic>, <italic>RPL5</italic>, <italic>RPL27a</italic>, <italic>RPL36a</italic>, and <italic>RPS6</italic> genes in the Brassicaceae reveals dynamic evolution of ribosomal protein gene families.</p></sec><sec sec-type="materials|methods" id="s1"><title>Materials and Methods</title><sec><title>Plant Materials and Growth Conditions</title><p><italic>Arabidopsis</italic> mutant <italic>rpl9c-1</italic> (formerly published as <italic>piggyback2-1</italic> (<italic>pgy2-1</italic>)) has been described previously (<xref rid="B36" ref-type="bibr">Pinon et al., 2008</xref>). <italic>rpl9d-1</italic> (SALK_111804) was obtained from The European <italic>Arabidopsis</italic> Stock Center (<xref rid="B41" ref-type="bibr">Scholl et al., 2000</xref>) and was backcrossed five times to Landsberg <italic>erecta</italic> prior to genetic analysis. Plants were grown in soil at 22°C with a day length of 16 h. Growth measurement data from eight plants of each genotype were analyzed using SPSS Statistics for Macintosh, Version 22.0 (IBM Corporation). One-way or repeated measures analysis of variance (ANOVA) tests were performed, followed by Scheffe’s multiple comparison <italic>post hoc</italic> test and <italic>P</italic> < 0.05 were considered as significant.</p></sec><sec><title>Molecular Biology</title><p>The genotype of wild type and mutant <italic>rpl9c</italic> and <italic>rpl9d</italic> alleles was determined by PCR using gene specific primers. <italic>RPL9D:RPL9D</italic> was generated by PCR amplification of an 4.5 kb genomic region encompassing <italic>RPL9D</italic> and cloning into the binary vector pMDC123 (<xref rid="B16" ref-type="bibr">Curtis and Grossniklaus, 2003</xref>). The construct was transformed into <italic>rpl9c</italic> by floral dip (<xref rid="B13" ref-type="bibr">Clough and Bent, 1998</xref>).</p></sec><sec><title>Phylogenetic and Synteny Analysis</title><p>Gene sequences were obtained from Phytozome (<xref rid="B23" ref-type="bibr">Goodstein et al., 2012</xref>). Designated gene names used in phylogenetic analysis and corresponding genomic unique locus identifiers are listed in Supplementary Tables <xref ref-type="supplementary-material" rid="SM1">S1</xref>–<xref ref-type="supplementary-material" rid="SM1">S8</xref>. Brassicaceae species included <italic>A. thaliana</italic>, <italic>Arabidopsis lyrata</italic>, <italic>Capsella rubella</italic>, and <italic>Capsella grandiflora</italic>, within the Camelineae, and <italic>Eutrema salsugineum</italic> (formerly <italic>Thellungiella halophila</italic>) and <italic>B. rapa</italic>. For Brassicaceae species, genome sequence assembly into chromosomes was incomplete for several species. Therefore designated <italic>RPL9, RPL4</italic>, <italic>RPL5</italic>, <italic>RPL27a</italic>, <italic>RPL36a</italic>, and <italic>RPS6</italic> gene names within a species were based on phylogenetic relationships. <italic>RPL9</italic> gene names for other dicot species and for monocot species that had complete genome assemblies were assigned according to map location. This included the dicot species <italic>Gossypium raimondii, Medicago truncatula, Phaseolus vulgaris, Poplar trichocarpa, Solanum lycopersicum</italic>, <italic>S. tuberosum</italic>, and <italic>Vitis vinifera</italic>, and the monocot species <italic>Brachypodium distachyon, Oryza sativa, Sorghum bicolor</italic>, and <italic>Zea mays. RPL9</italic> gene names for species where genome assembly was incomplete were arbitrarily assigned. This included the dicot species <italic>Aquilegia coerulea, Carica papaya, Citrus clementina, Citrus sinensis, Linum usitatissimum</italic>, and <italic>Mimulus guttatus</italic>, and the monocot species <italic>Panicum virgatum</italic> and <italic>Setaria italica</italic>. The CDS sequences were used to estimate phylogenetic relationships. Orthologous ribosomal proteins from <italic>Drosophila melanogaster</italic> were selected as the outgroup. Full-length sequences were aligned using ClustalW and phylogenetic relationships were inferred using MEGA6.06 (<xref rid="B48" ref-type="bibr">Tamura et al., 2013</xref>). Trees were constructed with the Maximum-Likelihood algorithm and default settings with 1000 bootstrap replications. Synteny analysis was carried out using CoGepedia (<xref rid="B29" ref-type="bibr">Lyons and Freeling, 2008</xref>; <xref rid="B30" ref-type="bibr">Lyons et al., 2008</xref>) with a sequence distance set to 100 kb.</p></sec></sec><sec><title>Results</title><sec><title><italic>RPL9C</italic> and <italic>RPL9D</italic> have Redundant Functions in Plant Growth</title><p><italic>Arabidopsis thaliana</italic> has three <italic>RPL9</italic> genes, <italic>RPL9B</italic>, <italic>RPL9C</italic>, and <italic>RPL9D</italic> (<xref rid="B2" ref-type="bibr">Barakat et al., 2001</xref>). The proteins encoded by <italic>RPL9B</italic> and <italic>RPL9C</italic> share 100% amino acid identity whereas <italic>RPL9B/RPL9C</italic> and <italic>RPL9D</italic> encoded proteins are more divergent and share 89% amino acid identity. Although all three genes are ubiquitously expressed, transcript levels of <italic>RPL9C</italic> are approximately twofold higher than <italic>RPL9D</italic> and threefold higher than <italic>RPL9B</italic> (<xref rid="B28" ref-type="bibr">Laubinger et al., 2008</xref>; <xref rid="B36" ref-type="bibr">Pinon et al., 2008</xref>). To determine whether divergent members of the <italic>RPL9</italic> gene family are redundant we compared phenotypes resulting from mutation in <italic>RPL9C</italic> and <italic>RPL9D</italic>. <italic>rpl9c</italic> (previously named <italic>pgy2</italic>) is a weak allele and has a splice-donor site point mutation that reduces the level of wild type transcript. <italic>rpl9c</italic> leaves are