SlWUS1; an X-linked gene having no homologous Y-linked copy in silene latifolia

G3: Genes, Genomes, Genetics

Volumn 2, Issue 10, 2012, Pages 1269-1278

  Kazama, Yusuke ^a   Nishihara, Kiyoshi ^a,b   Bergero, Roberta ^c   Fujiwara, Makoto T ^a,d   Abe, Tomoko ^a   Charlesworth, Deborah ^c   Kawano, Shigeyuki ^b  

^a RIKEN   (Japan)

^b UNIVERSITY OF TOKYO   (Japan)

^c UNIVERSITY OF EDINBURGH   (United Kingdom)

^d SOPHIA UNIVERSITY   (Japan)

Author keywords

Dioecious plant; Genetic degeneration; Silene latifolia; WUSCHEL; X linkage

Indexed keywords

AMINO ACID SEQUENCE; ARTICLE; CHROMOSOME MAP; CLASSIFICATION; FLOWER; GENE EXPRESSION REGULATION; GENETIC VARIABILITY; GENETICS; MOLECULAR GENETICS; PHYLOGENY; PLANT CHROMOSOME; PLANT GENE; PLANT LEAF; SEQUENCE ALIGNMENT; SEX CHROMOSOME; SILENE; X CHROMOSOMAL INHERITANCE;

AMINO ACID SEQUENCE; CHROMOSOME MAPPING; CHROMOSOMES, PLANT; DOSAGE COMPENSATION, GENETIC; FLOWERS; GENE EXPRESSION REGULATION, PLANT; GENES, PLANT; GENES, X-LINKED; GENETIC VARIATION; MOLECULAR SEQUENCE DATA; PHYLOGENY; PLANT LEAVES; SEQUENCE ALIGNMENT; SEX CHROMOSOMES; SILENE;

EID: 84883188266     PISSN: None     EISSN: 21601836     Source Type: Journal    
DOI: 10.1534/g3.112.003749     Document Type: Article

References (66)

