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Mitotic cyclin distribution during maize cell division: Implications for the sequence diversity and function of cyclins in plants

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Summary

Cyclin proteins are components of the regulatory system that controls the orderly progression of the events of cell division. Their sub-cellular location, as well as their fluctuating abundance and their affinities for the cyclin-dependent kinases (CDKs) to which they bind, determine their successive roles during the cell cycle. Here we employ species-specific antibodies to monitor changes in quantity and location of four maize cyclins and maize Cdc2-kinase in dividing maize root tip cells. Maize cyclin Ia occurs in the nuclear matrix and is released when the nuclear envelope breaks down. In contrast, cyclin Ib is cytoplasmic until prophase; it associates transiently with the nuclear envelope and preprophase band (PPB) just before these structures break down and then associates with the condensed chromosomes and spindle region before declining at anaphase. Cyclin II and Cdc2 also occur in the PPB. Occurrence of cyclin Ib and Cdc2 at the PPB concurrent with initiation of breakdown is consistent with previous studies in which microinjection of cyclin-dependent protein kinase indicated that removal of the PPB at the time of nuclear-envelope breakdown is catalysed by a CDK. While cyclins Ia and III are predominantly nuclear prior to mitosis, cyclins Ib and II are predominantly cytoplasmic until prophase then become nuclear. The initial cytoplasmic retention of cyclins Ib and II correlates with their possession of a sequence similar to the cytoplasmic-retention signal of animal cyclin B1. Cyclin II binds to all microtubule arrays during the cell cycle, becoming markedly concentrated in the phragmoplast, and cyclin III associates with the spindle and then the phragmoplast. Cdc2 also occurs in the phragmoplast. Persistence of mitotic cyclins and CDK after mitosis into the cytokinetic stage, as seen in maize, is not paralleled in animal cells, where the cytokinetic mid-body is not so labelled, presumably reflecting the key role of the phragmoplast apparatus in plant cell division.

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Abbreviations

CDK:

cyclin-dependent kinase

CRS:

cytoplasmicretention signal

NE:

nuclear envelope

NEB:

nuclear-envelope breakdown

NLS:

nuclear-location signal

PPB:

preprophase band

FITC:

fluorescein isothiocyanate

TRITC:

tetramethylrhodamine isothiocyanate

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Authors and Affiliations

  1. Plant Cell Biology Group, Research School of Biological Sciences, Australian National University, GPO Box 475, 2601, Canberra, ACT, Australia

    Miriam Mews, Frank J. Sek, Brian E. S. Gunning & Peter C. L. John

  2. Botanisches Institut der Universität Bonn, Bonn, Germany

    Miriam Mews & Dieter Volkmann

  3. Cooperative Research Centre for Plant Science, Australian National University, Canberra, ACT

    Robert Moore, Brian E. S. Gunning & Peter C. L. John

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  1. Miriam Mews
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  2. Frank J. Sek
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  3. Robert Moore
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  4. Dieter Volkmann
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  5. Brian E. S. Gunning
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  6. Peter C. L. John
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Correspondence to Peter C. L. John.

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Mews, M., Sek, F.J., Moore, R. et al. Mitotic cyclin distribution during maize cell division: Implications for the sequence diversity and function of cyclins in plants. Protoplasma 200, 128–145 (1997). https://doi.org/10.1007/BF01283289

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