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ARS Home » Plains Area » Fargo, North Dakota » Edward T. Schafer Agricultural Research Center » Sunflower and Plant Biology Research » Research » Publications at this Location » Publication #252511

Title: The compact Brachypodium genome conserves centromeric regions of a common ancestor with wheat and rice

Author
item Qi, Lili
item FRIEBE, BERND - Kansas State University
item WU, JIAJIE - University Of California
item Gu, Yong
item QIAN, CHEN - Kansas State University
item GILL, BIKRAM - Kansas State University

Submitted to: Functional and Integrative Genomics
Publication Type: Peer Reviewed Journal
Publication Acceptance Date: 8/24/2010
Publication Date: 9/15/2010
Citation: Qi, L., Friebe, B., Wu, J., Gu, Y., Qian, C., Gill, B.S. 2010. The compact Brachypodium genome conserves centromeric regions of a common ancestor with wheat and rice. Functional and Integrative Genomics. 10:477-492.

Interpretive Summary: Brachypodium distachyon is a wild temperate grass native to southern Europe, northern Africa, and southwestern Asia. The close relationship to temperate cereals such as wheat, barley, and oat, small genome size, ease of transformation, and short life cycle prompted the use of B. distachyon as an experimental model to link rice and temperate grasses. This paper compares the characteristics of the centromere region of B. distachyon with that of wheat and rice. The centromere is a prominent chromosome landmark. One and only one is needed on every chromosome for normal segregation during cell division. The evolution of the five chromosomes of B. distachyon (Bd) from a 12-chromosome ancestor of all grasses by chromosome fusions raises an interesting question about the fate of redundant centromeres. Three independent but complementary approaches were pursued to study the centromeric region similarities among the chromosomes of Brachypodium, wheat, and rice. DNA sequence alignment and DNA clone-FISH (fluorescence in situ hybridization) data were used to determine the approximate positions of active and inactive centromeres in the five B. distachyon chromosomes. Five rice centromeres similar to two wheat centromeres are active in five Brachypodium chromosomes, whereas six rice centromeres similar to five wheat centromeres were inactive in Brachypodium chromosomes. The conservation of centromere gene similarity among several sets of homologous centromeres of three species indicates that active genes can persist in ancient centromeres with over 40 million years of shared evolutionary history. Analysis of the 103,655-bp DNA sequence in the Brachypodium chromosome 3 which is similar to rice centromere 8 and and W7 pericentromeres, along with DNA clone-FISH data from inactive centromeres revealed that the centromere inactivation was accompanied by the loss of centromeric retrotransposons and turnover of centromere-specific satellites during Bd chromosome evolution. The data on the position of active and inactive centromeres in Brachypodium, wheat, and rice reported here provide a platform for studying the centromere structures and evolution in these and other grass genomes.

Technical Abstract: The evolution of five chromosomes of Brachypodium distachyon from a 12-chromosome ancestor of all grasses by dysploidy raises an interesting question about the fate of redundant centromeres. Three independent but complementary approaches were pursued to study centromeric region homologies among the chromosomes of Brachypodium, wheat, and rice. The genes present in pericentromeres of the basic set of seven chromosomes of wheat and the Triticeae, and the 80 rice centromeric genes spanning the CENH3 binding domain of centromeres 3, 4, 5, 7, and 8 were used as "anchor" markers to identify centromere locations in the B. distachyon chromosomes. Fifty-three B. distachyon BAC clones anchored by wheat pericentromeric ESTs were used as probes for BAC-FISH analysis of B. distachyon mitotic chromosomes. Integrated sequence alignment and BAC-FISH data were used to determine the approximate positions of active and inactive centromeres in the five B. distachyon chromosomes. The following syntenic relationships of the centromeres for Brachypodium (Bd), rice (R), and wheat (W) were evident: Bd1-R6, Bd2-R5-W1, Bd3-R10, Bd4-R11-W4, and Bd5-R4. Six rice centromeres syntenic to five wheat centromeres were inactive in Brachypodium chromosomes. The conservation of centromere gene synteny among several sets of homologous centromeres of three species indicates that active genes can persist in ancient centromeres with over 40 million years of shared evolutionary history. Annotation of a BAC contig spanning an inactive centromere in chromosome Bd3 which is syntenic to rice Cen8 and W7 pericentromeres, along with BAC FISH data from inactive centromeres revealed that the centromere inactivation was accompanied by the loss of centromeric retrotransposons and turnover of centromere-specific satellites during Bd chromosome evolution.