SERIAL-SECTION ANALYSIS O F CLUSTERING WITHIN ANTHERS
OF MAIZE MICROSPOROCYTES WITH SPECIFIC CROSSOVERS
MAJORIE P. MAGUIRE
Zoology Department, University of Texas, Austin, Texas 787112
Manuscript received July 9, 1979
Revised copy received January 7, 1980
ABSTRACT
The distribution within anthers of maize plants of microsporocytes of differing crossover class was studied by application of the serial-sectioning technique
to plants heterozygous for a paracentric inversion. In such material, cells with
four-strand double crossovers within the inversion are distinguishable from
cells with other classes of crossovers within the inverted region and from cells
with no crossovers within the inversion. Evidence was found for coarse clustering o€ cells with four-strand double crossovers within the inversion and for
coarse clustering of cells of other crossover classes (with at least one crossover
within the inversion). The local frequencies of these two major categories of
crossover cells appeared to vary independently of each other, with regional
increases in each occurring at the expense of noncrossover cells. There is also
some suggestion that cells with four-straqd doubles within the inversion may
he clustered independently of other double-crossover classes within the inversion, but these other classes are not directly scorable.
HE nature of the mechanisms that determine position of crossover sites repTresents one of the most deficient areas of genetic understanding. The usual
tendency for a somewhat nonrandom distribution has been recognized for many
years (and entitled crossover interference). On the basis of studies of crossover
frequency and distribution in the presence of a class of recombination-defective
meiotic mutants in Drosophila, it has been suggested that certain genes normally
function not only in the regulation of crossover frequency, but also in specifying
where crossovers may occur; normal alleles seem to promote nonrandomness of
distribution of crossovers with respect to the physical length of the chromosome
(for review see BAKERand HALL1976). It is recognized that while the latest
stage at which such genes might function in crossover-site determination may
be pachytene, it is not ruled out that they may indeed exert effects much earlier.
The idea that crossover interference may somehow be a function of the chromosome pairing process has, in fact, enjoyed a long history, possibly because of its
fundamental simplicity.
The distribution within meiotic tissue of cells of various crossover rank for a
given region may provide some information relevant to the problem of crossoversite determination. It is a common observation among cytogeneticists who have
examined large numbers of microsporocytes in smear preparation that cells with
Genetics 95: 143-157 May, 1980.
144
M. P. MAGUIRE
4
3
I
I
I
I
I
I
1
1
1
1
1
1
1
1
2
FIGURE
1.-Graphical representation of raw data from anther 1. Each bar of the histogram
represents a single section; the four locules are aligned by sections. Each square represents a
single cell. Within each locule, the lowest graph shows cells with no bridge or fragment, the
middle graph shows cells with a bridge and/or a fragment and the upper graph shows cells
with a double bridge and/or two fragments. Adjacent sections pooled in groups of four for
analysis are outlined with dotted lines.
cytologically recognized products of crossing over in specific chromosome regions
seem to be found close together in pairs or clusters (in spite of considerable
stirring of anther contents at the time of slide preparation). If such apparent
cell clusters reflect geographic clustering of similar cells within the anther, it
is of interest to know whether or not these cells are clonally related or share a
common physiological microclimate that is somehow conducive to a particular
type of crossover event. It would be expected, for example, that if sister cells
shared a common relevant experience from the previous cell generation, clustering would be very fine-grained. If a more distant clonal relationship or a
particular intercellular environment that affects a substantial portion of the
4
3
FIGURE2.-Graphical representation of raw data from anther 2. Explanation of plotting
given in legend to Figure 1.
anther were important, coarser clustering would be expected. REESand NAYLOR
( 1960) reported generalized chiasma frequency differences within quarteranthers of rye and suggested that these might be related to differences in
availability of nutrients.
Results of previous studies in maize have suggested that, within an anther,
clustering of cells of like crossover type in smear preparations may be statistically demonstrable at both intra- and inter-genic levels ( M ~ G U I R1970,1976).
E
Results of studies of serially sectioned anthers are reported here. It was found
that cells with four-strand double crossovers within a region heterozygous for
an inversion show an apparent tendency to be coarsely clustered.
