Forward Genetics Approach Reveals Host Genotype-Dependent Importance of Accessory Chromosomes in the Fungal Wheat Pathogen Zymoseptoria tritici

Forward Genetics Approach Reveals Host Genotype-Dependent Importance of Accessory Chromosomes in the Fungal Wheat Pathogen Zymoseptoria tritici
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DOI:
10.1128/mbio.01919-17
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发表时间:
2017-11-01
期刊:
影响因子:
6.4
通讯作者:
Stukenbrock, Eva Holtgrewe
Stukenbrock, Eva Holtgrewe
中科院分区:
生物学1区
文献类型:
--
作者:
Habig, Michael;Quade, Jakob;Stukenbrock, Eva Holtgrewe

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真菌小麦病原菌Zymoseptoria triumphora具有大量的辅助染色体,在分离株之间表现出存在/不存在多态性。这些染色体编码数百个基因;然而,它们的功能作用以及为什么染色体在漫长的进化时间中得以维持至今仍不清楚。在这项研究中,我们解决了8个辅助染色体的参考分离株IPO 323的功能相关性。我们诱导染色体丢失,抑制β-微管蛋白组装在有丝分裂过程中使用多菌灵,并产生了几个独立的等基因株,每个缺乏一个辅助染色体。我们通过电泳核型分析和全基因组测序证实了染色体丢失。为了评估个体染色体在宿主感染过程中的重要性,我们进行了植物试验,比较野生型和染色体突变株的疾病发展结果。辅助染色体14,16,18,19和21的损失导致小麦品种Runal的毒性增加,但不对品种Obelisk,Titlis和Riband。此外,一些辅助染色体影响的开关从活体营养型坏死缺乏辅助染色体14,18,19和21的菌株表现出显着更早的发病坏死比野生型的Runal品种。总的来说,我们观察到生活方式转变的时间会影响Z的健康。三个月。综合这些结果,本研究首次使用正向遗传学方法证明了Z辅助染色体的品种依赖性功能相关性。重要性三孢发酵壳孢(Zymoseptoria triacetylum)是世界性分布的小麦的重要真菌病原体。这种真菌显示出显着的基因组组织,具有大量的染色体,仅存在于一些分离株中,因此被认为是“辅助”染色体。迄今为止,对这些辅助染色体在Z.尽管在进化过程中它们在物种中的维持表明了功能上的相关性,但它们一直是未知的。在这里,我们删除整个辅助染色体,以测试这些染色体对寄主特异性和真菌的毒力的影响。本文首次证明了Z.真菌在宿主感染期间以依赖于品种的方式影响真菌的适合性。这些结果表明,辅助染色体编码宿主特异性的毒力决定因子具有负面影响的健身。了解小麦辅助染色体的群体动态以及病原菌与植株性状的分子互作对改进小麦育种策略至关重要。
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 beta-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.