The Plant Cell, Vol. 13, 1749-1759,
August 2001, Copyright © 2001,
American Society of Plant Biologists
Sequence Elimination and Cytosine Methylation Are Rapid and Reproducible Responses of the Genome to Wide Hybridization and Allopolyploidy in Wheat
Hezi Shaked1,
Khalil Kashkush1,
Hakan Ozkan2,
Moshe Feldman and
Avraham A. Levy3
Department of Plant Sciences, The Weizmann Institute of Science, Rehovot 76100, Israel
3 To whom correspondence should be addressed. E-mail avi.levy{at}weizmann.ac.il; fax 972-8-9344181
Interspecific or intergeneric hybridization, followed by chromosome doubling, can lead to the formation of new allopolyploid species. Recent studies indicate that allopolyploid formation is associated with genetic and epigenetic changes, although little is known about the type of changes that occur, how rapidly they occur, and the type of sequences involved. To address these matters, we have surveyed F1 hybrids between diploid species from the wheat (Aegilops and Triticum) group and their derived allotetraploids by screening a large number of loci using amplified fragment length polymorphism and DNA gel blot analysis and by assaying the extent of cytosine methylation. We found that sequence elimination is one of the major and immediate responses of the wheat genome to wide hybridization or allopolyploidy, that it affects a large fraction of the genome, and that it is reproducible. In one cross between Ae. sharonensis x Ae. umbellulata, 14% of the loci from Ae. sharonensis were eliminated compared with only 0.5% from Ae. umbellulata, with most changes occurring in the F1 hybrid. In contrast, crosses between Ae. longissima x T. urartu showed that sequence elimination was more frequent after chromosome doubling. Alterations in cytosine methylation occurred in 13% of the loci, either in the F1 hybrid or in the allopolyploid. For eight of nine bands that were isolated, the sequences that underwent elimination corresponded to low-copy DNA, whereas alterations in methylation patterns affected both repetitive DNA sequences, such as retrotransposons, and low-copy DNA in approximately equal proportions.
This article has been cited by other articles:

|
 |

|
 |
 
M. Chen, M. Ha, E. Lackey, J. Wang, and Z. J. Chen
RNAi of met1 Reduces DNA Methylation and Induces Genome-Specific Changes in Gene Expression and Centromeric Small RNA Accumulation in Arabidopsis Allopolyploids
Genetics,
April 1, 2008;
178(4):
1845 - 1858.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
X.-F. Ma and J. P. Gustafson
Allopolyploidization-accommodated Genomic Sequence Changes in Triticale
Ann. Bot.,
April 1, 2008;
101(6):
825 - 832.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
P. Smarda, P. Bures, L. Horova, B. Foggi, and G. Rossi
Genome Size and GC Content Evolution of Festuca: Ancestral Expansion and Subsequent Reduction
Ann. Bot.,
February 1, 2008;
101(3):
421 - 433.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
W. Li, L. Huang, and B. S. Gill
Recurrent Deletions of Puroindoline Genes at the Grain Hardness Locus in Four Independent Lineages of Polyploid Wheat1,[W],[OA]
Plant Physiology,
January 1, 2008;
146(1):
200 - 212.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
K. Kashkush and V. Khasdan
Large-Scale Survey of Cytosine Methylation of Retrotransposons and the Impact of Readout Transcription From Long Terminal Repeats on Expression of Adjacent Rice Genes
Genetics,
December 1, 2007;
177(4):
1975 - 1985.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
Y. Zhuang and K. L. Adams
Extensive Allelic Variation in Gene Expression in Populus F1 Hybrids
Genetics,
December 1, 2007;
177(4):
1987 - 1996.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
R. T. Gaeta, J. C. Pires, F. Iniguez-Luy, E. Leon, and T. C. Osborn
Genomic Changes in Resynthesized Brassica napus and Their Effect on Gene Expression and Phenotype
PLANT CELL,
November 1, 2007;
19(11):
3403 - 3417.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
J. Dubcovsky and J. Dvorak
Genome Plasticity a Key Factor in the Success of Polyploid Wheat Under Domestication
Science,
June 29, 2007;
316(5833):
1862 - 1866.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
B. J. Evans
Ancestry Influences the Fate of Duplicated Genes Millions of Years After Polyploidization of Clawed Frogs (Xenopus)
Genetics,
June 1, 2007;
176(2):
1119 - 1130.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
N. Shitsukawa, C. Tahira, K.-i. Kassai, C. Hirabayashi, T. Shimizu, S. Takumi, K. Mochida, K. Kawaura, Y. Ogihara, and K. Murai
Genetic and Epigenetic Alteration among Three Homoeologous Genes of a Class E MADS Box Gene in Hexaploid Wheat
PLANT CELL,
June 1, 2007;
19(6):
1723 - 1737.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
M. Popp and B. Oxelman
Origin and evolution of North American polyploid Silene (Caryophyllaceae)
Am. J. Botany,
March 1, 2007;
94(3):
330 - 349.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
T. K. Ezov, E. Boger-Nadjar, Z. Frenkel, I. Katsperovski, S. Kemeny, E. Nevo, A. Korol, and Y. Kashi
Molecular-Genetic Biodiversity in a Natural Population of the Yeast Saccharomyces cerevisiae From "Evolution Canyon": Microsatellite Polymorphism, Ploidy and Controversial Sexual Status
Genetics,
November 1, 2006;
174(3):
