High frequency of centromere inactivation resulting in stable dicentric chromosomes of maize

Han, Fangpu; Lamb, Jonathan C.; Birchler, James A.

doi:10.1073/pnas.0509650103

Cited by 295 publications

(274 citation statements)

References 23 publications

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“…However, such chromosomes should be stable if only one centromere remains active (30), or if the centromeres in the dicentric chromosome are physically close and coordinate their movement to one or the other pole (31). Inactivation of redundant centromeres have been found in maize and other grasses (30,32,33), and although the details underlying the inactivation are not clear yet, several recent studies have suggested that plant centromere function is an epigenetic process (30,(32)(33)(34). The molecular details of such an epigenetic loss, and whether it involves dominance of one centromere over another (as seen for instance with nucleoli in some nascent polyploids; ref.…”

Section: Resultsmentioning

confidence: 99%

Centromere retention and loss during the descent of maize from a tetraploid ancestor

Wang

Bennetzen

2012

Proc. Natl. Acad. Sci. U.S.A.

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Although centromere function is highly conserved in eukaryotes, centromere sequences are highly variable. Only a few centromeres have been sequenced in higher eukaryotes because of their repetitive nature, thus hindering study of their structure and evolution. Conserved single-copy sequences in pericentromeres (CSCPs) of sorghum and maize were found to be diagnostic characteristics of adjacent centromeres. By analyzing comparative map data and CSCP sequences of sorghum, maize, and rice, the major evolutionary events related to centromere dynamics were discovered for the maize lineage after its divergence from a common ancestor with sorghum. ( i ) Remnants of ancient CSCP regions were found for the 10 lost ancestral centromeres, indicating that two ancient homeologous chromosome pairs did not contribute any centromeres to the current maize genome, whereas two other pairs contributed both of their centromeres. ( ii ) Five cases of long-distance, intrachromosome movement of CSCPs were detected in the retained centromeres, with inversion the major process involved. ( iii ) The 12 major chromosomal rearrangements that led to maize chromosome number reduction from 20 to 10 were uncovered. ( iv ) In addition to whole chromosome insertion near (but not always into) other centromeres, translocation and fusion were found to be important mechanisms underlying grass chromosome number reduction. ( v ) Comparison of chromosome structures confirms the polyploid event that led to the tetraploid ancestor of modern maize.

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Section: Resultsmentioning

confidence: 99%

Centromere retention and loss during the descent of maize from a tetraploid ancestor

Wang

Bennetzen

2012

Proc. Natl. Acad. Sci. U.S.A.

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“…This procedure of engineered chromosome production does not rely on cloning centromere sequences from different plant species (38) and bypasses any complications of epigenetic components for centromere specification (39). Although the B chromosomes of various plant species (11) provide an attractive vehicle to produce engineered chromosomes, we present a proof of concept that minichromosomes can also be recovered from truncation events of A chromosomes.…”

Section: Discussionmentioning

confidence: 99%

Construction and behavior of engineered minichromosomes in maize

Han

Gao

et al. 2007

Proc. Natl. Acad. Sci. U.S.A.

