A defect in synapsis causes male sterility in a T‐DNA‐tagged Arabidopsis thaliana mutant

Abstract

Fluorescence microscopy was used to study meiosis in microsporocytes from wild-type Arabidopsis thaliana and a T-DNA-tagged meiotic mutant. Techniques for visualizing chromosomes and beta-tubulin in other plant species were evaluated and modified in order to develop a method for analyzing meiosis in A. thaliana anthers. Like most dicots, A. thaliana microsporocytes undergo simultaneous cytokinesis in which both meiotic divisions are completed prior to cytokinesis. However, two unique events were observed in wild-type A. thaliana that have not been reported in other angiosperms: (1) polarization of the microsporocyte cytoskeleton during prophase I prior to nuclear envelope breakdown, and (2) extensive depolymerization of microtubules just prior to metaphase II. The first observation could have implications regarding a previously uncharacterized mechanism for determining the axis of the metaphase I spindle during microsporogenesis. The second observation is peculiar since microtubules are known to be involved in chromosome alignment in other species; possible explanations will be discussed. A T-DNA-tagged meiotic mutant of A. thaliana (syn1), which had previously been shown to produce abnormal microspores with variable DNA content, was also cytologically characterized. The first observable defect occurs in microsporocytes at telophase I, where some chromosomes are scattered throughout the cytoplasm, usually attached to stray microtubules. Subsequent development stages are affected, leading to complete male sterility. Based on similarities to synaptic mutants that have been described in other species, it is suggested that this mutant is defective in synaptonemal complex formation and/or cohesion between sister chromatids.

Random Chromosome Segregation without Meiotic Arrest in Both Male and Female Meiocytes of a dmc1 Mutant of Arabidopsis

“…Sometimes one or more univalents seemed to lag in the middle, whereas others migrated to opposite poles of the cell, which can result in up to three discernible groups of univalents. These so-called laggards have been observed in other meiotic Arabidopsis mutants (e.g., syn1, Peirson et al, 1997;dsy1, Ross et al, 1997).…”

“…That the same meiotic defect affects both male and female sporogenesis in dmc1 plants supports the hypothesis that DMC1 possesses a central and fundamental function in plant meiosis, as was previously shown for the yeast (Bishop et al, 1992) and mouse (Pittman et al, 1998;Yoshida et al, 1998) homologs. Other mutations that might disturb general meiotic function have been described in Arabidopsis that are both male and female partial sterile, but female meiosis was not cytologically examined (Peirson et al, 1997;Ross et al, 1997). Furthermore, none of the genes responsible for these sterility phenotypes has been molecularly characterized.…”

“…Our observations may highlight some aspects of meiosis that are unique to Arabidopsis or plants in general. Meiosis completion is not specific to the Arabidopsis dmc1 mutant; other aberrant meioses have been described for plant mutants, and they all seem to go through meiosis without arresting (Neuffer et al, 1997;Peirson et al, 1997;Ross et al, 1997).…”

“…At this time, chromosomes reorganize into four groups of five chromosomes and start to decondense during diakinesis, while four independent cells reconstitute. In pollen mother cells, the second division is perpendicular to the first, thus resulting in four meiotic products set at the four poles of the cell that will turn into a tetrad (see Figure 4C; Ross et al, 1996;Peirson et al, 1997). On the other hand, in megaspore mother cells, the second division may be parallel or perpendicular to the first, result- ing in tetrads with a linear or a planar array of megaspores .…”

Functional conservation of the meiotic genes SDS and RCK in male meiosis in the monocot rice

“…Similarly, knock down of rice DMC1 leads to defects in bivalent formation and subsequent unequal chromosome segregation [44]. In Arabidopsis, sister chromatid cohesion is abnormal and chromosome condensation is also affected in the syn1 mutant, and meiocytes of the mutant produce chromosomal fragments [64,65]. The male meiocytes in OsRAD21-4-deficient lines showed overcondensation of chromosomes, precocious segregation of homologs and chromosome fragmentation.…”