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ASK1, a SKP1 homolog, is required for nuclear reorganization, presynaptic homolog juxtaposition and the proper distribution of cohesin during meiosis in Arabidopsis

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Abstract

Nuclear reorganization and juxtaposition of homologous chromosomes at late leptotene/early zygotene are essential steps before chromosome synapsis at pachytene. We report the results of detailed studies, which demonstrate that nuclear reorganization and homolog juxtapositioning processes are defective in a null mutant, ask1-1. Our results from 4, 6-diamino-2-phenylindole (DAPI)-stained spreads showed that the “synizetic knot”, which is typically found in wild type (WT) meiosis during late leptotene and zygotene, was missing in the ask1-1 mutant. Furthermore, ask1-1 meiocytes exhibited only limited homolog juxtaposition at centromere regions at early zygotene. Immunodetection of the cohesin protein SYN1 identified ask1 defects in cohesin distribution from zygotene to anaphase I. Analysis of meiotic chromosomes in ask1-1 and syn1 single mutants, as well as an ask1-1 syn1 double mutant indicate that ASK1 is required for normal SYN1 distribution during meiotic prophase I and suggest that ask1 associated defects may be primarily related to SYN1 mislocalization.

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Abbreviations

AE:

axial element

CE:

central element

DAPI:

4, 6-diamino-2-phenylindole

LEs:

lateral elements

SC:

synaptonemal complex

TEM:

transmission electron microscopy

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Acknowledgements

We thank A. Omeis and J. Wang for plant care. We also thank E. Harris and M. Henry for their help with the identification of the ask1-1 syn1 double mutant plants. We are grateful for comments on this manuscript from C. Chen, W. Li, L. Harper, W. Ni, G. Wang, L.M. Zahn, W. Zhang, and M. Zolan. This work was supported by grants from the National Science Foundation [MCB-0092075 (HM); MCB-0322171 (CAM)], the National Institutes of Health [RO1 GM63871 (HM)], and the Department of Energy [DE-FG02-02ER15332 (HM and DZ)] and by funds from the Department of Biology and the Huck Institutes of the Life Sciences at the Pennsylvania State University. H.M. gratefully acknowledges the support of the John Simon Guggenheim Memorial Foundation.

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  1. Nathan W. Rigel

    Present address: Department of Microbiology and Immunology, University of North Carolina, Chapel Hill, North Carolina, 27599-7290, USA

Authors and Affiliations

  1. Department of Biology and the Huck Institutes of the Life Sciences, The Pennsylvania State University, University Park, PA, 16802, USA

    Dazhong Zhao, Li Quan, Ljudmilla Timofejeva, Nathan W. Rigel & Hong Ma

  2. Department of Chemistry and Biochemistry, Miami University, Hughes Hall, Oxford, Ohio, 45056, USA

    Xiaohui Yang & Christopher A. Makaroff

  3. Department of Biological Sciences, University of Wisconsin-Milwaukee, Milwaukee, WI, 53211, USA

    Dazhong Zhao

  4. Department of Gene Technology, Tallinn University of Technology, Akadeemia tee 15, 19086, Tallinn, Estonia

    Ljudmilla Timofejeva

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  1. Dazhong Zhao
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  2. Xiaohui Yang
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Correspondence to Hong Ma or Christopher A. Makaroff.

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Zhao, D., Yang, X., Quan, L. et al. ASK1, a SKP1 homolog, is required for nuclear reorganization, presynaptic homolog juxtaposition and the proper distribution of cohesin during meiosis in Arabidopsis . Plant Mol Biol 62, 99–110 (2006). https://doi.org/10.1007/s11103-006-9006-1

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