MATERIALS A N D METHODS
Meiosis was studied in maize plants heterozygous for a paracentric inversion in the long
arm of chromosome 1. This inversion was originally designated 4305-25 and listed as a para-
146
NI. P. MAGUIRE
4
I
I
l
l
I
I
I
I
I
I
I
I
I
I
I
I
2
I
-----__
------
FIGURE3.-Graphical representation of raw data fro"
given i n legend to Figure 1.
anther 3. Explanation of plotting
centric inversion in the long arm of chromosome I (LONGLEY
1961). Breakpoints, as measured
in this laboratory, are at approximately 0.65 and 0.91 in the long arm of chromosome 1. Plants
were grown in a growth chamber, and microsporocyte samples were collected, fixed in ethanolacetic 3:l mixture and stored in a freczer pending further treatment and examination. From
such samples, using conventional techniques, anthers estimated to contain microsporocytes at
anaphase I through telophase I of meiosis were embedded i n paraffin, cross-sectioned at 25~1
thickness and the sections mounted on slides in serial order, one anther per slide. Slides were
then stained with Feulgen, mounted with Permount and examined with Zeiss Photomicroscope
bright field 1.3 N.A. optics. Six slides with relatively large numbers of cells at anaphase I and
telophase I were selected for detailed examination of cells within the locules of each anther. The
two adaxial (inner) locules (designated 1 and 2 here) are generally farther apart than the two
abaxial (outer) locules (designated 3 and 4 here). The distance between locules 1 and 2 is generally similar to that between locules 1 and 4 and between locules 2 and 3, and roughtly twice
that between locules 3 and 4 , l and 3 and 2 and 4.
Rccords were kept for each locule of each section of these slides as to number of cells per
147
C L U S T E R I N G O F CROSSOVER CELLS
-- -
-______
I
I
11-11
I
I
4
2
FIGURE
4.-Graphical representation of raw data from anther 4. Explanation of plotting
given in legend to Figure 1.
section at anaphase I or telophase I with respect to each of the following categories: no bridge
or fragment, single bridge and/or fragment and double bridge with two fragments. In practice,
it was found in these anthers that most cells were a t telophase I, with some cells at anaphase
I scattered among them. It was also found that bridges stained very faintly at telophase I (and
could have been missed i n some cases), while fragment presence remained unequivocal throughout telophase I (as reported by MCCLINTOCK
1938, i n studies with a different paracentric inversion). Thus, useful distinction could not be made between cells with a bridge and fragment
(expected usually to result from a single crossover within the inversion) and cells with a fragment only (expected to result from three-strand double crossovers within the inversion and
proximal to it). Also, all cells with 2 fragments were scored as double-bridge cells (expected
from four-strand double crossovers within the inversion), whether or not bridges were visible,
since the other most probable source of such cells should be rare as they arise from four-strand
double crossovers within the inversion plus an additional crossover in the region proximal to the
inversion of strands involved in each of the two crossovers within the inverson.
It should be recognized that sources of error include the occasional disappearance of a fragment because of its inclusion within a nucleus, the removal of a fragment and/or bridge by the
148
M. P. MAGUIRE
4
FIGURE
5.-Graphical representation of raw data from anther 5. Explanation of plotting
given i n legend to Figure 1.
passage of the knife at section cutting and possible failure to observe a bridge and/or fragment
in obliquely oriented cells. I t should also be noted that three-strand doubles within the inversion
are expected to produce a bridge and a fragment and are, therefore, indistinguishable from single
crossovers within the inversion. In the absence of chromatid interference, such doubles within
the inversion are expected to be twice as frequent as four-strand doubles, and two-strand doubles
within the inversion (which yield no bridge or fragment) are expected to occur with equal
frequency to four-strand doubles within the inversion. Evidence for absence of chromatid interference within a maize inversion has been reported by RHOADESand DEMPSEY
(1953). Additional
double crossover classes with 1 crossover within the inversion and 1 outside (either proximal
or distal) yield a bridgc and fragment and are indistinguishable from single crossovers within
the inversion. Higher multiples of crossovers are expected to be rare. Thus, only one-fourth of
the cells with double crossovers within the inversion may be scorable as such, half may appear
as singles within the inversion and other cells scored as singles within the inversion may, in
€act, represent other double-crossover classes. It is rasoned that error from these sources probably tends to contribute more to disorder than to order, so that any apparent clustering of cells
of like crossover types might be expected to be seen in spite of (rather than because of) such
experimental defects.
