Cargando…

Two Cdc2 Kinase Genes with Distinct Functions in Vegetative and Infectious Hyphae in Fusarium graminearum

Eukaryotic cell cycle involves a number of protein kinases important for the onset and progression through mitosis, most of which are well characterized in the budding and fission yeasts and conserved in other fungi. However, unlike the model yeast and filamentous fungi that have a single Cdc2 essen...

Descripción completa

Detalles Bibliográficos
Autores principales: Liu, Huiquan, Zhang, Shijie, Ma, Jiwen, Dai, Yafeng, Li, Chaohui, Lyu, Xueliang, Wang, Chenfang, Xu, Jin-Rong
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2015
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4470668/
https://www.ncbi.nlm.nih.gov/pubmed/26083253
http://dx.doi.org/10.1371/journal.ppat.1004913
_version_ 1782376799451217920
author Liu, Huiquan
Zhang, Shijie
Ma, Jiwen
Dai, Yafeng
Li, Chaohui
Lyu, Xueliang
Wang, Chenfang
Xu, Jin-Rong
author_facet Liu, Huiquan
Zhang, Shijie
Ma, Jiwen
Dai, Yafeng
Li, Chaohui
Lyu, Xueliang
Wang, Chenfang
Xu, Jin-Rong
author_sort Liu, Huiquan
collection PubMed
description Eukaryotic cell cycle involves a number of protein kinases important for the onset and progression through mitosis, most of which are well characterized in the budding and fission yeasts and conserved in other fungi. However, unlike the model yeast and filamentous fungi that have a single Cdc2 essential for cell cycle progression, the wheat scab fungus Fusarium graminearum contains two CDC2 orthologs. The cdc2A and cdc2B mutants had no obvious defects in growth rate and conidiation but deletion of both of them is lethal, indicating that these two CDC2 orthologs have redundant functions during vegetative growth and asexual reproduction. However, whereas the cdc2B mutant was normal, the cdc2A mutant was significantly reduced in virulence and rarely produced ascospores. Although deletion of CDC2A had no obvious effect on the formation of penetration branches or hyphopodia, the cdc2A mutant was limited in the differentiation and growth of infectious growth in wheat tissues. Therefore, CDC2A plays stage-specific roles in cell cycle regulation during infectious growth and sexual reproduction. Both CDC2A and CDC2B are constitutively expressed but only CDC2A was up-regulated during plant infection and ascosporogenesis. Localization of Cdc2A- GFP to the nucleus but not Cdc2B-GFP was observed in vegetative hyphae, ascospores, and infectious hyphae. Complementation assays with chimeric fusion constructs showed that both the N- and C-terminal regions of Cdc2A are important for its functions in pathogenesis and ascosporogenesis but only the N-terminal region is important for its subcellular localization. Among the Sordariomycetes, only three Fusarium species closely related to F. graminearum have two CDC2 genes. Furthermore, F. graminearum uniquely has two Aurora kinase genes and one additional putative cyclin gene, and its orthologs of CAK1 and other four essential mitotic kinases in the budding yeast are dispensable for viability. Overall, our data indicate that cell cycle regulation is different between vegetative and infectious hyphae in F. graminearum and Cdc2A, possibly by interacting with a stage-specific cyclin, plays a more important role than Cdc2B during ascosporogenesis and plant infection.
format Online
Article
Text
id pubmed-4470668
institution National Center for Biotechnology Information
language English
publishDate 2015
publisher Public Library of Science
record_format MEDLINE/PubMed
