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Corresponding author: Lorinda K. Anderson, Department of Biology, Colorado State University, Fort Collins, CO 80523., lorrie{at}lamar.colostate.edu (E-mail)
Communicating editor: R. S. HAWLEY
 | ABSTRACT |
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 TOP ABSTRACT MATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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Early recombination nodules (ENs) are protein complexes 
100 nm in diameter that are associated with forming synaptonemal complexes (SCs) during leptotene and zygotene of meiosis. Although their functions are not yet clear, ENs may have roles in synapsis and recombination. Here we report on the frequency and distribution of ENs in zygotene SC spreads from six plant species that include one lower vascular plant, two dicots, and three monocots. For each species, the number of ENs per unit length is higher for SC segments than for (asynapsed) axial elements (AEs). In addition, EN number is strongly correlated with SC segment length. There are statistically significant differences in EN frequencies on SCs between species, but these differences are not related to genome size, number of chromosomes, or phylogenetic class. There is no difference in the frequency of ENs per unit length of SC from early to late zygotene. The distribution of distances between adjacent ENs on SC segments is random for all six species, but ENs are found at synaptic forks more often than expected for a random distribution of ENs on SCs. From these observations, we conclude that in plants: (1) some ENs bind to AEs prior to synapsis, (2) most ENs bind to forming SCs at synaptic forks, and (3) ENs do not bind to already formed SCs.
DURING prophase I of meiosis, homologous chromosomes align, synapse, and cross over. Some or all of these events may be mediated by recombination nodules (RNs) that are multicomponent, proteinaceous ellipsoids that range from 50 to 200 nm in their longest dimension. RNs are found in association with axial elements (AEs) and synaptonemal complexes (SCs) from leptotene through pachytene (
While LNs are found at sites of crossing over along SCs during pachytene and probably represent the molecular factories that accomplish crossing over (e.g.,
In spite of the probable importance of ENs for synapsis and crossing over, there have been relatively few studies of ENs (
| MATERIALS AND METHODS |
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| TOPABSTRACTMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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Plants:
All plants used in the study were grown in a temperature-controlled (20°–25°) greenhouse. Data on ENs from A. cepa and C. betacea were obtained from one plant each, and data from L. esculentum (var. Cherry) were obtained from three plants. Data for P. nudum, T. edwardsiana, and L. longiforum were collected from plants in clonal populations that each represent essentially a single plant.
Spreading SCs:
The general procedure for spreading SCs was the same for all the species except L. longiflorum (see below). Details of the procedures used are described by
Microscopy, photography, and measurement:
Spreads of zygotene SCs were examined using an AEI 801 electron microscope (EM), and photographs were taken at magnifications ranging from x4000 to x10,000.
Zygotene SCs that were largely free from overlying chromatin, nucleolar remnants, and cellular debris and that had clearly visible ENs were selected for analysis. ENs were identified on the basis of their size, shape, staining characteristics, and association with SCs or AEs (
EM negatives were scanned at 300 dpi using an HP ScanJet 4c/T, and the digital images for each SC were assembled into a montage using Adobe Photoshop (version 5.0). The montage was then saved as a bitmap image. A working copy of each SC spread was printed and analyzed to determine the proper tracing of each bivalent and the location of each EN. ENs were identified according to the criteria of x32,000–50,000). The computer program MicroMeasure (
The frequency of ENs at synaptic forks was also determined. A "fork" was defined as an intersection between synapsis and asynapsis, i.e., the place where central element material ended and where the two axial elements could separate or come closer together because of the absence of transverse fibers and central elements of the SC. The central element was not well preserved in SC spreads from L. longiflorum, so we did not use its absence as a criterion for a fork in this species. In this case, paired lengths of AEs that were obviously parallel and separated by 100 nm were considered to be synapsed. Twists of SCs were not considered to be forks. Only ENs that were exactly at the change from synapsis and asynapsis were counted as being at a fork, so any fork in which the exact position could not be determined (for example, due to a twist in the lateral elements close to or at the fork) was excluded when analyzing EN frequency at forks.