For simplicity, cells with a double bridge and/o,r 2 fragments are hereafter referred to as the
149
CLUSTERING O F CROSSOVER CELLS
I
I
I. I
I
h I
I
I
I
I
I
I
In1
I I
I
In1
I
I
FIGURE
6.-Graphical representation of raw data from anther 6. Explanation of plotting
given in legend to Figure 1.
double-crossover class, and cells with a single bridge and/or fragment are referred to as the
single crossover class.
Those cells that were divided between 2 sections by the cutting process were consistently
scored as occupying the upper section. Error from this procedure is not expected to contribute
bias to the results.
RESULTS
Complete raw data from the six anthers are presented graphically in Figures
1through 6. Where similarly scored cells occupied the same or adjacent sections,
the relative positions of such cells were examined. All conditions were found to
prevail, such that while similar cells sometimes occupied adjacent positions,
frequently they were moderately or distantly dispersed. There is no compelling
evidence that cells of similar type in fact tend to be restricted to sister cells.
Statistical tests were performed as indicated below to test for the presence of
clustering of cells, of either the single or the double crossover class.
Within each anther, within-locule data from each adjacent four sections were
150
M. P. M A G U I R E
TABLE 1
Number of cells of each category in four consecutive adjacent section segments i n
anther no. 1,after pooling for analysis as indicated in the text and in Figure I
Cells with
no bridge or
fragment
Cells with one
bridge and/or
fragment
2
6
1
0
2
0
1
2
0
0
2
3
1
0
0
1
1
0
2
0
1
3
0
0
1
0
1
1
1
0
3
1
0
5
7
5
4
6
6
5
4
7
6
6
8
4
3
5
7
4
2
9
8
7
9
5
8
10
8
9
9
5
Cells w i d a
double bndge
and/or two
fragments
Cells with
no bridge or
fragment
Cells with one
bridge and/or
fragment
Cells w i d a
double bndge
and/or two
fragments
0
5
1
1
0
3
6
0
0
0
0
0
0
0
0
1
0
0
0
1
0
0
0
0
0
0
0
7
6
6
8
9
5
6
5
10
8
0
10
7
7
0
0
0
7
4
2,
3
0
4
4
0
0
0
0
1
0
0
0
1
2
6
3
6
6
6
3
7
9
7
0
1
1
1
0
0
2
3
4
0
1
0
0
0
1
0
0
0
0
1
2
3
0
0
0
0
1
0
0
0
0
1
1
0
3
0
0
a
3
0
3
2
1
1
1
1
0
2
2
0
1
pooled, skipping cases (for a fresh start) where as many as two adjacent of the
four sections were devoid of cells. Data for each anther compiled in this manner
are presented in Tables 1 through 6. Total data for each anther (Table 7 ) were
tested for homogeneity among the six anthers. Since anthers were found not to
be heterogeneous for frequency of double-crossover cells (P> 0.50), the data
were pooled for all six anthers. The pooled data were then subjected to the variand COCHRAN
ance test for homogeneity of binominal distribution (SNEDECOR
1967), and the anther segments (composed of four adjacent sections) were found
to be heterogeneous ( P < O.Ol), strongly suggesting clustering of cells of the
double-crossover class.
Data for the six anthers with respect to the frequency of single crossover class
151
CLUSTERING O F CROSSOVER CELLS
TABLE 2
Number of cells of each category in four consecutive adjacent section segments in
anther no. 2, after pooling for analysis as indicated in the text and in Figure 2
Cells with
no bridge or
fragment
Cells with one
2
2
3
3
4
4
4
7
bridge and/or
fragment
10
(Y
7
7
2
1
3
2
3
2
0
4
8
4
9
5
5
6
7
6
7
9
7
2
2
1
1
2
0
1
8
8
9
6
3
2
1
8
2
3
3
3
1
1
Cells with a
double bndge
and/or two
fragments
Cells with
no bndge or
fragment
Cells with one
bridge and/or
fragment
3
6
6
5
3
6
3
0
2
2
4
2
0
7
0
0
6
6
1
2
0
2
0
0
0
0
0
0
0
0
0
0
0
0
0
1
0
8
6
10
8
3
5
6
6
1
2
1
0
0
0.
