Experimental insights into genome reconstruction driven by horizontal transfer of supernumerary chromosomes in Magnaporthe oryzae

Summary

Many pathogenic fungi display ‘two-speed genome’, with the fast-evolving genomic compartments enriched with repetitive sequences, particularly the transposons, which have been shown to drive the variation of pathogenicity-associated genes. Supernumerary chromosomes (SCs) are known to facilitate genomic variation in fungal pathogens, but their specific role in such processes remains understudied.
In this study, we assessed the transferability of SCs between asexual Magnaporthe oryzae strains during co-culture and co-infection, and investigated their role in genome reconstruction through experimental evolution assays.
We found that SCs could be horizontally transferred between M. oryzae strains and revealed frequent structural variations facilitated by SCs, including deletions, duplications, translocations, and SC-core chromosome recombinations during and after horizontal transfer. Remarkably, all observed intra- and inter-chromosome rearrangements were confined to core chromosome ends and SCs, indicating a robust role of SCs in facilitating genetic exchange within fast-evolving genomic compartments. Additionally, SC carrying the avirulence gene AvrPik

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modulates M. oryzae virulence against Pikh rice through horizontal transfer, loss of whole SC, and segmental deletions.
Our findings establish SCs as critical players in shaping the diversity and dynamics of the pathogenic fungal genomes, highlighting them as a cradle for the variation of pathogenicity-associated genes.

概括

许多病原真菌具有“双速基因组”的特征, 其富含重复序列(特别是转座子)的快速进化基因组区已被证实可促进致病性相关基因的遗传变异。尽管超数染色体(Supernumerary chromosomes, SCs)在病原真菌基因组变异中的作用已被初步认识, 但其具体作用机制仍有待深入研究。
本研究以无性态稻瘟病菌(Magnaporthe oryzae)为模型, 通过共培养和共侵染实验评估了SCs的水平转移能力, 并利用实验进化群体深入解析了SCs在基因组重构中的动态作用。
我们发现SCs可在稻瘟病菌间发生水平转移, 揭示SCs介导了频繁的基因组结构变异, 包括在水平转移过程中及转移后发生的删除、复制、易位以及SC与核心染色体间的重组。值得注意的是, 所有观察到的染色体内和染色体间重排均局限于核心染色体末端和SCs上, 表明SCs在快速进化基因组区域的遗传交换中具有关键作用。此外, 携带无毒基因AvrPik

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的SC通过水平转移、整条染色体丢失以及片段删除等方式, 动态调控了稻瘟病菌对Pikh水稻的致病性。
我们的研究结果表明, SCs是塑造病原真菌基因组多样性和动态变化的关键因素, 凸显了其作为致病性相关基因变异”摇篮”的重要作用。

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