1. Atanassov, I., C. Delichére, D. A. Filatov, D. Charlesworth, I. Negrutiu et al., 2001 Analysis and evolution of two functional Y-linked loci in a plant sex chromosome system. Mol. Biol. Evol. 18: 2162-2168.
2. Bergero, R., and D. Charlesworth, 2011 Preservation of the Y transcriptome in a 10-million-year-old plant sex chromosome system. Curr. Biol. 21: 1470-1474.
3. Bergero, R., A. Forrest, E. Kamau, and D. Charlesworth, 2007 Evolutionary strata on the X chromosomes of the dioecious plant Silene latifolia: evidence from new sex-linked genes. Genetics 175: 1945-1954.
4. Bergero, R., D. Charlesworth, D. A. Filatov, and R. C. Moore, 2008 Defining regions and rearrangements of the Silene latifolia Y chromosome. Genetics 178: 2045-2053.
5. Brand, U., J. C. Fletcher, M. Hobe, E. M. Meyerowitz, and R. Simon, 2000 Dependence of stem cell fate in Arabidopsis on a feedback loop regulated by CLV3 activity. Science 289: 617-619.
6. Buzek, J.,H.Koutnikova, A. Houben,K. Ríha, B. Janousek et al., 1997 Isolation and characterization of X chromosome-derived DNA sequences from a dioecious plant Melandrium album. Chromosome Res. 5: 57-65.
7. Carrel, L., and H. F. Willard, 2005 X-inactivation profile reveals extensive variability in X-linked gene expression in females. Nature 434: 400-404.
8. Cegan, R., G. A. Marais, H. Kubekova, N. Blavet, A. Widmer et al., 2010 Structure and evolution of Apetala3, a sex-linked gene in Silene latifolia. BMC Plant Biol. 10: 180.
9. Charlesworth, B., 1996 The evolution of chromosomal sex determination and dosage compensation. Curr. Biol. 6: 149-162.
10. Chibalina, M., and D. Filatov, 2011 Plant Y chromosome degeneration is retarded by haploid purifying selection. Curr. Biol. 21: 1475-1479.
11. Coen, E. S., and E. M. Meyerowitz, 1991 The war of the whorls: genetic interactions controlling flower development. Nature 353: 31-37.
12. Delichere, C., J. Veuskens, M. Hernould, N. Barbacar, A. Mouras et al., 1999 SlY1, the first active gene cloned from a plant Y chromosome, encodes a WD-repeat protein. EMBO J. 18: 4169-4179.
13. Deyhle, F., A. K. Sarkar, E. J. Tucker, and T. Laux, 2007 WUSCHEL regulates cell differentiation during anther development. Dev. Biol. 302: 154-159.
14. Filatov, D. A., 2004 Substitution rates in a new Silene latifolia sex-linked gene, SlssX/Y. Mol. Biol. Evol. 22: 402-408.
15. Filatov, D. A., 2005 Evolutionary history of Silene latifolia sex chromosomes revealed by genetic mapping of four genes. Genetics 170: 975-979.
16. Filatov, D. A., and D. Charlesworth, 2002 Substitution rates in the X- and Y-linked genes of the plants, Silene latifolia and S. dioica. Mol. Biol. Evol. 19: 898-907.
17. Grant, S. R., B. Hunkirchen, and H. Saedler, 1994 Developmental differences between male and female flowers in the dioecious plant Silene latifolia. Plant J. 6: 471-480.
18. Guttman, D. S., and D. Charlesworth, 1998 An X-linked gene has a degenerate Y-linked homologue in the dioecious plant Silene latifolia. Nature 393: 263-266.
19. Haecker, A., R. Groβ-Hardt, B. Geiges, A. Sarkar, H. Breuninger et al., 2004 Expression dynamics of WOX genes mark cell fate decisions during early embryonic patterning in Arabidopsis thaliana. Development 131: 657-668.
20. Hobza, R., E. Kejnovsky, B. Vyskot, and A. Widmer, 2007 The role of chromosomal rearrangements in the evolution of Silene latifolia sex chromosomes. Mol. Genet. Genomics 278: 633-638.
21. Ishii, K., R. Sugiyama, M. Onuki, Y. Kazama, S. Matsunaga et al., 2008 The Y chromosome-specific STS marker MS2 and its peripheral regions on the Y chromosome of the dioecious plant Silene latifolia. Genome 51: 251-260.
22. Jamilena, M., B. Mariotti, and S. Manzano, 2008 Plant sex chromosomes: molecular structure and function. Cytogenet. Genome Res. 120: 255-264.
