Cellular Dynamics and Genomic Identity of Centromeres in Cereal Blast Fungus

ABSTRACT Precise kinetochore-microtubule interactions ensure faithful chromosome segregation in eukaryotes. Centromeres, identified as scaffolding sites for kinetochore assembly, are among the most rapidly evolving chromosomal loci in terms of the DNA sequence and length and organization of intrinsi...

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Autores principales:	Vikas Yadav, Fan Yang, Md. Hashim Reza, Sanzhen Liu, Barbara Valent, Kaustuv Sanyal, Naweed I. Naqvi
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2019
Materias:	CenpA centromeres rice blast wheat blast chromosome structure kinetochore dynamics Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/e0cecfdb65db48f2bd3486150e5f0298
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spelling	oai:doaj.org-article:e0cecfdb65db48f2bd3486150e5f02982021-11-15T16:22:11ZCellular Dynamics and Genomic Identity of Centromeres in Cereal Blast Fungus10.1128/mBio.01581-192150-7511https://doaj.org/article/e0cecfdb65db48f2bd3486150e5f02982019-08-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.01581-19https://doaj.org/toc/2150-7511ABSTRACT Precise kinetochore-microtubule interactions ensure faithful chromosome segregation in eukaryotes. Centromeres, identified as scaffolding sites for kinetochore assembly, are among the most rapidly evolving chromosomal loci in terms of the DNA sequence and length and organization of intrinsic elements. Neither the centromere structure nor the kinetochore dynamics is well studied in plant-pathogenic fungi. Here, we sought to understand the process of chromosome segregation in the rice blast fungus Magnaporthe oryzae. High-resolution imaging of green fluorescent protein (GFP)-tagged inner kinetochore proteins CenpA and CenpC revealed unusual albeit transient declustering of centromeres just before anaphase separation of chromosomes in M. oryzae. Strikingly, the declustered centromeres positioned randomly at the spindle midzone without an apparent metaphase plate per se. Using CenpA chromatin immunoprecipitation followed by deep sequencing, all seven centromeres in M. oryzae were found to be regional, spanning 57-kb to 109-kb transcriptionally poor regions. Highly AT-rich and heavily methylated DNA sequences were the only common defining features of all the centromeres in rice blast. Lack of centromere-specific DNA sequence motifs or repetitive elements suggests an epigenetic specification of centromere function in M. oryzae. PacBio genome assemblies and synteny analyses facilitated comparison of the centromeric/pericentromeric regions in distinct isolates of rice blast and wheat blast and in Magnaporthiopsis poae. Overall, this study revealed unusual centromere dynamics and precisely identified the centromere loci in the top model fungal pathogens that belong to Magnaporthales and cause severe losses in the global production of food crops and turf grasses. IMPORTANCE Magnaporthe oryzae is an important fungal pathogen that causes a loss of 10% to 30% of the annual rice crop due to the devastating blast disease. In most organisms, kinetochores are clustered together or arranged at the metaphase plate to facilitate synchronized anaphase separation of sister chromatids in mitosis. In this study, we showed that the initially clustered kinetochores separate and position randomly prior to anaphase in M. oryzae. Centromeres in M. oryzae occupy large genomic regions and form on AT-rich DNA without any common sequence motifs. Overall, this study identified atypical kinetochore dynamics and mapped functional centromeres in M. oryzae to define the roles of centromeric and pericentric boundaries in kinetochore assembly on epigenetically specified centromere loci. This study should pave the way for further understanding of the contribution of heterochromatin in genome stability and virulence of the blast fungus and its related species of high economic importance.Vikas YadavFan YangMd. Hashim RezaSanzhen LiuBarbara ValentKaustuv SanyalNaweed I. NaqviAmerican Society for MicrobiologyarticleCenpAcentromeresrice blastwheat blastchromosome structurekinetochore dynamicsMicrobiologyQR1-502ENmBio, Vol 10, Iss 4 (2019)
institution	DOAJ
collection	DOAJ
language	EN
topic	CenpA centromeres rice blast wheat blast chromosome structure kinetochore dynamics Microbiology QR1-502
spellingShingle	CenpA centromeres rice blast wheat blast chromosome structure kinetochore dynamics Microbiology QR1-502 Vikas Yadav Fan Yang Md. Hashim Reza Sanzhen Liu Barbara Valent Kaustuv Sanyal Naweed I. Naqvi Cellular Dynamics and Genomic Identity of Centromeres in Cereal Blast Fungus
