The blast fungus, Magnaporthe oryzae, causes severe destruction to rice and other crops worldwide. As the fungus infects rice, it develops unique cellular structures, such as an appressorium and a narrow penetration peg, to permit successful invasion of host rice cells. Fundamental knowledge about these cellular structures and how organelles, such as the nucleus, are positioned within them is still emerging. Previous studies show that a single nucleus becomes highly stretched during movement through the narrow penetration peg in an extreme nuclear migration event. Yet, the mechanism permitting this nuclear migration event remains elusive. Here, we investigate the role of the mitotic spindle in mediating nuclear migration through the penetration peg. We find that disruption of spindle function during nuclear migration through the penetration peg prevents development of invasive hyphae and virulence on rice. Furthermore, regulated expression of conserved kinesin motor proteins, MoKin5 and MoKin14, is essential to form and maintain the spindle, as well as, properly nucleate the primary hypha. Overexpression of MoKin5 leads to formation of aberrant microtubule protrusions, which contributes to formation of nuclear fragments within the appressorium and primary hypha. Conversely, overexpression of MoKin14 causes the spindle to collapse leading to the formation of monopolar spindles. These results establish a mechanistic model towards understanding the intricate subcellular dynamics of extreme nuclear migration through the penetration peg, a critical step in the development of rice blast disease.
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