pointed and have more prominent marginal serrations compared to wild type (<xref rid="B36" ref-type="bibr">Pinon et al., 2008</xref>) (<bold>Figure <xref ref-type="fig" rid="F1">1</xref></bold>). A T-DNA mutant <italic>rpl9d</italic> had an insertion in the first exon of <italic>RPL9D</italic> and was predicted to be a null allele. The leaf shape of <italic>rpl9d</italic> was not distinct from that of wild type (<bold>Figure <xref ref-type="fig" rid="F1">1</xref></bold>). This indicated either <italic>RPL9D</italic> has no function in leaf development or the contribution of <italic>RPL9D</italic> to leaf development is not significant in the presence of functional <italic>RPL9B</italic> and <italic>RPL9C</italic>. To determine whether or not <italic>RPL9D</italic> contributes to leaf development, the effect of reduced levels of <italic>RPL9C</italic> in the <italic>rpl9d</italic> mutant was examined. The double homozygous mutant is embryo lethal (see below). Therefore <italic>rpl9c/+ rpl9d</italic> plants were examined. <italic>rpl9c/+ rpl9d</italic> plants had mildly serrated leaves compared with <italic>rpl9d</italic> single mutants indicating partial loss of <italic>RPL9C</italic> function slightly modifies leaf development in the <italic>rpl9d</italic> background (<bold>Figure <xref ref-type="fig" rid="F1">1</xref></bold>). The effect of reduced <italic>RPL9D</italic> on the <italic>rpl9c</italic> mutant was also examined. The leaf phenotype of <italic>rpl9c rpl9d/+</italic> plants was more severe and leaves were smaller and more pointed than <italic>rpl9c</italic> (<bold>Figure <xref ref-type="fig" rid="F1">1</xref></bold>). This enhanced phenotype indicates <italic>RPL9D</italic> acts redundantly with <italic>RPL9C</italic> in leaf growth.</p><fig id="F1" position="float"><label>FIGURE 1</label><caption><p><bold><italic>RPL9C</italic> and <italic>RPL9D</italic> have redundant functions in leaf development.</bold> Silhouettes <bold>(left)</bold> and rosettes <bold>(right)</bold> of wild type, <italic>rpl9c</italic>, <italic>rpl9d, rpl9c/+ rpl9d, rpl9c rpl9d/+</italic>, and <italic>rpl9c</italic> homozygous for the transgene <italic>RPL9D:RPL9D</italic>.</p></caption><graphic xlink:href="fpls-06-01102-g001"></graphic></fig><p>To confirm that <italic>RPL9D</italic> is redundant with <italic>RPL9C</italic>, a genomic clone <italic>RPL9D:RPL9D</italic>, encompassing the gene promoter and coding region, was transformed into the <italic>rpl9c</italic> mutant to test for complementation. The leaf shape of progeny from 10 independent transformants was examined. All ten lines segregated plants that had a wild-type phenotype. Progeny from phenotypically wild type plants in two lines were confirmed as homozygous for <italic>RPL9D:RPL9D</italic> (<bold>Figure <xref ref-type="fig" rid="F1">1</xref></bold>). <italic>RPL9D:RPL9D</italic> is therefore able to replace the function of <italic>RPL9C</italic>.</p><p>In addition to leaf shape, mutations in ribosomal proteins result in slow growth, although there is limited information quantifying this growth defect. To compare the rate of growth of <italic>rpl9</italic> mutants relative to wild type, we measured the rate of leaf production, the time to flower and the rate of inflorescence elongation for wild type, <italic>rpl9c, rpl9d, rpl9c/+ rpl9d</italic>, and <italic>rpl9c rpl9d/+</italic> plants. Plants from two independent <italic>rpl9c RPL9D:RPL9D</italic> lines were also included in this analysis. All genotypes produced approximately 11 rosette and cauline leaves and transitioned to flowering on average 25.25–27.5 days after sowing, except for <italic>rpl9c/+ rpl9d</italic> and <italic>rpl9c rpl9d/+</italic>. Both of these genotypes produced more leaves (average 12.75 and 14.25 leaves, respectively, <italic>P</italic> < 0.05) and <italic>rpl9c rpl9d/+</italic> flowered later (average 32.1 days after sowing, <italic>P</italic> < 0.05) than wild type (<bold>Figures <xref ref-type="fig" rid="F2">2A,B</xref></bold>). Despite these differences, the rate of vegetative leaf initiation was similar for all genotypes (<bold>Figure <xref ref-type="fig" rid="F2">2C</xref></bold>). During growth of the inflorescence <italic>rpl9d</italic> plants were not affected but <italic>rpl9c</italic> (<italic>P</italic> = 0.04), <italic>rpl9c/+ rpl9d</italic> (<italic>P</italic> < 0.005) and <italic>rpl9c rpl9d/+</italic> (<italic>P</italic> < 0.005) plants appeared to be shorter than wild type at any given time point. The growth of the two independent <italic>rpl9c RPL9D::RPL9D</italic> plants were not significantly different from either wild type or <italic>rpl9c</italic> plants indicating that RPL9D can partially complement the <italic>rpl9c</italic> mutation (<bold>Figure <xref ref-type="fig" rid="F2">2D</xref></bold>).</p><fig id="F2" position="float"><label>FIGURE 2</label><caption><p><bold>Mutations in <italic>RPL9</italic> genes delay growth.</bold> The number of rosette (blue) and cauline (red) leaves <bold>(A)</bold>, days to flower <bold>(B)</bold>, rate of rosette leaf emergence <bold>(C)</bold>, and rate of inflorescence growth <bold>(D)</bold> are shown for the genotypes wild type, <italic>rpl9c</italic>, <italic>rpl9d, rpl9c/+ rpl9d, rpl9c rpl9d/+</italic>, and for two independent lines <italic>rpl9c</italic> homozygous for the transgene <italic>RPL9D:RPL9D</italic> (TG1 and TG2). Data is the mean ± SE (<italic>n</italic> = 8). Embryos from a silique of an <italic>rpl9c/+ rpl9d</italic> plant <bold>(E)</bold>. A mature wild type embryo (left) and a putative homozygous <italic>rpl9c rpl9d</italic> embryo arrested at a late globular stage of development (right).