THE GENUS COLLINSIA. XVII. A CYTOGENETIC STUDY OF RADIATION-INDUCED RECIPROCAL TRANSLOCATIONS IN C. HETEROPHYLLAl
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1 TH GNUS COLLINSIA. XVII. A CYTOGNTIC STUDY OF RADIATION-INDUCD RCIPROCAL TRANSLOCATIONS IN C. HTROPHYLLAl. D. GARBR AND T. S. DHILLON2 Department of Botany, University of Chicago, Chicago, Illinois Received November 2, 161 RCIPROCAL translocation between nonhomologous chromosomes may be Adetected cytologically by observing an interchange complex at metaphase I. The interchange complex may occur either as an alternate or adjacent configuration, that is, zigzag or open ring or chain. In some species, the frequency of pollen mother cells with one or the other configurations is approximately equal; in other species, the number of pollen mother cells with an alternate configuration is significantly higher than 50 percent (directed orientation). Reciprocal translocations within a species generally yield interchange complexes exhibiting either a random or directed orientation but not both (BURNHAM 156). Seventeen colchicine-induced reciprocal translocations in Collinsia heterophy2la Buist (n = ) gave interchange complexes with a random orientation at metaphase I ( SORIANO 15). Cytogenetic studies of radiation-induced reciprocal translocations to be reported in this paper indicate a high frequency of directed orientation of the interchange complexes at this stage. MATRIALS AND MTHODS Five reciprocal translocations () were studied. -A, -B, -C, and -D each gave an interchange complex of four chromosomes and -, one of six chromosomes. -A and -B were obtained from plants which had been exposed to 1,000r (X ray) at the prebud stage, -C from dry seed given 10,000r (X ray), and both -D and - from one plant grown from seed exposed to 16,000r (gamma rays from a cobalt therapy unit). Methods for germinating seed and for raising plants in the greenhouse and procedures for fixing anthers, staining smears of pollen mother cells with acetocarmine, and determining fertility have appeared in earlier papers in this series (GARBR 156; GORSIC 15; SORIANO 15). 1 This investigation was aided by grants from the National Science Foundation and from the Dr. Wallace C. and Clara A. Abbott Memorial Fund, University of Chicago. Present address: Department of Botany, University of Hong Kong. Genetics 4: April 162.
2 ~~ ~~ ~~ 462, D. GARBR AND T. S. DHILLON TABL 1 Frequency of ring and chain interchange complexes at metaphase I with alternate or adjacent orientation Rings Chains No of Plant PMC s Alternate Adjacent Alternate Adjacent A B C D l%l -1 6A RSULTS Interchange compkxes at metaphase I: (Table 1 ) The interchange complexes of four chromosomes occurred more frequently as rings than as chains at metaphase I; the interchange complex of six chromosomes yielded more chains than rings at this stage. Pollen mother cells with seven bivalents either did not occur or were rarely observed, depending on the interchange complex. Both rings and chains displayed a directed orientation at metaphase I. In interchange complexes of four chromosomes, approximately 0 percent of the rings and approximately 0 percent of the chains had an alternate arrangement; in the interchange complex of six chromosomes approximately 4 percent of the rings and approximately 6 percent of the chains also had an alternate arrangement. Chiasmata frequency at metaphase I in C. heterophylla ranged from 1.1 to 1.5 per bivalent (GARBR 156). The chiasmata frequency at this stage in plants with an interchange complex was calculated on the basis of the bivalents which were present and of the pairs of chromosomes in the interchange complex. Although the chiasmata frequency of the bivalents did not significantly differ from that for the species, the chiasmata frequency of the chromosomes in the interchange complexes was higher. The values for the interchange complexes of four chromosomes were , and for the one with six chromosomes, Transmission of the interchcrnge complexes: (Table 2) Plants with an interchange complex were self-pollinated and crossed as seed or pollen-parent with plants having seven bivalents. When the results of selfs and crosses are considered, approximately 50 percent of the plants in each case and for each reciprocal translocation had an interchange complex. Fertility: Although SORIANO (15) found that the percentage of stainable
3 RCIPROCAL TRANSLOCATIONS 46 TABL 2 Transmission of the interchange complexes A B c D A B C D A B C D Number of plants Interchange complex Total Present Absent : Self-pollinated : Seed-parent : Pollen-parent TABL Percent stainable pollen grains in progeny of self-pollinated plants with a heterozygous reciprocal translocation Interchange complex Present Absent No. of plants Percent Mean Range No of plants Percent Mean Range A B C D pollen grains was not a reliable criterion for detecting plants which were heterozygous for a colchicine-induced reciprocal translocation, it was possible to identify such plants when the percentage of stainable pollen was less than 50 percent. Plants which were heterozygous for a radiation-induced reciprocal translocation could not be detected by using percentage of stainable pollen grains (Table ). Although seed-set was reduced in plants with an interchange complex compared with plants lacking a complex (Table 4), the former plants had percent of the seed-set of the latter plants. Plants with an interchange complex of six chromosomes had 6 percent of the seed-set of plants lacking a complex in the same population.
