Variation and Inheritance of Nuclear Ribosomal DNA Clusters in Streptocarpus (Gesneriaceae) and Their Biological and Phylogenetic Implications

Chromosomal fluorescent in situ hybridization (FISH) and PCR fragment intensity analysis were used to determine the number and sizes of 45S nuclear ribosomal DNA (nrDNA) arrays and their inheritance in two Streptocarpus species, Streptocarpus rexii and Streptocarpus dunnii. A strong correlation between 45S nrDNA signals and PCR band intensity was observed. They revealed two loci in both species, with variation in nrDNA copy number within arrays: S. rexii had relatively homogeneous loci, while one individual of S. dunnii was heterozygous at the main locus, possessing a large and a small nrDNA array, and homozygous at the second locus, which was very small. This small nrDNA array was not PCR detectable and explains the non‐Mendelian results in some backcrosses. Our results indicated that nrDNA sequences in Streptocarpus were highly homogenized and that the inheritance of nrDNA was additive without any detectable recombination. PCR segregation of 45S nrDNA markers in backcross plants supported the hypothesis that the two loci detected by FISH were unlinked. The minute locus in S. dunnii may indicate a mechanism by which the number of nrDNA sites can change in plants. The backcross results demonstrated the dynamics of nrDNA inheritance and the swiftness of the replacement of parental types within two generations when hybridization is involved in plant evolution.

[1]  M. Möller,et al.  Refugia, dispersal and divergence in a forest archipelago: a study of Streptocarpus in eastern South Africa , 2005, Molecular ecology.

[2]  D. Soltis,et al.  Rapid Concerted Evolution of Nuclear Ribosomal DNA in Two Tragopogon Allopolyploids of Recent and Recurrent Origin Sequence data from this article have been deposited with the EMBL/GenBank Data Libraries under accession nos. AY458586, AY458588, AY458589, and AY458587 , 2005, Genetics.

[3]  J. Manen.  Are both sympatric species Ilex perado and Ilex canariensis secretly hybridizing? Indication from nuclear markers collected in Tenerife , 2004, BMC Evolutionary Biology.

[4]  D. Soltis,et al.  Molecular cytogenetic analysis of recently evolved Tragopogon (Asteraceae) allopolyploids reveal a karyotype that is additive of the diploid progenitors. , 2004, American journal of botany.

[5]  J. Doyle,et al.  Multiple origins and nrDNA internal transcribed spacer homeologue evolution in the Glycine tomentella (Leguminosae) allopolyploid complex. , 2004, Genetics.

[6]  P. Ruas,et al.  Characterization of Diploid, Tetraploid and Hexaploid Helianthus Species by Chromosome Banding and FISH with 45S rDNA Probe , 2002, Genetica.

[7]  K. Yamato,et al.  Bryophyte 5S rDNA was inserted into 45S rDNA repeat units after the divergence from higher land plants , 1999, Plant Molecular Biology.

[8]  J. S. Heslop-Harrison,et al.  rRNA gene activity and control of expression mediated by methylation and imprinting during embryo development in wheat x rye hybrids , 1995, Theoretical and Applied Genetics.

[9]  R. Jansen,et al.  Comparisons of phylogenetic hypotheses among different data sets in dwarf dandelions (Krigia, Asteraceae): Additional information from internal transcribed spacer sequences of nuclear ribosomal DNA , 1994, Plant Systematics and Evolution.

[10]  K. Bachmann,et al.  Nuclear DNA markers of the Australian tetraploid Microseris scapigera and its North American diploid relatives , 1993, Theoretical and Applied Genetics.

[11]  P. Taberlet,et al.  Universal primers for amplification of three non-coding regions of chloroplast DNA , 1991, Plant Molecular Biology.

[12]  S. Rogers,et al.  Ribosomal RNA genes in plants: variability in copy number and in the intergenic spacer , 1987, Plant Molecular Biology.

[13]  R. Jorgensen,et al.  Structure and variation in ribosomal RNA genes of pea , 2004, Plant Molecular Biology.

[14]  J. Wendel,et al.  Ribosomal ITS sequences and plant phylogenetic inference. , 2003, Molecular phylogenetics and evolution.

[15]  S. Harris,et al.  Characterization of angiosperm nrDNA polymorphism, paralogy, and pseudogenes. , 2003, Molecular phylogenetics and evolution.

[16]  M. Möller,et al.  PLASTID INHERITANCE IN STREPTOCARPUS ( GESNERIACEAE ) AND AN INFERRED HYBRID ORIGIN FOR A POPULATION OF S . AFF. PRIMULIFOLIUS FROM IGODA RIVER, SOUTH AFRICA , 2003 .

