The plastid chromosome of Atropa belladonna and its comparison with that of Nicotiana tabacum: the role of RNA editing in generating divergence in the process of plant speciation.

The nuclear and plastid genomes of the plant cell form a coevolving unit which in interspecific combinations can lead to genetic incompatibility of compartments even between closely related taxa. This phenomenon has been observed for instance in Atropa-Nicotiana cybrids. We have sequenced the plastid chromosome of Atropa belladonna (deadly nightshade), a circular DNA molecule of 156,688 bp, and compared it with the corresponding published sequence of its relative Nicotiana tabacum (tobacco) to understand how divergence at the level of this genome can contribute to nuclear-plastid incompatibilities and to speciation. It appears that (1) regulatory elements, i.e., promoters as well as translational and replicational signal elements, are well conserved between the two species; (2) genes--including introns--are even more highly conserved, with differences residing predominantly in regions of low functional importance; and (3) RNA editotypes differ between the two species, which makes this process an intriguing candidate for causing rapid reproductive isolation of populations.

[1]  P. Medgyesy,et al.  Intertrubal chloroplast transfer by protoplast fusion between Nicotiana tabacum and Salpiglossis sinuata , 1988, Molecular and General Genetics MGG.

[2]  F. Sanger,et al.  DNA sequencing with chain-terminating inhibitors. , 1977, Proceedings of the National Academy of Sciences of the United States of America.

[3]  M. Kunnimalaiyaan,et al.  Fine mapping of replication origins (ori A and ori B) in Nicotiana tabacum chloroplast DNA. , 1997, Nucleic acids research.

[4]  F. Takaiwa,et al.  The complete nucleotide sequence of the tobacco chloroplast genome: its gene organization and expression , 1986, The EMBO journal.

[5]  K. Isono,et al.  Structural features of a wheat plastome as revealed by complete sequencing of chloroplast DNA , 2001, Zeitschrift für Induktive Abstammungs- und Vererbungslehre.

[6]  F. Zito,et al.  Mutations of cytochrome b6 in Chlamydomonas reinhardtii disclose the functional significance for a proline to leucine conversion by petB editing in maize and tobacco , 2004, Plant Molecular Biology.

[7]  V. Ramakrishnan,et al.  Another piece of the ribosome: solution structure of S16 and its location in the 30S subunit. , 2000, Structure.

[8]  D. Karcher,et al.  The Amino Acid Sequence of a Plastid Protein Is Developmentally Regulated by RNA Editing* , 2002, The Journal of Biological Chemistry.

[9]  S. Berger,et al.  Functional cybrid plants possessing a Nicotiana genome and an Atropa plastome , 1987, Molecular and General Genetics MGG.

[10]  M. Sugiura,et al.  The chloroplast genome. , 1992, Plant molecular biology.

[11]  T. Hirose,et al.  RNA editing sites in tobacco chloroplast transcripts: editing as a possible regulator of chloroplast RNA polymerase activity , 1999, Molecular and General Genetics MGG.

[12]  P. Maliga,et al.  Transcription from heterologous rRNA operon promoters in chloroplasts reveals requirement for specific activating factors. , 1998, Plant physiology.

[13]  M. Sugiura,et al.  Targeted deletion of sprA from the tobacco plastid genome indicates that the encoded small RNA is not essential for pre-16S rRNA maturation in plastids , 1997, Molecular and General Genetics MGG.

[14]  R. Bock,et al.  Introduction of a heterologous editing site into the tobacco plastid genome: the lack of RNA editing leads to a mutant phenotype. , 1994, The EMBO journal.

[15]  E. Pohl,et al.  The Structure of the Chloroplast F1-ATPase at 3.2 Å Resolution* , 2001, The Journal of Biological Chemistry.

[16]  J. Palmer,et al.  Function and evolution of a minimal plastid genome from a nonphotosynthetic parasitic plant. , 1992, Proceedings of the National Academy of Sciences of the United States of America.

[17]  Weihe,et al.  Transcription and the architecture of promoters in chloroplasts. , 1999, Trends in plant science.

[18]  The ndhH genes of gramminean plastomes are linked with the junctions between small single copy and inverted repeat regions , 1990, Current Genetics.

[19]  R. Herrmann,et al.  Heterologous, splicing‐dependent RNA editing in chloroplasts: allotetraploidy provides trans‐factors , 2001, The EMBO journal.

[20]  J. Hamill,et al.  Somatic hybridization of Nicotiana tabacum and Petunia hybrida , 1986, Molecular and General Genetics MGG.

[21]  G. B. Golding,et al.  The mosaic nature of the eukaryotic nucleus. , 1998, Molecular biology and evolution.