4 ~ ~ ~~ 464. D. GARBR AND T. S. DHILLON TABL 4 Seed-set in progeny of self-pollinated plants with a heterozygous reciprocal translocation Present Interchange complex Absent No. of Seed/capsule No. of Seed/capsule plants Mean Range plants Mean Range A B C D TABL 5 Interchange complexes in plants with two heterozygous reciprocal translocations from crosses Reciprocal translocations D C n A lq4* B C 104 none D 104 * Q mdlcatei an inteilhange comp1e.r TABL 6 Tests for linkage between white flower (w ) and five reciprocal translocations Number nl plants with interchange complex Present Absent -_ Segr. * Dominant Recessive Dominant Recessive A TC B TC G C F2 5 1 TC D F, TC F, 5 TC (testcross)-plants heterozygous for both gene and reciprocal translocation crossed with plants homozygous for recessive gene and with seven bivalents. F,-self-pollinated plants heterozygous for both gene and reciprocal translocations. Identification of chromosomes in interchange complexes: (Table 5 ) Plants with different heterozygous reciprocal translocations were crossed in all possible combinations and the hybrids were examined to determine their chromosome associations at metaphase I. Only the interchange complexes which were observed in the hybrids were entered into the table. One of the two chromosomes involved in -A did not occur in the other reciprocal translocations; one of the two chromosomes in -B was also present in the interchange complexes of -C, -D, and -; the same two chromosomes occurred in -C and in -D; two of the three chromosomes in the interchange complex for - were the same as those in -C and -D.
5 RCIPROCAL TRANSLOCATIONS 465 Genetic studies: (Table 6) Although populations were relatively small, a preliminary genetic study involving the gene (w) for white flower (GORSIC 15) and the five reciprocal translocations indicated that this gene was linked with -A and -B. Since these reciprocal translocations had a common chromosome, the gene was probably located on this chromosome. DISCUSSION Two observations distinguished interchange complexes in Collinsia heterophylla obtained after colchicine treatment or from ionizing radiation. The former interchange complexes occurred as a ring or chain or as bivalents and exhibited a random orientation at metaphase I; the latter occurred either as a ring or chain and displayed a directed orientation at this stage. It has been possible to explain these differences by assuming that each mutagen was responsible for chromosome breakage at different sites. GARBR and BLL (162) were able to account for the chromosome associations at metaphase I which were observed in diploid interspecific hybrids by assuming that chiasmata were formed either in terminal or subterminal segments of the chromosomes. If colchicine-induced breaks occurred in the chiasma-forming segments and radiation-induced breaks in the internal segment of the chromosomes, two types of interchange complexes would result. These types have been diagrammed at pachytene in Figure l. ach arm of a bivalent has not more than one chiasma at metaphase I (GARBR 156, 158). Depending on the position of the first chiasma formed adjacent to the site of breakage in colchicine-induced reciprocal translocations, it is possible to get a ring or chain of chromosomes or bivalents; only a ring or chain FIGUR 1.-Diagrams of interchange complexes at pachytene obtained by colchicine treatment (left, center) or by ionizing radiation (right). Interrupted chrosmosomal segments represent sites of chiasma formation; homologous regions have identical numbers; and dotted crosses indicate possible chiasmata (explanation in text).