spelling pubmed-44706682015-06-29 Two Cdc2 Kinase Genes with Distinct Functions in Vegetative and Infectious Hyphae in Fusarium graminearum Liu, Huiquan Zhang, Shijie Ma, Jiwen Dai, Yafeng Li, Chaohui Lyu, Xueliang Wang, Chenfang Xu, Jin-Rong PLoS Pathog Research Article Eukaryotic cell cycle involves a number of protein kinases important for the onset and progression through mitosis, most of which are well characterized in the budding and fission yeasts and conserved in other fungi. However, unlike the model yeast and filamentous fungi that have a single Cdc2 essential for cell cycle progression, the wheat scab fungus Fusarium graminearum contains two CDC2 orthologs. The cdc2A and cdc2B mutants had no obvious defects in growth rate and conidiation but deletion of both of them is lethal, indicating that these two CDC2 orthologs have redundant functions during vegetative growth and asexual reproduction. However, whereas the cdc2B mutant was normal, the cdc2A mutant was significantly reduced in virulence and rarely produced ascospores. Although deletion of CDC2A had no obvious effect on the formation of penetration branches or hyphopodia, the cdc2A mutant was limited in the differentiation and growth of infectious growth in wheat tissues. Therefore, CDC2A plays stage-specific roles in cell cycle regulation during infectious growth and sexual reproduction. Both CDC2A and CDC2B are constitutively expressed but only CDC2A was up-regulated during plant infection and ascosporogenesis. Localization of Cdc2A- GFP to the nucleus but not Cdc2B-GFP was observed in vegetative hyphae, ascospores, and infectious hyphae. Complementation assays with chimeric fusion constructs showed that both the N- and C-terminal regions of Cdc2A are important for its functions in pathogenesis and ascosporogenesis but only the N-terminal region is important for its subcellular localization. Among the Sordariomycetes, only three Fusarium species closely related to F. graminearum have two CDC2 genes. Furthermore, F. graminearum uniquely has two Aurora kinase genes and one additional putative cyclin gene, and its orthologs of CAK1 and other four essential mitotic kinases in the budding yeast are dispensable for viability. Overall, our data indicate that cell cycle regulation is different between vegetative and infectious hyphae in F. graminearum and Cdc2A, possibly by interacting with a stage-specific cyclin, plays a more important role than Cdc2B during ascosporogenesis and plant infection. Public Library of Science 2015-06-17 /pmc/articles/PMC4470668/ /pubmed/26083253 http://dx.doi.org/10.1371/journal.ppat.1004913 Text en © 2015 Liu et al http://creativecommons.org/licenses/by/4.0/ This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are properly credited.
spellingShingle Research Article
Liu, Huiquan
Zhang, Shijie
Ma, Jiwen
Dai, Yafeng
Li, Chaohui
Lyu, Xueliang
Wang, Chenfang
Xu, Jin-Rong
Two Cdc2 Kinase Genes with Distinct Functions in Vegetative and Infectious Hyphae in Fusarium graminearum
title Two Cdc2 Kinase Genes with Distinct Functions in Vegetative and Infectious Hyphae in Fusarium graminearum
title_full Two Cdc2 Kinase Genes with Distinct Functions in Vegetative and Infectious Hyphae in Fusarium graminearum
title_fullStr Two Cdc2 Kinase Genes with Distinct Functions in Vegetative and Infectious Hyphae in Fusarium graminearum
title_full_unstemmed Two Cdc2 Kinase Genes with Distinct Functions in Vegetative and Infectious Hyphae in Fusarium graminearum
title_short Two Cdc2 Kinase Genes with Distinct Functions in Vegetative and Infectious Hyphae in Fusarium graminearum
title_sort two cdc2 kinase genes with distinct functions in vegetative and infectious hyphae in fusarium graminearum
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4470668/
https://www.ncbi.nlm.nih.gov/pubmed/26083253
http://dx.doi.org/10.1371/journal.ppat.1004913
work_keys_str_mv AT liuhuiquan twocdc2kinasegeneswithdistinctfunctionsinvegetativeandinfectioushyphaeinfusariumgraminearum
AT zhangshijie twocdc2kinasegeneswithdistinctfunctionsinvegetativeandinfectioushyphaeinfusariumgraminearum
AT majiwen twocdc2kinasegeneswithdistinctfunctionsinvegetativeandinfectioushyphaeinfusariumgraminearum
AT daiyafeng twocdc2kinasegeneswithdistinctfunctionsinvegetativeandinfectioushyphaeinfusariumgraminearum
AT lichaohui twocdc2kinasegeneswithdistinctfunctionsinvegetativeandinfectioushyphaeinfusariumgraminearum
AT lyuxueliang twocdc2kinasegeneswithdistinctfunctionsinvegetativeandinfectioushyphaeinfusariumgraminearum
AT wangchenfang twocdc2kinasegeneswithdistinctfunctionsinvegetativeandinfectioushyphaeinfusariumgraminearum
AT xujinrong twocdc2kinasegeneswithdistinctfunctionsinvegetativeandinfectioushyphaeinfusariumgraminearum