ALTERNATE-1 AND ALTERNATE-2 DISJUNCTIONS IN
HETEROZYGOUS RECIPROCAL TRANSLOCATIONS
J. E. ENDRIZZI
Department of Agronomy and Plant Genetics, Uniuersity of
Arizona, Tucson, Arizona 85721
Manuscript received December 4, 1973
ABSTRACT
Alternate-1 and alternate-2 orientation of chromosomes, as well as the two
types of adjacent orientation, were observed cytologically in the ring configurations of three reciprocal translocation heterozygotes of Gossypium hirsutum
L. The observations indicate that the two types of alternate orientation should
be characteristic of ring-forming translocations.
A reciprocal chromosomal translocation involves the exchange of segments of
non-homologous chromosomes. If members of the pair of non-homologs have
near median centromeres, if the two interchanged segments are long, and if the
chiasmata are confined to the pairing segments, the configuration that is generally
observed at diakinesis or metaphase I in the heterozygote is a ring-of-four. The
ring-of-four can exhibit two basic types of orientation: (a) a “zigzag” or alternate
and (b) an “open” or adjacent orientation. As far back as the 1930’s, the “open”
or adjacent orientation was demonstrated cytologically and genetically to be of
two types: (a) adjacent-1 in which non-homologous centromeres pass to the same
pole and (b) adjacent4 in which homologous centromeres pass to the same pole.
I n the “zigzag” or alternate orientation, as in the adjacent-I, homologous centromeres pass to opposite poles (see BURNHAM
1956, 1962; JOHNand LEWIS1965,
for extensive reviews of chromosomal translocations and their behavior). I n
terms of co-orientation of centromeres, if there are two types of adjacent orientation there should be two types of alternate orientation: alternate-l and alternate-2
(JOHN
and LEWIS1965), both of which result in complete genetic balance of the
four gametic cells. It is not possible, therefore, to distinguish genetically the two
types of alternate disjunction; however, with reciprocal translocations containing
special cytomorphological features, it should be possible t o distinguish cytologically between the two types of alternate orientations.
As opposed to alternate orientations, adjacent orientations are quite conspicuous and easily observable. In most species, translocations that have sufficient
differences in the cytomorphological features to adequately distinguish cytologically between adjacent-1 and adjacent-2, such differences in alternate configurations are usually obscured by the close association or compact nature of the
Coutnbutian no. 2197 from Arizona Agnculture Experiment Statmu. Part of this work was done under Regional
Research Project S-77,Genetics and Cytology of Cotton I1
Genetics 7 7 : 55-60 blay 1974
56
J. E. E N D R I Z Z I
alternate arrangement of chromosomes. Up to now, the two possible types of
alternate disjunction have not been demonstrated even though it has been postulated that they should occur (JOHN and LEWIS1965). Textbooks discussing the
behavior of translocations illustrate and discuss only three possible kinds of
orientations of rings-of-four that give numerically-equal separations; these are
alternate, adjacent-I and adjacent-2. BURNHAM(1934) does suggest that the
50% sterility which is characteristic of many translocations might be explained
by assuming for each “open type of orientation” an equal chance of alternate.
JOHN
and LEWIS(1965) point out that for each type of adjacent orientation there
should be a corresponding alternate arrangement. They state that the “zigzag
orientations are actually of two types. In one, the twist occurs between the associated arms which join non-homologous centromeres (the alternate equivalent of
adjacent non-homologous orientation) while in the other it occurs in the arms
joining homologous centromeres (the equivalent of adjacent homologous o,rientation) .” These are alternate-I and alternate-2, respectively. The four orientations
are illustrated in Table 1 and Fig. 2.
The data presented here illustrate both alternate-I and alternate-2 orientations,
as well as the two types of adjacent orientation, in three heterozygous reciprocal
TABLE 1
Orientation of a ring of four in translocation heterozygotes of Gossypium hirsutum
Adjacent I
T4-5
48
Alternate 1
45
Adjacent 2
16
Alternate 2
37
68
60
31
30
AG184 20
20
6
13
Tlo-19
The top row of diagrams illustrates the four expected t y p e s of orientations for the adjacent and
alternate arrangements of the T4-5 translocation. With reference to Figure 1, the knob is between
1 and 11 and 1 = 5A,, 11 = 5Ah, 2 = 4 4 , and 21 = 4Ah. The bottom row of diagrams illustrates
the four expected types of orientations for the adjacent and alternate arrangements of the two
A-D translocations T10-19 and AG184. The thick and thin bars refer, respectively, to the large A
chromosomes and the small D chromosomes.