6 466. D. GARBR AND T. S. DHILLON would be expected for a radiation-induced interchange complex. Although several mechanisms have been offered to explain directed orientation of an interchange complex (as reviewed by BURNHAM 156), it has not yet been possible to apply any one of these to explain the directed orientation of the interchange complexes observed in the radiation-induced reciprocal translocations of C. heterophylla. It is possible that the differences in the length of translocated segments may be responsible for the differences in the frequencies of the two configurations at metaphase I. Although it was necessary to assume that colchicine-induced breaks were restricted to the chiasma-forming segments. radiation-induced breaks need not be restricted to the internal segment, that is, proximal to the centromere, of the chromosomes. If the latter segment were relatively much longer than the chiasmaforming segments, random hits by ionizing radiation would have been expected to occur more frequently in the internal segment. A large number of radiationinduced interchange complexes is needed to determine if the breaks are restricted to the internal segment or are randomly distributed. Many interspecific hybrids in Collinsia exhibited interchange complexes at metaphase I (GARBR and GORSIC 156; AHLOOWALIA and GARBR 161; BLL and GARBR 161). In some hybrids, the interchange complexes occurred as a ring or chain or as bivalents and univalents, the rings or chains displaying a random orientation at metaphase I; in other hybrids, the complexes occurred as a ring or chain which displayed a directed orientation at this stage. The random uersus directed orientation of these interchange complexes may reflect different sites of spontaneous chromosome breaks in their chromosomes. By assigning an arbitrary number to the chromosomes of C. heterophylla, it was possible to determine which chromosomes were involved in the radiationinduced reciprocal translocations. Using the information in Table 5 and the procedure followed for Oenothera ( CLLAND 16), the following chromosomes were involved in each of the five reciprocal translocations: A-1 and 2, B-2 and, C and D- and 4, and -, 4, and 5. Consequently, five of the seven chromosomes in this species occurred in the reciprocal translocations. Since the gene for white flower was linked with -A and -B, it is reasonable to assume that this gene is on chromosome 2 which is the one common to both reciprocal translocations. Granting that larger populations might have shown some recombination between this gene and the two reciprocal translocations with which it is linked, it is possible to interpret the apparently complete linkage as indicating that the gene is in the internal segment of chromosome 2. In such an event, no recombinants would have been expected. This explanation is currently being tested by using larger populations. SUMMARY Four reciprocal translocations involving two nonhomologous chromosomes and one involving three nonhomologous chromosomes were obtained either from plants of Collinsia heterophylla (n = ) at the prebud stage or from seed which
7 RCIPROCAL TRANSLOCATIONS 46 had been exposed to ionizing radiation from an X-ray source or from a cobalt therapy unit. The interchange complexes occurred either as a ring or chain but rarely as bivalents at metaphase I; the rings and chains displayed a directed orientation at this stage. Although the percentage of stainable pollen grains and the number of seed per capsule were reduced in plants with an interchange complex, the plants were not semisterile; plants with an interchange complex of six chromosomes had a lower seed-set than plants with an interchange complex of four chromosomes. Five of the seven chromosomes in the complement are involved in the five reciprocal translocations. The gene for white flower is linked with two different reciprocal translocations which have one chromosome in common. The chromosomes of this species are assumed to have a terminal or subterminal chiasma-forming segment in each arm. To account for the different types of interchange complex obtained after colchicine treatment or exposure to ionizing radiation, it is assumed that the former treatment is responsible for chromosome breaks in the chiasma-forming segments and the latter for breaks in the segment of the chromosome proximal to the centromere. ACKNOWLDGMNTS We are indebted to DR. N. J. SCULLY, Argonne National Laboratory, for assistance in exposing plants and seed to X ray and to DR. L. SKAGGS, Argonne Cancer Research Hospital, for assistance in exposing seed to gamma rays from a cobalt therapy unit. We are particularly indebted to DR. C. R. BURNHAM for valuable suggestions in preparing the manuscript. LITRATUR CITD AHLOOWALIA, B. S., and. D. GARBR, 161 The genus Collinsia. XIII. Cytogenetic studies of interspecific hybrids involving species with pediceled flowers. Botan. Gaz. 122 : BLL, SANDRA L., and. D. GARBR, 161 The genus Collinsia. XII. Cytogenetic studies of interspecific hybrids involving species with sessile flowers. Botan. Gaz. 122 : BURNHAM, C. R., 156 Chromosomal interchanges in plants. Botan. Rev. 22: CLLAND, R.., 16 Some aspects of the cytogenetics of Oenothera. Botan. Rev. 2: GARBR,. D., 156 The genus Collinsia. I. Chromosome number and chiasma frequency of species in the two sections. Botan. Gaz. 1: 1-. GARBR,. D., and J. GORSIC, 156 The genus Collinsia.. Interspecific hybrids involving C. heterophylla, C. concolor, and C. sparsifzora. Botan. Gaz. 1: -. GARBR,. D., and SANDRA L. BLL, 162 The genus Collinsia. XV. A cytogenetic study of fertile interspecific hybrids with an interchange complex of six chromosomes. Botan. Gaz. (In press.) GORSIC, J., 15 The genus Collinsia. V. Genetic studies in C. heterophylla. Botan. Gaz. 1: SORIANO, J. D., 15 The genus Collinsia. IV. The cytogenetics of colchicine-induced reciprocal translocations in C. heterophylla. Botan. Gaz. 1:
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