4
0
0
2
3
5
1
6
0
9
0
2
1
3
1
0
0
1
7
6
9
6
0
5
Cells with a
double bridge
and/or two
fragments
0
0
0
0
0
0
0
1
0
0
0
0
0
0
(Y
0
0
2
2
2
0
0
0
0
0
2
cells, however, were found to be heterogeneous. Therefore, for further tests of
this class, data from only those anthers not heterogeneous ( P > 0.90) were pooled
(anthers 2, 4 and 6 ) . These similar anthers were also not heterogeneous (P >
0.25) for the frequency of anaphase I cells (15%) uersus frequency of telophase
I cells and, thus, are presumed to have been fixed at similar stages. Similarity
in the frequency of single-crossover cells in these three anthers is, therefore,
thought to have resulted mainly from similar scoring capability (i.e., similar
frequencies of loss of a fragment into a nucleus and disappearance of a bridge
at telophase I). These scoring difficulties, for the most part, do not arise with
respect to double-crossover cells since fragments (which persist very well in any
case) are rarely included in a nucleus (for reasons to be discussed elsewhere).
Locule-segment (four adjacent sections) data for single crossover cells, pooled
for these three antlers, were found to be borderline for heterogeneity ( P 0.05).
In further tests of single-crossover cell frequencies of these three anthers, it was
found that when locule-segment size was increased to eight adjacent sections,
152
M. P. MAGUIRE
TABLE 3
Number of cells of each category in four consecutive adjacent section segments in
anther no. 3, after pooling for analysis as indicated in the text and in Figure 3
Cells with
no bridge or
fragment
Cells with one
bridge and/or
fragment
Cells wi+ a
double bndge
and/or two
fragments
3
1
0
4
4
1
2
3
1
3
2
1
9
2
2
2
2
2
3
2
2
2
1
3
28
1
0
0
1
2
0
1
3
4
0
0
2
2
3
5
7
2
7
6
3
0
3
4
3
8
0
0
0
0
1
1
0
Cells with a
double bridge
and/or two
fragments
Cells with
no bridge or
fragment
Cells with one
bridge and/or
fragment
8
9
6
9
6
6
1
0
0
3
3
0
0
0
3
5
0
0
0
0
0
0
1
4
6
3
2
7
4
2
2
6
9
9
e
4
0
1
1
2
4
3
2
1
2
1
0
0
0
0
0
0
0
0
segments were heterogeneous (P < 0.025), but when locule segment size was
further increased to 16 adjacent sections, segments were not heterogeneous
( P >> 0.05). Thus, there is evidence for a level of coarse clustering of cells of
the single-crossover class within locules. Data for double-crossover cells, pooled
for these three anthers, showed very significant heterogeneity ( P < 0.01) for
all three locule-segment sizes (four sections, eight sections and 16 sections).
Thus, evidence for coarse clustering of cells of the double-crossover class was
also demonstrated by these tests.
A number of tests were applied to probe whether occurrences of double- and
single-crossover cell clusters were related or independent. Rank difference correlation tests were performed on data from the three similar anthers for locule
segments of four- and eight-section size for single-crossover cell frequency
uersus that of double-crossover cells in segments with at least one cell of the
double-crossover class. Correlation coefficients were not significant: +0.05 and
-0.03, respectively ( P >> 0.05). Rank difference correlation tests were similarly performed on data from the three similar anthers f o r locule segments of
four- and eight-section size for frequency of noncrossover cells versus frequency
of single-crossover cells. Correlation coefficients were highly significant: -0.90
and -0.82 (P < 0.01). Similar tests for frequency of noncrossover cells versus
that of double-crossover cells (in segments with at least one double-crossover
.cell) gave a significant correlation coefficient for four-section segments (-0.43,
153
CLUSTERING OF CROSSOVER CELLS
TABLE 4
Number of cells of each category in four consecutive adjacent section segments in
anther no. 4, after pooling for analysis as indicated in the text and in Figure 4
Cells with
no bridge or
fragment
10
4
3
6
9
6
5
5
10
Cells with one
bridge and/or
fragment
Cells with a
double bridge
and/or two
fragments
Cells with
no bridge or
fragment
Cells with one
0
0
7
3
1
1
0
0
8
7
0
4
1
1
6
0
1
1
2
8
5
2
3
2
1
0
0
4
4
4
4
0
0
5
4
3
2
3
2
3
6
8
6
5
4
4
1
4
7
5
2
0
7
6
8
6
9
8
9
3
1
0
0
0
0
0
0
2
2
0
0
2
0
0
0
0
2
8
8
8
8
8
3
10
10
12
11
15
9
bridge and/or
fragment
4
4
4
1
2
3
3
1
2
Cells with a
double bridge
and/or two
fragments
0
0
0
0
1
0
1
0
1
0
0
0
0
0
0
0
0
0
1
0
0
0
< 0.05), but not for eight-section segments (-0.26, P >> 0.05). It should
be noted that the frequency of cells of the double-crossover class relative to that
of no-crossover cells is substantially smaller than the frequency of double-crossover relative to single-crossover cells, rendering any correlation more difficult
to detect in the former case. Thus, the evidence points to independence of the
distribution of single-crossover cells with respect to that of double-crossover cells,
and to an inverse relationship of each crossover class to the no-crossover class
of cell distribution.
