Autophagy provides nutrients for nonassimilating fungal structures and is necessary for plant colonization but not for infection in the necrotrophic plant pathogen Fusarium graminearum

Josefsen, L.; Droce, Aida; Søndergaard, Teis Esben; Sørensen, Jens Laurids; Bormann, Jörg; Schäfer, Wilhelm; Giese, Henriette; Olsson, Stefan

doi:10.4161/auto.18705

Cited by 103 publications

(108 citation statements)

References 44 publications

(67 reference statements)

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“…2,4 Interestingly, both Mratg8Δ and Moatg8Δ showed a significant reduction in the ability to infect insect and rice hosts, respectively, while the ability of F. graminearum Fgatg8Δ to infect barley and wheat remained like the WT. 41 Similar to Aoatg4Δ and Aoatg15Δ of A. orzyae, 42 Mratg4Δ and Mratg15Δ lost the ability to form conidia. In contrast, Moatg4Δ and Moatg15 of M. oryzae can produce conidia but exhibit significantly reduced abilities of conidgiogenesis.…”

Section: Discussionmentioning

confidence: 94%

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Linkage of autophagy to fungal development, lipid storage and virulence inMetarhizium robertsii

et al. 2013

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Autophagy is a highly conserved process that maintains intracellular homeostasis by degrading proteins or organelles in all eukaryotes. The effect of autophagy on fungal biology and infection of insect pathogens is unknown. here, we report the function of MrATG8, an ortholog of yeast ATG8, in the entomopathogenic fungus Metarhizium robertsii. MrATG8 can complement an ATG8-defective yeast strain and deletion of MrATG8 impaired autophagy, conidiation and fungal infection biology in M. robertsii. compared with the wild-type and gene-rescued mutant, Mratg8Δ is not inductive to form the infection-structure appressorium and is impaired in defense response against insect immunity. in addition, accumulation of lipid droplets (LDs) is significantly reduced in the conidia of Mratg8Δ and the pathogenicity of the mutant is drastically impaired. We also found that the cellular level of a LD-specific perilipin-like protein is significantly lowered by deletion of MrATG8 and that the carboxyl terminus beyond the predicted protease cleavage site is dispensable for MrAtg8 function. To corroborate the role of autophagy in fungal physiology, the homologous genes of yeast ATG1, ATG4 and ATG15, designated as MrATG1, MrATG4 and MrATG15, were also deleted in M. robertsii. in contrast to Mratg8Δ, these mutants could form appressoria, however, the LD accumulation and virulence were also considerably impaired in the mutant strains. Our data showed that autophagy is required in M. robertsii for fungal differentiation, lipid biogenesis and insect infection. The results advance our understanding of autophagic process in fungi and provide evidence to connect autophagy with lipid metabolism.

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Section: Discussionmentioning

confidence: 94%

“…Indeed, it has been observed in F. graminearum that deletions of autophagy genes block LD degradation in mycelia upon nutrient deprivation. 6,41 of F. graminearum. 6 Studies in different organisms indicate that autophagy has evolved multiple times.…”

Section: Discussionmentioning

confidence: 99%

Linkage of autophagy to fungal development, lipid storage and virulence inMetarhizium robertsii

et al. 2013

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“…193,194,[798][799][800][801] In addition, macroautophagy seems to be involved in many normal developmental processes such as sexual and asexual reproduction, where there is a need for reallocation of nutrients from one part of the mycelium to another to supply the developing spores and spore-bearing structures. 194,798,799,801,802 Similarly, autophagy also affects conidial germination under nitrogen-limiting conditions. 194 In Podospora anserina, autophagy has been studied in relation to incompatibility reactions between mating strains where it seems to play a prosurvival role.…”

