Dynamic epigenetic states of maize centromeres

Abstract

The centromere is a specialized chromosomal region identified as the major constriction, upon which the kinetochore complex is formed, ensuring accurate chromosome orientation and segregation during cell division. The rapid evolution of centromere DNA sequence and the conserved centromere function are two contradictory aspects of centromere biology. Indeed, the sole presence of genetic sequence is not sufficient for centromere formation. Various dicentric chromosomes with one inactive centromere have been recognized. It has also been found that de novo centromere formation is common on fragments in which centromeric DNA sequences are lost. Epigenetic factors play important roles in centromeric chromatin assembly and maintenance. Non-disjunction of the supernumerary B chromosome centromere is independent of centromere function, but centromere pairing during early prophase of meiosis I requires an active centromere. This review discusses recent studies in maize about genetic and epigenetic elements regulating formation and maintenance of centromere chromatin, as well as centromere behavior in meiosis.

Keywords: centromere inactivation; centromere pairing; de novo centromere; epigenetics; maize; neocentromere; non-disjunction.

FIGURE 1

Different kinds of dicentric chromosomes in maize. Dicentric chromosome T1-5 is derived from an A-A translocation with an active centromere 1. 9Bic-1 is derived from a B-A translocation with active centromere 9. Dic15, sDic15, and minichromosome #5 are derived from combining B centromeres using a reverse duplication of 9S on the TB-9Sb translocation as described in the text. CRM is in green; B-repeat is red.

FIGURE 2

Centromere inactivation through the process of BFB cycle in maize. Reciprocal translocation between chromosome 9 and the B chromosome produced chromosome B-9, with an active B centromere and 9S. Duplication of 9S on B-9 generated chromosome B9-Dp9. The arrows indicate the orientation of the duplicated regions. Intrachromosomal recombination of B9-Dp9 produced dicentric chromosomes with two B centromere regions and a chromosomal fragment without a centromere region. This dicentric chromosome undergoes a BFB cycle, and produced different kinds of new dicentric chromosomes. Most of these dicentric chromosomes are with two B centromere regions, while in 9Bic-1, centromere 9 is active and the B centromere is inactive. The inactive B centromere region on 9Bic-1 remains adhered at the second pollen mitosis, which causes the chromosome to break. The broken piece formed a new A-B translocated chromosome 7Bic-1 with an inactive B centromere.

FIGURE 3

Regaining centromere activity in maize. The hybridization between plants with translocation chromosome B9-Dp9 and those with B centromere misdivision derivative T3-5(+) produced dicentric chromosome Dic15 with one big centromere and one small centromere with the small one inactive. Intrachromosomal recombination of Dic15 can generate new dicentric chromosomes with two big centromeres or two small centromeres. sDic15 is a dicentric chromosome with small centromeres that regained centromere activity via a 723 kb genomic DNA sequence de novo centromere.

FIGURE 4

Inactive centromeres (7Bic-1 in green) can not pair at the leptotene stage, when the ten pairs of functional centromeres pair completely. Immuno-FISH using an antibody against centromeric histone CENH3 in red and B repeat probe in green; chromosomes are counterstained with DAPI in blue. The inactive B centromeres are separated but the ten active A centromeres are all paired. Bar = 10 μm.

FIGURE 5

A model for centromere pairing in meiotic early prophase I in maize. We suggest a model of homologous chromosome initiation in maize in which homologous chromosomes find each other at the leptotene stage and are recognized at centromeres via a centromere function dependent mechanism. The inactive centromeres do not participate in this pairing. Then chromosome pairing is further facilitated by telomere bouquet formation and synaptonemal complex (SC)-dependent pathways.

FIGURE 6

De novo centromere formation in maize. (A) De novo centromere generated by centromere misdivision. B centromere misdivision on the B-9 chromosome causes a broken centromere that fuses with the telomere region of the same chromosome to produce a ring chromosome. The ring chromosome broke and became linear and gained a 288 kb de novo centromere in derivative 3-3. In the derivative of 3-3, this de novo centromere was inactivated and another 200 kb de novo centromere arose. (B) sDic15 has a de novo centromere derived from a 723 kb sequence. (C) Irradiated acentric chromosomal fragments can acquire a de novo centromere by CENH3 seeding at that position. Chromosome fragment Dp3a has a 350 kb de novo centromere from a sequence on the long arm of chromosome 3.