Chapter 7 : Meiosis

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This chapter discusses the hallmarks of meiosis, crossover (chiasma) distribution, genes necessary for meiosis, and the transcriptional program of meiosis, with a focus on recent studies. A recent review, as a model fungus for studies in cytogenetics and sexual biology at Stanford, is highly recommended as a complement to this chapter. Filamentous fungi display the interesting characteristic of maintaining haploid nuclei throughout mycelial development until nuclear fusion (karyogamy), which begins meiosis. Filamentous fungi have several advantages for the study of meiosis. First, the meiotic program and chromosome behavior in filamentous fungi are similar to those of more complex organisms. The genetic and cytological tractability of fungal systems allows genes to be well characterized, shedding light on the functions of conserved proteins. Second, unique aspects of development in filamentous fungi provide ideal conditions for analysis of certain meiotic events. Third, the chromosomes of some filamentous fungi are particularly accessible for meiotic study, within intact cells or by surface spreads of meiotic nuclei. Studies of mutants in filamentous fungi have made substantial contributions to the analysis of the two core features of meiosis: the structure of meiotic chromosomes and the role of interhomolog crossovers in meiotic chromosome structure and behavior. Regulation of meiosis at the epigenetic level, manipulation of recombination hot spots, and targeted disruption of cohesion complex components are also exciting targets for future analyses of the meiotic process in filamentous fungi.

Citation: Burns C, Pukkila P, Zolan M. 2010. Meiosis, p 81-95. In Borkovich K, Ebbole D (ed), Cellular and Molecular Biology of Filamentous Fungi. ASM Press, Washington, DC. doi: 10.1128/9781555816636.ch7
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Image of FIGURE 1

Progression and timing of meiosis in . Meiosis in is synchronous and begins directly after karyogamy (K). Homologs pair, condense, and synapse, and all meiotic cells are in pachytene 6 h postkaryogamy. After a further 2 to 3 h, homologs separate in the first meiotic division. Twelve hours after karyogamy, the second division has occurred, resulting in four meiotic products. Six hours subsequently, nuclei have migrated into basidiopores. Reproduced from the ( ), with the permission of the publisher.

Citation: Burns C, Pukkila P, Zolan M. 2010. Meiosis, p 81-95. In Borkovich K, Ebbole D (ed), Cellular and Molecular Biology of Filamentous Fungi. ASM Press, Washington, DC. doi: 10.1128/9781555816636.ch7
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Image of FIGURE 2

Electron microscopy of SC formation in . (A) At karyogamy, haploid nuclei fuse, and chromosomes are relatively uncondensed. Two nucleoli (dark structures indicated by an arrow) are apparent. (B) During leptotene, chromosomes condense and homologs start to pair. (C) During zygotene, chromosomes condense further and are paired along their length (note the pair in the upper right-hand corner of the image). The SC begins to form (arrow). (D) In pachytene, chromosomes are fully condensed, and homolog pairs are fully synapsed along their lengths. Scale bar, 1 μm. Reproduced from ( ), with the permission of the publisher.

Citation: Burns C, Pukkila P, Zolan M. 2010. Meiosis, p 81-95. In Borkovich K, Ebbole D (ed), Cellular and Molecular Biology of Filamentous Fungi. ASM Press, Washington, DC. doi: 10.1128/9781555816636.ch7
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Image of FIGURE 3