1455 - 1468.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
Y. Q. Gu, J. Salse, D. Coleman-Derr, A. Dupin, C. Crossman, G. R. Lazo, N. Huo, H. Belcram, C. Ravel, G. Charmet, et al.
Types and Rates of Sequence Evolution at the High-Molecular-Weight Glutenin Locus in Hexaploid Wheat and Its Ancestral Genomes
Genetics,
November 1, 2006;
174(3):
1493 - 1504.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
J. A. Udall and J. F. Wendel
Polyploidy and Crop Improvement
Crop Sci.,
November 1, 2006;
46(Supplement_1):
S-3 - S-14.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
L. G. QUINTANILLA and A. ESCUDERO
Spore Fitness Components Do Not Differ Between Diploid and Allotetraploid Species of Dryopteris (Dryopteridaceae)
Ann. Bot.,
September 1, 2006;
98(3):
609 - 618.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
A. L. Keyte, R. Percifield, B. Liu, and J. F. Wendel
Infraspecific DNA Methylation Polymorphism in Cotton (Gossypium hirsutum L.)
J. Hered.,
September 1, 2006;
97(5):
444 - 450.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
B. C. Thomas, B. Pedersen, and M. Freeling
Following tetraploidy in an Arabidopsis ancestor, genes were removed preferentially from one homeolog leaving clusters enriched in dose-sensitive genes
Genome Res.,
July 1, 2006;
16(7):
934 - 946.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
J. A. Tate, Z. Ni, A.-C. Scheen, J. Koh, C. A. Gilbert, D. Lefkowitz, Z. J. Chen, P. S. Soltis, and D. E. Soltis
Evolution and Expression of Homeologous Loci in Tragopogon miscellus (Asteraceae), a Recent and Reciprocally Formed Allopolyploid
Genetics,
July 1, 2006;
173(3):
1599 - 1611.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
K. Y. Lim, K. Souckova-Skalicka, V. Sarasan, J. J. Clarkson, M. W. Chase, A. Kovarik, and A. R. Leitch
A genetic appraisal of a new synthetic Nicotiana tabacum (Solanaceae) and the Kostoff synthetic tobacco
Am. J. Botany,
June 1, 2006;
93(6):
875 - 883.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
B. A. Chapman, J. E. Bowers, F. A. Feltus, and A. H. Paterson
Buffering of crucial functions by paleologous duplicated genes may contribute cyclicality to angiosperm genome duplication
PNAS,
February 21, 2006;
103(8):
2730 - 2735.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
M. Tuna, K. P. Vogel, and K. Arumuganathan
Cytogenetic and Nuclear DNA Content Characterization of Diploid Bromus erectus and Bromus variegatus
Crop Sci.,
February 1, 2006;
46(2):
637 - 641.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
R. T. GRANT-DOWNTON and H. G. DICKINSON
Epigenetics and its Implications for Plant Biology 2. The 'Epigenetic Epiphany': Epigenetics, Evolution and Beyond
Ann. Bot.,
January 1, 2006;
97(1):
11 - 27.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
J. S.S. Ammiraju, M. Luo, J. L. Goicoechea, W. Wang, D. Kudrna, C. Mueller, J. Talag, H. Kim, N. B. Sisneros, B. Blackmon, et al.
