Excessive Variation in Y Chromosomal DNA in Rumex acetosa (Polygonaceae)

Abstract

Rumex acetosa is one of the few angiosperms that possesses sex chromosomes. The same types of abundant repetitive sequences cover both heterochromatic Y chromosomes present in males. The aim of this study was to investigate genetic variation in paternally inherited Y chromosomal DNA and in maternally inherited cpDNA, and to find out whether the examined genomic regions are suited to a phylogeographic study in R. acetosa. DNA sequence polymorphisms present in the 850-bp heterochromatic segment on the Y chromosomes were compared to variation in the 409-bp long chloroplast section (trnL-trnF spacer) in R. acetosa originating from several European locations and from the Altai mountains in Russia. A great amount of genetic variation was detected within the Y chromosomal region while only four chloroplast genotypes were detected. Although the chloroplast haplotypes possessed some geographic pattern, no clear phylogeographic pattern was detected based on the variable Y chromosomes. The mean Y chromosomal nucleotide diversity among all samples equaled 6.6 %, and the mean proportion of polymorphic sites per individual equaled 8.2 % among SNP sites and 1.7 % among all sites investigated. The high number of substitutions detected in the Y chromosomal DNA shows that this heterochromatic sequence has a high mutation rate. The diversity pattern indicates that gene flow via pollen is extensive and it blurs any geographical pattern in the Y chromosomal variation. The high number of repeats and uncertainty concerning the extent of recombination between the two Y chromosomes impair the usability of the Y chromosomal segment for phylogeographic or population genetic studies.

Key words

Genetic variation - Rumex acetosa - satellite-DNA - SNP polymorphism - trnL-trnF spacer - Y chromosome.