Formation of a crossover and its role in meiotic segregation. (A) The arrangement of sister chromatids and homologs, shown end-on. Sister chromatids (one pair in black and one pair in gray) are held together with cohesin (black ring). Homolog association is stabilized in many organisms by the SC (dark gray). This arrangement allows a sister from one homolog to interact with either sister from the second homolog. (B) Initiation of recombination. Spo11, a conserved protein, makes a DNA double-strand break, which is then resected in the 5’-to-3’ direction (C). To simplify, only one chromatid from each homolog is shown. Note that in panels B through I, both DNA strands are shown for the two chromatids. In panels J through M, all four chromatids are shown, each of which have two DNA strands (not shown), constituting eight strands in a pair of homologs. (D) The single strand invades a nonsister duplex, displacing a loop. The invading strand extends by replication, using the opposing duplex as template. The displaced loop may or may not be captured by the second single strand. If not captured, the invading strand and loop retract, and no crossover results. If captured, the second single strand expands, using the loop as a template (E). The invading strand is recaptured by the original sister, forming a double Holliday junction (F), which can then migrate (F and G). To resolve the junction, the DNA is nicked as shown by the arrows (G and H), forming a crossover (I). Note that the ends of the chromatids have exchanged, as represented by the different colors; this is a single crossover. (J) Crossovers are represented at the chromosomal level. Sister chromatids within homologs are shown, and chromosomes are compacted at this stage. Two crossovers are shown, as is typical in . Although the two crossovers are illustrated here as formed between the same chromatids, note that, due to the orientation illustrated in panel A, crossovers can and do form with either chromatid of the opposing homolog. Sister chromatids are held together by cohesin (rings), and this, combined with the crossover, is what holds homologs together while under tension at kinetochores. (K) Upon release of arm, but not centromere-associated, cohesin, homologs immediately begin to separate; this is the first meiotic division. For the second meiotic division, centromeric cohesin is released, allowing sister separation (L) and formation of the four meiotic products (M).

Citation: Burns C, Pukkila P, Zolan M. 2010. Meiosis, p 81-95. In Borkovich K, Ebbole D (ed), Cellular and Molecular Biology of Filamentous Fungi. ASM Press, Washington, DC. doi: 10.1128/9781555816636.ch7
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Image of FIGURE 4

Variation in number of chiasmata per bivalent in fungi. (A) Meiotic bivalent from with 12 chiasmata diagrammed in prophase (left) and metaphase (right). (B) Meiotic bivalent from with two chiasmata diagrammed in prophase (left) and metaphase (right). Each chiasma results from a reciprocal exchange involving one chromatid from each homolog.

Citation: Burns C, Pukkila P, Zolan M. 2010. Meiosis, p 81-95. In Borkovich K, Ebbole D (ed), Cellular and Molecular Biology of Filamentous Fungi. ASM Press, Washington, DC. doi: 10.1128/9781555816636.ch7
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Image of FIGURE 5

Time course of Rad51 association with meiotic chromosomes. Chromosome spreads were stained with DAPI (4’,6-diamino-2-phenylindole) (top panels) and antibody against Rad51 (bottom panel), which was detected using fluorescein isothiocyanate-labeled antirabbit antibody. (A) Preleptotene image taken 1 h after karyogamy (K + 1). (B) Leptotene image taken at K + 2. (C) Zygotene image taken at K + 4. (D) Pachytene image taken at K + 6. (E) Diplotene image taken at K + 8. Arrows in panel E show ribosomal DNA, which does not synapse, within the nucleolus. Scale bars represent 2 μm for all images. All panels except panel A are reproduced from ( ), with the permission of the publisher.

Citation: Burns C, Pukkila P, Zolan M. 2010. Meiosis, p 81-95. In Borkovich K, Ebbole D (ed), Cellular and Molecular Biology of Filamentous Fungi. ASM Press, Washington, DC. doi: 10.1128/9781555816636.ch7
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Image of FIGURE 6

The mutation suppressed synapsis defects of . Surface spreads of meiotic chromosomes were stained with silver nitrate and photographed using transmission electron microscopy. (A) ; (B) ; (C) double mutant. Scale bars represent 2 μm for all images. All images are reproduced from ), with the permission of the publisher.

Citation: Burns C, Pukkila P, Zolan M. 2010. Meiosis, p 81-95. In Borkovich K, Ebbole D (ed), Cellular and Molecular Biology of Filamentous Fungi. ASM Press, Washington, DC. doi: 10.1128/9781555816636.ch7
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Some core meiotic genes and their functions and conservation among fungi

Citation: Burns C, Pukkila P, Zolan M. 2010. Meiosis, p 81-95. In Borkovich K, Ebbole D (ed), Cellular and Molecular Biology of Filamentous Fungi. ASM Press, Washington, DC. doi: 10.1128/9781555816636.ch7

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