P
DISCUSSION A N D CONCLUSIONS
A previous study (MAGUIRE
1976) of smear preparations, utilizing a different
inversion in the long arm of chromosome 1, provided evidence of clustering of
cells within anthers with single crossovers within the inversion and of cells with
three-strand double crossovers within and proximal to the inversion, but was
inconclusive with respect to cells with four-strand doubles within the inversion.
In the present study, statistical tests support the impression gained from direct
observation of the raw data that there is genuine clustering of cells (within
locules) with four-strand double crossovers within the inversion and that such
154
M. P. M A G U I R E
TABLE 5
Number of cells of each category in four consecutive adjacent section segments in
anther no. 5, after pooling for analysis as indicated in the text and in Figure 5
2
6
5
6
0
0
4
6
0
1
0
4
1
2
1
2
4
2
0
1
3
1
3
01
0
0
0
0
0
0
0
2
0
8
3
1
7
6
6
7
9
9
10
11
13
0
5
01
0'
1
4
11
7
2
2
2
1
2
3
2
3
2
3
1
2
1
0
0
2
0
1
2
1
1
3
8
8
0
0
0
0
4
0
2
0
3
0
4
5
8
4
5
6
5
e
3
7
7
9
8
7
1
1
4
6
0
8
2
0
8
Cells with a
double bridge
and/or two
Cells with one
bridge and/or
fragment
Cells with one
bridge and/or
fragment
2
8
8
9
10
6
6
Cells with a
double bridge
and/or two
fragments
Cells with
no bridge or
fragment
Cells with
no bridge or
fragment
0
0
1
0
0
1
01
0
0
0
0
0
0
____
7
fragments
1
0
0
0
0
0
0
0
0
0
0
0
0
0
0
0
clusters are coarse grained. Appearance suggests that rather large regions within
locules tend to be especially susceptible to the occurrence of such double crossovers. Data are inadequate to permit judgment as to whether such susceptibility
may extend across anthers to include adjacent portions of two or more locules
at a given level, but there seems to be no very striking evidence that this is so.
Statistical evidence for coarse-grained clustering of cells with a single bridge
and/or fragment was also found. But in the present study, this class of cells
includes cells with a single crossover within the inversion, cells with three-strand
doubles within and proximal to the inversion and, because of the relatively high
frequency of cells with four-strand doubles within the inversion (assuming no
chromatid interference), a substantial proportion of cells with three-strand
doubles within the inversion.
Evidence was also found for independence of distribution of cells with fourstrand doubles within the inversion as opposed to the other cells with detectable
crossing over within the inversion (these latter all scored as a composite singlecrossover class). This may be particularly surprising in view of the fact that
155
C L U S T E R I N G O F CROSSOVER CELLS
TABLE 6
Number of cells of euch category in four consecutive adjacent section segments in
anther no. 6, after pooling for analysis as indicated in the text and in Figure 6
Cells with
no bridge or
Cells with one
bridge and/or
7
7
1
1
0
0
0
3
2
fragment
6
8
7
4
8
6
Cells with a
double bndge
and/or two
fragments
fragment
0
0
0
0
0
2
0
I
6
7
1
1
8
6
7
6
3
3
3
5
4
4
6
6
5
4
8
Cells with one
bridge and/or
fragment
Cells with a
double bridge
and/or two
fragments
0
0
1
0
4
4
8
10
2
5
3
6
1
2
0
0
0
0
0
0
8
11
5
5
0
0
2
1
0
0
0
0
0
1
Cells with
no bndge or
fragment
3
3
5
7
4
9
5
0
2
2
0
0
0
0
5
4
4
2
0
0.
