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Many studies have researched several pathogenic pathways in rice blast fungi, including cAMP signaling, which is associated with surface recognition and appressorium formation, and the Pmk1 pathway, which is essential for appressorium formation and plant invasion [ 55 ]. Recent research shows that the endocytosis pathway is required and plays a major role in rice blast fungal morphogenesis, vacuole fusion, stress resistance and pathogenicity [ 17 , 19 , 35 ].

However, until recently, few studies have elaborated on the crosstalk between these signaling pathways in pathogenic fungi. An increasing body of evidence suggests the existence of crosstalk between autophagy and endocytosis, and some genes have been identified to be involved in both autophagy and other pathways Table 3. In addition, some Rab proteins, such as PoRab5 and MoYpt7, which function in the fusion of either late endosomes or autophagosomes with vacuoles, are involved in the regulation of autophagy in M.

In addition, some ATG proteins are involved in the apoptosis pathway in mammals: the conjugation of Atg12 with Atg3 inhibits mitochondrial fission and apoptosis, independent of autophagy, and Bcl-2 interacts with Beclin-1 to inhibit autophagy [ 59 ]. However, none of the available lines of evidence directly reveals the interrelations between autophagy and apoptosis in filamentous fungi. Vps34 recruits Atg6 under the action of Vps38 to induce endosomal endocytosis. Simultaneously, Atg6 is recruited by Vps34 under the action of Atg14 to target the PAS, which participates in the autophagy pathway.

Both autophagosome and endosome fusion with the vacuole require the Ypt7 protein. Nuclear-localized Tpc1 then activates the transcription of genes required for polar growth, autophagy, and glycogen degradation. Although the autophagy pathway is a conserved process in eukaryotes, some differences have been found between M. First, multiple PAS-like sites are found in each cell of the M.

In addition, Atg1 and Atg13 are conserved from yeast to mammals and form the Atg1-Atg13 complex, which is essential for autophagy in the yeast system [ 62 , 63 ]. We hypothesize that MoAtg13 loses its function during the autophagy process of M. Second, the basal level of autophagy under normal conditions is stronger in M. In addition, several proteins have double or multiple functions and are involved in crosstalk between autophagy and other pathways [ 17 , 19 , 53 ,, 64 ]. These results have not been reported in S. Although the autophagy process has been well studied, the following questions require additional research: What is the origin of the autophagic membrane?

Where does the energy required for autophagic formation originate? How do autophagic bodies autophagosomes move within the cell? Can autophagosomes travel between cells? A key challenge for autophagy in plant-pathogen interactions is the accurate regulation of autophagy by pathogenic fungi at different phases.

This is of particular interest during pathogen invasion because the roles of the autophagy pathway in the expansion of the pathogen within the host remain unknown. The appressoria of M. National Center for Biotechnology Information , U. Journal List Virulence v. Published online Dec 3. Author information Article notes Copyright and License information Disclaimer. Received Aug 31; Accepted Nov Introduction Autophagy is an evolutionarily conserved process in eukaryotes. Interactions between pathogenic fungi and plants In recent years, the mechanisms underlying the interactions between plants and fungi have been a hot topic in plant pathology research, and the corresponding results should broaden the theoretical foundation of plant resistance mechanisms and aid the breeding of resistant plants.

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Core autophagy genes related to pathogenicity in filamentous fungi. Table 2. New factors that regulate autophagy in filamentous fungi. Autophagy and endocytosis in pathogenesis The mechanism through which the autophagy pathways affect the pathogenicity of pathogenic fungi is a topic that has been investigated by many researchers in recent years. Figure 2. Autophagy process in filamentous fungi. Figure 3. Autophagy mediates the infection of filamentous fungi and cell survival.

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Crosstalk between autophagy and endocytosis in pathogenic fungi In M. Table 3. Proteins with dual roles in autophagy and endocytosis. Protein Species Functions References PoVps21 Magnaporthe oryzae Involved in autophagic closure and the formation of the early endosome [ 19 , 54 ] MoYpt7 Magnaporthe oryzae Essential for autophagic fusion and required for late endosome formation [ 37 ] MoAtg6 Magnaporthe oryzae Primary cellular activator of autophagy and endocytosis [ 19 ] MoVps35 Magnaporthe oryzae Involved in the origin of the autophagosomal membrane and endosome formation [ 42 ] MoEnd3 Magnaporthe oryzae Mediates endocytosis and autophagy [].