The Oryza bacterial artificial chromosome library resource: Construction and analysis of 12 deep-coverage large-insert BAC libraries that represent the 10 genome types of the genus Oryza
Genome Res.,
January 1, 2006;
16(1):
140 - 147.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
L. N. Lukens, J. C. Pires, E. Leon, R. Vogelzang, L. Oslach, and T. Osborn
Patterns of Sequence Loss and Cytosine Methylation within a Population of Newly Resynthesized Brassica napus Allopolyploids
Plant Physiology,
January 1, 2006;
140(1):
336 - 348.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
K. L. Adams and J. F. Wendel
Allele-Specific, Bidirectional Silencing of an Alcohol Dehydrogenase Gene in Different Organs of Interspecific Diploid Cotton Hybrids
Genetics,
December 1, 2005;
171(4):
2139 - 2142.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
T. Nomura, A. Ishihara, R. C. Yanagita, T. R. Endo, and H. Iwamura
Three genomes differentially contribute to the biosynthesis of benzoxazinones in hexaploid wheat
PNAS,
November 8, 2005;
102(45):
16490 - 16495.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
J. F. HANCOCK
Contributions of Domesticated Plant Studies to our Understanding of Plant Evolution
Ann. Bot.,
November 1, 2005;
96(6):
953 - 963.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
P. D. Rabinowicz, R. Citek, M. A. Budiman, A. Nunberg, J. A. Bedell, N. Lakey, A. L. O'Shaughnessy, L. U. Nascimento, W. R. McCombie, and R. A. Martienssen
Differential methylation of genes and repeats in land plants
Genome Res.,
October 1, 2005;
15(10):
1431 - 1440.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
Y.-M. Wang, Z.-Y. Dong, Z.-J. Zhang, X.-Y. Lin, Y. Shen, D. Zhou, and B. Liu
Extensive de Novo Genomic Variation in Rice Induced by Introgression From Wild Rice (Zizania latifolia Griseb.)
Genetics,
August 1, 2005;
170(4):
1945 - 1956.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
F. Han, G. Fedak, W. Guo, and B. Liu
Rapid and Repeatable Elimination of a Parental Genome-Specific DNA Repeat (pGc1R-1a) in Newly Synthesized Wheat Allopolyploids
Genetics,
July 1, 2005;
170(3):
1239 - 1245.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
N. Chantret, J. Salse, F. Sabot, S. Rahman, A. Bellec, B. Laubin, I. Dubois, C. Dossat, P. Sourdille, P. Joudrier, et al.
Molecular Basis of Evolutionary Events That Shaped the Hardness Locus in Diploid and Polyploid Wheat Species (Triticum and Aegilops)
PLANT CELL,
April 1, 2005;
17(4):
1033 - 1045.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
O. Pontes, N. Neves, M. Silva, M. S. Lewis, A. Madlung, L. Comai, W. Viegas, and C. S. Pikaard
Chromosomal locus rearrangements are a rapid response to formation of the allotetraploid Arabidopsis suecica genome
PNAS,
December 28, 2004;
101(52):
18240 - 18245.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
A. MADLUNG and L. COMAI
The Effect of Stress on Genome Regulation and Structure
Ann. Bot.,
October 1, 2004;
94(4):
481 - 495.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
B. S. Gill, R. Appels, A.-M. Botha-Oberholster, C. R. Buell, J. L. Bennetzen, B. Chalhoub, F. Chumley, J. Dvorak, M. Iwanaga, B. Keller, et al.
A Workshop Report on Wheat Genome Sequencing: International Genome Research on Wheat Consortium
Genetics,
October 1, 2004;
168(2):
1087 - 1096.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
J. C. Pires, K. Y. Lim, A. Kovarik, R. Matyasek, A. Boyd, A. R. Leitch, I. J. Leitch, M. D. Bennett, P. S. Soltis, and D. E. Soltis
Molecular cytogenetic analysis of recently evolved Tragopogon (Asteraceae) allopolyploids reveal a karyotype that is additive of the diploid progenitors
Am. J. Botany,
July 1, 2004;
91(7):
1022 - 1035.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
A. A. Andalis, Z. Storchova, C. Styles, T. Galitski, D. Pellman, and G. R. Fink
Defects Arising From Whole-Genome Duplications in Saccharomyces cerevisiae
Genetics,
July 1, 2004;
167(3):
1109 - 1121.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
G. Blanc and K. H. Wolfe
Widespread Paleopolyploidy in Model Plant Species Inferred from Age Distributions of Duplicate Genes
PLANT CELL,
July 1, 2004;
16(7):
1667 - 1678.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
S. Joly, J. T. Rauscher, S. L. Sherman-Broyles, A. H. D. Brown, and J. J. Doyle
Evolutionary Dynamics and Preferential Expression of Homeologous 18S-5.8S-26S Nuclear Ribosomal Genes in Natural and Artificial Glycine Allopolyploids
Mol. Biol. Evol.,
July 1, 2004;
21(7):
1409 - 1421.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
C. B. Della Vedova and K. C. Cone
Paramutation: The Chromatin Connection
PLANT CELL,
June 1, 2004;
16(6):
1358 - 1364.
