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A CENH3 mutation promotes meiotic exit and restores fertility in SMG7-deficient Arabidopsis

Meiosis in angiosperm plants is followed by mitotic divisions to form multicellular haploid gametophytes. Termination of meiosis and transition to gametophytic development is, in Arabidopsis, governed by a dedicated mechanism that involves SMG7 and TDM1 proteins. Mutants carrying the smg7-6 allele a...

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Autores principales: Capitao, Claudio, Tanasa, Sorin, Fulnecek, Jaroslav, Raxwal, Vivek K., Akimcheva, Svetlana, Bulankova, Petra, Mikulkova, Pavlina, Crhak Khaitova, Lucie, Kalidass, Manikandan, Lermontova, Inna, Mittelsten Scheid, Ortrun, Riha, Karel
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8509889/
https://www.ncbi.nlm.nih.gov/pubmed/34591845
http://dx.doi.org/10.1371/journal.pgen.1009779
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author Capitao, Claudio
Tanasa, Sorin
Fulnecek, Jaroslav
Raxwal, Vivek K.
Akimcheva, Svetlana
Bulankova, Petra
Mikulkova, Pavlina
Crhak Khaitova, Lucie
Kalidass, Manikandan
Lermontova, Inna
Mittelsten Scheid, Ortrun
Riha, Karel
author_facet Capitao, Claudio
Tanasa, Sorin
Fulnecek, Jaroslav
Raxwal, Vivek K.
Akimcheva, Svetlana
Bulankova, Petra
Mikulkova, Pavlina
Crhak Khaitova, Lucie
Kalidass, Manikandan
Lermontova, Inna
Mittelsten Scheid, Ortrun
Riha, Karel
author_sort Capitao, Claudio
collection PubMed
description Meiosis in angiosperm plants is followed by mitotic divisions to form multicellular haploid gametophytes. Termination of meiosis and transition to gametophytic development is, in Arabidopsis, governed by a dedicated mechanism that involves SMG7 and TDM1 proteins. Mutants carrying the smg7-6 allele are semi-fertile due to reduced pollen production. We found that instead of forming tetrads, smg7-6 pollen mother cells undergo multiple rounds of chromosome condensation and spindle assembly at the end of meiosis, resembling aberrant attempts to undergo additional meiotic divisions. A suppressor screen uncovered a mutation in centromeric histone H3 (CENH3) that increased fertility and promoted meiotic exit in smg7-6 plants. The mutation led to inefficient splicing of the CENH3 mRNA and a substantial decrease of CENH3, resulting in smaller centromeres. The reduced level of CENH3 delayed formation of the mitotic spindle but did not have an apparent effect on plant growth and development. We suggest that impaired spindle re-assembly at the end of meiosis limits aberrant divisions in smg7-6 plants and promotes formation of tetrads and viable pollen. Furthermore, the mutant with reduced level of CENH3 was very inefficient haploid inducer indicating that differences in centromere size is not the key determinant of centromere-mediated genome elimination.
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spelling pubmed-85098892021-10-13 A CENH3 mutation promotes meiotic exit and restores fertility in SMG7-deficient Arabidopsis Capitao, Claudio Tanasa, Sorin Fulnecek, Jaroslav Raxwal, Vivek K. Akimcheva, Svetlana Bulankova, Petra Mikulkova, Pavlina Crhak Khaitova, Lucie Kalidass, Manikandan Lermontova, Inna Mittelsten Scheid, Ortrun Riha, Karel PLoS Genet Research Article Meiosis in angiosperm plants is followed by mitotic divisions to form multicellular haploid gametophytes. Termination of meiosis and transition to gametophytic development is, in Arabidopsis, governed by a dedicated mechanism that involves SMG7 and TDM1 proteins. Mutants carrying the smg7-6 allele are semi-fertile due to reduced pollen production. We found that instead of forming tetrads, smg7-6 pollen mother cells undergo multiple rounds of chromosome condensation and spindle assembly at the end of meiosis, resembling aberrant attempts to undergo additional meiotic divisions. A suppressor screen uncovered a mutation in centromeric histone H3 (CENH3) that increased fertility and promoted meiotic exit in smg7-6 plants. The mutation led to inefficient splicing of the CENH3 mRNA and a substantial decrease of CENH3, resulting in smaller centromeres. The reduced level of CENH3 delayed formation of the mitotic spindle but did not have an apparent effect on plant growth and development. We suggest that impaired spindle re-assembly at the end of meiosis limits aberrant divisions in smg7-6 plants and promotes formation of tetrads and viable pollen. Furthermore, the mutant with reduced level of CENH3 was very inefficient haploid inducer indicating that differences in centromere size is not the key determinant of centromere-mediated genome elimination. Public Library of Science 2021-09-30 /pmc/articles/PMC8509889/ /pubmed/34591845 http://dx.doi.org/10.1371/journal.pgen.1009779 Text en © 2021 Capitao et al https://creativecommons.org/licenses/by/4.0/This is an open access article distributed under the terms of the Creative Commons Attribution License (https://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
spellingShingle Research Article
Capitao, Claudio
Tanasa, Sorin
Fulnecek, Jaroslav
Raxwal, Vivek K.
Akimcheva, Svetlana
Bulankova, Petra
Mikulkova, Pavlina
Crhak Khaitova, Lucie
Kalidass, Manikandan
Lermontova, Inna
Mittelsten Scheid, Ortrun
Riha, Karel
A CENH3 mutation promotes meiotic exit and restores fertility in SMG7-deficient Arabidopsis
title A CENH3 mutation promotes meiotic exit and restores fertility in SMG7-deficient Arabidopsis
title_full A CENH3 mutation promotes meiotic exit and restores fertility in SMG7-deficient Arabidopsis
title_fullStr A CENH3 mutation promotes meiotic exit and restores fertility in SMG7-deficient Arabidopsis
title_full_unstemmed A CENH3 mutation promotes meiotic exit and restores fertility in SMG7-deficient Arabidopsis
title_short A CENH3 mutation promotes meiotic exit and restores fertility in SMG7-deficient Arabidopsis
title_sort cenh3 mutation promotes meiotic exit and restores fertility in smg7-deficient arabidopsis
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8509889/
https://www.ncbi.nlm.nih.gov/pubmed/34591845
http://dx.doi.org/10.1371/journal.pgen.1009779
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