Reactivation of an Inactive Centromere Reveals Epigenetic and Structural Components for Centromere Specification in Maize

Han, Fangpu; Gao, Zhi; Birchler, James A.

doi:10.1105/tpc.109.066662

Cited by 154 publications

(114 citation statements)

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“…24 and 25 and this study) and barley (22), it is likely that de novo centromeres are initiated regularly in chromosome arms, but when opposed in anaphase against the large canonical centromere, they are as quickly inactivated, leaving no trace. Previous work suggests that the smaller centromere in functionally dicentric chromosomes is prone to inactivation in both maize (30) and wheat (32). These findings indicate that if a centromere is not used during a particular anaphase it becomes epigenetically inactivated and inherited in that state.…”

Section: Discussionmentioning

confidence: 79%

“…The regular occurrence of de novo centromeres found here and previously (24,25) indicates that they are capable of being formed regularly on chromosomal fragments that are structurally acentric; however, they do not persist in normal chromosomes. The reason might reside in the previous observation in maize (30) and wheat (32) that in functional dicentrics the smaller centromere becomes inactive in a tug of war between large and small. However, in the absence of a normal centromere, the present work illustrates that de novo centromeres can persist.…”

Section: Significancementioning

confidence: 99%

“…In maize, many dicentric chromosomes have been reported from B-A translocation chromosome derivatives (29). Dicentric chromosomes can be produced through the process of the chromosome type breakage-fusion-bridge (BFB) cycle, and the inactive centromeres can be reactivated by intrachromosomal recombination (30). The DNA sequences of the active and inactive centromeres of dicentric chromosomes are essentially identical, but the centromere activity states are completely different.…”

Section: Significancementioning

confidence: 99%

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Sequential de novo centromere formation and inactivation on a chromosomal fragment in maize

Liu

Pang

et al. 2015

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

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The ability of centromeres to alternate between active and inactive states indicates significant epigenetic aspects controlling centromere assembly and function. In maize (Zea mays), misdivision of the B chromosome centromere on a translocation with the short arm of chromosome 9 (TB-9Sb) can produce many variants with varying centromere sizes and centromeric DNA sequences. In such derivatives of TB-9Sb, we found a de novo centromere on chromosome derivative 3-3, which has no canonical centromeric repeat sequences. This centromere is derived from a 288-kb region on the short arm of chromosome 9, and is 19 megabases (Mb) removed from the translocation breakpoint of chromosome 9 in TB-9Sb. The functional B centromere in progenitor telo2-2 is deleted from derivative 3-3, but some B-repeat sequences remain. The de novo centromere of derivative 3-3 becomes inactive in three further derivatives with new centromeres being formed elsewhere on each chromosome. Our results suggest that de novo centromere initiation is quite common and can persist on chromosomal fragments without a canonical centromere. However, we hypothesize that when de novo centromeres are initiated in opposition to a larger normal centromere, they are cleared from the chromosome by inactivation, thus maintaining karyotype integrity.centromere misdivision | epigenetics | de novo centromere | centromere inactivation T he centromere is an important chromosomal region responsible for correct chromosome segregation during cell division. Centromeres are found in the primary constriction region on the chromosome, upon which the kinetochore complex assembles to produce a platform for spindle binding (1). Centromere function is conserved among different species, and several epigenetic markers of active centromeres have been found, including a histone H3 variant referred to as CENH3 in plants (2, 3) or CENP-A in animals (4-6) and phosphorylation of histone H2A at Thr133 in plants (7). Correct loading of CENH3 to the centromere region is a key component of kinetochore assembly (8). Centromeric DNA sequences have experienced rapid evolution (9, 10), and arrangements of DNA sequence in centromere regions differ in species and even in different chromosomes of an individual organism (11). Myriad repeat sequences exist in the centromeres of higher plants. In maize (Zea mays), there are two major types of centromere specific DNA sequences: the simple satellite repeat sequence CentC (12) and centromeric retrotransposon of maize (CRM) (3). Many epigenetic features have been identified in centromeric regions, including DNA methylation levels, histone variants, histone modifications, and RNA components (11). Both epigenetic elements and DNA sequences take part in centromere formation and maintenance, but it is still unknown how genetic and epigenetic factors work together in this process.The centromere is one of the most complex regions on the chromosome, and complete DNA sequencing through the centromeric region is difficult to obtain due to their highly repetitive nature...

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Section: Discussionmentioning

confidence: 79%

Section: Significancementioning

confidence: 99%

Section: Significancementioning

confidence: 99%

See 1 more Smart Citation

Sequential de novo centromere formation and inactivation on a chromosomal fragment in maize

Liu

Pang

et al. 2015

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

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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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“…Thus, the other centromere was inactivated [45]. Interestingly, when these dicentric chromosomes broke into two parts, each with one centromeric region, the inactive centromere could regain activity [46]. As another example, a translocation formed between maize chromosomes 1 and 5 captured a centromere that became inactive showing no CENPC and H3S10ph staining, which is otherwise typical of active centromeres [47,48].…”

Section: Centromere Identity Is Epigenetically Determinedmentioning

confidence: 99%

Recent advances in plant centromere biology

Feng

Liu

et al. 2015

Sci. China Life Sci.

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The centromere, which is one of the essential parts of a chromosome, controls kinetochore formation and chromosome segregation during mitosis and meiosis. While centromere function is conserved in eukaryotes, the centromeric DNA sequences evolve rapidly and have few similarities among species. The histone H3 variant CENH3 (CENP-A in human), which mostly exists in centromeric nucleosomes, is a universal active centromere mark in eukaryotes and plays an essential role in centromere identity determination. The relationship between centromeric DNA sequences and centromere identity determination is one of the intriguing questions in studying centromere formation. Due to the discoveries in the past decades, including "neocentromeres" and "centromere inactivation", it is now believed that the centromere identity is determined by epigenetic mechanisms. This review will present recent progress in plant centromere biology. centromere, epigenetics, CENH3

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Reactivation of an Inactive Centromere Reveals Epigenetic and Structural Components for Centromere Specification in Maize

Cited by 154 publications

References 46 publications

Sequential de novo centromere formation and inactivation on a chromosomal fragment in maize

Sequential de novo centromere formation and inactivation on a chromosomal fragment in maize

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

Recent advances in plant centromere biology

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