23. Janousek, B., S. R. Grant, and B. Vyskot, 1998 Non-transmissibility of the Y chromosome through the female line in androhermaphrodite plants of Melandrium album. Heredity 80: 576-583.
24. Kaiser, V. B., R. Bergero, and D. Charlesworth, 2009 Slcyt, a newly identified sex-linked gene, has recently moved onto the X chromosome in Silene latifolia (Caryophyllaceae). Mol. Biol. Evol. 26: 2343-2351.
25. Kaiser, V. B., R. Bergero, and D. Charlesworth, 2011 A new plant sex-linked gene with high sequence diversity and possible introgression of the X copy. Heredity 106: 339-347.
26. Kazama, Y., and S. Matsunaga, 2008 The use of repetitive DNA in cytogenetic studies of plant sex chromosomes. Cytogenet. Genome Res. 120: 247-254.
27. Kazama, Y., R. Sugiyama, S. Matsunaga, F. Shibata, W. Uchida et al., 2003 Organization of the KpnI family of chromosomal distal-end satellite DNAs in Silene latifolia. J. Plant Res. 116: 317-326.
28. Kazama, Y., R. Sugiyama, Y. Suto, W. Uchida, and S. Kawano, 2006 The clustering of four subfamilies of satellite DNA at individual chromosome ends in Silene latifolia. Genome 49: 520-530.
29. Kazama, Y., M. T. Fujiwara, A. Koizumi, K. Nishihara, R. Nishiyama et al., 2009 A SUPERMAN-like gene is exclusively expressed in female flowers of the dioecious plant Silene latifolia. Plant Cell Physiol. 50: 1127-1141.
30. Kazama, Y., T. Hirano, H. Saito, Y. Liu, S. Ohbu et al., 2011 Characterization of highly efficient heavy-ion mutagenesis in Arabidopsis thaliana. BMC Plant Biol. 11: 161.
31. Kejnovsky, E., and B. Vyskot, 2010 Silene latifolia: the classical model to study heteromorphic sex chromosomes. Cytogenet. Genome Res. 129: 250-262.
32. Kejnovsky, E., Z. Kubat, R. Hobza, M. Lengerova, S. Sato et al., 2006 Accumulation of chloroplast DNA sequences on the Y chromosome of Silene latifolia. Genetica 128: 167-175.
33. Kejnovsky, E., R. Hobza, T. Cermak, Z. Kubat, and B. Vyskot, 2009 The role of repetitive DNA in structure and evolution of sex chromosomes in plants. Heredity 102: 533-541.
34. Koizumi, A., K. Yamanaka, K. Nishihara, Y. Kazama, T. Abe et al., 2010 Two separate pathways including SlCLV1, SlSTM and SlCUC that control carpel development in a bisexual mutant of Silene latifolia. Plant Cell Physiol. 51: 282-293.
35. Kosambi, D. D., 1944 The estimation of map distances from recombination values. Ann. Eugen. 12: 172-175.
36. Laux, T., K. F. Mayer, J. Berger, and G. Jürgens, 1996 The WUSCHEL gene is required for shoot and floral meristem integrity in Arabidopsis. Development 122: 87-96.
37. Lebel-Hardenack, S., E. Hauser, T. F. Law, J. Schmid, and S. R. Grant, 2002 Mapping of sex determination loci on the white campion (Silene latifolia) Y chromosome using amplified fragment length polymorphism. Genetics 160: 717-725.
38. Lengerova, M., R. C. Moore, S. R. Grant, and B. Vyskot, 2003 The sex chromosomes of Silene latifolia revisited and revised. Genetics 165: 935- 938.
39. Liu, Z., P. H. Moore, H. Ma, C. M. Ackerman, M. Ragiba et al., 2004 A primitive Y chromosome in papaya marks incipient sex chromosome evolution. Nature 427: 348-352.
40. Matsunaga, S., E. Isono, E. Kejnovsky, B. Vyskot, J. Dolezel et al., 2003 Duplicative transfer of a MADS box gene to a plant Y chromosome. Mol. Biol. Evol. 20: 1062-1069.
41. Matsunaga, S., S. Kawano, T. Michimoto, T. Higashiyama, S. Nakao et al., 1999 Semi-automatic laser beam microdissection of the Y chromosome and analysis of Y chromosome DNA in a dioecious plant, Silene latifolia. Plant Cell Physiol. 40: 60-68.
42. Mayer, K. F., H. Schoof, A. Haecker, M. Lenhard, G. Jurgens et al., 1998 Role of WUSCHEL in regulating stem cell fate in the Arabidopsis shoot meristem. Cell 95: 805-815.
43. Ming, R., S. Hou, Y. Feng, Q. Yu, A. Dionne-Laporte et al., 2008 The draft genome of the transgenic tropical fruit tree papaya (Carica papaya Linnaeus). Nature 452: 991-996.