Statistics:
The computer program Minitab (version 12.0) was used for most statistical tests. To evaluate whether ENs were randomly distributed along the length of SC segments, we measured the distances between adjacent ENs on uninterrupted SC segments. The distributions of distances between adjacent ENs on SC segments for different species were compared with predicted continuous (normal and gamma) distributions using the Kolmogorov-Smirnov one-sample goodness-of-fit test (
= mean ÷ ß).
| RESULTS |
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| TOPABSTRACTMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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Frequency of ENs per unit length of AEs and SCs during zygotene:
Examples of spreads of zygotene SCs with early nodules from each of the six plant species are presented in Fig 1. As noted before for plants (50 x 50 nm (L. esculentum) to a maximum of 250 x 290 nm (C. betacea). Most of the data used in this study were obtained from middle-to-late zygotene bivalents with 60–80% of their length synapsed (Table 1). However, because there was some breakage of axial elements in all species except tomato, the amount of synapsis per bivalent is probably somewhat overestimated. Presumably most of the synapsis was homologous since no partner trades and only a few short regions of foldback synapsis were observed. Because bivalent length and amount of asynapsis per bivalent varied, EN data were expressed as the number of ENs per micrometer of AE or per micrometer of SC. The number of ENs on a pair of AEs that had begun to synapse was determined by measuring the length of one AE but counting ENs on both (presumably) homologous AEs. The number of ENs per micrometer of SC (frequency) ranged from 0.38 for A. cepa to 1.61 for L. longiflorum, while the number of ENs per micrometer of AE ranged from 0.06 for A. cepa to 0.58 for L. longiflorum and T. edwardsiana (Table 1). Overall, ENs are 2.5–7.5 times more numerous per unit length for SC compared to AE. Because the low frequency of ENs associated with AE could be caused by using mainly middle-to-late zygotene bivalents in which heterochromatic segments (that synapse late and have few ENs) may be overrepresented among remaining AEs, we also determined the frequency of ENs associated with AE for bivalents with <50% synapsis. In this case, the frequency of ENs per micrometer of AE went up for two species, L. esculentum (0.22–0.27) and P. nudum (0.14–0.19), but there were still at least 5 times more ENs associated with SC than with AE for both species.
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Relationship between the number of ENs and SC segment length:
The numbers of ENs per SC segment length are plotted for each species in Fig 2, and the summary of the regression equations is presented in Table 2. For each species, there is a strong linear relationship between EN number and SC segment length. The intercept of each regression line is not significantly different from zero (with the exception of P. nudum), and the slope of each regression line is positive and significantly different from zero. The slopes of the regression lines range from 0.38 (A. cepa) to 1.50 (L. longiflorum). These numbers are similar but slightly lower than the frequencies of ENs per micrometer of SC calculated in Table 1. The differences between the slopes are significant (P < 0.001;
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Relationship between the progress of synapsis and the frequency of ENs:
To determine if there is a difference in the number of ENs on SC segments that form early in zygotene compared to SC segments that form late in zygotene, we examined the relationship between the frequency of ENs on SC segments and the percentage of the bivalent length that is synapsed. We assume that bivalents that are earlier in zygotene have a smaller fraction of their length synapsed. The primary analysis was limited to L. esculentum in which a bivalent could be verified to be intact by the presence of telomeres at both ends (
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Frequency of ENs at synaptic forks:
A casual examination of zygotene SCs and ENs suggests that ENs are located at synaptic forks more often than would be expected if ENs occur at random along formed SC segments. To investigate this possibility, we examined a total of 140 synaptic forks among the six species. We did not attempt to distinguish whether forks were present in euchromatic or heterochromatic regions. We found that 22–50% of the forks had an EN (Table 3). Assuming that an EN occupies 0.1 µm of SC, we calculated the number of ENs per micrometer of SC at forks and compared that to the observed frequency of ENs along SCs for each species. This comparison shows that ENs are 1.6–12.2 times more common at synaptic forks than along zygotene SCs in general.
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Spacing between adjacent ENs:
To determine if there is a pattern in the spacing of ENs along SCs, we measured the distance between adjacent ENs for each species. Because the frequency of ENs is low on AEs, we considered only the distances between adjacent ENs on the same synapsed segments. Thus, distances between two ENs on adjacent synapsed and asynapsed segments, distances between adjacent ENs on two SC segments that were separated by an asynapsed segment, and distances between ENs on asynapsed segments were not included in this analysis.
As expected, species with higher frequencies of ENs per micrometer of SC have lower average distances between adjacent nodules, and species with a lower frequency of ENs per micrometer of SC have longer average distances between adjacent ENs (Table 1 and Table 4). The minimum distance between two ENs is 0.1 µm for all six species, but the maximum distance between two ENs varies greatly depending on the species. L. longiflorum has the smallest maximum value between two adjacent ENs (3 µm), and A. cepa has the largest maximum value (18 µm). The distribution of distances between ENs is presented in a histogram (Fig 4). For each species, the distribution is skewed to the left. Statistical tests confirm that the distributions are not normal (Anderson-Darling normality test, P < 0.001 for each species). Therefore we compared the values for the different species using the Mood median test that does not require normal distributions (Table 4). The species fall into three statistically different (P < 0.001) categories with regard to median distance between adjacent ENs: (1) A. cepa (median = 1.89), (2) C. betacea and P. nudum (medians = 1.08 and 0.88, respectively), and (3) L. longiflorum, L. esculentum, and T. edwardsiana (medians = 0.46, 0.49, and 0.48, respectively).
