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Infection-Associated Nuclear Degeneration in the Rice Blast Fungus Magnaporthe oryzae Requires Non-Selective Macro-Autophagy

He, Min, Kershaw, Michael J., Soanes, Darren M., Xia, Yuxian, Talbot, Nicholas J.·2012·PLoS ONE
DOI 10.1371/journal.pone.0033270PMC PMC3308974
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Figure 1 Nuclear degeneration occurs during appressorium development in M. oryzae. (A). Upper panel: time course live cell imaging experiment showing nuclear division and nuclear degeneration during appressorium development in M. oryzae. Guy11 conidia expressing H1:RFP were examined by epifluorescence microscopy at indicated time points during appressorium development. Lower panel: bar charts showing the percentage of spore germlings in Guy11 containing between 0 and 4 nuclei (mean ± SD, n>100, triple replications) during a timecourse of appressorium development. Scale bar = 10 µm.
Figure 1 Nuclear degeneration occurs during appressorium development in M. oryzae. (A). Upper panel: time course live cell imaging experiment showing nuclear division and nuclear degeneration during appressorium development in M. oryzae. Guy11 conidia expressing H1:RFP were examined by epifluorescence microscopy at indicated time points during appressorium development. Lower panel: bar charts showing the percentage of spore germlings in Guy11 containing between 0 and 4 nuclei (mean ± SD, n>100, triple replications) during a timecourse of appressorium development. Scale bar = 10 µm.CC BY · PubMed Central
Figure 2 Bioinformatic identification of components of the S. cerevisiae PMN pathway in M. oryzae. (A) Alignment of acylation modification amino acids in the N-terminus of Vac8p from M. oryzae and S. cerevisiae. Triangles indicate putative myristoylation modification site (Gly) and stars indicate palmitoylation modification sites (Cys) that have been shown to be important for localisation and function of Vac8p in S. cerevisiae. Similar acylation modification sites are present in MoVac8p. (B) ARM repeat organization in MoVac8p is distinct from that of S. cerevisiae Vac8p. Upper panel: alignment of 9 ARM repeats from M. oryzae Vac8p. A dot indicates a space. Lower panel: Comparison of distribution of the ARM repeats in Vac8p between M. oryzae and S. cerevisiae. Scale bar indicate 100 amino acids. (C) MoTsc13p shares the same topology of six tramsmembrane domains as S. cerevisiae Tsc13p.
Figure 2 Bioinformatic identification of components of the S. cerevisiae PMN pathway in M. oryzae. (A) Alignment of acylation modification amino acids in the N-terminus of Vac8p from M. oryzae and S. cerevisiae. Triangles indicate putative myristoylation modification site (Gly) and stars indicate palmitoylation modification sites (Cys) that have been shown to be important for localisation and function of Vac8p in S. cerevisiae. Similar acylation modification sites are present in MoVac8p. (B) ARM repeat organization in MoVac8p is distinct from that of S. cerevisiae Vac8p. Upper panel: alignment of 9 ARM repeats from M. oryzae Vac8p. A dot indicates a space. Lower panel: Comparison of distribution of the ARM repeats in Vac8p between M. oryzae and S. cerevisiae. Scale bar indicate 100 amino acids. (C) MoTsc13p shares the same topology of six tramsmembrane domains as S. cerevisiae Tsc13p.CC BY · PubMed Central
Figure 3 Sub-cellular localisation of MoVac8p and MoTsc13p in Magnaporthe oryzae. (A) MoVac8p-GFP is localised at the vacuolar membrane in both conidia and appressoria. FM4–64 was used to stain vacuoles and endosomes of Guy11, expressing MoVAC8:GFP. Conidia were collected and resuspended in 50 µl of CM with 7.5 µM FM4–64. Appressorium development was observed on coverslips at indicated time points. (B) MoVac8p-GFP is localised on the vacuolar membrane in penetration pegs and invasive hyphae. Penetration of onion epidermis was examined at indicated time points. (C) Tsc13p-GFP is associated with of perinuclear and peripheral ER in both conidium and appressorium. (D) Tsc13p-GFP is associated with perinuclear and peripheral ER in penetration pegs and invasive hyphae. Images were taken from onion epidermis infected with Guy11 expressing MoTSC13:GFP at 24 hpi. (E) MoTsc13p-GFP is localised at the perinuclear and peripheral ER in hyphae grown in CM. DAPI was used to stain nuclei of Guy11 expressing MoTSC13:GFP. Scale bar = 10 µm.
