Cargando…

A Functional Kinase Is Necessary for Cyclin-Dependent Kinase G1 (CDKG1) to Maintain Fertility at High Ambient Temperature in Arabidopsis

Maintaining fertility in a fluctuating environment is key to the reproductive success of flowering plants. Meiosis and pollen formation are particularly sensitive to changes in growing conditions, especially temperature. We have previously identified cyclin-dependent kinase G1 (CDKG1) as a master re...

Descripción completa

Detalles Bibliográficos
Autores principales: Nibau, Candida, Dadarou, Despoina, Kargios, Nestoras, Mallioura, Areti, Fernandez-Fuentes, Narcis, Cavallari, Nicola, Doonan, John H.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Frontiers Media S.A. 2020
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7683410/
https://www.ncbi.nlm.nih.gov/pubmed/33240303
http://dx.doi.org/10.3389/fpls.2020.586870
_version_ 1783612870971359232
author Nibau, Candida
Dadarou, Despoina
Kargios, Nestoras
Mallioura, Areti
Fernandez-Fuentes, Narcis
Cavallari, Nicola
Doonan, John H.
author_facet Nibau, Candida
Dadarou, Despoina
Kargios, Nestoras
Mallioura, Areti
Fernandez-Fuentes, Narcis
Cavallari, Nicola
Doonan, John H.
author_sort Nibau, Candida
collection PubMed
description Maintaining fertility in a fluctuating environment is key to the reproductive success of flowering plants. Meiosis and pollen formation are particularly sensitive to changes in growing conditions, especially temperature. We have previously identified cyclin-dependent kinase G1 (CDKG1) as a master regulator of temperature-dependent meiosis and this may involve the regulation of alternative splicing (AS), including of its own transcript. CDKG1 mRNA can undergo several AS events, potentially producing two protein variants: CDKG1L and CDKG1S, differing in their N-terminal domain which may be involved in co-factor interaction. In leaves, both isoforms have distinct temperature-dependent functions on target mRNA processing, but their role in pollen development is unknown. In the present study, we characterize the role of CDKG1L and CDKG1S in maintaining Arabidopsis fertility. We show that the long (L) form is necessary and sufficient to rescue the fertility defects of the cdkg1-1 mutant, while the short (S) form is unable to rescue fertility. On the other hand, an extra copy of CDKG1L reduces fertility. In addition, mutation of the ATP binding pocket of the kinase indicates that kinase activity is necessary for the function of CDKG1. Kinase mutants of CDKG1L and CDKG1S correctly localize to the cell nucleus and nucleus and cytoplasm, respectively, but are unable to rescue either the fertility or the splicing defects of the cdkg1-1 mutant. Furthermore, we show that there is partial functional overlap between CDKG1 and its paralog CDKG2 that could in part be explained by overlapping gene expression.
format Online
Article
Text
id pubmed-7683410
institution National Center for Biotechnology Information
language English
publishDate 2020
publisher Frontiers Media S.A.
record_format MEDLINE/PubMed
spelling pubmed-76834102020-11-24 A Functional Kinase Is Necessary for Cyclin-Dependent Kinase G1 (CDKG1) to Maintain Fertility at High Ambient Temperature in Arabidopsis Nibau, Candida Dadarou, Despoina Kargios, Nestoras Mallioura, Areti Fernandez-Fuentes, Narcis Cavallari, Nicola Doonan, John H. Front Plant Sci Plant Science Maintaining fertility in a fluctuating environment is key to the reproductive success of flowering plants. Meiosis and pollen formation are particularly sensitive to changes in growing conditions, especially temperature. We have previously identified cyclin-dependent kinase G1 (CDKG1) as a master regulator of temperature-dependent meiosis and this may involve the regulation of alternative splicing (AS), including of its own transcript. CDKG1 mRNA can undergo several AS events, potentially producing two protein variants: CDKG1L and CDKG1S, differing in their N-terminal domain which may be involved in co-factor interaction. In leaves, both isoforms have distinct temperature-dependent functions on target mRNA processing, but their role in pollen development is unknown. In the present study, we characterize the role of CDKG1L and CDKG1S in maintaining Arabidopsis fertility. We show that the long (L) form is necessary and sufficient to