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Using parameters taken from the observed distributions, the predicted normal and gamma distributions for each species have been plotted for comparison (Fig 4). Visually, gamma distributions fit the observed distributions much better than normal distributions. These results were confirmed by using the Kolmogorov-Smirnov one-sample goodness-of-fit test (Table 4; = 0.05, it is likely that the distribution of distances between ENs for T. edwardsiana is also gamma. In contrast, the distribution of distances between ENs for L. esculentum is significantly different from a gamma distribution. However, when we consider only SC segments in euchromatin by limiting the data to bivalents in which SC segments comprised 50% or less of the total bivalent length, then the distribution of distances between adjacent ENs is not significantly different from a gamma distribution. Therefore, for each of the six plant species, the observed distributions of distances between ENs are not significantly different from the predicted gamma distributions. We were not able to detect a recurrent distance (or a multiple of a recurrent distance) between adjacent ENs that would imply ENs are laid down in a regular, repeated pattern.
| DISCUSSION |
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| TOPABSTRACTMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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The frequency of ENs is higher on SC segments compared to axial element segments:
The frequency of ENs associated with SCs ranged from 0.38 to 1.61 ENs/µm of SC for the six plant species (Table 1). These numbers are comparable to those reported by
What could account for the lower frequency of ENs on AEs compared to SC segments for each species? One possibility is that the frequency is artificially low due to using middle-to-late zygotene bivalents in which a significant proportion of the remaining asynapsed AEs may be located in heterochromatic regions that typically synapse late and have few ENs (e.g., 2000 foci per leptotene nucleus—our calculated number derived from their observations). Assuming that these nuclei have no SC [see comments by 0.33 foci/ µm of AE (2000 foci/6000 µm AE). In comparison, we found a frequency of 0.58 ENs/µm AE at zygotene for L. longiflorum. Considering the assumptions required to estimate the Rad51p foci frequencies, the probability that two closely adjacent ENs would appear as one fluorescent focus (
SC segment length is an excellent predictor of EN number:
We observed a strong linear relationship (r2 = 0.81–0.95) between EN number and SC segment length for each species (Fig 2 and Table 2), although there were statistically significant differences between the slopes of the regression lines for the different species. Other investigators have also noted a positive linear relationship between EN number and SC length (human,
The frequency of ENs per unit length of zygotene SC varies between plant species:
We observed up to a fourfold difference in the frequency of ENs per micrometer of SC segment among these six plant species (Table 1 and Table 2), and these differences are reflected in the average distance between adjacent ENs on SC segments (Table 4). There is no obvious pattern of EN frequency with regard to phylogenetic class, genome size, or chromosome number. For example, species with higher frequencies of ENs on SCs (>1 EN/µm SC) include the lower vascular plant P. nudum (2n 
200 and a large genome; S. M. STACK, unpublished observations), the dicot L. esculentum (2n = 24; 4C = 4 pg), and two monocots, L. longiflorum (2n = 24; 4C = 141 pg) and T. edwardsiana (2n = 12; 4C = 120 pg). The two species with lower frequencies of ENs on SCs (<1 EN/µm SC) include the monocot A. cepa (2n = 16; 4C = 67 pg) and the dicot C. betacea (2n = 24; 4C = 30 pg; DNA contents for all species except P. nudum are from
Plant ENs attach to AE and forming SC, but not to formed SC:
Because ENs are identifiable as discrete structures only by electron microscopy, we often refer to them as if they were preformed complexes that attach to AEs and SC. However, it is more likely that ENs are progressively assembled, probably at sites of DNA double-strand breaks (DSBs). DSBs are required to form Rad51p foci (and probably ENs;
There are three possible times/locations at which ENs could associate with zygotene bivalents during synapsis: (1) with AEs prior to synapsis, (2) with SC after synapsis, and/or (3) at synaptic forks during synapsis. In regard to the first possibility, we and others (e.g., 0.11–0.33 convergences/µm of SC (see references in
Do ENs bind to already formed SC during zygotene?
An alternative explanation for the lower frequency on ENs on AEs compared to SCs is that ENs bind to SCs at synaptic forks. Here we define a synaptic fork as the interface between synapsis (tripartite SC) and asynapsis (two separated axial elements). 7–77) and also higher than along SC segments (by a factor of 2–12). These results indicate that ENs bind to SCs at synaptic forks. However, if ENs assemble at forks without otherwise interfering with the progress of synapsis, one would expect the frequency of ENs at forks to be the same as the frequency of ENs along SC in general. Since this is not the case, synapsis may be delayed temporarily at forks while ENs are assembled. Then it is likely that synapsis would resume and progress until delayed again as another EN assembles, and so on. In this scenario, ENs that bind at synaptic forks would not be necessary to nucleate SC formation. However, this interpretation does not preclude the possibility that ENs at convergence sites are important for synaptic initiation.
