Further evidence for a role of centromeric heterochromatin in B chromosome nondisjunction

The high loss phenomenon was described by Rhoades et al. (PNAS 57:1626-32, 1967). It was found that B chromosomes cause A chromosomes to undergo a faulty nondisjunctional process at the second pollen mitosis, which results in chromosome breakage. The event only occurs in a certain genetic background and is believed to depend on non-replication of heterochromatic knobs. Rhoades and Dempsey (Gen. 71:73-96, 1972) interpreted the high loss phenomenon as evidence for a role of heterochromatin in B chromosome nondisjunction. Specifically, they proposed that centromeric heterochromatin of the B fails to replicate at the second pollen mitosis, resulting in nondisjunction. Evidence was later presented showing that identical types of heterochromatin are present in both A chromosome knobs and centromeric heterochromatin of the B (Pryor et al., PNAS 77:6705-9, 1980).

Independent support for a role of centromeric heterochromatin in nondisjunction was presented recently by Carlson and Chou (Gen. 97:379-89, 1981). They reported work with the B-A translocation B-9Sb and a B-9 isochromosome derived from it. The isochromosome was found to be a pseudoisochromosome because of asymmetry in the centromeric region. One arm of the isochromosome contains a complete B-9 (except the short arm) whereas the other arm has little or no centromeric heterochromatin. The pseudoisochromosome (also called the original isochromosome) is unstable, and six telocentric derivatives were obtained from it. Four of the telocentrics came from the isochromosome arm that lacks centromeric heterochromatin while two arose from the opposite arm. The ability to carry out nondisjunction at the second pollen mitosis was extremely low in telocentrics lacking centromeric heterochromatin but not in those which contained it.

Since the comparisons made between telocentric B-9's with or without centromeric heterochromatin were not carried out using similar genetic backgrounds, an inbreeding procedure was begun. Inbreeding of the telocentrics will take several generations. However, a comparison of inbred isochromosome stocks can be made now. The original isochromosome contains centromeric heterochromatin as already described. A second isochromosome that lacks centromeric heterochromatin was also isolated (Gen. 97:378-89, Fig. 8). The isochromosome lacking centromeric heterochromatin (also called the new isochromosome) was derived by misdivision of a telocentric B-9, which in turn came from the original isochromosome.

Both the original isochromosome (+ heterochromatin) and the new isochromosome (- heterochromatin) were inbred for four generations to a Bz Bz wx wx tester line. From each inbred line, four plants carrying an iso B-9 were selected crosses were: bz bz wx wx X 9(bz wx) 9-B(Wx) iso B-9(Bz Bz). The results of classifying three ears per male parent are given below:

Table.

In the crosses of both the original isochromosome and the new isochromosome the rate of Wx transmission was well below 50% (13.5 - 15%). Selection against Wx resulted from genetic imbalance of the 9-B(Wx) iso B-9(Bz Bz) chromosome combination. The more successful meiotic products contained 9(Bz wx).

Comparative nondisjunction rates of the isochromosomes were determined as bz Wx kernels (class II nondisjunction) per total Wx. For the original isochromosome, nondisjunction was 16.8% (114/679) whereas for the new isochromosome the rate was 2.5% (20/794). The difference seen here again shows that centromeric heterochromatin has a strong effect on nondisjunction rate.

Chimeric (Bz/bz) phenotypes were recorded in the table because of their frequent occurrence in isochromosome crosses. A previous comparison between the original isochromosome and the standard B-9 showed a more than 10-fold difference in the rate of Bz/bz kernels (Gen. 97:379-89, 1981). In the table above, rates of chimeric kernels for the original isochromosome and the new isochromosome are 8.4% (57/679) and 8.1% (64/794) respectively. The control groups containing a normal 9(wx) gave rates of 0.3% (14/4335) and 0.2% (9/4485). Clearly, the isochromosomes show unusually high rates of endosperm instability. In addition, the rates of instability are quite similar between the two isochromosomes, suggesting that centromeric heterochromatin may not affect these rates. However, a true isochromosome with centromeric heterochromatin on both sides of the centromere has not yet been tested for rate of chimeric kernels. (True isochromosomes were recently characterized by Brannen--Ph.D. thesis, U. Iowa, 1980). As proposed earlier (Gen. 97:379-89, 1981), the absence of the B short arm in isochromosomes may produce frequent isochromosome misdivision at the second pollen mitosis, resulting in unstable telocentrics being transmitted to the next generation.

W. R. Carlson


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