</p></caption><graphic xlink:href="fpls-06-01102-g002"></graphic></fig><p>The <italic>rpl9c rpl9d</italic> mutant was not identified in progeny of <italic>rpl9c rpl9d/+</italic> or <italic>rpl9c/+ rpl9d</italic>. Plants of these two genotypes showed 24.3% (<italic>n</italic> = 236) and 22.6% (<italic>n</italic> = 260) white seed, respectively, consistent with the double homozygous mutant being embryo lethal. By comparison, siliques of the single <italic>rpl9c</italic> and <italic>rpl9d</italic> mutants had 0% (<italic>n</italic> = 205) and 0.6% (<italic>n</italic> = 309) white seed, respectively. Examination of siliques from <italic>rpl9c/+ rpl9d</italic> plants showed embryos that were arrested at a late globular stage of development (<bold>Figure <xref ref-type="fig" rid="F2">2E</xref></bold>). Thus RPL9 levels in the <italic>rpl9c rpl9d</italic> double homozygous mutant are sufficient to support early stages of embryogenesis but are not sufficient to maintain growth throughout embryogenesis.</p></sec><sec><title><italic>RPL9</italic> Genes in the Brassicaceae</title><p><italic>RPL9B</italic> and <italic>RPL9C</italic> are tandem genes, separated by 11,136 bp on Chromosome 1. Comparison of <italic>RPL9B</italic> and <italic>RPL9C</italic> nucleotide sequence revealed a region of identical sequence extending from -927 bp upstream to +623 bp downstream of the AUG initiation codon (<bold>Figure <xref ref-type="fig" rid="F3">3A</xref></bold>). This sequence included the first exon, first intron and the 5′ half of the second exon. Nucleotide sequences of the 3′ half of the second exon and the third exon diverged and were 97% identical, whereas there was no significant sequence identity between the third intron of <italic>RPL9B</italic> and <italic>RPL9C</italic>. Comparison of these two genes with <italic>RPL9D</italic>, on Chromosome 4, showed that <italic>RPL9D</italic> is more divergent with the CDS sequence sharing 80% nucleotide sequence identity with <italic>RPL9B</italic> and <italic>RPL9C</italic> (<bold>Figure <xref ref-type="fig" rid="F3">3A</xref></bold>). <italic>RPL9B/RPL9C</italic> and <italic>RPL9D</italic> are located in syntenic regions of <italic>A. thaliana</italic> Chromosomes 1 and 4 (<bold>Supplementary Figure <xref ref-type="supplementary-material" rid="SM1">S1A</xref></bold>). These two regions are part of a recent whole genome duplication, the α duplication, which occurred 24–40 million years ago (<xref rid="B42" ref-type="bibr">Simillion et al., 2002</xref>; <xref rid="B4" ref-type="bibr">Blanc et al., 2003</xref>; <xref rid="B6" ref-type="bibr">Bowers et al., 2003</xref>).</p><fig id="F3" position="float"><label>FIGURE 3</label><caption><p><bold><italic>RPL9</italic> genes in Brassicaceae.</bold> Diagrammatic representation of <italic>A. thaliana</italic><bold>(A)</bold>, <italic>Arabidopsis lyrata</italic><bold>(B)</bold>, and <italic>Eutrema salsugineum</italic><bold>(C)</bold> genes showing UTR’s (red), exons (blue), non-coding upstream, and intron sequences (black line), and regions of 100% nucleotide sequence identity (green). Percentage nucleotide sequence identity of exons (excluding region in green box) is shown for gene pairs. Phylogenetic tree shown in <bold>(D)</bold> includes <italic>A. thaliana</italic>, <italic>A. lyrata</italic> (<italic>AlRPL9</italic>), <italic>Capsella rubella</italic> (<italic>CrRPL9</italic>), <italic>C. grandiflora</italic> (<italic>CagraRPL9</italic>), <italic>E. salsuginum</italic> (<italic>EsRPL9</italic>), <italic>B. rapa</italic> (<italic>BrRPL9</italic>), and <italic>Drosophila melanogaster</italic> (<italic>DmRPL9</italic>) genes.</p></caption><graphic xlink:href="fpls-06-01102-g003"></graphic></fig><p>To determine whether duplicate <italic>RPL9</italic> genes in <italic>A. thaliana</italic> are conserved in closely related species we compared <italic>RPL9</italic> family genes from <italic>A. lyrata</italic>, <italic>C. rubella, C. grandiflora, B. rapa</italic>, and <italic>E. salsugineum</italic> (<xref rid="B26" ref-type="bibr">Hu et al., 2011</xref>; <xref rid="B54" ref-type="bibr">Wang et al., 2011</xref>; <xref rid="B43" ref-type="bibr">Slotte et al., 2013</xref>; <xref rid="B57" ref-type="bibr">Yang et al., 2013</xref>). <italic>A. lyrata</italic>, which is most closely related to <italic>A. thaliana</italic>, has three <italic>RPL9</italic> genes. We notionally designated these genes <italic>AlRPL9B</italic>, <italic>AlRPL9C</italic>, and <italic>AlRPL9D</italic> according to the most closely related <italic>A. thaliana</italic> gene (Supplementary Table <xref ref-type="supplementary-material" rid="SM1">S1</xref>). As in <italic>A. thaliana, AlRPL9B</italic>, and <italic>AlRPL9C</italic> are linked by 8,119 bp and share a region of identical nucleotide sequence, extending from –167 to +245 bp, which includes the 5′ region of the first exon (<bold>Figure <xref ref-type="fig" rid="F3">3B</xref></bold>). The remaining coding regions of these two genes are 96% identical with no significant identity between the introns. <italic>AlRPL9D</italic> is more divergent and shares 80% sequence identity with <italic>AlRPL9B.</italic> Phylogenetic analysis showed the three genes in <italic>A. thaliana</italic> and <italic>A. lyrata</italic> fall into two distinct clades, which we named B and D group genes (<bold>Figure <xref ref-type="fig" rid="F3">3D</xref></bold>).