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Three different patterns of desynapsis in maize microsporogenesis
Abstract
Cytogenetic features of three different types of desynapsis expression were observed in mate meiosis of some plants of four inbred maize lines. Moderate chromosome stickiness during diakinesis, presence of only univalents in most of the affected cells and irregular segregation of chromosomes in both divisions occurred in the first. In the second, most or all chromosomes were univalents at diakinesis, with irregular chromosome segregation in both divisions despite normal congression of univalents in some meiocytes, and chromatin stickiness and degeneration during the final stages of meiosis II. The third showed loss of sister-chromatid cohesion at prometaphase I, chromatin disintegration from meiosis I and irregular congression and distribution of chromatids during both meiosis. As a result of irregular chromosome segregation, many micronuclei were observed in the microspores of the three types of desynapsis, culminating in sterile pollen grains. The frequency of cells showing desynapsis varied among lines, plants and anthers.
Variable B chromosome desynapsis was observed in different maize plants. The present study was carried on with the objective of determining whether the frequencies of B chromosome desynapsis were variable not only among plants within populations, but also among flowers, anthers and anther locules within plants, from different parts of a tassel. Plants from different racial and geographic origin containing 2B chromosomes were analyzed. The suspected frequency variation was found not only among plants in three populations (e.g., from 0.39% to 29.53%, in Nayarit 39 of the race Reventador, 0.62% to 10.25%, in Jalisco 163 of the race Reventador, and 2.47% to 57.44% in Jalisco 148 of the race Tabloncillo, at diakinesis), but also among anthers within flowers in plants with an average low desynapsis frequency (e.g., 0% to 10.38% in Oaxaca 179 of the race Zapalote Chico) and in plants with a high average desynapsis frequency (e.g., from 32.90% to 58.60% in Jalisco 148 of the race Tabloncillo) and among anther locules within anthers in plants with a low desynapsis frequency (e.g., from 0% to 7.27% in Oaxaca 179 of the race Zapalote Chico) and in plants with high desynapsis frequency (e.g., from 46.28% to 64.04% in Jalisco 148 of the race Tabloncillo). In many cases the rates of variation within tassels showed statistical significant differences. Since different populations were planted in different years, the variation among plants could be the effect of environmental factors variation, but when the frequency variation within plants were found it was clear that the B chromosome desynapsis variation was due to genetic, rather than environmental causes. The data indicate that this desynapsis is B chromosome specific. It was tentatively proposed that desynapsis variation could be due to the action of transposable elements. A theoretical general model is proposed based on transposable elements acting upon genes controlling sister chromatid cohesion for explaining desynapsis frequency variation among plants within populations and among flowers, anthers and anther locules within plants. However, further data are needed that confirm this genetic explanation.
In order to determine the influence of soil acidity on the meiotic behavior of maize microsporocytes, materials not selected for low pH soils consisting of inbred lines, single and double-cross hybrids were cultivated on acid and corrected soils in the Brazilian Central Plateau and in the Southern Region of the country. Cytologic analysis revealed the occurrence of countless chromosome abnormalities, among them figures closely resembling a phenomenon previously described in the literature that affects both mitosis and meiosis. This abnormality is characterized by intense chromosome fragmentation. The phenomenon was spontaneous its phenotypic expression was very intense and its incidence was higher in inbred lines cultivated on acid soil. Possible effects of genotypic and environmental factors are suggested as the origin of this phenomenon.
A large number of maize genotypes are currently being evaluated to determine the effect of environmental stress caused by the aluminum found in cerrado soils on meiotic behavior. In the present study we report the occurrence of cell fusion followed or not by chromatin degeneration in meiocytes of some plants of an inbred line of maize grown on acid and corrected soil in the Brazilian central plateau. The results suggest the absence of any soil effect on the irregularities observed since the number of affected plants was higher among those grown on corrected soil. The possible causes of these irregularities and their influence on male sterility are discussed.
