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Cohesin proteins load sequentially during prophase I in tomato primary microsporocytes

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Abstract

Proteins of the cohesin complex are essential for sister chromatid cohesion and proper chromosome segregation during both mitosis and meiosis. Cohesin proteins are also components of axial elements/lateral elements (AE/LEs) of synaptonemal complexes (SCs) during meiosis, and cohesins are thought to play an important role in meiotic chromosome morphogenesis and recombination. Here, we have examined the cytological behavior of four cohesin proteins (SMC1, SMC3, SCC3, and REC8/SYN1) during early prophase I in tomato microsporocytes using immunolabeling. All four cohesins are discontinuously distributed along the length of AE/LEs from leptotene through early diplotene. Based on current models for the cohesin complex, the four cohesin proteins should be present at the same time and place in equivalent amounts. However, we observed that cohesins often do not colocalize at the same AE/LE positions, and cohesins differ in when they load onto and dissociate from AE/LEs of early prophase I chromosomes. Cohesin labeling of LEs from pachytene nuclei is similar through euchromatin, pericentric heterochromatin, and kinetochores but is distinctly reduced through the nucleolar organizer region of chromosome 2. These results indicate that the four cohesin proteins may form different complexes and/or perform additional functions during meiosis in plants, which are distinct from their essential function in sister chromatid cohesion.

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Abbreviations

3D-SIM:

three-dimensional structured illumination microscopy

AE:

axial element

CCD:

charge coupled device

DAPI:

4’,6-diamidino-2-phenylindole

DIF1:

protein determinant infertile 1

LE:

lateral element

NOR:

nucleolar organizer region

rDNA:

ribosomal DNA

REC8:

meiotic recombination protein REC8

REC11:

meiotic recombination protein REC11

SMC1:

structural maintenance of chromosomes protein 1

SMC3:

structural maintenance of chromosomes protein 3

SC:

synaptonemal complex

SCC:

sister chromatid cohesion

SCC1:

sister chromatid cohesion protein 1

SCC3:

sister chromatid cohesion protein 3

STAG3:

stromalin 3 protein

SYN1:

synaptic mutant

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Acknowledgments

We thank Chris Makaroff (University of Miami, Ohio) and Christine Mezard and Liudmila Chelysheva (Versailles, France) for generously providing antibodies to AtSYN1 and AtSCC3, respectively. We also thank two anonymous reviewers for their helpful comments. This work was supported by the National Science Foundation (MCB-064344 and MCB-1019708).

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  1. Huanyu Qiao

    Present address: Department of Microbiology, University of California, Davis, CA, 95616, USA

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  1. Department of Biology and Program in Molecular Plant Biology, Colorado State University, 1878 Campus Delivery, Fort Collins, CO, 80523-1878, USA

    Huanyu Qiao, Leslie D. Lohmiller & Lorinda K. Anderson

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  1. Huanyu Qiao
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Qiao, H., Lohmiller, L.D. & Anderson, L.K. Cohesin proteins load sequentially during prophase I in tomato primary microsporocytes. Chromosome Res 19, 193–207 (2011). https://doi.org/10.1007/s10577-010-9184-1

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