Translocations T4-5 (IV,) and T10-I9 (1626) are from the G. hirsutum translocation stocks
developed by DR. METAS . BROWNat the Beasley Laboratory, Texas Agricultural Experiment
Station.
DISJUNCTION I N TRANSLOCATION
57
translocations of cotton, Gossypium hirsutum L. The three heterozygotes possess
certain cytomorphological features (Table 1) which make it feasible to detect
these four possible types of co-orientation of the centromeres, particularly the
the alternate-1 and alternate-2 arrangements which have not been previously
demonstrated. All cytological observations were made from iron-propionic-carmine-haemotoxylin squashes of pollen mother cells killed and fixed in 7:3 alcoholacetic acid.
G. hirsutum L. is an amphidiploid (2n = 4X = 52) which regularly shows
13 A genome bivalents and 13 D genome bivalents at metaphase I. The A genome
chromosomes are about twice the size of the D genome chromosomes.
The T4-5 interchange was originally isolated from the G. hirsutum-G.
arboreum L. species hybrid, and was transferred to G. hirsutum by repeated
backcrosses. G. arboreum is a diploid whose chromosomes belong to the A genome
and are designated A,. Chromosomes 4 and 5 of this species are standard normals
in relation to chromosomes 4 and 5 of G. hirsutum. Chromosomes 4 and 5 of the
latter species are, therefore, the translocated ones (MENZELand BROWN 1954).
The two translocated chromosomes are about equal in size; however, in G.
arboreum, chromosome 4 is much larger than chromosome 5 (Figures 1 and 2).
The configuration at MI is quite large and the two chromosomes from each
species can be identified in the heterozygote by their size and the constant position
of an ever-present “knob” as described below.
In crosses with monosomic and telosomic stocks of G. hirsutum, it was determined that the G . hirsutum chromosomes 4Ah and 5Ah are located in the lower
right and upper left positions, respectively, of the adjacent chain shown in
Figure 1. This automatically places the two G. arboreum chromosomes, 4Apand
5AI in the remaining two alternate positions. These are referred to as G. arboreum
chromosomes, but as the result of backcrossing, it is highly probable that they
now consist primarily of G. hirsutum genetic material but with the G. arboreum
end arrangement. Chromosome 4A, is much larger than the other three chromo-
FIGURE
1.-Adjacent-1 chain configuration of the T4-5 translocation. Note that chromosome
44, is larger than the other three chromosomes; also note the large ‘‘knob” associated with the
5Ah and 5.4, pair of chromosomes.
58
J. E. E N D R I Z Z I
FIGURE
2.-Ink drawings of typical metaphase I configurations of the T4-5translocation (top
row) and the T10-19translocation (bottom row). I n each row from left to right, the first two
Configurations show adjacent-1 and alternate-1 orientations, and the second two configurations
show adjacent-2 and alternate-&orientations, respectively.
somes (Figure 1) and can be easily recognized in both alternate and adjacent
orientations. The other important identifying characteristic of this structural
change is the constant existence of a large “knob”, undoubtedly the result of
nonterminalization of one or more chiasmata, between 5Ah and 5A, as shown
in Figure 1. The “knob” can be easily seen in alternate and adjacent configurations. Thus, the large size of the ring plus the large size of the 4A, chromosome
and the position of the “knob” make it possible to recognize readily the four
chromosomes and to identify easily the four types of orientation (Figure 2, top
row). The four expected types of orientation for the alternate and adjacent
arrangements for T4-5 and the frequency of their occurrence are illustrated in
Table 1.