Analysis of the meiotic behavior of inbred lines, single-cross hybrids, double-cross hybrids and varieties belonging to two maize breeding companies revealed the presence of common abnormalities among the genotypes evaluated. We report here the spontaneous occurrence of syncyte formation, absence of cytokinesis and spindle irregularities in some genotypes and discuss the influence of these abnormalities on gamete formation.
The meiotic behaviour of 7 X-ray induced weakly fertile desynaptic mutants of Pisum sativum was studied with regard to the number of univalents and the number of microspores per pollen mother cell. The genotypes can be subdivided into two groups according to the degree of desynapsis. If we consider the high degree of meiotic irregularities in microsporogenesis, an extremely low seed production should be expected in the first group whereas the genotypes of the second group should be completely sterile. Both groups, however, produce essentially more seeds than expected. The dfindings demonstrate that the 7 ds-genes studied influence microsporogenesis much stronger than macrosporogenesis.
In most eukaryotes, homologous chromosomes undergo synapsis during the first meiotic prophase. A consequence of mutations that interfere with the fidelity or completeness of synapsis can be failure in the formation or maintenance of bivalents, resulting in univalent formation at diakinesis and production of unbalanced spores or gametes. Such mutations, termed desynaptic mutations, can result in complete or partial sterility. We have examined the effect of the maize desynaptic1-9101 mutation on synapsis, using the nuclear spread technique and electron microscopy to examine microsporocytes ranging from early pachytene until the diplotene stage of prophase I. Throughout the pachytene stage, there was an average of about 10 sites of lateral element divergence (indicating nonhomologous synapsis), and during middle and late pachytene, an average of two and three sites of foldback (intrachromosomal) synapsis, per mutant nucleus, respectively. By the diplotene stage, the number of sites of lateral element divergence had decreased to seven, and there was an average of one foldback synapsis site per nucleus. Lateral element divergence and foldback synapsis were not found in spread pachytene nuclei from normal plants. These results imply that the normal expression of the dsy1 gene is essential for the restriction of chromosome synapsis to homologues. The abundance of nonhomologous synapsis and the persistence of extended stretches of unsynapsed axial elements throughout the pachytene stage of dsy1–9101 meiocytes suggests that this mutation disrupts both the fidelity of homology search and the forward course of the synaptic process. This mutation may identify a maize mismatch repair gene. Dev. Genet. 21:146–159, 1997. © 1997 Wiley-Liss, Inc.
Analysis of microsporogenesis in the gms mutant in watermelon ( Citrullus lanatus , 2 n = 2 x = 22) showed that the cause of male sterility was desynapsis of the homologous chromosomes. The number of univalents in gms pollen mother cells (PMCs) at metaphase I ranged from 0 to 22, with a mean of 11.6. Male-fertile control plants averaged 11 bivalents per PMC, with univalents occurring infrequently. The chiasma frequencies per bivalent (1.4) and per PMC (15.7) were lower in the gms plants than in the male-fertile plants (2.0 chiasmata per bivalent and 21.6 chiasmata per PMC).
This chapter discusses the genetic control of meiosis. Meiosis presents a seemingly paradoxical situation in which universality and uniqueness are harmoniously combined. All organisms, irrespective of their evolved complexity, meiotically reduce the chromosome number on beginning sexual reproduction. Genetic recombination and the associated cytological phenomena—chromosome pairing and formation of the synaptonemal complex (sc) and chiasmata—all occur in meiotically dividing cells. The majority of genes do not turn the meiotic process entirely off; they rather interfere with its distinct steps. These comparisons of meiotic mutants make it possible to distinguish between primary and secondary abnormalities caused by mutations in different genes. Other meiotic mutants can serve as points plotted on a genetic flowchart depicting the sequential switching on of meiotic genes. Chromosome behavior appears to be controlled at two levels. There seems to exist a group of genes controlling the behavior of all the chromosomes in the nucleus and another group that controls the behavior of single chromosomes.