Section: 792mentioning

confidence: 99%

“…192,802 Of special interest to many researchers of autophagy in filamentous fungi has been the possible involvement of autophagy in plant pathogen infection and growth inside the host. 193,798,799,[803][804][805] Autophagy also appears to be necessary for the development of aerial hyphae, 194,798,802,804 and for appresorium function in Magnaporthe oryzae and Colletotrichum orbiculare. 193,803,804 Some of these effects could be caused by the absence of autophagic processing of storage lipids (lipophagy) to generate glycerol for increasing turgor.…”

Section: 792mentioning

confidence: 99%

Guidelines for the use and interpretation of assays for monitoring autophagy

Klionsky¹,

Abdalla²,

Abeliovich³

et al. 2012

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In 2008 we published the first set of guidelines for standardizing research in autophagy. Since then, research on this topic has continued to accelerate, and many new scientists have entered the field. Our knowledge base and relevant new technologies have also been expanding. Accordingly, it is important to update these guidelines for monitoring autophagy in different organisms. Various reviews have described the range of assays that have been used for this purpose. Nevertheless, there continues to be confusion regarding acceptable methods to measure autophagy, especially in multicellular eukaryotes. A key point that needs to be emphasized is that there is a difference between measurements that monitor the numbers or volume of autophagic elements (e.g., autophagosomes or autolysosomes) at any stage of the autophagic process vs. those that measure flux through the autophagy pathway (i.e., the complete process); thus, a block in macroautophagy that results in autophagosome accumulation needs to be differentiated from stimuli that result in increased autophagic activity, defined as increased autophagy induction coupled with increased delivery to, and degradation within, lysosomes (in most higher eukaryotes and some protists such as Dictyostelium) or the vacuole (in plants and fungi). In other words, it is especially important that investigators new to the field understand that the appearance of more autophagosomes does not necessarily equate with more autophagy. In fact, in many cases, autophagosomes accumulate because of a block in trafficking to lysosomes without a concomitant change in autophagosome biogenesis, whereas an increase in autolysosomes may reflect a reduction in degradative activity. Here, we present a set of guidelines for the selection and interpretation of methods for use by investigators who aim to examine macroautophagy and related processes, as well as for reviewers who need to provide realistic and reasonable critiques of papers that are focused on these processes. These guidelines are not meant to be a formulaic set of rules, because the appropriate assays depend in part on the question being asked and the system being used. In addition, we emphasize that no individual assay is guaranteed to be the most appropriate one in every situation, and we strongly recommend the use of multiple assays to monitor autophagy. In these guidelines, we consider these various methods of assessing autophagy and what information can, or cannot, be obtained from them. Finally, by discussing the merits and limits of particular autophagy assays, we hope to encourage technical innovation in the field

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“…Deletion of FgATG8 in the necrotrophic plant pathogen F. graminearum results in loss of perithecia, reduced conidiation, and collapse of the aerial hyphae [64]. Lipid utilization is dependent on autophagy in F. graminearum for providing nutrients for the nonassimilating portion of the fungi.…”

Section: The Two Ubiquitin-like Systems In Autophagymentioning

confidence: 99%

Autophagy in Plant Pathogenic Fungi

Shi¹,

Liang²,

Huang³

et al. 2016

Autophagy in Current Trends in Cellular Physiology and Pathology

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Autophagy is a ubiquitous and conserved process in eukaryotic cells from yeasts to mammals. It also appears to play vital roles in plant pathogenic fungi, impacting growth, morphology, development, and pathogenicity. In this chapter, we have introduced a new concept to delineate the role of autophagy in homeostasis of plant pathogenic fungi and in their interaction with host cells, in breach of host barrier, and in the mechanisms of plant fungal infection.

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Autophagy provides nutrients for nonassimilating fungal structures and is necessary for plant colonization but not for infection in the necrotrophic plant pathogen Fusarium graminearum

Cited by 103 publications

References 44 publications

Linkage of autophagy to fungal development, lipid storage and virulence inMetarhizium robertsii

Linkage of autophagy to fungal development, lipid storage and virulence inMetarhizium robertsii

Guidelines for the use and interpretation of assays for monitoring autophagy

Autophagy in Plant Pathogenic Fungi

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