Figure 4. Conclusions and perspectives Although the autophagy pathway is a conserved process in eukaryotes, some differences have been found between M. Disclosure statement No potential conflict of interest was reported by the authors. New advances in autophagy in plants: regulation, selectivity and function. Semin Cell Dev Biol. Autophagy vitalizes the pathogenicity of pathogenic fungi. Molecular dissection of autophagy: two ubiquitin-like systems. Nat Rev Mol Cell Biol. Dynamics and diversity in autophagy mechanisms: lessons from yeast.

Autophagosome formation: core machinery and adaptations. Nat Cell Biol. Atg1 family kinases in autophagy initiation. Cell Mol Life Sci. Membrane recruitment of Aut7p in the autophagy and cytoplasm to vacuole targeting pathways requires Aut1p, Aut2p, and the autophagy conjugation complex. J Cell Biol. Atg4 recycles inappropriately lipidated Atg8 to promote autophagosome biogenesis.

Phosphatidylinositolphosphate clearance plays a key role in autophagosome completion. Curr Biol. Roles of the lipid-binding motifs of Atg18 and Atg21 in the cytoplasm to vacuole targeting pathway and autophagy. J Biol Chem. On the trail of a cereal killer: exploring the biology of Magnaporthe grisea. Annu Rev Microbiol. Pipecolic acid confers systemic immunity by regulating free radicals.

Sci Adv. Protein kinases in plant-pathogenic fungi: conserved regulators of infection. Annu Rev Phytopathol. Plos Genet. Autophagy induced by rapamycin and carbon-starvation have distinct proteome profiles in Aspergillus nidulans. Biotechnol Bioeng. Autophagy in plant pathogenic fungi. Sorting nexin MoVps17 is required for fungal development and plant infection by regulating endosome dynamics in the rice blast fungus. Environ Microbiol.

A HOPS protein, MoVps41, is crucially important for vacuolar morphogenesis, vegetative growth, reproduction and virulence in Magnaporthe oryzae. Front Plant Sci. VPS9 domain-containing proteins are essential for autophagy and endocytosis in Pyricularia oryzae. Autophagy during conidiation, conidial germination and turgor generation in Magnaporthe grisea. Genome-wide functional analysis reveals that infection-associated fungal autophagy is necessary for rice blast disease.

Self-eating to grow and kill: autophagy in filamentous ascomycetes. Appl Microbiol Biotechnol. Autophagosome formation involves cycling of ATG9. Mammalian Atg9 contributes to the post-Golgi transport of lysosomal hydrolases by interacting with adaptor protein FEBS Lett. Sci Rep. The autophagy-related gene BcATG1 is involved in fungal development and pathogenesis in Botrytis cinerea.

Mol Plant Pathol. Genome-wide functional analysis reveals that autophagy is necessary for growth, sporulation, deoxynivalenol production and virulence in Fusarium graminearum. Sci Rep-UK. Analysis of autophagy in Aspergillus oryzae by disruption of Aoatg13, Aoatg4, and Aoatg15 genes. Autophagy promotes survival in aging submerged cultures of the filamentous fungus Aspergillus niger.

Network and role analysis of autophagy in Phytophthora sojae. Microbiol Res. Vesicle trafficking, organelle functions, and unconventional secretion in fungal physiology and pathogenicity. Curr Opin Microbiol. Ubiquitin-like activating enzymes BcAtg3 and BcAtg7 participate in development and pathogenesis of Botrytis cinerea. Curr Genet.

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PLoS One. Autophagy-related protein MoAtg14 is involved in differentiation, development and pathogenicity in the rice blast fungus Magnaporthe oryzae. The cysteine protease MoAtg4 interacts with MoAtg8 and is required for differentiation and pathogenesis in Magnaporthe oryzae. Atgassisted mitophagy in the foot cells is necessary for proper asexual differentiation in Magnaporthe oryzae. Functional analysis of AoAtg11 in selective autophagy in the filamentous fungus Aspergillus oryzae.

Fungal Biol-UK. In the phagosomal system, this is accompanied by the release of hydrolytic enzymes and toxic metabolites into the phagosome and lowering of the phagolysomal pH to aid in pathogen killing. Proteins required for oxidative stress resistance were recently found to be components of the extracellular proteome of H. Expression of genes encoding superoxide dismutase is also induced when P.

In order to neutralize or prevent RNS production, H. In addition, P. Macrophage vaculolar ATPases pump protons into the phagolysosome to lower the pH, however, phagolysosomes containing H. The establishment of thermal homeostasis requires heat shock proteins HSPs to respond to changes in environmental temperature. HSPs function as chaperones to regulate correct protein folding, transport and assembly of protein complexes. Hsf1 from P. Hsp30, Hsp70, Hsp82 and Hsp are highly abundant during the yeast phase of P.