</p><p><italic>Capsella rubella</italic> and <italic>C. grandiflora</italic> were found to have two and three <italic>RPL9</italic> genes, respectively. In contrast to <italic>A. thaliana</italic> and <italic>A. lyrata</italic>, the two <italic>Capsella</italic> species had B group but not D group genes (<bold>Figure <xref ref-type="fig" rid="F3">3D</xref></bold>). The additional gene in <italic>C. grandiflora</italic> appeared to be due to a recent gene duplication. <italic>CagraRPL9C1</italic> and <italic>CagraRPL9C2</italic> were adjacent direct repeats differing in a single nucleotide that altered the AUG initiation codon of <italic>CagraRPL9C2</italic> to TTG (<bold>Supplementary Figure <xref ref-type="supplementary-material" rid="SM1">S2</xref></bold>). This change to a non-canonical initiation codon suggests <italic>CagraRPL9C2</italic> may not encode a functional protein (<xref rid="B50" ref-type="bibr">Tikole and Sankararamakrishnan, 2006</xref>). <italic>E. salsugineum</italic> and <italic>B. rapa</italic> each had two B and two D group <italic>RPL9</italic> genes (<bold>Figure <xref ref-type="fig" rid="F3">3D</xref></bold>). <italic>E. salsugineum</italic> genes occurred as pairs of tandem genes. The B group genes <italic>EsRPL9B</italic> and <italic>EsRPL9C</italic> were linked by 12,130 bp, and the D group genes <italic>EsRPL9D</italic> and <italic>EsRPL9E</italic> were linked by 9,155 bp (Supplementary Table <xref ref-type="supplementary-material" rid="SM1">S1</xref>). Unlike the <italic>A. thaliana</italic> and <italic>A. lyrata</italic> B group genes, <italic>EsRPL9B</italic> and <italic>EsRPL9C</italic> did not share an extended region of identical sequence. However, <italic>EsRPL9D</italic> and <italic>EsRPL9E</italic> shared identical sequence extending from -287 bp upstream to +713 bp downstream of the AUG initiation codon. The 3′ exon and intron sequences had only four base pair differences, and the third exon in these two genes shared 99% identity (<bold>Figure <xref ref-type="fig" rid="F3">3C</xref></bold>).</p><p>The relationship between <italic>A. thaliana</italic>, <italic>A. lyrata, C. rubella</italic>, and <italic>E. salsugineum RPL9</italic> family genes was further investigated by determining whether these genes map to syntenic regions between each genome. Consistent with the phylogeny, B group genes of <italic>A. lyrata, C. rubella</italic> and <italic>E. salsugineum</italic> were in regions of synteny with <italic>A. thaliana</italic> Chromosome 1 carrying <italic>RPL9B</italic> and <italic>RPL9C</italic> genes (<bold>Supplementary Figure <xref ref-type="supplementary-material" rid="SM1">S1A</xref></bold>). Synteny was also identified between chromosomal regions carrying D group genes of <italic>A. thaliana, A. lyrata</italic> and <italic>E. salsugineum</italic> (<bold>Supplementary Figure <xref ref-type="supplementary-material" rid="SM1">S1B</xref></bold>). Notably the tandem gene pair <italic>EsRPL9D</italic>/<italic>EsRPL9E</italic> in <italic>E. salsugineum</italic> was located in a region of synteny with the single gene <italic>RPL9D</italic> in <italic>A. thaliana</italic> (<bold>Supplementary Figure <xref ref-type="supplementary-material" rid="SM1">S1B</xref></bold>). This suggests that there has been either a single gene loss or gain following the divergence of <italic>Arabidopsis</italic> and <italic>E. salsugineum</italic>. Potentially the pre-α duplication genome had two tandem <italic>RPL9</italic> genes. Subsequent to the α duplication the <italic>Arabidopsis</italic> lineage has lost one <italic>RPL9</italic> gene.</p></sec><sec><title><italic>RPL9</italic> Genes in Eudicots and Monocots</title><p>To further investigate the evolution of <italic>RPL9</italic> families within plants we analyzed <italic>RPL9</italic> genes from thirteen dicot and six monocot species. These represent a diverse range of plant taxa for which whole genome sequence was available. The number of <italic>RPL9</italic> genes in the dicot and monocot species ranges from 2 to 4 copies (<bold>Figure <xref ref-type="fig" rid="F4">4</xref></bold>). As in the Brassicaceae, tandem genes were found in the dicot species <italic>P. tichocarpa</italic>, <italic>P. vulgaris</italic>, and <italic>Carica papaya</italic> but were not found in the monocot species (Supplementary Table <xref ref-type="supplementary-material" rid="SM1">S1</xref>). Phylogenetic analysis showed that <italic>RPL9</italic> genes within a species tended to be more closely related to each other than to orthologs in distantly related species. The exceptions were for closely related species. The two <italic>Citrus</italic> and two <italic>Solanum</italic> species had one gene in each of three clusters (<bold>Figure <xref ref-type="fig" rid="F4">4A</xref></bold>). The closely related monocots <italic>Z. mays</italic> and <italic>S. bicolor</italic>, had <italic>RPL9</italic> genes in two separate clusters (<bold>Figure <xref ref-type="fig" rid="F4">4B</xref></bold>). The estimated gene trees suggest that <italic>RPL9</italic> family members undergo homogenization over time, leading to limited variation between genes within a species and greater variation of gene families between species. This lack of concordance between species and gene trees is a hallmark of concerted evolution (<xref rid="B1" ref-type="bibr">Arguello and Connallon, 2011</xref>).</p><fig id="F4" position="float"><label>FIGURE 4</label><caption><p><bold>Phylogeny of <italic>RPL9</italic> genes from angiosperm species.</bold> Tree for dicot species <bold>(A)</bold><italic>Aquilegia coerulea</italic> (<italic>AcRPL9</italic>)<italic>, Carica papaya</italic> (<italic>CpRPL9</italic>)<italic>, Citrus clementina</italic> (<italic>CcRPL9</italic>)<italic>, C. sinensis</italic> (<italic>CsRPL9</italic>)<italic>, Gossypium raimondii</italic> (<italic>GrRPL9</italic>)<italic>, Linum usitatissimum</italic> (<italic>LuRPL9</italic>)<italic>, Medicago truncatula</italic> (<italic>MtRPL9</italic>)<italic>, Mimulus guttatus</italic> (<italic>MgRPL9</italic>), <italic>P. vulgaris</italic> (<italic>PhvRPL9</italic>)<italic>, Poplar trichocarpa</italic> (<italic>PtRPL9</italic>)<italic>, Solanum lycopersicum</italic> (<italic>SlRPL9</italic>), <italic>S. tuberosum</italic> (<italic>StRPL9</italic>), and <italic>Vitis vinifera</italic> (<italic>VvRPL9</italic>). Tree for monocot species <bold>(B)</bold><italic>Brachypodium distachyon</italic> (<italic>BdRPL9</italic>)<italic>, Oryza sativa</italic> (<italic>OsRPL9</italic>)<italic>, Panicum virgatum</italic> (<italic>PvRPL9</italic>)<italic>, Setaria italica</italic> (<italic>SiRPL9</italic>), <italic>S. bicolor</italic> (<italic>SbRPL9</italic>), and <italic>Zea mays</italic> (<italic>ZmRPL9</italic>). <italic>D. melanogaster RPL9</italic> gene (<italic>DmRPL9</italic>) is the outgroup.