The distribution of distances between adjacent ENs on SC segments is random:
The continuous distribution of distances between adjacent ENs for each plant species is presented in histogram form in Fig 4. Each distribution is skewed to the left, and the extent of the shift is related to the different frequencies of ENs per micrometer of SC observed for the different plant species (Table 1 and Table 4). While most adjacent ENs are <1 µm apart (except for A. cepa), a few adjacent ENs are separated by 3–18 µm. The longer distances between adjacent ENs may be due to SC in heterochromatic regions that have few ENs.
Two curves have been fitted to each of the observed distributions in Fig 4, using parameters derived from the data. One curve is a normal distribution based on the mean and standard deviation, and the other curve is a gamma distribution based on and ß parameters. Both normal and gamma distributions are random distributions for continuous variables, but a gamma distribution differs from a normal distribution in that there can be only positive numbers. This means that normal and gamma distributions will look quite different when means are close to zero, but as means become larger, gamma distributions will look more and more like normal distributions. This is similar to the behavior of Poisson distributions that are used for discrete variables. The constraint of only positive values for gamma distributions is expected when measuring distances between two adjacent ENs since this measurement will always yield a positive number. In addition, there is another constraint on the measurement of internodule distances because the minimum measurable distance between two nodules is limited to the center-to-center distance between two touching ENs. This physical limitation in measuring the distance between adjacent nodules accounts for the scarcity of measured distances 
0.1 µm since only a few nodules are smaller than 0.1 µm in size and very few of those are touching (Fig 4). For each species, the predicted gamma distribution fits the data better than the predicted normal distribution. This result is supported by Kolmogorov-Smirnov one-sample goodness-of-fit statistical tests that show that the distribution of distances between ENs in euchromatin is random and best fits a gamma distribution for each plant species. Although we occasionally observed several adjacent ENs (up to five in one case) that appeared to be evenly spaced, we were unable to detect a recurrent separation distance (or multiple of a recurrent distance) between adjacent ENs in any of the six plant species. Therefore, we conclude that in plants, ENs are randomly spaced along SC segments with respect to one another.
The general appearance of the internodule distance distributions for each plant is similar to those of Coprinus, Bombyx, and humans, as shown by RASMUSSEN and HOLM (1978), HOLM and RASMUSSEN (1980, 1983), and
Relation of ENs to LNs:
Observations that ENs are randomly distributed in euchromatin do not necessarily imply that crossovers are randomly distributed. Indeed, hot spots for recombination are well documented in a number of different organisms (
Model for the distribution of early nodules:
Our results suggest the following model for the frequency and distribution of ENs in plants. Many (perhaps all) ENs associated with AEs serve to link axial elements together at convergence sites where SC formation begins. Assuming that these ENs remain after SCs form, they represent only a minority (10–40%) of the ENs that ultimately will be associated with SCs. The majority (60–90%) of ENs associated with SC are added at synaptic forks. The higher frequency of ENs at synaptic forks is most likely due to a delay in the progress of synapsis while ENs assemble. As synapsis progresses, ENs bind randomly at forks over time so that the distribution of spacing between ENs along SCs is described by a gamma distribution. Thus, beginning at synaptic initiation sites, ENs along a segment of SC represent consecutive events in time. In the context of this model, we suggest two different possibilities for EN composition and behavior: There are two types of ENs, one that initially associates with AEs and another that associates with synaptic forks of SCs. This difference in behavior may be based on a difference in composition and function; e.g., the former might function in synaptic initiation while the latter might function in recombination. Alternatively, all ENs begin with the same basic molecular composition, but ENs progressively change over time. This means that ENs along a segment of SC would represent a developmental hierarchy with the more mature nodules lying closer to synaptic initiation sites and the less mature ENs lying closer to synaptic forks. A more mature EN is more likely to achieve a crossover and become a late nodule than a less mature EN. Once a crossover has been achieved, other nearby ENs would not be able to achieve a crossover due to interference, and these ENs would be lost from the SC en mass (
| ACKNOWLEDGMENTS |
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We thank Jonathan Holland and James zumBrunnen from the Statistics Department at Colorado State University for their assistance with the statistical analysis. We also thank Terry Ashley and Maria Pigozzi for their comments on the manuscript. This work was supported by the National Science Foundation (MCB-9728673) including an REU supplement for K.H.
Manuscript received March 5, 2001; Accepted for publication August 16, 2001.
| LITERATURE CITED |
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| TOPABSTRACTMATERIALS AND METHODSRESULTSDISCUSSIONLITERATURE CITED |
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