Likewise, hsp60, hsp70 and hsp82 are highly expressed during the hyphal-to-yeast dimorphic switch in H. Studies in T. It should be noted that these studies were conducted in two different T. The expression of hsp70 and its virulence and thermal tolerance was assessed by measuring the proportion of viable cells at increasing temperature increments, in a number of different H.

The results suggested a direct correlation between increased hsp70 expression, increased thermal tolerance and pathogenicity in H. However, this correlation is not observed in P. There have been extensive studies on HSPs in C. Hsp90 in S. Clearly, the role of the heat shock response in morphogenesis and pathogenicity for the dimorphic fungi is patchy and warrants further investigation. Surviving within the macrophage phagolysosome poses many metabolic challenges for intracellular dimorphic pathogens, including a lack of essential trace elements such as iron and zinc reviewed in Schaible and Kaufmann Host cells restrict available iron through sequestration by high-affinity iron-binding proteins such as transferrin and ferritin to prevent intracellular microbial proliferation.

Intracellular yeast growth of H. Recently, proteomic analysis of P. This suggests that P. Under iron-limiting conditions, fungi utilize high-affinity iron uptake systems such as reductive iron assimilation RIA and non-reductive, siderophore-based iron assimilation non-RIA Fig. For example, C. The exception is C. High-affinity iron uptake systems in dimorphic fungi. Most dimorphic fungi utilize both RIA and non-RIA systems to mediate high-affinity iron uptake when bioavailable iron is low, such as within host phagocytes. Expression of the genes required for siderophore biosynthesis, transport and utilization in H.

Mutation of H. Expression of sidA sid1 orthologue , sit1 msf1 orthologue and the gene encoding the bZIP transcription factor hapX is increased during iron deprivation in P. SreB in B. CaM can also activate calmodulin-dependent kinases to elicit responses. Expression of the genes encoding calmodulin and the calcineurin regulatory subunit are induced during the hyphal-to-yeast dimorphic switch in P. Similarly, inhibitors of calmodulin and the calmodulin-dependent kinases in S. Reduction of calmodulin-dependent kinase 1 levels by RNAi inhibited S. It has been known for some time that calcium plays an important role in H.

Large amounts of calcium are essential for H. Deletion of Cbp1, the major yeast-specific calcium-binding protein secreted during H. The addition of exogenous Cbp1 results in increased cellular incorporation of calcium suggesting that Cbp1 may function to provide calcium in low calcium environments.

Bad1 also called WI-1 is a yeast-specific calcium-binding protein which is essential for pathogenicity in B. Genetic manipulation of dimorphic fungal pathogens has been previously limited due to a complete lack of DNA-mediated transformation, poor integration of introduced DNA or high frequencies of non-homologous DNA integration, making the generation of gene deletion or allelic replacement strains difficult.

However, recent advances in genome-wide expression approaches, RNA inhibition and the development of strains containing mutations to increase the frequency of homologous integration have greatly accelerated our understanding of this group of medically relevant pathogens. Recent studies suggest that the core signalling pathways that sense and respond to the host are conserved in dimorphic species.

Of significant interest is the central conserved role of the HHK of the two-component signalling system.


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Drk1 orthologues play conserved roles in regulating not only the dimorphic switch but also a number of traits known to be important for intracellular pathogenic growth. The future characterization of downstream components of this pathway and genome-wide expression analysis in mutants of these components will provide invaluable insight into the processes required for dimorphic switching and survival in the host. Additional pathways involving the pactivated kinases are also likely to impinge on the dimorphic switch and the way temperature and host signals are interpreted by the cell.

It is tempting to speculate that these pathways will culminate in the activation of orthologues of the RYP1—4 transcription factors in the various dimorphic fungi and these transcription factors will regulate not only genes required for the morphological transition but the additional mechanisms used to adapt to the host environment. This would include those required for the onset and extent of sporulation the infectious agent , remodelling the fungal cell wall to avoid immune detection, adapting or neutralizing oxidative and osmotic stress and the physiological response to the host environment.

Despite the emerging, albeit embryonic, convergence of factors that are involved in dimorphic switching across this group of fungi, there will no doubt be differences amongst them owing to their independent evolutionary histories. It is clear that dimorphic switching has polyphyletic origins but is one that rests on a core set of existing attributes that have been co-opted.

Future investigations of the mechanisms by which dimorphic fungal pathogens sense and respond to the host environment will provide important insights into fungal pathogenesis and host—pathogen interactions. Oxford University Press is a department of the University of Oxford. It furthers the University's objective of excellence in research, scholarship, and education by publishing worldwide.

