Forward Genetics Approach Reveals Host Genotype-Dependent Importance of Accessory Chromosomes in the Fungal Wheat Pathogen <italic toggle="yes">Zymoseptoria tritici</italic>

ABSTRACT The fungal wheat pathogen Zymoseptoria tritici possesses a large complement of accessory chromosomes showing presence/absence polymorphism among isolates. These chromosomes encode hundreds of genes; however, their functional role and why the chromosomes have been maintained over long evolut...

Descripción completa

Guardado en:

Detalles Bibliográficos
Autores principales:	Michael Habig, Jakob Quade, Eva Holtgrewe Stukenbrock
Formato:	article
Lenguaje:	EN
Publicado:	American Society for Microbiology 2017
Materias:	genome plasticity functional dissection host-pathogen interactions induced chromosome deletions virulence Microbiology QR1-502
Acceso en línea:	https://doaj.org/article/d3bdf6901f674b39b0b3f346f4a8860f
Etiquetas:	Agregar Etiqueta Sin Etiquetas, Sea el primero en etiquetar este registro!

id	oai:doaj.org-article:d3bdf6901f674b39b0b3f346f4a8860f
record_format	dspace
spelling	oai:doaj.org-article:d3bdf6901f674b39b0b3f346f4a8860f2021-11-15T15:51:55ZForward Genetics Approach Reveals Host Genotype-Dependent Importance of Accessory Chromosomes in the Fungal Wheat Pathogen <italic toggle="yes">Zymoseptoria tritici</italic>10.1128/mBio.01919-172150-7511https://doaj.org/article/d3bdf6901f674b39b0b3f346f4a8860f2017-12-01T00:00:00Zhttps://journals.asm.org/doi/10.1128/mBio.01919-17https://doaj.org/toc/2150-7511ABSTRACT The fungal wheat pathogen Zymoseptoria tritici possesses a large complement of accessory chromosomes showing presence/absence polymorphism among isolates. These chromosomes encode hundreds of genes; however, their functional role and why the chromosomes have been maintained over long evolutionary times are so far not known. In this study, we addressed the functional relevance of eight accessory chromosomes in reference isolate IPO323. We induced chromosome losses by inhibiting the β-tubulin assembly during mitosis using carbendazim and generated several independent isogenic strains, each lacking one of the accessory chromosomes. We confirmed chromosome losses by electrophoretic karyotyping and whole-genome sequencing. To assess the importance of the individual chromosomes during host infection, we performed in planta assays comparing disease development results in wild-type and chromosome mutant strains. Loss of the accessory chromosomes 14, 16, 18, 19, and 21 resulted in increased virulence on wheat cultivar Runal but not on cultivars Obelisk, Titlis, and Riband. Moreover, some accessory chromosomes affected the switch from biotrophy to necrotrophy as strains lacking accessory chromosomes 14, 18, 19, and 21 showed a significantly earlier onset of necrosis than the wild type on the Runal cultivar. In general, we observed that the timing of the lifestyle switch affects the fitness of Z. tritici. Taking the results together, this study was the first to use a forward-genetics approach to demonstrate a cultivar-dependent functional relevance of the accessory chromosomes of Z. tritici during host infection. IMPORTANCE Zymoseptoria tritici is a prominent fungal pathogen of wheat of worldwide distribution. This fungus shows a remarkable genome organization, with a large number of chromosomes that are present in only some isolates and therefore considered to be “accessory” chromosomes. To date, the function of these accessory chromosomes in Z. tritici has been unknown, although their maintenance in the species over evolutionary times suggests a functional relevance. Here we deleted whole accessory chromosomes to test the effect of these chromosomes on host specificity and virulence of the fungus. We show for the first time that some accessory chromosomes of Z. tritici affect the fitness of the fungus during host infection in a cultivar-dependent manner. These results show that the accessory chromosomes encode host-specific virulence determinants having a negative effect on fitness. Understanding the population dynamic of the accessory chromosomes and the molecular interaction of pathogen and plant traits is crucial to improve wheat-breeding strategies.Michael HabigJakob QuadeEva Holtgrewe StukenbrockAmerican Society for Microbiologyarticlegenome plasticityfunctional dissectionhost-pathogen interactionsinduced chromosome deletionsvirulenceMicrobiologyQR1-502ENmBio, Vol 8, Iss 6 (2017)
institution	DOAJ
collection	DOAJ
language	EN
topic	genome plasticity functional dissection host-pathogen interactions induced chromosome deletions virulence Microbiology QR1-502
spellingShingle	genome plasticity functional dissection host-pathogen interactions induced chromosome deletions virulence Microbiology QR1-502 Michael Habig Jakob Quade Eva Holtgrewe Stukenbrock Forward Genetics Approach Reveals Host Genotype-Dependent Importance of Accessory Chromosomes in the Fungal Wheat Pathogen <italic toggle="yes">Zymoseptoria tritici</italic>
