Infection-associated nuclear degeneration in the rice blast fungus Magnaporthe oryzae requires non-selective macro-autophagy.

School of Biosciences, University of Exeter, Exeter, Devon, United Kingdom.
PLoS ONE (Impact Factor: 3.73). 01/2012; 7(3):e33270. DOI: 10.1371/journal.pone.0033270
Source: PubMed

ABSTRACT The rice blast fungus Magnaporthe oryzae elaborates a specialized infection structure called an appressorium to breach the rice leaf surface and gain access to plant tissue. Appressorium development is controlled by cell cycle progression, and a single round of nuclear division occurs prior to appressorium formation. Mitosis is always followed by programmed cell death of the spore from which the appressorium develops. Nuclear degeneration in the spore is known to be essential for plant infection, but the precise mechanism by which it occurs is not known.
In yeast, nuclear breakdown requires a specific form of autophagy, known as piecemeal microautophagy of the nucleus (PMN), and we therefore investigated whether this process occurs in the rice blast fungus. Here, we report that M. oryzae possesses two conserved components of a putative PMN pathway, MoVac8 and MoTsc13, but that both are dispensable for nuclear breakdown during plant infection. MoVAC8 encodes a vacuolar membrane protein and MoTSC13 a peri-nuclear and peripheral ER protein.
We show that MoVAC8 is necessary for caffeine resistance, but dispensable for pathogenicity of M. oryzae, while MoTSC13 is involved in cell wall stress responses and is an important virulence determinant. By functional analysis of ΔMoatg1 and ΔMoatg4 mutants, we demonstrate that infection-associated nuclear degeneration in M. oryzae instead occurs by non-selective macroautophagy, which is necessary for rice blast disease.

  • [Show abstract] [Hide abstract]
    ABSTRACT: Specific localization of appropriate sets of proteins and lipids is central to functions and integrity of organelles, which in turn underlie cellular activities of eukaryotes. Vesicle trafficking is a conserved mechanism of intracellular transport, which ensures such a specific localization to a subset of organelles. In this review article, we summarize recent advances in our understanding of how vesicle trafficking and related organelles support physiology and pathogenicity of filamentous fungi. Examples include a link between Golgi organization and polarity maintenance during hyphal tip growth, a new role of early endosomes in transport of translational machinery, involvement of endosomal/vacuolar compartments in secondary metabolite synthesis, and functions of vacuoles and autophagy in fungal development, nutrient recycling and allocation. Accumulating evidence showing the importance of unconventional secretion in fungal pathogenicity is also summarized.
    Current opinion in microbiology. 05/2014; 20C:1-9.
  • Source
    [Show abstract] [Hide abstract]
    ABSTRACT: Under certain circumstances, the removal of damaged or non-essential parts of the nucleus, or even an entire nucleus, is crucial in order to promote cell longevity and enable proper function. A selective form of autophagy, known as nucleophagy, can be used to accomplish the degradation of nucleusderived material. In this Cell Science at a Glance article and the accompanying poster, we summarize the similarities and differences between the divergent modes of nucleophagy that have been described to date, emphasizing, where possible, the molecular mechanism, the membrane interactions and rearrangements, and the nature of the nucleus-derived material that is degraded. In turn, we will consider nucleophagy processes in the lower eukaryotes, the budding yeast Saccharomyces cerevisiae, filamentous fungi Aspergillus and Magnaporthe oryzae and the ciliated protozoan Tetrahymena thermophila, and finally in mammalian cells. We will also briefly discuss the emerging links between nucleophagy and human disease.
    Journal of Cell Science 09/2013; · 5.88 Impact Factor
  • [Show abstract] [Hide abstract]
    ABSTRACT: Autophagy is a tightly controlled degradation process in which eukaryotic cells digest their own cytoplasm containing protein complexes and organelles in the vacuole or lysosome. Two types of autophagy have been described: macroautophagy and microautophagy. Both types can be further divided into nonselective and selective processes. Molecular analysis of autophagy over the last two decades has mostly used the unicellular ascomycetes Saccharomyces cerevisiae and Pichia pastoris. Genetic analysis in these yeasts has identified 36 autophagy-related (atg) genes; many are conserved in all eukaryotes, including filamentous ascomycetes. However, the autophagic machinery also evolved significant differences in fungi, as a consequence of adaptation to diverse fungal lifestyles. Intensive studies on autophagy in the last few years have shown that autophagy in filamentous fungi is not only involved in nutrient homeostasis but in other cellular processes such as cell differentiation, pathogenicity and secondary metabolite production. This mini-review focuses on the specific roles of autophagy in filamentous fungi.
    Applied Microbiology and Biotechnology 09/2013; · 3.69 Impact Factor

Full-text (2 Sources)

Available from
May 15, 2014