Sign In or Create an Account. Sign In. Advanced Search. Article Navigation. Close mobile search navigation Article Navigation. Volume Article Contents. Fungal dimorphism: the switch from hyphae to yeast is a specialized morphogenetic adaptation allowing colonization of a host Kylie J. Oxford Academic. Google Scholar. Alex Andrianopoulos. Article history.

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  • View large Download slide. Table 1. Repression of vegetative spore production in liquid conidia.

    Linking fungal morphogenesis with virulence

    Regulates the expression of phase specific genes. Germination of conidia in macrophages. Cellular division of conidiophores and macrophage-engulfed yeast cells. Yeast-to-hyphal dimorphic switch. View Large. Cdc42p controls yeast-cell shape and virulence of Paracoccidioides brasiliensis. Search ADS.

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    Genes potentially relevant in the parasitic phase of the fungal pathogen Paracoccidioides brasiliensis. The abaA homologue of Penicillium marneffei participates in two developmental programmes: conidiation and dimorphic growth. A pactivated kinase is required for conidial germination in Penicillium marneffei. The CDC42 Homolog of the dimorphic fungus Penicillium marneffei is required for correct cell polarization during growth but not development.

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    Calcium binding by the essential virulence factor BAD-1 of Blastomyces dermatitidis. Structure and function of a fungal adhesion that binds heparin and mimics thrombospondin-1 by blocking T cell activation and effector function. Targeted gene disruption reveals an adhesin indispensable for pathogenicity of Blastomyces dermatitidis. Tools for high effeciency genetic manipulation of the human pathogen Penicillium marneffei. HgrA is necessary and sufficient to drive hyphal growth in the dimorphic pathogen Penicillium marneffei.

    A conserved transcriptional regulator governs fungal morphology in widely diverged species. Evolution of the primary immune response to Histoplasma capsulatum in murine lung. Evidence for the role of calcineurin in morphogenesis and calcium homeostasis during mycelium-to-yeast dimorphism of Paracoccidioides brasiliensis.

    Inhibitory effect of deferoxamine or macrophage activation on transformation of Paracoccidioides brasiliensis conidia ingested by macrophages: reversal by holotransferrin. The fungal type II myosin in Penicillium marneffei , MyoB, is essential for chitin deposition at nascent septation sites but not actin localization.

    Heat shock 70 gene is differentially expressed in Histoplasma capsulatum strains with different levels of thermotolerance and pathogenicity. Whole-genome analysis of two-component signal transduction genes in fungal pathogens. Response to environmental stresses, cell-wall integrity, and virulence are orchestrated through the calcineurin pathway in Ustilago hordei. Protein profiling of the dimorphic, pathogenic fungus.

    Penicillium marneffei. Spectroscopic and kinetic studies of Nor1, a cytochrome P nitric oxide reductase from the fungal pathogen Histoplasma capsulatum. The cAMP pathway is important for controlling the morphological switch to the pathogenic yeast form of Paracoccidioides brasiliensis. Involvement of distinct G-proteins, Gpa2 and Ras, in glucose- and intracellular acidification-induced cAMP signalling in the yeast Saccharomyces cerevisiae. Superoxide dismutase influences the virulence of Cryptococcus neoformans by affecting growth within macrophages. Da Silva. Differential expression of an hsp70 gene during transition from the mycelial to the infective yeast form of the human pathogenic fungus Paracoccidioides brasiliensis.

    De Carvalho.

    Functional and genetic characterization of calmodulin from the dimorphic and pathogenic fungus Paracoccidioides brasiliensis. Inhibitory effect of deferoxamine on Paracoccidioides brasiliensis survival in human monocytes: reversal by holotransferrin not by apotransferrin. The yeast-phase virulence requirement for alpha-glucan synthase differs among Histoplasma capsulatum chemotypes. Transcriptional profile of ras1 and ras2 and the potential role of farnesylation in the dimorphism of the human pathogen Paracoccidioides brasiliensis.

    Flavia Popi. GP43 from Paracoccidioides brasiliensis inhibits macrophage functions. An evasion mechanism of the fungus. A fungus-specific ras homolog contributes to the hyphal growth and virulence of Aspergillus fumigatus. Collaborative induction of inflammatory responses by dectin-1 and Toll-like receptor 2. Expressed sequence tag analysis of the human pathogen Paracoccidioides brasiliensis yeast phase: identification of putative homologues of Candida albicans virulence and pathogenicity genes.