</p></caption><graphic xlink:href="fpls-06-01102-g004"></graphic></fig></sec><sec><title><italic>RPL4, RPL5</italic>, <italic>RPL27a, RPL36a</italic>, and <italic>RPS6</italic> Genes in the Brassicaceae</title><p>We have shown that <italic>RPL9</italic> family genes have largely been retained during the divergence of the Brassicaceae but there is also evidence of rearrangements since divergence of different species. To investigate whether such rearrangements are common to other ribosomal protein gene families we examined phylogenetic relationships between members of five other ribosomal protein gene families in the Brassicaceae. The gene families selected for analysis included genes encoding RPL4, RPL5, RPL27a, RPL36a, and RPS6. In <italic>A. thaliana</italic>, each of these ribosomal proteins is encoded by two functional and redundant genes (<xref rid="B58" ref-type="bibr">Yao et al., 2008</xref>; <xref rid="B20" ref-type="bibr">Fujikura et al., 2009</xref>; <xref rid="B15" ref-type="bibr">Creff et al., 2010</xref>; <xref rid="B40" ref-type="bibr">Rosado et al., 2010</xref>; <xref rid="B10" ref-type="bibr">Casanova-Sáez et al., 2014</xref>; <xref rid="B59" ref-type="bibr">Zsögön et al., 2014</xref>).</p><p>The <italic>RPL4</italic> family in <italic>A. thaliana</italic> comprises two functional genes, <italic>RPL4A</italic> and <italic>RPL4D</italic>, which are in syntenic regions retained from the α duplication (<xref rid="B6" ref-type="bibr">Bowers et al., 2003</xref>; <xref rid="B40" ref-type="bibr">Rosado et al., 2010</xref>) (<bold>Figure <xref ref-type="fig" rid="F5">5A</xref></bold>, <bold>Supplementary Figure <xref ref-type="supplementary-material" rid="SM1">S3a</xref></bold>). Phylogenetic analysis showed that <italic>A. lyrata, C. rubella, C. grandiflora</italic>, and <italic>E. salsuginum</italic> had one gene that clustered with <italic>RPL4A</italic> and another gene that clustered with <italic>RPL4D</italic>, forming A and D groups (<bold>Figure <xref ref-type="fig" rid="F5">5C</xref></bold>). <italic>B. rapa</italic> had two genes in each of these groups. Analysis of <italic>A. thaliana, A. lyrata</italic>, and <italic>C. rubella</italic> chromosomal regions carrying A or D group genes showed these genes were in regions sharing synteny, indicating retention of A and D group genes in these species following the α duplication (<bold>Supplementary Figure <xref ref-type="supplementary-material" rid="SM1">S3a</xref></bold>). The <italic>RPL4</italic> family in <italic>A. thaliana</italic> also includes two pseudogenes, <italic>RPL4B</italic> and <italic>RPL4C</italic>, which comprise partial sequences (<xref rid="B2" ref-type="bibr">Barakat et al., 2001</xref>) (<bold>Figure <xref ref-type="fig" rid="F5">5A</xref></bold>). <italic>RPL4</italic> pseudogenes were also found in <italic>A. lyrata</italic> and <italic>C. rubella</italic> species (<bold>Figure <xref ref-type="fig" rid="F5">5B</xref></bold>). The pseudogenes formed distinct clusters, which we designated P group genes (<bold>Figure <xref ref-type="fig" rid="F5">5C</xref></bold>). In the P group, a single gene, <italic>EsRPL4C</italic>, was full length and was predicted to encode a functional protein (<bold>Supplementary Figure <xref ref-type="supplementary-material" rid="SM1">S4</xref></bold>). Although some P group genes occurred in regions of synteny, <italic>RPL4B, RPL4C, AlRPL4B</italic>, and <italic>CrRPL4C</italic> retained different <italic>RPL4</italic> sequences, and <italic>AlRPL4C</italic> had a base change that generated a premature stop codon (<bold>Supplementary Figures <xref ref-type="supplementary-material" rid="SM1">S3b</xref></bold> and <bold><xref ref-type="supplementary-material" rid="SM1">S4</xref></bold>). This suggests the pseudogenes were derived from independent events.</p><fig id="F5" position="float"><label>FIGURE 5</label><caption><p><bold><italic>RPL4</italic> genes in Brassicaceae.</bold> Diagrammatic representation of <italic>A. thaliana</italic> A group <bold>(A)</bold> and P group genes <bold>(B)</bold> showing UTR’s (red), exons (blue), non-coding upstream, and intron sequences (black line), and putative non-functional coding sequences (light blue). Percentage nucleotide sequence identity of exons is shown for <italic>A. thaliana</italic> genes and pseudogene pair. Phylogenetic tree of <italic>RPL4</italic> genes in Brassicaceae <bold>(C)</bold> includes genes of species listed in <bold>Figure <xref ref-type="fig" rid="F3">3</xref></bold>. The <italic>C. grandiflora RPL4C</italic> gene sequence used in phylogenetic analysis is likely incomplete.