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...

Descripción completa

Guardado en:
Detalles Bibliográficos
Autores principales: Claudio Capitao, Sorin Tanasa, Jaroslav Fulnecek, Vivek K Raxwal, Svetlana Akimcheva, Petra Bulankova, Pavlina Mikulkova, Lucie Crhak Khaitova, Manikandan Kalidass, Inna Lermontova, Ortrun Mittelsten Scheid, Karel Riha
Formato: article
Lenguaje:EN
Publicado: Public Library of Science (PLoS) 2021
Materias:
Acceso en línea:https://doaj.org/article/e7cd73f985f246cab1f4184b3d27a750
Etiquetas: Agregar Etiqueta
Sin Etiquetas, Sea el primero en etiquetar este registro!
id oai:doaj.org-article:e7cd73f985f246cab1f4184b3d27a750
record_format dspace
spelling oai:doaj.org-article:e7cd73f985f246cab1f4184b3d27a7502021-12-02T20:03:01ZA CENH3 mutation promotes meiotic exit and restores fertility in SMG7-deficient Arabidopsis.1553-73901553-740410.1371/journal.pgen.1009779https://doaj.org/article/e7cd73f985f246cab1f4184b3d27a7502021-09-01T00:00:00Zhttps://doi.org/10.1371/journal.pgen.1009779https://doaj.org/toc/1553-7390https://doaj.org/toc/1553-7404Meiosis 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.Claudio CapitaoSorin TanasaJaroslav FulnecekVivek K RaxwalSvetlana AkimchevaPetra BulankovaPavlina MikulkovaLucie Crhak KhaitovaManikandan KalidassInna LermontovaOrtrun Mittelsten ScheidKarel RihaPublic Library of Science (PLoS)articleGeneticsQH426-470ENPLoS Genetics, Vol 17, Iss 9, p e1009779 (2021)
institution DOAJ
collection DOAJ
language EN
topic Genetics
QH426-470
spellingShingle Genetics
QH426-470
Claudio Capitao
Sorin Tanasa
Jaroslav Fulnecek
Vivek K Raxwal
Svetlana Akimcheva
Petra Bulankova
Pavlina Mikulkova
Lucie Crhak Khaitova
Manikandan Kalidass
Inna Lermontova
Ortrun Mittelsten Scheid
Karel Riha
A CENH3 mutation promotes meiotic exit and restores fertility in SMG7-deficient Arabidopsis.
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.
format article
author Claudio Capitao
Sorin Tanasa
Jaroslav Fulnecek
Vivek K Raxwal
Svetlana Akimcheva
Petra Bulankova
Pavlina Mikulkova
Lucie Crhak Khaitova
Manikandan Kalidass
Inna Lermontova
Ortrun Mittelsten Scheid
Karel Riha
author_facet Claudio Capitao
Sorin Tanasa
Jaroslav Fulnecek
Vivek K Raxwal
Svetlana Akimcheva
Petra Bulankova
Pavlina Mikulkova
Lucie Crhak Khaitova
Manikandan Kalidass
Inna Lermontova
Ortrun Mittelsten Scheid
Karel Riha
author_sort Claudio Capitao
title 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_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_sort cenh3 mutation promotes meiotic exit and restores fertility in smg7-deficient arabidopsis.
publisher Public Library of Science (PLoS)
publishDate 2021
url https://doaj.org/article/e7cd73f985f246cab1f4184b3d27a750
work_keys_str_mv AT claudiocapitao acenh3mutationpromotesmeioticexitandrestoresfertilityinsmg7deficientarabidopsis
AT sorintanasa acenh3mutationpromotesmeioticexitandrestoresfertilityinsmg7deficientarabidopsis
AT jaroslavfulnecek acenh3mutationpromotesmeioticexitandrestoresfertilityinsmg7deficientarabidopsis
AT vivekkraxwal acenh3mutationpromotesmeioticexitandrestoresfertilityinsmg7deficientarabidopsis
AT svetlanaakimcheva acenh3mutationpromotesmeioticexitandrestoresfertilityinsmg7deficientarabidopsis
AT petrabulankova acenh3mutationpromotesmeioticexitandrestoresfertilityinsmg7deficientarabidopsis
AT pavlinamikulkova acenh3mutationpromotesmeioticexitandrestoresfertilityinsmg7deficientarabidopsis
AT luciecrhakkhaitova acenh3mutationpromotesmeioticexitandrestoresfertilityinsmg7deficientarabidopsis
AT manikandankalidass acenh3mutationpromotesmeioticexitandrestoresfertilityinsmg7deficientarabidopsis
AT innalermontova acenh3mutationpromotesmeioticexitandrestoresfertilityinsmg7deficientarabidopsis
AT ortrunmittelstenscheid acenh3mutationpromotesmeioticexitandrestoresfertilityinsmg7deficientarabidopsis
AT karelriha acenh3mutationpromotesmeioticexitandrestoresfertilityinsmg7deficientarabidopsis
AT claudiocapitao cenh3mutationpromotesmeioticexitandrestoresfertilityinsmg7deficientarabidopsis
AT sorintanasa cenh3mutationpromotesmeioticexitandrestoresfertilityinsmg7deficientarabidopsis
AT jaroslavfulnecek cenh3mutationpromotesmeioticexitandrestoresfertilityinsmg7deficientarabidopsis
AT vivekkraxwal cenh3mutationpromotesmeioticexitandrestoresfertilityinsmg7deficientarabidopsis
AT svetlanaakimcheva cenh3mutationpromotesmeioticexitandrestoresfertilityinsmg7deficientarabidopsis
AT petrabulankova cenh3mutationpromotesmeioticexitandrestoresfertilityinsmg7deficientarabidopsis
AT pavlinamikulkova cenh3mutationpromotesmeioticexitandrestoresfertilityinsmg7deficientarabidopsis
AT luciecrhakkhaitova cenh3mutationpromotesmeioticexitandrestoresfertilityinsmg7deficientarabidopsis
AT manikandankalidass cenh3mutationpromotesmeioticexitandrestoresfertilityinsmg7deficientarabidopsis
AT innalermontova cenh3mutationpromotesmeioticexitandrestoresfertilityinsmg7deficientarabidopsis
AT ortrunmittelstenscheid cenh3mutationpromotesmeioticexitandrestoresfertilityinsmg7deficientarabidopsis
AT karelriha cenh3mutationpromotesmeioticexitandrestoresfertilityinsmg7deficientarabidopsis
_version_ 1718375694785839104