description	ABSTRACT The fungal wheat pathogen Zymoseptoria tritici possesses a large complement of accessory chromosomes showing presence/absence polymorphism among isolates. These chromosomes encode hundreds of genes; however, their functional role and why the chromosomes have been maintained over long evolutionary times are so far not known. In this study, we addressed the functional relevance of eight accessory chromosomes in reference isolate IPO323. We induced chromosome losses by inhibiting the β-tubulin assembly during mitosis using carbendazim and generated several independent isogenic strains, each lacking one of the accessory chromosomes. We confirmed chromosome losses by electrophoretic karyotyping and whole-genome sequencing. To assess the importance of the individual chromosomes during host infection, we performed in planta assays comparing disease development results in wild-type and chromosome mutant strains. Loss of the accessory chromosomes 14, 16, 18, 19, and 21 resulted in increased virulence on wheat cultivar Runal but not on cultivars Obelisk, Titlis, and Riband. Moreover, some accessory chromosomes affected the switch from biotrophy to necrotrophy as strains lacking accessory chromosomes 14, 18, 19, and 21 showed a significantly earlier onset of necrosis than the wild type on the Runal cultivar. In general, we observed that the timing of the lifestyle switch affects the fitness of Z. tritici. Taking the results together, this study was the first to use a forward-genetics approach to demonstrate a cultivar-dependent functional relevance of the accessory chromosomes of Z. tritici during host infection. IMPORTANCE Zymoseptoria tritici is a prominent fungal pathogen of wheat of worldwide distribution. This fungus shows a remarkable genome organization, with a large number of chromosomes that are present in only some isolates and therefore considered to be “accessory” chromosomes. To date, the function of these accessory chromosomes in Z. tritici has been unknown, although their maintenance in the species over evolutionary times suggests a functional relevance. Here we deleted whole accessory chromosomes to test the effect of these chromosomes on host specificity and virulence of the fungus. We show for the first time that some accessory chromosomes of Z. tritici affect the fitness of the fungus during host infection in a cultivar-dependent manner. These results show that the accessory chromosomes encode host-specific virulence determinants having a negative effect on fitness. Understanding the population dynamic of the accessory chromosomes and the molecular interaction of pathogen and plant traits is crucial to improve wheat-breeding strategies.
format	article
author	Michael Habig Jakob Quade Eva Holtgrewe Stukenbrock
author_facet	Michael Habig Jakob Quade Eva Holtgrewe Stukenbrock
author_sort	Michael Habig
title	Forward Genetics Approach Reveals Host Genotype-Dependent Importance of Accessory Chromosomes in the Fungal Wheat Pathogen <italic toggle="yes">Zymoseptoria tritici</italic>
title_short	Forward Genetics Approach Reveals Host Genotype-Dependent Importance of Accessory Chromosomes in the Fungal Wheat Pathogen <italic toggle="yes">Zymoseptoria tritici</italic>
title_full	Forward Genetics Approach Reveals Host Genotype-Dependent Importance of Accessory Chromosomes in the Fungal Wheat Pathogen <italic toggle="yes">Zymoseptoria tritici</italic>
title_fullStr	Forward Genetics Approach Reveals Host Genotype-Dependent Importance of Accessory Chromosomes in the Fungal Wheat Pathogen <italic toggle="yes">Zymoseptoria tritici</italic>
title_full_unstemmed	Forward Genetics Approach Reveals Host Genotype-Dependent Importance of Accessory Chromosomes in the Fungal Wheat Pathogen <italic toggle="yes">Zymoseptoria tritici</italic>
title_sort	forward genetics approach reveals host genotype-dependent importance of accessory chromosomes in the fungal wheat pathogen <italic toggle="yes">zymoseptoria tritici</italic>
publisher	American Society for Microbiology
publishDate	2017
url	https://doaj.org/article/d3bdf6901f674b39b0b3f346f4a8860f
work_keys_str_mv	AT michaelhabig forwardgeneticsapproachrevealshostgenotypedependentimportanceofaccessorychromosomesinthefungalwheatpathogenitalictoggleyeszymoseptoriatriticiitalic AT jakobquade forwardgeneticsapproachrevealshostgenotypedependentimportanceofaccessorychromosomesinthefungalwheatpathogenitalictoggleyeszymoseptoriatriticiitalic AT evaholtgrewestukenbrock forwardgeneticsapproachrevealshostgenotypedependentimportanceofaccessorychromosomesinthefungalwheatpathogenitalictoggleyeszymoseptoriatriticiitalic
_version_	1718427306745135104

Forward Genetics Approach Reveals Host Genotype-Dependent Importance of Accessory Chromosomes in the Fungal Wheat Pathogen <italic toggle="yes">Zymoseptoria tritici</italic>

Ejemplares similares