</p></caption><graphic xlink:href="fpls-06-01102-g005"></graphic></fig><p><italic>A. thaliana</italic> has two functional <italic>RPL5</italic> genes, <italic>RPL5A</italic> (also known as <italic>ATL5</italic>, <italic>PIGGYBACK3</italic>, <italic>ASYMMETRIC LEAVES1/2 ENHANCER6</italic>, <italic>OLIGOCELLULA5)</italic> and <italic>RPL5B</italic> (also known as <italic>OLIGOCELLULA7</italic>), as well as one pseudogene, <italic>RPL5C</italic> (<xref rid="B2" ref-type="bibr">Barakat et al., 2001</xref>; <xref rid="B36" ref-type="bibr">Pinon et al., 2008</xref>; <xref rid="B58" ref-type="bibr">Yao et al., 2008</xref>; <xref rid="B20" ref-type="bibr">Fujikura et al., 2009</xref>). Comparison of <italic>RPL5B</italic> and the pseudogene showed that they shared a 109 bp region of identical nucleotide sequence (<bold>Figure <xref ref-type="fig" rid="F6">6A</xref></bold>). Unlike <italic>RPL9</italic> and <italic>RPL4</italic>, the <italic>RPL5</italic> genes were not in syntenic regions of the <italic>A. thaliana</italic> genome, indicating these genes have not been retained from a recent genome duplication or that synteny in these chromosomal regions has been lost since genome duplication. Phylogenetic analysis showed that <italic>A. lyrata</italic>, <italic>C. rubella</italic>, and <italic>C. grandiflora</italic> had one gene that clustered with <italic>RPL5A</italic> and one gene that clustered with <italic>RPL5B</italic>, forming A and B groups (<bold>Figure <xref ref-type="fig" rid="F6">6B</xref></bold>). The <italic>A. thaliana, A. lyrata</italic>, and <italic>C. rubella</italic> genes in each group were in regions of synteny indicating a common origin (<bold>Supplementary Figures <xref ref-type="supplementary-material" rid="SM1">S5A,B</xref></bold>). A third <italic>A. lyrata</italic> gene, <italic>AlRPL5E</italic>, two <italic>E. salsuginum</italic>, and three <italic>B. rapa</italic> genes clustered into a group that was distinct from genes in <italic>Arabidopsis</italic> and <italic>Capsella</italic> species (<bold>Figure <xref ref-type="fig" rid="F6">6B</xref></bold>). <italic>AlRPL5E</italic> had no apparent ortholog in <italic>A. thaliana</italic> although <italic>AlRPL5E</italic> was located in a region of synteny with <italic>RPL5A</italic> (<bold>Supplementary Figure <xref ref-type="supplementary-material" rid="SM1">S5A</xref></bold>).</p><fig id="F6" position="float"><label>FIGURE 6</label><caption><p><bold><italic>RPL5</italic> genes in Brassicaceae.</bold> Diagrammatic representation of <italic>A. thaliana RPL5</italic> genes <bold>(A)</bold> showing UTR’s (red), exons (blue), non-coding upstream, and intron sequences (black line), exons of pseudogenes (light blue) and regions of 100% nucleotide identity (green). Percentage nucleotide sequence identity of exons is shown for genes and pseudogene. The phylogenetic tree of <italic>RPL5</italic> genes in Brassicaceae <bold>(B)</bold> includes genes of species as listed in <bold>Figure <xref ref-type="fig" rid="F3">3</xref></bold>.</p></caption><graphic xlink:href="fpls-06-01102-g006"></graphic></fig><p>The phylogeny of <italic>RPL27a</italic> showed two gene clusters. All species had a single gene in each cluster, except <italic>B. rapa</italic> where <italic>RPL27a</italic> genes were more closely related to each other than to <italic>RPL27a</italic> genes in the other Brassicaceae species (<bold>Supplementary Figure <xref ref-type="supplementary-material" rid="SM1">S6A</xref></bold>). In <italic>A. thaliana</italic>, the <italic>RPL36a</italic> family comprises <italic>RPL36aA</italic> and <italic>RPL36aB</italic> (also known as <italic>APICULATA2</italic>) (<xref rid="B2" ref-type="bibr">Barakat et al., 2001</xref>; <xref rid="B10" ref-type="bibr">Casanova-Sáez et al., 2014</xref>). Each Brassicaceae species had a <italic>RPL36a</italic> family member that clustered with <italic>RPL36aA</italic> and a member that clustered with <italic>RPL36aB</italic>, except for <italic>C. grandiflora</italic>, which only had one <italic>RPL36a</italic> gene, and <italic>B. rapa</italic>, which had several genes in each cluster (<bold>Supplementary Figure <xref ref-type="supplementary-material" rid="SM1">S6B</xref></bold>). Likewise, <italic>RPS6</italic> genes clustered into A and B groups and all species had a single gene in each group, with two exceptions. <italic>A. lyrata</italic> had no A group and two B group genes, and <italic>B. rapa</italic> had multiple genes in each group (<bold>Supplementary Figure <xref ref-type="supplementary-material" rid="SM1">S6C</xref></bold>).</p><p>In summary, the phylogenies of <italic>RPL4, RPL5</italic>, <italic>RPL27a, RPL36a</italic>, and <italic>RPS6</italic> ribosomal protein gene families show evidence of retention of genes following whole genome duplication. However, there is also evidence of gene gain and loss, partial gene loss, and some instances concerted evolution of genes within a species.</p></sec></sec><sec><title>Discussion</title><p>All ribosomal proteins in <italic>A. thaliana</italic> are encoded by small gene families. Typically members of a family encode proteins sharing 95–100% identity, although there are several exceptions where family members encode proteins that show as little as 70% amino acid identity (<xref rid="B2" ref-type="bibr">Barakat et al., 2001</xref>). Family members may be required to maintain the dose of a ribosomal protein or each member may encode a variant of a ribosomal protein that contributes to production of functionally heterogeneous ribosome populations (<xref rid="B11" ref-type="bibr">Chang et al., 2005</xref>; <xref rid="B9" ref-type="bibr">Carroll et al., 2007</xref>; <xref rid="B8" ref-type="bibr">Byrne, 2009</xref>; <xref rid="B25" ref-type="bibr">Horiguchi et al., 2012</xref>; <xref rid="B56" ref-type="bibr">Xue and Barna, 2012</xref>). <italic>RPL9C</italic> encodes a protein that shares 89% amino acid identity to the <italic>RPL9D</italic> encoded protein. Despite this divergence, genetic analysis indicates <italic>RPL9C</italic> and <italic>RPL9D</italic> are redundant. Firstly, mutation in <italic>RPL9D</italic> enhanced <italic>rpl9c</italic>, and conversely, mutation in <italic>RPL9C</italic> enhanced the phenotype of <italic>rpl9d</italic>. Secondly, increasing expression of <italic>RPL9D</italic>, by