References

• 1 Birky Jr. C. W., Fuerst P., Maruyama T.. Organelle gene diversity under migration, mutation, and drift: equilibrium expectations, approach to equilibrium, effects of heteroplasmic cells, and comparison to nuclear genes.  Genetics. (1989);  121 613-628
• 2 Charlesworth B.. The evolution of chromosomal sex determination and dosage compensation.  Current Biology. (1996);  6 149-162
• 3 Charlesworth B., Sniegowski P., Stephan W.. The evolutionary dynamics of repetitive DNA in eukaryotes.  Nature. (1994);  371 215-220
• 4 Felsenstein J.. PHYLIP (Phylogeny Inference Package) version 3.6. Distributed by the author. Department of Genome Sciences, University of Washington, Seattle, USA. (2004)
• 5 Felsenstein J., Churchill G. A.. A hidden Markov model approach to variation among sites in rate of evolution.  Molecular Biology and Evolution. (1996);  13 93-104
• 6 Filatov D. A., Moneger F., Negrutiu I., Charlesworth D.. Low variability in a Y-linked plant gene and its implications for Y-chromosomal evolution.  Nature. (2000);  404 388-390
• 7 Fitch W. M., Margoliash E.. Construction of phylogenetic trees.  Science. (1967);  155 279-284
• 8 Ge X. J., Liu M. H., Wang W. K., Schaal B. A., Chiang T. Y.. Population structure of wild bananas, Musa balbisiana, in China determined by SSR fingerprinting and cpDNA PCR-RFLP.  Molecular Ecology. (2005);  14 933-944
• 9 Hu X.-S., Ennos R. A.. Impacts of seed and pollen flow on population genetic structure for plant genomes with three contrasting modes of inheritance.  Genetics. (1999);  152 441-450
• 10 Jobling M. A., Tyler-Smith C.. The human Y chromosome: an evolutionary marker comes of age.  Nature Reviews Genetics. (2003);  4 598-612
• 11 Jukes T., Cantor C.. Evolution of protein molecules. Munro, H. N., ed. Mammalian Protein Metabolism. New York; Academic Press (1969): 21-132
• 12 Kihara H., Ono T.. Cytological studies on Rumex L. I. Chromosomes of Rumex acetosa L.  Botanical Magazine (Tokyo). (1923);  37 84-90
• 13 Korpelainen H.. A genetic method to resolve gender complements investigations on sex ratios in Rumex acetosa.  Molecular Ecology. (2002);  11 2151-2156
• 14 Korpelainen H.. The evolutionary processes of mitochondrial and chloroplast genomes differ from those of nuclear genomes.  Naturwissenschaften. (2004);  91 505-518
• 15 Mantel N.. The detection of disease clustering and a generalized regression approach.  Cancer Research. (1967);  27 209-220
• 16 Matsuoka Y., Yamazaki Y., Ogihara Y., Tsunewaki K.. Whole chloroplast genome comparison of rice, maize, and wheat: implications for chloroplast gene diversification and phylogeny of cereals.  Molecular Biology and Evolution. (2002);  19 2084-2091
• 17 McCauley D. E.. Contrasting the distribution of chloroplast DNA and allozyme polymorphism among local populations of Silene alba: implications for studies of gene flow in plants.  Proceedings of the National Academy of Sciences of the USA. (1994);  91 8127-8131
• 18 McCauley D. E.. The use of chloroplast DNA polymorphism in studies of gene flow in plants.  Trends in Ecology and Evolution. (1995);  10 198-202
• 19 Mogensen H. L.. The hows and whys of cytoplasmic inheritance in seed plants.  American Journal of Botany. (1996);  83 383-404
• 20 Navajas-Pérez R., de la Herran R., Lopez Gonzalez G., Jamilena M., Lozano R., Ruiz Rejón C., Ruiz Rejón M., Garrido-Ramos M. A.. The evolution of reproductive systems and sex-determining mechanisms within Rumex (Polygonaceae) inferred from nuclear and chloroplastidial sequence data.  Molecular Biology and Evolution. (2005 a);  22 1929-1939
• 21 Navajas-Pérez R., de la Herrán R., Jamilena M., Lozano R., Ruiz Rejón C., Ruiz Rejón M., Garrido-Ramos M. A.. Reduced rates of sequence evolution of Y-linked satellite DNA in Rumex (Polygonaceae).  Journal of Molecular Evolution. (2005 b);  60 391-399
• 22 Navajas-Pérez R., Schwarzacher T., de la Herrán R., Ruiz Rejón C., Ruiz Rejón M., Garrido-Ramos M. A.. The origin and evolution of the variability in a Y-specific satellite-DNA of Rumex acetosa and its relatives.  Gene. (2006);  368 61-71
• 23 Ono T.. Chromosomen und Sexualität von Rumex acetosa.  Science Reports of the Tohoku Imperial University IV. (1935);  10 41-210
• 24 Parker J. S., Clark M.-S.. Dosage sex-chromosome systems in plants.  Plant Science. (1991);  80 79-92
• 25 Petit R. J., Duminil J., Fineschi S., Hampe A., Salvini D., Vendramin G. G.. Comparative organization of chloroplast, mitochondrial and nuclear diversity in plant populations.  Molecular Ecology. (2005);  14 689-701
• 26 Rodriguez S., Chen X., Miller G. J., Day I. N. M.. Non-recombining chromosome Y haplogroups and centromeric HindIII RFLP in relation to blood pressure in 2,743 middle-aged Caucasian men from the UK.  Human Genetics. (2005);  116 311-318
• 27 Ruiz Rejón C., Jamilena M., Garrido-Ramos M. A., Parker J. S., Ruiz Rejón M.. Cytogenetic and molecular analysis of the multiple sex chromosome system of Rumex acetosa.  Heredity. (1994);  72 209-215
• 28 Schneider S., Roessli D., Excoffier L.. ARLEQUIN 2.000. Distributed by the authors. Department of Anthropology and Ecology, University of Geneva, Switzerland. (2000)
• 29 Semino O., Passarino G., Oefner P. J., Lin A. A., Arbuzova S., Beckman L. E., De Benedictis G., Francalacci P., Kouvatsi A., Limborska S., Marciki M., Mika A., Mika B., Primorac D., Santachiara-Benerecetti A. S., Cavalli-Sforza L. L., Underhill P. A.. The genetic legacy of paleolithic Homo sapiens sapiens in extant Europeans: a Y chromosome perspective.  Science. (2000);  290 1155-1159
• 30 Shibata F., Hizume M., Kuroki Y.. Chromosome painting of Y chromosome and isolation of a Y chromosome-specific repetitive sequence in the dioecious plant Rumex acetosa.  Chromosoma. (1999);  108 266-270
• 31 Stehlik I.. Glacial history of the alpine herb Rumex nivalis (Polygonaceae): a comparison of common phylogeographic methods with nested clade analysis.  American Journal of Botany. (2002);  89 2007-2016
• 32 Stehlik I., Blattner F. R.. Sex-specific SCAR markers in the dioecious plant Rumex nivalis (Polygonaceae) and implications for the evolution of sex chromosomes.  Theoretical and Applied Genetics. (2004);  108 238-242
• 33 Taberlet P., Gielly L., Pauton G., Bouvet J.. Universal primers for amplification of three non-coding regions of chloroplast DNA.  Plant Molecular Biology. (1991);  17 1105-1109
• 34 Thompson J. D., Higgins D. G., Gibson T. J.. Clustal W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice.  Nucleic Acids Research. (1994);  22 4673-4680
• 35 Ugarkovic D., Plohl M.. Variation in satellite DNA profiles - causes and effects.  The EMBO Journal. (2002);  21 5955-5959
• 36 Vyskot B., Hobza R.. Gender in plants: sex chromosomes are emerging from the fog.  Trends in Genetics. (2004);  20 432-438

Editor: F. Salamini