[17]  Antony V. Cox,et al.  Molecular systematics, GISH and the origin of hybrid taxa in Nicotiana (Solanaceae). , 2003, Annals of botany.

[18]  J. Plummer,et al.  Cyto-evolution of Boronia genomes revealed by fluorescent in situ hybridization with rDNA probes. , 2003, Genome.

[19]  A. Santos‐Guerra,et al.  Genome organization in diploid hybrid species of Argyranthemum (Asteraceae) in the Canary Islands , 2003 .

[20]  G. Hoarau,et al.  Inheritance patterns of ITS1, chloroplasts and mitochondria in artificial hybrids of the seaweeds Fucus serratus and F. evanescens (Phaeophyceae) , 2002 .

[21]  Q. Cronk,et al.  Evolution in Aeschynanthus (Gesneriaceae) inferred from ITS sequences , 2001, Plant Systematics and Evolution.

[22]  Q. Cronk,et al.  Evolution and alignment of the hypervariable arm 1 of Aeschynanthus (Gesneriaceae) ITS2 nuclear ribosomal DNA. , 2001, Molecular phylogenetics and evolution.

[23]  Q. Cronk,et al.  EVOLUTION OF MORPHOLOGICAL NOVELTY: A PHYLOGENETIC ANALYSIS OF GROWTH PATTERNS IN STREPTOCARPUS (GESNERIACEAE) , 2001, Evolution; international journal of organic evolution.

[24]  T. Morikawa,et al.  Intraspecific variation of 18S-5.8S-26S rDNA sites revealed by FISH and RFLP in wild oat, Avena agadiriana. , 2001, Genes & genetic systems.

[25]  C. Schlötterer,et al.  Three divergent rDNA clusters predate the species divergence in Quercus petraea (Matt.) Liebl. and Quercus robur L. , 2001, Molecular biology and evolution.

[26]  M. Chase,et al.  Ribosomal DNA evolution and phylogeny in Aloe (Asphodelaceae). , 2000, American journal of botany.

[27]  Q. Cronk,et al.  High intraindividual variation in internal transcibed spacer sequences in Aeschynanthus (Gesneriaceae): implications for phylogenetics , 2000, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[28]  M. Möller.  HOW UNIVERSAL ARE UNIVERSAL rDNA PRIMERS? A CAUTIONARY NOTE FOR PLANT SYSTEMATISTS AND PHYLOGENETICISTS , 2000 .

[29]  R. Matyášek,et al.  Molecular cytogenetic analyses and phylogenetic studies in the Nicotiana section Tomentosae , 2000, Chromosoma.

[30]  R. Matyášek,et al.  Gene conversion of ribosomal DNA in Nicotiana tabacum is associated with undermethylated, decondensed and probably active gene units , 2000, Chromosoma.

[31]  C. Vosa.  A revised cytotaxonomy of the genus Tulbaghia (Alliaceae) , 2000 .

[32]  O. Panaud,et al.  Molecular-cytogenetic studies of ribosomal genes and heterochromatin reveal conserved genome organization among 11 Quercus species , 1999, Theoretical and Applied Genetics.

[33]  T. Sang,et al.  Physical mapping of ribosomal RNA genes in peonies (Paeonia, Paeoniaceae) by fluorescent in situ hybridization: implications for phylogeny and concerted evolution. , 1999, American journal of botany.

[34]  A. Franzke,et al.  Recent hybrid speciation in Cardamine (Brassicaceae) – conversion of nuclear ribosomal ITS sequences in statu nascendi , 1999, Theoretical and Applied Genetics.

[35]  J. Crouch,et al.  Molecular Cytogenetics of Musa Species, Cultivars and Hybrids: Location of 18S-5.8S-25S and 5S rDNA and Telomere-like Sequences , 1998 .

[36]  R. Jiménez,et al.  Sequential silver staining and in situ hybridization reveal a direct association between rDNA levels and the expression of homologous nucleolar organizing regions: a hypothesis for NOR structure and function. , 1998, Journal of cell science.

[37]  Q. Cronk,et al.  Phylogeny and disjunct distribution: evolution of Saintpaulia (Gesneriaceae) , 1997, Proceedings of the Royal Society of London. Series B: Biological Sciences.

[38]  J. S. Heslop-Harrison,et al.  Physical mapping of the 5S ribosomal RNA genes in Arabidopsis thaliana by multi-color fluorescence in situ hybridization with cosmid clones. , 1997, The Plant journal : for cell and molecular biology.

[39]  Q. Cronk,et al.  Origin and relationships of Saintpaulia (Gesneriaceae) based on ribosomal DNA internal transcribed spacer (ITS) sequences. , 1997, American journal of botany.

[40]  M. Koch,et al.  Molecular phylogenetics of Thlaspi s.l. (Brassicaceae) based on chloroplast DNA restriction site variation and sequences of the internal transcribed spacers of nuclear ribosomal DNA. , 1997 .