6
6
8
I
0
4
0
0
1
1
5
0
2
0
0
0
0
1
0
0
1
0
0
0
1
2
1
2
1
1
three-strand double crossing over within the inversion would be expected to be
twice as frequent as four-strand double crossing over within the inversion, with
the assumption of no chromatid interference within locule regions. In fact, within
regions of large apparent clusters of four-strand doubles, it appears probable that
not only must there be a deficiency of cells with three-strand doubles within the
inversion, but also a deficiency of cells with two-strand doubles within the inverTABLE 7
Total number of cells in each category in each anther
~
Anther no.
~
Cells with
no bridge
or fragment
3 72
313
177
308
322
257
Cells with
one bndge
and/or fragment
61
88
78
93
73
68
Cells with
a double bridge
and/or two fragments
20
12
10
14
9
9
156
NI. P. M A G U I R E
sion, for the total number of cells is generally less than or not markedly greater
than four times the number of cells with four-strand doubles. Examples or such
regional clusters can be seen in: Figure 1, locule 2 (a region with five cells with
four-strand doubles among 28 total cells) ;locule 4 (a region with four cells with
four-strand doubles among 25 total cells); Figure 2, locule 4 (a region with six
cells with four-strand doubles among 20 total cells) ;Figure 3, locule 1 (a region
with seven cells with four-strand doubles among 36 total cells) ; Figure 4, locule
1 (a region with eight cells with four-strand doubles among 30 total cells).
Thus, the very limited data within these arbitrarily selected regions seem to
hint that clusters of cells may involve specific crossover classes, i.e., four-strand
doubles within the inversion as opposed t o all classes of doubles within
the inversion, and not simply doubles, as opposed to singles, within the inversion. Early cytological evidence strongly suggested that relatively closely
located double chiasmata tended to be either two-strand doubles or four-strand
1935; HUSKINS
and NEWCOMBE
1941), with
doubles (HEARNEand HUSKINS
distinction between these two classes not possible (SYBENGA
1975). Chromatid
interference, in fact, favoring four-strand doubles within a region as short as
that bounded by the inversion breakpoints could give rise to the findings described
above. It is not unreasonable to suppose that the inversion in which RHOADES
and DEMPSEY
(1953) found no evidence for chromatid interference may encompass a substantially longer extent of the genetic map than the inversion studied
here.
If clustering arises as a result of events in a common ancestral cell, pertinent
relationship is probably not restricted to sister cells, but likely includes cells
removed from a common ancestor by two, three or even more cell generations.
Shared physiological conditions among the cells involved within a common
region of a locule might account for clustering, but if this is the case, it appears
that the conditions may foster crossing over of a specific rank and type within
a specific chromosome region. The results do not seem consistent with expectation from a generalized crossover-frequency increase in cells within some
regions of locules relative to others. A potential, probably localized, sensitivity
to environment of the crossover mechanism is illustrated by the report of KITANI
and WHITEHOUSE
[1974) that conversion patterns in Sordaria may be affected
by the relative proportions of nuclei of the two parental genotypes in the heterokaryon, with different effects on different alleles. The Question remains unanswered whether apparent regional effects on cells within meiotic tissues result
from events in an ancestral cell that tend to preset a resultant clone f o r specific
types of crossover events or from a common physiological environment of a
cluster of meiocytes. Both systems impose difficult constraints f o r interferencemodel builders, but the constraints imposed by the latter system seem particularly
severe at present.
The author is grateful to ELLENDEMPSEY
for supplying the seeds used. This work as supported by Grant GM-19582 from the Public Health Service.
C L U S T Z R I N G O F CROSSOVER CELLS
157
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Corresponding editor: R. L. PHILLIPS