[22]  M. Sugiura,et al.  Cis‐acting elements and trans‐acting factors for accurate translation of chloroplast psbA mRNAs: development of an in vitro translation system from tobacco chloroplasts. , 1996, The EMBO journal.

[23]  R. Bock,et al.  The two largest chloroplast genome-encoded open reading frames of higher plants are essential genes. , 2000, The Plant journal : for cell and molecular biology.

[24]  M. Sugiura,et al.  Regulation of gene expression in chloroplasts of higher plants , 1996, Plant Molecular Biology.

[25]  P. Bell,et al.  Viral Eukaryogenesis: Was the Ancestor of the Nucleus a Complex DNA Virus? , 2001, Journal of Molecular Evolution.

[26]  R. Bock Sense from nonsense: how the genetic information of chloroplasts is altered by RNA editing. , 2000, Biochimie.

[27]  Hiro Iguchi,et al.  Chloroplast RNA Editing Required for Functional Acetyl-CoA Carboxylase in Plants* , 2001, The Journal of Biological Chemistry.

[28]  Wen-Hsiung Li,et al.  Rates of nucleotide substitution vary greatly among plant mitochondrial, chloroplast, and nuclear DNAs. , 1987, Proceedings of the National Academy of Sciences of the United States of America.

[29]  H. A. Orr,et al.  The genetics of species differences. , 2001 .

[30]  M. Hasegawa,et al.  Gene transfer to the nucleus and the evolution of chloroplasts , 1998, Nature.

[31]  R. Bock,et al.  Extraplastidic site‐specific factors mediate RNA editing in chloroplasts , 1997, The EMBO journal.

[32]  R. Brimacombe,et al.  A new model for the three-dimensional folding of Escherichia coli 16 S ribosomal RNA. II. The RNA-protein interaction data. , 1997, Journal of molecular biology.

[33]  H. Carrer,et al.  Site‐specific factor involved in the editing of the psbL mRNA in tobacco plastids. , 1995, The EMBO journal.

[34]  B. Sears,et al.  Plastome-genome interactions affect plastid transmission in Oenothera. , 1993, Genetics.

[35]  J. Palmer,et al.  Isolation and structural analysis of chloroplast DNA , 1986 .

[36]  W. Martin,et al.  Distribution and Nomenclature of Protein-coding Genes in 12 Sequenced Chloroplast Genomes , 1998, Plant Molecular Biology Reporter.

[37]  M. Renard,et al.  Intergeneric cytoplasmic hybridization in cruciferae by protoplast fusion , 1983, Molecular and General Genetics MGG.

[38]  Y. Du,et al.  RbcS suppressor mutations improve the thermal stability and CO2/O2 specificity of rbcL- mutant ribulose-1,5-bisphosphate carboxylase/oxygenase. , 2000, Proceedings of the National Academy of Sciences of the United States of America.

[39]  P. Maliga,et al.  Conservation of RNA editing between rice and maize plastids: are most editing events dispensable? , 2000, Molecular Genetics and Genomics.

[40]  Vincent Savolainen,et al.  The atpB and rbcL promoters in plastid DNAs of a wide dicot range , 1994, Journal of Molecular Evolution.

[41]  F. Cohen,et al.  Co-evolution of proteins with their interaction partners. , 2000, Journal of molecular biology.

[42]  H. Koop,et al.  Integration of foreign sequences into the tobacco plastome via polyethylene glycol-mediated protoplast transformation , 2004, Planta.

[43]  M. Sugiura,et al.  A novel RNA gene in the tobacco plastid genome: its possible role in the maturation of 16S rRNA. , 1994, The EMBO journal.

[44]  Petra Fromme,et al.  Three-dimensional structure of cyanobacterial photosystem I at 2.5 Å resolution , 2001, Nature.

[45]  G. Schuster,et al.  Processing and degradation of chloroplast mRNA. , 2000, Biochimie.

[46]  E. Merlin,et al.  The role of insertions/deletions in the evolution of the intergenic region betweenpsbA andtrnH in the chloroplast genome , 1988, Current Genetics.

[47]  P. Michaelis Cytoplasmic inheritance in Epilobium and its theoretical significance. , 1954, Advances in genetics.

[48]  A. Barkan,et al.  Participation of nuclear genes in chloroplast gene expression. , 2000, Biochimie.

[49]  H. Kössel,et al.  Occurrence of plastid RNA editing in all major lineages of land plants. , 1997, Proceedings of the National Academy of Sciences of the United States of America.

[50]  R. Brimacombe,et al.  A new model for the three-dimensional folding of Escherichia coli 16 S ribosomal RNA. I. Fitting the RNA to a 3D electron microscopic map at 20 A. , 1997, Journal of molecular biology.

[51]  B. Stoebe,et al.  Gene-cluster analysis in chloroplast genomics. , 1999, Trends in genetics : TIG.