description	ABSTRACT Precise kinetochore-microtubule interactions ensure faithful chromosome segregation in eukaryotes. Centromeres, identified as scaffolding sites for kinetochore assembly, are among the most rapidly evolving chromosomal loci in terms of the DNA sequence and length and organization of intrinsic elements. Neither the centromere structure nor the kinetochore dynamics is well studied in plant-pathogenic fungi. Here, we sought to understand the process of chromosome segregation in the rice blast fungus Magnaporthe oryzae. High-resolution imaging of green fluorescent protein (GFP)-tagged inner kinetochore proteins CenpA and CenpC revealed unusual albeit transient declustering of centromeres just before anaphase separation of chromosomes in M. oryzae. Strikingly, the declustered centromeres positioned randomly at the spindle midzone without an apparent metaphase plate per se. Using CenpA chromatin immunoprecipitation followed by deep sequencing, all seven centromeres in M. oryzae were found to be regional, spanning 57-kb to 109-kb transcriptionally poor regions. Highly AT-rich and heavily methylated DNA sequences were the only common defining features of all the centromeres in rice blast. Lack of centromere-specific DNA sequence motifs or repetitive elements suggests an epigenetic specification of centromere function in M. oryzae. PacBio genome assemblies and synteny analyses facilitated comparison of the centromeric/pericentromeric regions in distinct isolates of rice blast and wheat blast and in Magnaporthiopsis poae. Overall, this study revealed unusual centromere dynamics and precisely identified the centromere loci in the top model fungal pathogens that belong to Magnaporthales and cause severe losses in the global production of food crops and turf grasses. IMPORTANCE Magnaporthe oryzae is an important fungal pathogen that causes a loss of 10% to 30% of the annual rice crop due to the devastating blast disease. In most organisms, kinetochores are clustered together or arranged at the metaphase plate to facilitate synchronized anaphase separation of sister chromatids in mitosis. In this study, we showed that the initially clustered kinetochores separate and position randomly prior to anaphase in M. oryzae. Centromeres in M. oryzae occupy large genomic regions and form on AT-rich DNA without any common sequence motifs. Overall, this study identified atypical kinetochore dynamics and mapped functional centromeres in M. oryzae to define the roles of centromeric and pericentric boundaries in kinetochore assembly on epigenetically specified centromere loci. This study should pave the way for further understanding of the contribution of heterochromatin in genome stability and virulence of the blast fungus and its related species of high economic importance.
format	article
author	Vikas Yadav Fan Yang Md. Hashim Reza Sanzhen Liu Barbara Valent Kaustuv Sanyal Naweed I. Naqvi
author_facet	Vikas Yadav Fan Yang Md. Hashim Reza Sanzhen Liu Barbara Valent Kaustuv Sanyal Naweed I. Naqvi
author_sort	Vikas Yadav
title	Cellular Dynamics and Genomic Identity of Centromeres in Cereal Blast Fungus
title_short	Cellular Dynamics and Genomic Identity of Centromeres in Cereal Blast Fungus
title_full	Cellular Dynamics and Genomic Identity of Centromeres in Cereal Blast Fungus
title_fullStr	Cellular Dynamics and Genomic Identity of Centromeres in Cereal Blast Fungus
title_full_unstemmed	Cellular Dynamics and Genomic Identity of Centromeres in Cereal Blast Fungus
title_sort	cellular dynamics and genomic identity of centromeres in cereal blast fungus
publisher	American Society for Microbiology
publishDate	2019
url	https://doaj.org/article/e0cecfdb65db48f2bd3486150e5f0298
work_keys_str_mv	AT vikasyadav cellulardynamicsandgenomicidentityofcentromeresincerealblastfungus AT fanyang cellulardynamicsandgenomicidentityofcentromeresincerealblastfungus AT mdhashimreza cellulardynamicsandgenomicidentityofcentromeresincerealblastfungus AT sanzhenliu cellulardynamicsandgenomicidentityofcentromeresincerealblastfungus AT barbaravalent cellulardynamicsandgenomicidentityofcentromeresincerealblastfungus AT kaustuvsanyal cellulardynamicsandgenomicidentityofcentromeresincerealblastfungus AT naweedinaqvi cellulardynamicsandgenomicidentityofcentromeresincerealblastfungus
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Cellular Dynamics and Genomic Identity of Centromeres in Cereal Blast Fungus

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