[41]  R. Jiménez,et al.  Interchromosomal, intercellular and interindividual variability of NORs studied with silver staining and in situ hybridization , 1997, Heredity.

[42]  D. Soltis,et al.  The Origins of Arabidopsis suecica (Brassicaceae) as Indicated by Nuclear rDNA Sequences , 1996 .

[43]  C. Pikaard,et al.  Two-dimensional RFLP analyses reveal megabase-sized clusters of rRNA gene variants in Arabidopsis thaliana, suggesting local spreading of variants as the mode for gene homogenization during concerted evolution. , 1996, The Plant journal : for cell and molecular biology.

[44]  A. Wolfe,et al.  Evidence of Chloroplast Capture and Pollen-mediated Gene Flow in Penstemon sect. Peltanthera (Scrophulariaceae) , 1995 .

[45]  J. Wendel,et al.  An unusual ribosomal DNA sequence from Gossypium gossypioides reveals ancient, cryptic, intergenomic introgression. , 1995, Molecular phylogenetics and evolution.

[46]  J. Elder,et al.  Concerted Evolution of Repetitive DNA Sequences in Eukaryotes , 1995, The Quarterly Review of Biology.

[47]  D. Soltis,et al.  DISCORDANCE BETWEEN NUCLEAR AND CHLOROPLAST PHYLOGENIES IN THE HEUCHERA GROUP (SAXIFRAGACEAE) , 1995, Evolution; international journal of organic evolution.

[48]  T. Sang,et al.  Documentation of reticulate evolution in peonies (Paeonia) using internal transcribed spacer sequences of nuclear ribosomal DNA: implications for biogeography and concerted evolution. , 1995, Proceedings of the National Academy of Sciences of the United States of America.

[49]  G. Drouin,et al.  The concerted evolution of 5S ribosomal genes linked to the repeat units of other multigene families. , 1995, Molecular biology and evolution.

[50]  J. Wendel,et al.  Bidirectional interlocus concerted evolution following allopolyploid speciation in cotton (Gossypium). , 1995, Proceedings of the National Academy of Sciences of the United States of America.

[51]  G. Dover.  Concerted evolution, molecular drive and natural selection , 1994, Current Biology.

[52]  Christian Schlötterer,et al.  Chromosomal homogeneity of Drosophila ribosomal DNA arrays suggests intrachromosomal exchanges drive concerted evolution , 1994, Current Biology.

[53]  S. Albini.  A karyotype of the Arabidopsis thaliana genome derived from synaptonemal complex analysis at prophase I of meiosis , 1994 .

[54]  J. S. Heslop-Harrison,et al.  Physical mapping of rDNA loci in Brassica species. , 1993, Genome.

[55]  D. Hillis,et al.  Ribosomal DNA: Molecular Evolution and Phylogenetic Inference , 1991, The Quarterly Review of Biology.

[56]  D. Soltis,et al.  Multiple Origins of the Allotetraploid Tragopogon mirus (Compositae): rDNA Evidence , 1991 .

[57]  T. White.  Amplification and direct sequencing of fungal ribosomal RNA genes for phylogenetics , 1990 .

[58]  J. Feder,et al.  A Commentary on the Use of Ribosomal DNA in Systematic Studies , 1988 .

[59]  D. Hillis,et al.  Ribosomal DNA: Intraspecific Polymorphism, Concerted Evolution, and Phylogeny Reconstruction , 1988 .

[60]  E. Nevo,et al.  Variation in the Intergenic Spacer of Ribosomal DNA of Wild Wheat, Triticum dicoccoides. In Israel , 1986 .

[61]  R. Jorgensen,et al.  Ribosomal DNA spacer-length polymorphisms in barley: mendelian inheritance, chromosomal location, and population dynamics. , 1984, Proceedings of the National Academy of Sciences of the United States of America.

[62]  T. Nagylaki,et al.  Intrachromosomal gene conversion and the maintenance of sequence homogeneity among repeated genes. , 1982, Genetics.

[63]  E. Coen,et al.  Springcleaning ribosomal DNA: a model for multigene evolution? , 1981, Nature.

[64]  E. Pahlich,et al.  A rapid DNA isolation procedure for small quantities of fresh leaf tissue , 1980 .

[65]  T. Butterfass.  Patterns of Chloroplast Reproduction: A Developmental Approach to Protoplasmic Plant Anatomy , 1979 .

[66]  G. P. Smith,et al.  Unequal crossover and the evolution of multigene families. , 1974, Cold Spring Harbor symposia on quantitative biology.

[67]  O. M. Hilliard,et al.  Streptocarpus: an African plant study , 1972 .