The cytological basis of the failure of non-disjunction associated with a B-10 translocation

During a routine propagation (r-g x r-g 10B B10 (R-scm) B10 (R-scm)) of translocation TB-10(30), an ear with an unusual segregation pattern was observed. It contained only two seed classes (colored and colorless) instead of four as found on the sib ears (Table 1). The two missing classes are the ones with discordant embryo and endosperm phenotypes, which are the descendants of pollen grains whose B10 undergoes non-disjunction during the second pollen mitosis. It is speculated that B10 in the paternal plant of this exceptional ear had lost its nondisjunctional activity. Furthermore, the fact that both B10's of this plant were unable to non-disjoin, having been able to in the previous generation, suggests 10B as responsible for such failure. This conjecture is substantiated by the fact that B10 non-disjunction was restored after incorporation of intact B's into the plants growing from the seeds of the exceptional ear.

Table 1.

The failure of 10B to promote the non-disjunction of B10 may be due to a structural mutation that occurred either prior to or after the second pollen mitosis. According to the first explanation, 10B would have been defective ever since or shortly after it was isolated. Its defectiveness had not been identified due to the presence of intact B's in the same stock. When B's disappeared as a result of successive test-crosses and preferential fertilizations toward the endosperm, B10 became unable to non-disjoin. The latter model predicts that 10B possessed the ability of inducing B10 non-disjunction prior to the second pollen division but it changed its structure and lost such ability afterwards. Results of the following experiments are in agreement with the first explanation:

(1) Chromosome counts of root tips from the colored seeds on the exceptional ear gave an expected number, 13 out of 14 being 21 and one being 20, while the counts from seeds with colored embryo but colorless endosperm on the normal sib ears are unexpected, 15 out of 33 being 22, 16 being 24 and the last two being 25 and 27, respectively. Since their karyotype is supposed to be identical to the paternal parent (namely 10 10B B10 B10), the expected chromosome number is 22. Without exception, the extra chromosomes are telocentric.

(2) Test-crosses (r-g r-g x r-g 10B B10 (R-scm) B10 (R-scm)) of seeds with colored embryo but colorless endosperm from two normal sib ears gave nearly 1:1 (33:27) proportion of normal (same as the paternal ear) and abnormal (same as the exceptional ear) ears. This ratio is not unexpected if the paternal parent contained two B chromosomes. Each derived 10B B10 microspore would carry a single B which would undergo non-disjunction at the second pollen division as did B10. The resulting two B10's and two B's would then move with 50% chance to the same or different poles. The former yields a sperm which possesses both B's and B10's and fertilizes preferentially the egg; the second sperm, devoid of both chromosomes, joins with the polar nuclei. The latter results in two sperms which carry either two B's or two B10's and conjugate with the egg randomly (Carlson, 1969, Genetics 62:543-554). As a consequence, a little more than 50% of the 10B B10 B10 embryos would contain two B's and the remaining embryos would not. Following testcrosses as staminate plants, the former would give rise to the normal ears and the latter to the abnormal.

(3) Nine seeds with colored embryo but colorless endosperm on a normal sib ear were germinated, root tips were excised, and the seedlings were transplanted to the field and then test-crossed on r-g r-g plants at maturity. Four of these contained 22 chromosomes and gave rise to abnormal ears similar to the exceptional ones. Four others possessed 24 chromosomes, all of which resulted in normal ears. The last one had 23 chromosomes and its test-crossed ear was likewise normal but the frequency of discordant seeds was only 60% of the regular normal ears.

The cytological analysis of 10B structure yields an interesting result. Assuming one breakage on the B long arm, as in most of the other 37 B-10 translocations isolated by the writer, the pachytene figure of 10 JOB B10 tassels should contain a trivalent synapsing in a T-shaped configuration. Pairing on two of the arms of this configuration should be complete because they represent the homologous pairing between the 10 portions of TB-10(30) and chromosome 10. Pairing on the third arm, however, would not be complete since this consists of two non-homologous B portions. The B portion associated with B10 consists of the short arm, the centromere and the proximal end of the long arm. The B portion born on 10B includes the distal end of the long arm. The pairing pattern observed contradicts this expectation. The three arms of the T-shaped trivalent paired perfectly. As was assumed, the break on B is on the euchromatic region of the long arm close to the heterochromatic block and that on chromosome 10 is at about 0.12 10L. B10 possesses an expected structure, but, surprisingly, 10B carries the same B fragment as B10, including the short arm, the centromere and the euchromatic region of the B long arm.

This cytological picture furnishes several interesting views:

(1) It provides an answer to the question why 10B cannot promote B10 nondisjunction. 10B lacks the distal tip of the B long arm which is essential for B non-disjunction (Ward, 1973, Genetics 73:387-391).

(2) 10B is a dicentric chromosome, containing the B and 10 centromeres.

(3) Since 10B carries the same B portion as B10, it may be able to non-disjoin as does B10 in the presence of intact B's. Yet, the preliminary test of this possibility gave a negative result. A more critical test is being currently undertaken.

(4) 10B may originate from either the effect of x-irradiation during the initial isolation of this translocation or as the result of non-homologous crossing-over between proximal and distal portions of the B long arm. Study of these two possibilities is underway.

Bor-yaw Lin

Please Note: Notes submitted to the Maize Genetics Cooperation Newsletter may be cited only with consent of the authors.

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