[52]  P. Taberlet,et al.  The use of chloroplast DNA to resolve plant phylogenies: noncoding versus rbcL sequences. , 1994, Molecular biology and evolution.

[53]  W. F. Thompson,et al.  Rapid isolation of high molecular weight plant DNA. , 1980, Nucleic acids research.

[54]  M. Kunnimalaiyaan,et al.  Analysis of the tobacco chloroplast DNA replication origin (oriB) downstream of the 23 S rRNA gene. , 1997, Journal of molecular biology.

[55]  E. Babiychuk,et al.  Nucleo-cytoplasmic incompatibility in cybrid plants possessing an Atropa genome and a Nicotiana plastome , 1991, Molecular and General Genetics MGG.

[56]  P. Maliga,et al.  High-frequency plastid transformation in tobacco by selection for a chimeric aadA gene. , 1993, Proceedings of the National Academy of Sciences of the United States of America.

[57]  M. Sugiura,et al.  Evolution and mechanism of translation in chloroplasts. , 1998, Annual review of genetics.

[58]  E. Galun,et al.  Nuclear-organelle interaction in Solanum: Interspecific cybridizations and their correlation with a plastome dendrogram , 1991, Molecular and General Genetics MGG.

[59]  H. Uchimiya,et al.  Location and nucleotide sequence of a tobacco chlorophlast DNA segment capable of replication in yeast , 1984, Molecular and General Genetics MGG.

[60]  P. Maliga,et al.  Light‐responsive and transcription‐enhancing elements regulate the plastid psbD core promoter. , 1995, The EMBO journal.

[61]  W Zerges,et al.  Translation in chloroplasts. , 2000, Biochimie.

[62]  R. Mache,et al.  The plastid chromosome of spinach (Spinacia oleracea): complete nucleotide sequence and gene organization , 2001, Plant Molecular Biology.

[63]  H. A. Orr,et al.  The population genetics of speciation: the evolution of hybrid incompatibilities. , 1995, Genetics.

[64]  K. Umesono,et al.  Comparative and functional anatomy of group II catalytic introns--a review. , 1989, Gene.

[65]  K. Steinback,et al.  Fusion-mediated transfer of triazine-resistant chloroplasts: Characterization of Nicotiana tabacum cybrid plants , 1986, Molecular and General Genetics MGG.

[66]  John M. Hancock,et al.  Simple sequences and the expanding genome. , 1996, BioEssays : news and reviews in molecular, cellular and developmental biology.

[67]  C. C. Lindegren CYTOPLASMIC INHERITANCE , 1957, Annals of the New York Academy of Sciences.

[68]  O. Renner Artbastarde bei Pflanzen , 1929 .

[69]  Monique Turmel,et al.  Ancestral chloroplast genome in Mesostigma viride reveals an early branch of green plant evolution , 2000, Nature.

[70]  M. Sugiura,et al.  Identification of Two Essential Sequence Elements in the Nonconsensus Type II PatpB-290 Plastid Promoter by Using Plastid Transcription Extracts from Cultured Tobacco BY-2 Cells , 1999, Plant Cell.

[71]  M. W. Gray,et al.  Evolution of organellar genomes. , 1999, Current opinion in genetics & development.

[72]  P. Maliga,et al.  In vitro characterization of the tobacco rpoB promoter reveals a core sequence motif conserved between phage‐type plastid and plant mitochondrial promoters , 1999, The EMBO journal.

[73]  B. Sears,et al.  Proliferation of direct repeats near the Oenothera chloroplast DNA origin of replication. , 1996, Molecular biology and evolution.

[74]  C. Shaw Plant molecular biology: a practical approach. , 1988 .

[75]  G. Igloi,et al.  Complete sequence of the maize chloroplast genome: gene content, hotspots of divergence and fine tuning of genetic information by transcript editing. , 1995, Journal of molecular biology.

[76]  M. Sugiura,et al.  Comparative Analysis of RNA Editing Sites in Higher Plant Chloroplasts , 2001, Journal of Molecular Evolution.

[77]  C. dePamphilis,et al.  Purifying selection detected in the plastid gene matK and flanking ribozyme regions within a group II intron of nonphotosynthetic plants. , 2000, Molecular biology and evolution.

[78]  Richard H. Ebright,et al.  Promoter structure, promoter recognition, and transcription activation in prokaryotes , 1994, Cell.

[79]  A. Barkan,et al.  Molecular cloning of the maize gene crp1 reveals similarity between regulators of mitochondrial and chloroplast gene expression , 1999, The EMBO journal.

[80]  L A Allison,et al.  The role of sigma factors in plastid transcription. , 2000, Biochimie.

[81]  G. Gutman,et al.  Slipped-strand mispairing: a major mechanism for DNA sequence evolution. , 1987, Molecular biology and evolution.