an <italic>RPL9D:RPL9D</italic> transgene, repressed the <italic>rpl9c</italic> mutant. Thirdly, the <italic>rpl9c rpl9d</italic> double homozygous mutant arrested at the globular stage of development. Embryo arrest at the globular stage is similar to the phenotype of <italic>aml1</italic>, and to <italic>embryo-defective</italic> (<italic>emb</italic>) mutants <italic>emb2167</italic> and <italic>emb2296</italic>, which correspond to mutations in cytoplasmic ribosomal protein genes <italic>RPL8A</italic> and <italic>RPL40B</italic> (<xref rid="B55" ref-type="bibr">Weijers et al., 2001</xref>; <xref rid="B51" ref-type="bibr">Tzafrir et al., 2004</xref>; <xref rid="B32" ref-type="bibr">Meinke, 2013</xref>). Deficiency of any one ribosomal protein impairs ribosome assembly or results in inefficient formation of translation-competent ribosomes (<xref rid="B18" ref-type="bibr">de la Cruz et al., 2015</xref>). As such it is predicted that inadequate levels of RPL9 lead to a reduction in ribosome production and impairment of translation.</p><p>Whole genome duplication is common in flowering plants and several duplications have occurred in dicot and monocot lineages (<xref rid="B6" ref-type="bibr">Bowers et al., 2003</xref>; <xref rid="B35" ref-type="bibr">Paterson et al., 2004</xref>). Genes encoding proteins that are dosage sensitive, such as transcription factors, signaling pathway, proteasome and ribosomal protein genes are preferentially retained following whole genome duplication (<xref rid="B19" ref-type="bibr">Freeling, 2009</xref>). The most recent genome duplication in the rosids, the α duplication, occurred prior to the <italic>Arabidopsis-Brassica</italic> split (<xref rid="B42" ref-type="bibr">Simillion et al., 2002</xref>; <xref rid="B4" ref-type="bibr">Blanc et al., 2003</xref>; <xref rid="B6" ref-type="bibr">Bowers et al., 2003</xref>). The phylogenetic trees of <italic>RPL9, RPL4, RPL5</italic>, <italic>RPL27a, RPL36a</italic>, and <italic>RPS6</italic> families in the Brassicaceae showed that genes clustered into two main groups, consistent with retention of ribosomal protein genes following the α duplication. Furthermore, <italic>RPL9</italic>, <italic>RPL4</italic>, and <italic>RPL5</italic> genes within a group map to regions of synteny indicating retention following genome duplication. However, there were exceptions in which closely related species varied in ribosomal protein gene copy number indicating recent gain or loss of family members. For example, an additional <italic>RPL9</italic> gene in <italic>E. salsugineum</italic> suggested loss of one <italic>RPL9</italic> gene after the divergence of the Camelineae species and <italic>E. salsugineum.</italic> Further <italic>RPL9</italic> gene loss and gene duplication appears to have occurred in <italic>Capsella</italic> species. Compared with <italic>A. thaliana</italic>, <italic>A. lyrata</italic> had an additional <italic>RPL5</italic> gene. <italic>B. rapa</italic> has undergone a recent whole genome triplication following divergence from <italic>A. thaliana</italic> (<xref rid="B54" ref-type="bibr">Wang et al., 2011</xref>). Retention of ribosomal protein genes following genome triplication would predict <italic>B. rapa</italic> to have six members of each ribosomal protein compared to two members in other Brassicaceae. All ribosomal protein families examined showed <italic>B. rapa</italic> genes occurred in higher copy number indicating that these genes have been retained following genome triplication. However, all families had fewer than six genes indicating a tendency toward loss of ribosomal protein genes. Pseudogenes resulting from partial gene deletion were present in several families and were most notable in the <italic>RPL4</italic> family. Surprisingly <italic>RPL4</italic> pseudogenes appeared to have been generated through independent deletion events. Potentially these genes are in chromosomal regions subject to frequent rearrangements.</p><p>Phylogenies of <italic>RPL9</italic> genes in distantly related dicot and monocot species showed clustering of genes within a species rather than between species. A trend where genes within a species are closely related and cluster in a phylogenetic tree was also evident for some <italic>RPL5</italic> and <italic>RPL27a</italic> genes in the Brassicaceae. Such gene relationships indicate ribosomal protein genes in plants undergo concerted evolution (<xref rid="B1" ref-type="bibr">Arguello and Connallon, 2011</xref>). Furthermore <italic>RPL9</italic> genes in <italic>A. thaliana</italic>, <italic>A. lyrata</italic>, and <italic>E. salsuginum</italic> showed extended regions of identical nucleotide sequence characteristic of recent gene conversion events through homologous recombination between tandem copies of ribosomal protein genes (<xref rid="B12" ref-type="bibr">Chen et al., 2007</xref>). Concerted evolution of ribosomal protein genes is also observed in <italic>Saccharomyces cereviseae</italic> and closely related yeast species (<xref rid="B21" ref-type="bibr">Gao and Innan, 2004</xref>). Gene conversion could serve to maintain conservation of proteins that contribute to a complex macromolecule. In this case, amino acids that have low functional significance in a ribosomal protein would vary between between plant species. Interestingly, tandemly arrayed ribosomal RNA genes also undergo concerted evolution and maintain a high level of sequence homogeneity in eukaryotes (<xref rid="B7" ref-type="bibr">Brown et al., 1972</xref>; <xref rid="B14" ref-type="bibr">Copenhaver and Pikaard, 1996</xref>; <xref rid="B22" ref-type="bibr">Gonzalez and Sylvester, 2001</xref>; <xref rid="B44" ref-type="bibr">Stage and Eickbush, 2007</xref>). Potentially, ribosomal protein genes and rRNA co-evolve in order to maintain optimal RNA-protein interactions in the ribosome and limit synthesis of inefficient ribosomes (<xref rid="B38" ref-type="bibr">Roberts et al., 2008</xref>).