The other two translocations probably involve reciprocal translocations
between A and D genome chromosomes of G. hirsutum. The T10-19 translocation consists of a reciprocal interchange between chromosome 10 of the A genome
personal
(large) and chromosome 19 of the D genome (small) (METAS. BROWN,
communication). The two non-homologous chromosomes involved in the AG184
translocation have not been identified. The size difference between the chromosomes indicates that this also involves a large pair of A genome chromosomes and
a small pair of D genome chromosomes sinc. it gives ring and chain configurations quite similar to T10-19. The identifying features of these two heterozygous translocations are the orientations of the two large chromosomos in relation
to the two small chromosomes. It was concluded from MI observations that in
both heterozygotes, the two large chromosomes carry the centromeres of the A
chromosolres and that the two small chromosomes carry the centromeres of the
D I S J U N C T I O N IN TRANSLOCATION
59
D chromosomes. However, the only evidence I have that this is the case is with
the AG184 translocation. Occasionally in this translocation a “frying-pan” type
of configuration is observed in which a chiasma exists in the interstitial segment
of the two small chromosomes, indicating that their centromeres are homologous
and that they consist of a standard normal D chromosome and an interchange D
chromosome, i.e., DA.The diagrams in Table 1 and drawings in Figure 2 (bottom
row) illustrate how the size differences between A and D chromosomes appear
in different orientations.
The two types of alternate and two types of adjacent configurations could be
identified with a reasonable degree of accuracy by noting the orientational relationships oi the two large and two small chromosomes. The four types and their
frequencies for these two interchanges are given in Table 1.
According to JOHN and LEWIS(1965), the orientation of multiples, such as in
the above heterozygous translocations, is based on “the random behavior of two
pairs of co-oriented adjacent centromeres” which they identify as ‘‘realistic
randomness”. Thus, the expected is 1 alternate : 1 adjacent. Since there are two
possible types of adjacent segregation, there should be for each adjacent-1 segregation a corresponding alternate-1 arrangement and for each adjacent-2 arrangement there should be a corresponding alternate-2 arrangement. Results for both
the T10-19 and AG184 heterozygotes fit this assumption. For T10-19 there are
68 adjacent-1 to 60 alternate-1 (P = 0.5-0.3) and 31 adjacent-2 to 30 alternate-2
(P = 0.9) and for AG184 there are 20 adjacent-1 to 20 alternate-1 and 6 adjacent-2 to 13 alternate-2 (P = 0.2-0.1). For the T4-5 translocation this relationship applies to the adjacent-I : alternate-1 orientation (48:45, P = 0.8-0.7), but
not to the adjacent-2 : alternate-2 relationship (16:37, P = 0.01). The deficiency
here is in the adjacent-2 class which is due most likely to the “knob” or rather to
the nonterminalized chiasma that causes a higher frequency of co-orientation of
the two centromeres 5Ah and 5A, to opposite poles. The occurrence of a chiasma
in the interstitial region has not been observed in this translocation, and, therefore, it is not likely to be a factor contributing to the discrepancy between adjacent-2 and alternate-2 in this case. An excess of alternate orientation over adjacent
orientation has been noted previously for this translocation (see 2872 translocation in Table 1 of ENDRIZZI
1958).
JOHN and LEWIS(1965) have inferred that the four types of orientations, due
to the random behavior of two pairs of co-oriented adjacent centromeres, should
occur in any reciprocal translocation which can f o r m ring configurations in
meiosis. The results presented here for the three heterozygous translocations in
G. hirsutun demonstrate that their inference is indeed correct. Furthermore, this
type of random centromere behavior should be characteristic of multivalents
such as quadrivalents (JOHN and LEWIS
1965). In light of this, DR.C. R. BURNHAM, in personal correspondence, has pointed out that one would predict the
possibility of 1/8 maximum equational segregation instead of the 1/6 that has
normally been assumed.
60
J. E. ENDRIZZI
LITERATURE CITED
BURNHAM,
C. R., 1934 Cytogenetic studies of an interchange between chromosomes 8 and 9 in
maize. Genetics 19: 430-447. -,
1956 Chromosomal interchanges in plants. Bot.
Rev. 22: 419-552. -,
1962 Discussions in Cytogenetics. Burgess Publishing Co.,
Minneapolis.
J. E., 1958 The orientation of interchange complexes and quadrivalents in Gossypium
ENDRIZZI,
hirsutum and Eu-Sorghum. Cytologia 23: 362-371.
JOHN,B. and K. R. LEWIS,1965 The meiotic system. Protoplasmatologia6: 1-335.
MENZEL,MARGARET
Y. and METAS. BROWN,1954 The significance of multivalent formation
in three species Gossypium hybrids. Genetics 39: 546-557.
Correspondingeditor: R. W. ALLARD