44. Moore, R. C., O. Kozyreva, S. Lebel-Hardenack, J. Siroky, R. Hobza et al., 2003 Genetic and functional analysis of DD44, a sex-linked gene from the dioecious plant Silene latifolia, provides clues to early events in sex chromosome evolution. Genetics 163: 321-334.
45. Muyle, A., N. Zemp, C. Deschamps, S. Mousset, A. Widmer et al., 2012 Rapid de novo evolution of X chromosome dosage compensation in Silene latifolia, a plant with young sex chromosomes. PLoS Biol. 10: e1001308.
46. Na, J. K., J. Wang, J. E. Murray, A. R. Gschwend, W. Zhang et al., 2012 Construction of physical maps for the sex-specific regions of papaya sex chromosomes. BMC Genomics 13: 176.
47. Nicolas, M., G. Marais, V. Hykelova, B. Janousek, V. Laporte et al., 2005 A gradual process of recombination restriction in the evolutionary history of the sex chromosomes in dioecious plants. PLoS Biol. 3: 47-56.
48. Nishiyama, R., K. Ishii, E. Kifune, Y. Kazama, K. Nishihara et al., 2010 Sex chromosome evolution revealed by physical mapping of SIAP3X/Y in the dioecious plant Silene latifolia. Cytologia (Tokyo) 75: 319-325.
49. Ogawa, M., H. Shinohara, Y. Sakagami, and Y. Matsubayashi, 2008 Arabidopsis CLV3 peptide directly binds CLV1 ectodomain. Science 319: 294.
50. Ohta, M., K. Matsui, K. Hiratsu, H. Shinshi, and M. Ohme-Takagi, 2001 Repression domains of class II ERF transcriptional repressors share an essential motif for active repression. Plant Cell 13: 1959-1968.
51. Onodera, Y., I. Yonaha, H.Masumo, A. Tanaka, S. Niikura et al., 2011 Mapping of the genes for dioecism and monoecism in Spinacia oleracea L.: evidence that both genes are closely linked. Plant Cell Rep. 30: 965-971.
52. Pamilo, P., and N. Bianchi, 1993 Evolution of the Zfx and Zfy, genes: rates and interdependence between the genes. Mol. Biol. Evol. 10: 271-281.
53. Park, C., L. Carrel, and K. D. Makova, 2010 Strong purifying selection at genes escaping X chromosome inactivation. Mol. Biol. Evol. 27: 2446- 2450.
54. Parker, J. S., 1990 Sex chromosomes and sexual differentiation in flowering plants. Chromosomes Today 10: 187-198.
55. Sablowski, R., 2007 Flowering and determinacy in Arabidopsis. J. Exp. Bot. 58: 899-907.
56. Saitou, N., and M. Nei, 1987 The neighbor-joining method: a new method for reconstructing phylogenetic trees. Mol. Biol. Evol. 4: 406-425.
57. Tamura, K., J. Dudley, M. Nei, and S. Kumar, 2007 MEGA4: molecular evolutionary genetics analysis (MEGA) software version 4.0. Mol. Biol. Evol. 24: 1596-1599.
58. Telgmann-Rauber, A., A. Jamsari, M. S. Kinney, J. C. Pires, and C. Jung, 2007 Genetic and physical maps around the sex-determining M-locus of the dioecious plant asparagus. Mol. Genet. Genomics 278: 221-234.
59. Thompson, J. D., T. J. Gibson, F. Plewniak, F. Jeanmougin, and D. G. Higgins, 1997 The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res. 25: 4876-4882.
60. van der Graaff, E., T. Laux, and S. A. Rensing, 2009 The WUS homeoboxcontaining (WOX) protein family. Genome Biol. 10: 248.
61. Vyskot, B., A. Araya, J. Veuskens, I. Negrutiu, and A. Mouras, 1993 DNA methylation of sex chromosomes in a dioecious plant, Melandrium album. Mol. Gen. Genet. 239: 219-224.
62. Weigel, D., and E. M. Meyerowitz, 1994 The ABCs of floral homeotic genes. Cell 78: 203-209.
63. Westergaard, M., 1946 Aberrant Y chromosomes and sex expression in Melandrium album. Hereditas 32: 419-443.
64. Westergaard, M., 1958 The mechanism of sex determination in dioecious flowering plants. Adv. Genet. 9: 217-281.
65. Zluvova, J., M. Nicolas, A. Berger, I. Negrutiu, and F. Moneger, 2006 Premature arrest of the male flower meristem precedes sexual dimorphism in the dioecious plant Silene latifolia. Proc. Natl. Acad. Sci. USA 103: 18854-18859.
66. Zluvova, J., S. Georgiev, B. Janousek, D. Charlesworth, B. Vyskot et al., 2007 Early events in the evolution of the Silene latifolia Y chromosome: male specialization and recombination arrest. Genetics 177: 375-386.