</p><p>Ribosomal protein gene copy number in plants appears to be under constraint consistent with the gene balance hypothesis. Mechanisms maintaining gene copy number involves retention of paralogs following whole genome duplication. However, partial or whole gene deletion, tandem duplication and gene conversion are prominent features of ribosomal protein gene families across species, reflecting dynamic evolution of these genes.</p></sec><sec><title>Author Contributions</title><p>DD, SF, ZL, and MB carried out the experiments, prepared the figures, and reviewed the manuscript. MB wrote the manuscript.</p></sec><sec><title>Conflict of Interest Statement</title><p>The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.</p></sec></body><back><ack><p>We thank Simon Ho for advice on phylogenetic analyses. This work was supported by the University of Sydney and Australian Research Council Discovery Project grant DP130101186.</p></ack><sec sec-type="supplementary material"><title>Supplementary Material</title><p>The Supplementary Material for this article can be found online at: <ext-link ext-link-type="uri" xlink:href="http://journal.frontiersin.org/article/10.3389/fpls.2015.01102">http://journal.frontiersin.org/article/10.3389/fpls.2015.01102</ext-link></p><supplementary-material content-type="local-data" id="SM1"><media xlink:href="Image_1.PDF"><caption><p>Click here for additional data file.</p></caption></media><p><bold>FIGURE S1 |<italic>RPL9</italic> genes in Brassicaceae occur in regions of synteny.</bold> CoGe outputs showing chromosomal regions of synteny. Region of <italic>A. thaliana</italic> Chromosome 1, around <italic>RPL9B</italic> and <italic>RPL9C</italic>, aligned with the region of Chromosome 4 carrying <italic>RPL9D</italic>, <italic>A. lyrata</italic> region around <italic>AlRPL9B</italic> and <italic>AlRPL9C</italic>, and <italic>E. salsuginum</italic> region around <italic>EsRPL9B</italic> and <italic>EsRPL9C</italic><bold>(A)</bold>. Region of <italic>A. thaliana RPL9D</italic> aligned with <italic>A. lyrata</italic> region around <italic>AlRPL9D</italic> and <italic>E. salsuginum</italic> region around <italic>EsRPL9D</italic> and <italic>EsRPL9E</italic><bold>(B)</bold>. Chromosomes are indicated as dotted black lines with genes (green) indicated on both Watson and Crick strands. Unsequenced regions are marked (orange). Regions of identified sequence similarity (pink) are shown above the chromosomes. Interconnecting lines between chromosomes (pink) mark <italic>RPL9</italic> genes.</p><p><bold>FIGURE S2 | Tandem <italic>C. grandiflora RPL9</italic> genes.</bold> Nucleotide sequence of <italic>CagraRPL9C1</italic> (solid underline) and <italic>CagraRPL9C2</italic> (dotted underline) genes. Exons (orange) and introns (black, lower case) are shown with initiation codons highlighted in green and stop codons highlighted in yellow.</p><p><bold>FIGURE S3 |<italic>RPL4</italic> genes in Brassicaceae occur in regions of synteny.</bold> CoGe outputs showing regions of synteny around <italic>A. thaliana RPL4D</italic> and <italic>RPL4A</italic>, <italic>A. thaliana RPL4D</italic> and <italic>A. lyrata AlRPL4D</italic> and <italic>A. thaliana RPL4D</italic>, and <italic>C. rubella CrRPL4D</italic><bold>(A)</bold>, and regions of synteny around <italic>A. thaliana RPL4C</italic> and <italic>A. lyrata AlRPL4C</italic>, and <italic>A. thaliana RPL4C</italic> and <italic>C. rubella CrRPL4C</italic><bold>(B)</bold>. Chromosomes are indicated as dotted black lines with genes (green) indicated on both Watson and Crick strands. Regions of identified sequence similarity (pink) are shown above the chromosomes. Interconnecting lines between chromosomes (pink) mark <italic>RPL4</italic> genes.</p><p><bold>FIGURE S4 | <italic>RPL4</italic> pseudogenes in Brassicaceae.</bold> Alignment of nucleotide sequences of P group genes. Start and stop codons are highlighted in red. The <italic>C. grandiflora RPL4C</italic> gene sequence is likely incomplete.</p><p><bold>FIGURE S5 |<italic>RPL5</italic> genes in Brassicaceae occur in regions of synteny.</bold> CoGe outputs showing regions of synteny around <italic>A. thaliana RPL5A</italic><bold>(A)</bold> and <italic>RPL5B</italic><bold>(B)</bold> genes with <italic>RPL5</italic> genes in <italic>A. lyrata</italic> and <italic>C. rubella.</italic> Chromosomes are indicated as dotted black lines with genes (green) indicated on both Watson and Crick strands. Regions of identified sequence similarity (pink) are shown above the chromosomes. Interconnecting lines between chromosomes (pink) mark <italic>RPL5</italic> genes.</p><p><bold>FIGURE S6 | Phylogenetic trees of <italic>RPL27a, RPL36a</italic>, and <italic>RPS6</italic> genes in Brassicaceae.</bold> Phylogenetic trees of <italic>RPL27a</italic><bold>(A)</bold><italic>, RPL36a</italic><bold>(B),</bold> and <italic>RPS6</italic><bold>(C)</bold> includes <italic>A. thaliana</italic>, <italic>A. lyrata</italic>, <italic>C. rubella</italic>, <italic>C. grandiflora</italic>, <italic>E. salsuginum</italic>, <italic>B. rapa</italic>, and <italic>D. melanogaster</italic> genes.</p></supplementary-material><supplementary-material content-type="local-data" id="S1"><media xlink:href="Image_1.PDF"><caption><p>Click here for additional data file.</p></caption></media></supplementary-material></sec><ref-list><title>References</title><ref id="B1"><mixed-citation publication-type="journal"><person-group person-group-type="author"><name><surname>Arguello</surname><given-names>J. 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