rescue the fertility defects of the cdkg1-1 mutant, while the short (S) form is unable to rescue fertility. On the other hand, an extra copy of CDKG1L reduces fertility. In addition, mutation of the ATP binding pocket of the kinase indicates that kinase activity is necessary for the function of CDKG1. Kinase mutants of CDKG1L and CDKG1S correctly localize to the cell nucleus and nucleus and cytoplasm, respectively, but are unable to rescue either the fertility or the splicing defects of the cdkg1-1 mutant. Furthermore, we show that there is partial functional overlap between CDKG1 and its paralog CDKG2 that could in part be explained by overlapping gene expression. Frontiers Media S.A. 2020-11-10 /pmc/articles/PMC7683410/ /pubmed/33240303 http://dx.doi.org/10.3389/fpls.2020.586870 Text en Copyright © 2020 Nibau, Dadarou, Kargios, Mallioura, Fernandez-Fuentes, Cavallari and Doonan. http://creativecommons.org/licenses/by/4.0/ This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) and the copyright owner(s) are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.
spellingShingle Plant Science
Nibau, Candida
Dadarou, Despoina
Kargios, Nestoras
Mallioura, Areti
Fernandez-Fuentes, Narcis
Cavallari, Nicola
Doonan, John H.
A Functional Kinase Is Necessary for Cyclin-Dependent Kinase G1 (CDKG1) to Maintain Fertility at High Ambient Temperature in Arabidopsis
title A Functional Kinase Is Necessary for Cyclin-Dependent Kinase G1 (CDKG1) to Maintain Fertility at High Ambient Temperature in Arabidopsis
title_full A Functional Kinase Is Necessary for Cyclin-Dependent Kinase G1 (CDKG1) to Maintain Fertility at High Ambient Temperature in Arabidopsis
title_fullStr A Functional Kinase Is Necessary for Cyclin-Dependent Kinase G1 (CDKG1) to Maintain Fertility at High Ambient Temperature in Arabidopsis
title_full_unstemmed A Functional Kinase Is Necessary for Cyclin-Dependent Kinase G1 (CDKG1) to Maintain Fertility at High Ambient Temperature in Arabidopsis
title_short A Functional Kinase Is Necessary for Cyclin-Dependent Kinase G1 (CDKG1) to Maintain Fertility at High Ambient Temperature in Arabidopsis
title_sort functional kinase is necessary for cyclin-dependent kinase g1 (cdkg1) to maintain fertility at high ambient temperature in arabidopsis
topic Plant Science
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7683410/
https://www.ncbi.nlm.nih.gov/pubmed/33240303
http://dx.doi.org/10.3389/fpls.2020.586870
work_keys_str_mv AT nibaucandida afunctionalkinaseisnecessaryforcyclindependentkinaseg1cdkg1tomaintainfertilityathighambienttemperatureinarabidopsis
AT dadaroudespoina afunctionalkinaseisnecessaryforcyclindependentkinaseg1cdkg1tomaintainfertilityathighambienttemperatureinarabidopsis
AT kargiosnestoras afunctionalkinaseisnecessaryforcyclindependentkinaseg1cdkg1tomaintainfertilityathighambienttemperatureinarabidopsis
AT malliouraareti afunctionalkinaseisnecessaryforcyclindependentkinaseg1cdkg1tomaintainfertilityathighambienttemperatureinarabidopsis
AT fernandezfuentesnarcis afunctionalkinaseisnecessaryforcyclindependentkinaseg1cdkg1tomaintainfertilityathighambienttemperatureinarabidopsis
AT cavallarinicola afunctionalkinaseisnecessaryforcyclindependentkinaseg1cdkg1tomaintainfertilityathighambienttemperatureinarabidopsis
AT doonanjohnh afunctionalkinaseisnecessaryforcyclindependentkinaseg1cdkg1tomaintainfertilityathighambienttemperatureinarabidopsis
AT nibaucandida functionalkinaseisnecessaryforcyclindependentkinaseg1cdkg1tomaintainfertilityathighambienttemperatureinarabidopsis
AT dadaroudespoina functionalkinaseisnecessaryforcyclindependentkinaseg1cdkg1tomaintainfertilityathighambienttemperatureinarabidopsis
AT kargiosnestoras functionalkinaseisnecessaryforcyclindependentkinaseg1cdkg1tomaintainfertilityathighambienttemperatureinarabidopsis
AT malliouraareti functionalkinaseisnecessaryforcyclindependentkinaseg1cdkg1tomaintainfertilityathighambienttemperatureinarabidopsis
AT fernandezfuentesnarcis functionalkinaseisnecessaryforcyclindependentkinaseg1cdkg1tomaintainfertilityathighambienttemperatureinarabidopsis
AT cavallarinicola functionalkinaseisnecessaryforcyclindependentkinaseg1cdkg1tomaintainfertilityathighambienttemperatureinarabidopsis
AT doonanjohnh functionalkinaseisnecessaryforcyclindependentkinaseg1cdkg1tomaintainfertilityathighambienttemperatureinarabidopsis