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136

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Engineered minichromosomes were constructed in maize by modifying natural A and supernumerary B chromosomes. By using telomere-mediated chromosomal truncation, it was demonstrated that such an approach is feasible for the generation of minichromosomes of normal A chromosomes by selection of spontaneous polyploid events that compensate for the deficiencies produced. B chromosomes are readily fractionated by biolistic transformation of truncating plasmids. Foreign genes were faithfully expressed from integrations into normal B chromosomes and from truncated miniB chromosomes. Site-specific recombination between the terminal transgene on a miniA chromosome and a terminal site on a normal chromosome was demonstrated. It was also found that the miniA chromosome did not pair with its progenitor chromosomes during meiosis, indicating a useful property for such constructs. The miniB chromosomes are faithfully transmitted from one generation to the next but can be changed in dosage in the presence of normal B chromosomes. This approach for construction of engineered chromosomes can be easily extended to other plant species because it does not rely on cloned centromere sequences, which are species-specific. These platforms will provide avenues for studies on plant chromosome structure and function and for future developments in biotechnology and agriculture.artificial chromosomes ͉ FISH ͉ genetic engineering ͉ telomere truncation A rtificial chromosomes involving de novo centromere formation on an independently assembled unit and engineered minichromosomes produced by telomere truncation provide striking advantages over traditional methods of gene transformation in yeast and mammalian cells (1-5). The development of such chromosomes in plants would provide these advantages for many applications in basic studies, biotechnology, and agriculture. These chromosomes could be used as independent platforms for foreign gene expression without random integration into the normal chromosomes. Further additions of unlimited amounts of DNA could be added to these platforms in a sequential manner via different site-specific recombination cassettes. Genes introduced in this way would be present in a defined context and thus could be expressed at a more predictable level than through random integration (6). Hence, additional genes, multigene complexes, or even whole metabolic pathways could potentially be added to a genotype. Moreover, engineered or artificial chromosomes could be easily introduced or removed from a genotype by genetic crosses and would facilitate introgression of transgenes to different genetic backgrounds.To extend engineered chromosome technology to plants, we developed a method of telomere-mediated chromosomal truncation in maize by Agrobacterium-mediated transformation of constructs with multiple copies of the telomere sequence (7). Here, we report the use of this technology to produce minichromosome platforms by truncating both normal A and supernumerary B maize chromosomes and at the same time introducing site-spe...

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“…The centromere inactivation will ensure regular meiotic segregation of the fusion chromosome and can result in evolutionary fixed reduction of chromosome number. Several cases of inactivated ancestral centromeres as well as the emergence of neocentromeres (centromere repositioning) were reported in mammalian species (e.g., Ferreri et al, 2005;Ventura et al, 2007), but only a few examples of centromere inactivation (and reactivation; F. ) in plants, including dicentric chromosomes of Trititiceae (Sears and Camara, 1952;Luo et al, 2009), maize (Zea mays) B chromosomes (F. Han et al, 2006, and potentially also chromosomes of two cucurbit species (Y. . Except for the heterochromatic knob on chromosome SN3 corresponding to the AK5 centromere, no heterochromatin was observed at sites of the other 17 presumably inactivated centromeres.…”

Section: Species-specific Dysploidy Following the Wgdmentioning

confidence: 99%

Fast Diploidization in Close Mesopolyploid Relatives ofArabidopsis

et al. 2010

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Mesopolyploid whole-genome duplication (WGD) was revealed in the ancestry of Australian Brassicaceae species with diploid-like chromosome numbers (n = 4 to 6). Multicolor comparative chromosome painting was used to reconstruct complete cytogenetic maps of the cryptic ancient polyploids. Cytogenetic analysis showed that the karyotype of the Australian Camelineae species descended from the eight ancestral chromosomes (n = 8) through allopolyploid WGD followed by the extensive reduction of chromosome number. Nuclear and maternal gene phylogenies corroborated the hybrid origin of the mesotetraploid ancestor and suggest that the hybridization event occurred ;6 to 9 million years ago.The four, five, and six fusion chromosome pairs of the analyzed close relatives of Arabidopsis thaliana represent complex mosaics of duplicated ancestral genomic blocks reshuffled by numerous chromosome rearrangements. Unequal reciprocal translocations with or without preceeding pericentric inversions and purported end-to-end chromosome fusions accompanied by inactivation and/or loss of centromeres are hypothesized to be the main pathways for the observed chromosome number reduction. Our results underline the significance of multiple rounds of WGD in the angiosperm genome evolution and demonstrate that chromosome number per se is not a reliable indicator of ploidy level.

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High frequency of centromere inactivation resulting in stable dicentric chromosomes of maize

Cited by 295 publications

References 23 publications

Centromere retention and loss during the descent of maize from a tetraploid ancestor

Centromere retention and loss during the descent of maize from a tetraploid ancestor

Construction and behavior of engineered minichromosomes in maize

Fast Diploidization in Close Mesopolyploid Relatives ofArabidopsis

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