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First published online 15 August 2006
doi: 10.1242/jcs.03095

Journal of Cell Science 119, 3655-3663 (2006)
Published by The Company of Biologists 2006
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Paternal chromosome segregation during the first mitotic division determines Wolbachia-induced cytoplasmic incompatibility phenotype

Uyen Tram1,2,*, Kurt Fredrick2, John H. Werren3 and William Sullivan1

1 University of California, Santa Cruz, Molecular, Cellular, and Developmental Biology, 319 Sinsheimer Laboratories, Santa Cruz, CA 95064, USA
2 The Ohio State University, Department of Microbiology, 484 W. 12th Avenue, Columbus, OH 43210, USA
3 University of Rochester, Department of Biology, Rochester, NY 14627, USA


Figure 1
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  		Fig. 1. CI in N. vitripennis. (A) Category 1. In 5% of N. vitripennis CI embryos, chromosome segregation is normal, indicating that the egg was unfertilized. (B,C) Category 2. In 26% of N. vitripennis CI embryos, the paternal genome is not segregated. (B) Nuclear cycle 2, there are two normal nuclei and one highly condensed nucleus (arrow). (C) Nuclear cycle 3, there are four normal nuclei and one highly condensed nucleus (arrow). (D-F) Category 3. In 48% of N. vitripennis CI embryos, the paternal genome segregated to one daughter nucleus at the end of nuclear cycle 1. (D) Nuclear cycle 1, one nucleus is normal whereas the other appears to be a composite of two nuclei (arrowhead). (E) Nuclear cycle 2, two normal nuclei are present and the composite nucleus attempts to divide (arrowhead). (F) Nuclear cycle 2, two normal nuclei are present and the composite nucleus divides to give one normal-looking nucleus (bottom of bracket), one misshapen nucleus (top of bracket), and one highly condensed nucleus (middle of bracket). (G,H) Category 4. In 22% of N. vitripennis CI embryos, the paternal genome is mis-segregated to both daughter nuclei. (G) Nuclear cycle 2, a chromatin bridge connects the two daughter nuclei. (H) Nuclear cycle 3, all four nuclei are misshapen and of different sizes. (I) Nuclear cycle 3 uninfected control embryo, all nuclei are of uniform size and shape. (J) Nuclear cycle 12 CI embryo; 78% of CI embryos reach at least the syncytial blastoderm stage. (K) CI embryo in which development has arrested; 22% arrested with a few, highly condensed nuclei. Bars, 8 µm (A-I).

 

Figure 2
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  		Fig. 2. CI in N. giraulti. (A) Category 1. Nuclear cycle 2 embryo in which chromosomes were segregated correctly. (B) Category 2. Nuclear cycle 2 embryo in which the paternal genome was not segregated. There are two normal nuclei and one highly condensed nucleus (arrow). (C) Category 3. Nuclear cycle 2 embryo in which the paternal genome had segregated to one daughter nuclear at the end of the previous cycle. There are two normal nuclei and one composite nucleus (arrowhead). (D-F) Category 4. In 83% of giraulti CI embryos, the paternal genome mis-segregates to both daughter nuclei. (D) Nuclear cycle 2, the two nuclei are connected by a chromatin bridge. (E) Nuclear cycle 3, all four nuclear products are connected by chromatin bridges. (F) Several embryos contained one massive nucleus composed of diffuse DNA. (G) Control uninfected embryo at nuclear cycle 9, note nuclei are evenly spaced from each other. (H) The majority of CI embryos arrest development with a few highly condensed nuclei. (I) A few CI embryos reach the syncytial blastoderm stage but notice nuclei are not evenly spaced from neighbors and chromosome fragments are present. Bars, 8 µm (A-F).

 

Figure 3
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  		Fig. 3. CI in N. longicornis. (A) Category 1. In 13% of N. longicornis CI embryos, normal segregation is observed. (B) Category 2. In 2% of N. longicornis CI embryos, the paternal genome is not segregated (arrow). (C,D) Category 3. In 21% of N. longicornis CI embryos, the paternal genome segregates to one daughter. (C) Nuclear cycle 2, one normal nucleus and one composite nucleus (arrowhead). (D) Nuclear cycle 3, two normal nuclei and one composite nucleus (arrowhead) that attempts mitosis. (E-G) Category 4. In 65% of N. longicornis CI embryos, the paternal genome mis-segregates to both daughter nuclei. (E) Nuclear cycle 2, the nuclei are tear-shaped indicating aneuploidy. (F) Nuclear cycle 3, all four nuclei are connected by chromatin bridges. (G) The embryo is composed of a single, diffuse mass of DNA. (H,I) Control uninfected embryos. (H) Nuclear cycle 3, all nuclear are uniform in size and shape. (I) A small number of control embryos contain an odd number of nuclei. Bars, 8 µm.

 

Figure 4
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  		Fig. 4. Model of how Wolbachia exploits the unique structure of the gonomeric spindle to produce both embryonic mortality and conversion to haploid male development in Nasonia. In control embryos, the maternal (red) and paternal (blue) genomes align in separate regions of the metaphase plate. Both sets of chromosomes are segregated equally to produce two diploid nuclei, where the maternal and paternal genomes mingle for the first time. In CI embryos, the paternal genome is somehow modified by Wolbachia and this causes its segregation at anaphase to be aberrant. One explanation for the range in segregation behavior of the paternal genome is that the level of Wolbachia modification varies from high to low. When Wolbachia modification is high, the paternal genome is not segregated and two haploid nuclei of maternal origin (two red nuclei) are produced (category 2). These embryos develop into males. When Wolbachia modification is moderate to low, the paternal genome is segregated abnormally. The paternal genome is either wholly segregated to one side of the spindle (category 3), producing one haploid nucleus of maternal origin (red nucleus) and one abnormal nucleus of maternal and paternal origin (red-blue nucleus); or the paternal genome is unequally segregated to both daughter nuclei (category 4), producing two nuclei that contain the maternal genome and unequal quantities of the paternal genome. Often the resulting nuclei are connected by chromatin bridges. Category 3 embryos continue development into a haploid male whereas category 4 embryos arrest development in early embryogenesis.

 

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