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Identification of Arabidopsis meiotic cyclins reveals functional diversification among plant cyclin genes.

Bulankova P, Akimcheva S, Fellner N, Riha K - PLoS Genet. (2013)

Bottom Line: We found six A-type cyclins and a single B-type cyclin (CYCB3;1) to be expressed in male meiosis.We further show that cyclin SDS does not contain a D-box and is constitutively expressed throughout meiosis.Our phenotypic and expression data provide extensive evidence that multiplication of cyclins is in plants accompanied by functional diversification.

View Article: PubMed Central - PubMed

Affiliation: Gregor Mendel Institute, Austrian Academy of Sciences, Vienna, Austria.

ABSTRACT
Meiosis is a modified cell division in which a single S-phase is followed by two rounds of chromosome segregation resulting in the production of haploid gametes. The meiotic mode of chromosome segregation requires extensive remodeling of the basic cell cycle machinery and employment of unique regulatory mechanisms. Cyclin-dependent kinases (CDKs) and cyclins represent an ancient molecular module that drives and regulates cell cycle progression. The cyclin gene family has undergone a massive expansion in angiosperm plants, but only a few cyclins were thoroughly characterized. In this study we performed a systematic immunolocalization screen to identify Arabidopsis thaliana A- and B-type cyclins expressed in meiosis. Many of these cyclins exhibit cell-type-specific expression in vegetative tissues and distinct subcellular localization. We found six A-type cyclins and a single B-type cyclin (CYCB3;1) to be expressed in male meiosis. Mutant analysis revealed that these cyclins contribute to distinct meiosis-related processes. While A2 cyclins are important for chromosome segregation, CYCB3;1 prevents ectopic cell wall formation. We further show that cyclin SDS does not contain a D-box and is constitutively expressed throughout meiosis. Analysis of plants carrying cyclin SDS with an introduced D-box motif determined that, in addition to its function in recombination, SDS acts together with CYCB3;1 in suppressing unscheduled cell wall synthesis. Our phenotypic and expression data provide extensive evidence that multiplication of cyclins is in plants accompanied by functional diversification.

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Immunolocalization of CYC:GUS proteins in PMCs.DNA was counterstained with DAPI, microtubules were detected with anti-α-tubulin antibody. Bar = 10 µm.
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pgen-1003508-g001: Immunolocalization of CYC:GUS proteins in PMCs.DNA was counterstained with DAPI, microtubules were detected with anti-α-tubulin antibody. Bar = 10 µm.

Mentions: To determine which cyclins are expressed in meiosis, we looked for the presence of the immunolocalization signal in PMCs. In total, one B- and six A-type cyclins produced specific staining in cells undergoing meiosis (Figure 1, Table 1). We previously showed that TAM is present in the cytoplasm of PMCs from leptotene to pachytene, but diminishes in the later meiotic stages [19]. CYCA2;1:GUS immunostaining is reminiscent of the cyclin TAM. Expression of CYCA2;2, CYCA3;2 and CYCA3;4 was restricted to leptotene where these cyclins preferentially localized to nuclei. CYCA3;3 likely evolved from CYCA3;2, and lost a part of N-terminal domain that includes a D-box. CYCA3;3 was present throughout entire meiosis, but we did not observe any specific signal in somatic cells. The only B-type cyclin expressed in PMCs was CYCB3;1. Its signal was detectable from zygotene to metaphase I, where it localized to the spindle, disappeared in anaphase I, and again reappeared at the spindle in metaphase II (Figure 1).


Identification of Arabidopsis meiotic cyclins reveals functional diversification among plant cyclin genes.

Bulankova P, Akimcheva S, Fellner N, Riha K - PLoS Genet. (2013)

Immunolocalization of CYC:GUS proteins in PMCs.DNA was counterstained with DAPI, microtubules were detected with anti-α-tubulin antibody. Bar = 10 µm.
© Copyright Policy
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC3649987&req=5

pgen-1003508-g001: Immunolocalization of CYC:GUS proteins in PMCs.DNA was counterstained with DAPI, microtubules were detected with anti-α-tubulin antibody. Bar = 10 µm.
Mentions: To determine which cyclins are expressed in meiosis, we looked for the presence of the immunolocalization signal in PMCs. In total, one B- and six A-type cyclins produced specific staining in cells undergoing meiosis (Figure 1, Table 1). We previously showed that TAM is present in the cytoplasm of PMCs from leptotene to pachytene, but diminishes in the later meiotic stages [19]. CYCA2;1:GUS immunostaining is reminiscent of the cyclin TAM. Expression of CYCA2;2, CYCA3;2 and CYCA3;4 was restricted to leptotene where these cyclins preferentially localized to nuclei. CYCA3;3 likely evolved from CYCA3;2, and lost a part of N-terminal domain that includes a D-box. CYCA3;3 was present throughout entire meiosis, but we did not observe any specific signal in somatic cells. The only B-type cyclin expressed in PMCs was CYCB3;1. Its signal was detectable from zygotene to metaphase I, where it localized to the spindle, disappeared in anaphase I, and again reappeared at the spindle in metaphase II (Figure 1).

Bottom Line: We found six A-type cyclins and a single B-type cyclin (CYCB3;1) to be expressed in male meiosis.We further show that cyclin SDS does not contain a D-box and is constitutively expressed throughout meiosis.Our phenotypic and expression data provide extensive evidence that multiplication of cyclins is in plants accompanied by functional diversification.

View Article: PubMed Central - PubMed

Affiliation: Gregor Mendel Institute, Austrian Academy of Sciences, Vienna, Austria.

ABSTRACT
Meiosis is a modified cell division in which a single S-phase is followed by two rounds of chromosome segregation resulting in the production of haploid gametes. The meiotic mode of chromosome segregation requires extensive remodeling of the basic cell cycle machinery and employment of unique regulatory mechanisms. Cyclin-dependent kinases (CDKs) and cyclins represent an ancient molecular module that drives and regulates cell cycle progression. The cyclin gene family has undergone a massive expansion in angiosperm plants, but only a few cyclins were thoroughly characterized. In this study we performed a systematic immunolocalization screen to identify Arabidopsis thaliana A- and B-type cyclins expressed in meiosis. Many of these cyclins exhibit cell-type-specific expression in vegetative tissues and distinct subcellular localization. We found six A-type cyclins and a single B-type cyclin (CYCB3;1) to be expressed in male meiosis. Mutant analysis revealed that these cyclins contribute to distinct meiosis-related processes. While A2 cyclins are important for chromosome segregation, CYCB3;1 prevents ectopic cell wall formation. We further show that cyclin SDS does not contain a D-box and is constitutively expressed throughout meiosis. Analysis of plants carrying cyclin SDS with an introduced D-box motif determined that, in addition to its function in recombination, SDS acts together with CYCB3;1 in suppressing unscheduled cell wall synthesis. Our phenotypic and expression data provide extensive evidence that multiplication of cyclins is in plants accompanied by functional diversification.

Show MeSH
Related in: MedlinePlus