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
A. Cuadrado, R. Acevedo, S. Moreno Diaz de la Espina, N. Jouve, and C. de la Torre
Genome remodelling in three modern S. officinarumxS. spontaneum sugarcane cultivars
J. Exp. Bot.,
April 1, 2004;
55(398):
847 - 854.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
W. Gregor, M. F. Mette, C. Staginnus, M. A. Matzke, and A. J.M. Matzke
A Distinct Endogenous Pararetrovirus Family in Nicotiana tomentosiformis, a Diploid Progenitor of Polyploid Tobacco
Plant Physiology,
March 1, 2004;
134(3):
1191 - 1199.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
M. E. Schranz and T. C. Osborn
De novo variation in life-history traits and responses to growth conditions of resynthesized polyploid Brassica napus (Brassicaceae)
Am. J. Botany,
February 1, 2004;
91(2):
174 - 183.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
K. Ilic, P. J. SanMiguel, and J. L. Bennetzen
A complex history of rearrangement in an orthologous region of the maize, sorghum, and rice genomes
PNAS,
October 14, 2003;
100(21):
12265 - 12270.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
H. Ozkan, M. Tuna, and K. Arumuganathan
Nonadditive Changes in Genome Size During Allopolyploidization in the Wheat (Aegilops-Triticum) Group
J. Hered.,
May 1, 2003;
94(3):
260 - 264.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
L. Lukens, F. Zou, D. Lydiate, I. Parkin, and T. Osborn
Comparison of a Brassica oleracea Genetic Map With the Genome of Arabidopsis thaliana
Genetics,
May 1, 2003;
164(1):
359 - 372.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
K. L. Adams, R. Cronn, R. Percifield, and J. F. Wendel
Genes duplicated by polyploidy show unequal contributions to the transcriptome and organ-specific reciprocal silencing
PNAS,
April 15, 2003;
100(8):
4649 - 4654.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
D. S. Senchina, I. Alvarez, R. C. Cronn, B. Liu, J. Rong, R. D. Noyes, A. H. Paterson, R. A. Wing, T. A. Wilkins, and J. F. Wendel
Rate Variation Among Nuclear Genes and the Age of Polyploidy in Gossypium
Mol. Biol. Evol.,
April 1, 2003;
20(4):
633 - 643.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
A. A. Levy and M. Feldman
The Impact of Polyploidy on Grass Genome Evolution
Plant Physiology,
December 1, 2002;
130(4):
1587 - 1593.
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
A. Baumel, M. Ainouche, R. Kalendar, and A. H. Schulman
Retrotransposons and Genomic Stability in Populations of the Young Allopolyploid Species Spartina anglica C.E. Hubbard (Poaceae)
Mol. Biol. Evol.,
August 1, 2002;
19(8):
1218 - 1227.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
E. Emshwiller and J. J. Doyle
Origins of domestication and polyploidy in oca (Oxalis Tuberosa: Oxalidaceae). 2. Chloroplast-expressed glutamine synthetase data
Am. J. Botany,
July 1, 2002;
89(7):
1042 - 1056.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
A. Madlung, R. W. Masuelli, B. Watson, S. H. Reynolds, J. Davison, and L. Comai
Remodeling of DNA Methylation and Phenotypic and Transcriptional Changes in Synthetic Arabidopsis Allotetraploids
Plant Physiology,
June 1, 2002;
129(2):
733 - 746.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
K. Kashkush, M. Feldman, and A. A. Levy
Gene Loss, Silencing and Activation in a Newly Synthesized Wheat Allotetraploid
Genetics,
April 1, 2002;
160(4):
1651 - 1659.
[Abstract]
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
N. A. Eckardt
A Sense of Self: The Role of DNA Sequence Elimination in Allopolyploidization
PLANT CELL,
August 1, 2001;
13(8):
1699 - 1704.
[Full Text]
[PDF]
|
 |
|

|
 |

|
 |
 
H. Ozkan, A. A. Levy, and M. Feldman
Allopolyploidy-Induced Rapid Genome Evolution in the Wheat (Aegilops-Triticum) Group
PLANT CELL,
August 1, 2001;
13(8):
1735 - 1747.
[Abstract]
[Full Text]
[PDF]
|
 |
|
|
|