    Coccidioides releases a soluble factor that suppresses nitric oxide production by murine primary macrophages. Role of iron in the nitric oxide-mediated fungicidal mechanism of IFN-gamma-activated murine macrophages against Paracoccidioides brasiliensis conidia. Histoplasma capsulatum utilizes siderophores for intracellular iron acquisition in macrophages. The Histoplasma capsulatum vacuolar ATPase is required for iron homeostasis, intracellular replication in macrophages and virulence in a murine model of histoplasmosis. Altered expression of surface alpha-1,3-glucan in genetically related strains of Blastomyces dermatitidis that differ in virulence.

    Definition of the extracellular proteome of pathogenic-phase Histoplasma capsulatum. Bistable expression of WOR1 , a master regulator of white-opaque switching in Candida albicans. Histoplasma requires SID1 , a member of an iron-regulated siderophore gene cluster, for host colonization. The 3-hydroxy-methylglutaryl coenzyme A lyase HCL1 is required for macrophage colonization by human fungal pathogen Histoplasma capsulatum. HapX positively and negatively regulates the transcriptional response to iron deprivation in Cryptococcus neoformans. Iron regulation of the major virulence factors in the AIDS-associated pathogen Cryptococcus neoformans.

    Induction of stress protein synthesis in Histoplasma capsulatum by heat, low pH and hydrogen peroxide. Fungi pathogenic to humans: molecular bases of virulence of Candida albicans, Cryptococcus neoformans and Aspergillus fumigatus. Molecular cloning and sequence analysis of yps-3 , a yeast-phase-specific gene in the dimorphic fungal pathogen Histoplasma capsulatum. Development and application of a green fluorescent protein sentinel system for identification of RNA interference in Blastomyces dermatitidis illuminates the role of septin in morphogenesis and sporulation.

    Cloning, characterization and differential expression of an hsp70 gene from the pathogenic dimorphic fungus, Penicillium marneffei. Expression of inducible nitric oxide synthase by stimulated macrophages correlates with their antihistoplasma activity. Iron limitation and the gamma interferon-mediated antihistoplasma state of murine macrophages.

    Ras links cellular morphogenesis to virulence by regulation of the MAP kinase and cAMP signalling pathways in the pathogenic fungus Candida albicans. A yeast mitogen-activated protein kinase homolog Mpk1p mediates signalling by protein kinase C. Calcineurin plays key roles in the dimorphic transition and virulence of the human pathogenic zygomycete Mucor circinelloides. Co-regulation of pathogenesis with dimorphism and phenotypic switching in Candida albicans , a commensal and a pathogen. An alpha- 1,4 -amylase is essential for alpha- 1,3 -glucan production and virulence in Histoplasma capsulatum.

    Identification of genes preferentially expressed in the pathogenic yeast phase of Paracoccidioides brasiliensis , using suppression subtraction hybridization and differential macroarray analysis. Molecular cloning and expression of hsp82 gene of the dimorphic pathogenic fungus Histoplasma capsulatum. Recognition and blocking of innate immunity cells by Candida albicans chitin. A two-component histidine kinase of the rice blast fungus is involved in osmotic stress response and fungicide action. Chloroquine induces human macrophage killing of Histoplasma capsulatum by limiting the availability of intracellular iron and is therapeutic in a murine model of histoplasmosis.

    Recent advances in our understanding of the environmental, epidemiological, immunological, and clinical dimensions of coccidioidomycosis. Temperature-induced switch to the pathogenic yeast form of Histoplasma capsulatum requires Ryp1, a conserved transcriptional regulator.

    A novel regulator couples sporogenesis and trehalose biogenesis in Aspergillus nidulans. Role of the heat shock transcription factor, Hsf1, in a major fungal pathogen that is obligately associated with warm-blooded animals. Transcriptome analysis of Paracoccidioides brasiliensis cells undergoing mycelium-to-yeast transition. Characterization of mutations in the two-component histidine kinase gene that confer fludioxonil resistance and osmotic sensitivity in the os-1 mutants of Neurospora crassa.

    Characterisation of the heat shock factor of the human thermodimorphic pathogen Paracoccidioides lutzii. Proteomic analysis reveals that iron availability alters the metabolic status of the pathogenic fungus Paracoccidioides brasiliensis. Cell-type-specific transcriptional profiles of the dimorphic pathogen Penicillium marneffei reflect distinct reproductive, morphological, and environmental demands.

    Interaction of the heterotrimeric G protein alpha subunit SSG-1 of Sporothrix schenckii with proteins related to stress response and fungal pathogenicity using a yeast two-hybrid assay.