Figure 3 Sub-cellular localisation of MoVac8p and MoTsc13p in Magnaporthe oryzae. (A) MoVac8p-GFP is localised at the vacuolar membrane in both conidia and appressoria. FM4–64 was used to stain vacuoles and endosomes of Guy11, expressing MoVAC8:GFP. Conidia were collected and resuspended in 50 µl of CM with 7.5 µM FM4–64. Appressorium development was observed on coverslips at indicated time points. (B) MoVac8p-GFP is localised on the vacuolar membrane in penetration pegs and invasive hyphae. Penetration of onion epidermis was examined at indicated time points. (C) Tsc13p-GFP is associated with of perinuclear and peripheral ER in both conidium and appressorium. (D) Tsc13p-GFP is associated with perinuclear and peripheral ER in penetration pegs and invasive hyphae. Images were taken from onion epidermis infected with Guy11 expressing MoTSC13:GFP at 24 hpi. (E) MoTsc13p-GFP is localised at the perinuclear and peripheral ER in hyphae grown in CM. DAPI was used to stain nuclei of Guy11 expressing MoTSC13:GFP. Scale bar = 10 µm.CC BY · PubMed Central
Figure 4 MoTSC13 is functionally equivalent to S. cerevisiae TSC13, while MoVAC8 only partially substitutes for VAC8. (A) MoTSC13 complemented the temperature-sensitive lethality of the yeast strain TDY2058 (double mutant tsc13-1 Δelo). Yeast tsc13-1 Δelo mutants were transformed either with empty vector or a plasmid expressing MoTSC13 cDNA under control of the galactose-inducible GAL1 promoter. Cells were grown in YPDA overnight, normalized to and subjected to 10-fold serial dilutions, spotted onto SD+Gal plates and incubated at 26°C, 30°C or 37°C for 3 days prior to photographing. The experiments were carried out in triplicate, examining two independent yeast transformants. (B) MoVAC8 complemented the caffeine sensitivity of yeast strain BY4741 vac8Δ::KANMX4. Yeast vac8Δ::KANMX4 mutants were transformed with empty vector or a plasmid expressing MoVAC8 cDNA under the control of the GAL1 promoter. Cells were grown in YPDA overnight, normalized and subjected to 10-fold serial dilutions, spotted onto SD+Gal plates containing either 0.05% or 0.1% caffeine, and incubated at 26°C for the indicated period of time. The experiments were carried out in triplicate, examining two independent yeast transformants. (C) MoVAC8 does not complement vacuole morphology and vacuole inheritance defects of yeast mutant vac8Δ::KANMX4. FM4–64 was used to stain cells of S. cerevisiae, vac8Δ::KANMX4 and vac8Δ::KANMX4 strain, expressing MoVAC8 by pulse-chase labelling. Arrows indicates presence (b) or absence (d, f, h, j) of segregating vacuoles. (D) MoVAC8 failed to complement vacuole inheritance defects of yeast mutant vac8Δ::KANMX4 during budding. Pulse-chase labelled S. cerevisiae cells by FM4–64 were counted for the proportion of daughter cells carrying vacuoles inherited from the mother cell during budding. (N indicates the total number of cells counted). (E) MoTSC13p localises to the perinuclear and peripheral ER membrane in S. cerevisiae. yEGFP tagged MoTSC13p was expressed in yeast strain TDY2058 under control of the GAL1 promoter in plasmid pYES2. Cells were stained with DAPI to visualise nuclei. (F) MoVAC8p failed to accumulate at the vacuolar membrane in S. cerevisiae. yEGFP tagged MoVAC8p was expressed in yeast strain vac8Δ::KANMX4 under control of GAL1p promoter in plasmid pYES2.
Figure 4 MoTSC13 is functionally equivalent to S. cerevisiae TSC13, while MoVAC8 only partially substitutes for VAC8. (A) MoTSC13 complemented the temperature-sensitive lethality of the yeast strain TDY2058 (double mutant tsc13-1 Δelo). Yeast tsc13-1 Δelo mutants were transformed either with empty vector or a plasmid expressing MoTSC13 cDNA under control of the galactose-inducible GAL1 promoter. Cells were grown in YPDA overnight, normalized to and subjected to 10-fold serial dilutions, spotted onto SD+Gal plates and incubated at 26°C, 30°C or 37°C for 3 days prior to photographing. The experiments were carried out in triplicate, examining two independent yeast transformants. (B) MoVAC8 complemented the caffeine sensitivity of yeast strain BY4741 vac8Δ::KANMX4. Yeast vac8Δ::KANMX4 mutants were transformed with empty vector or a plasmid expressing MoVAC8 cDNA under the control of the GAL1 promoter. Cells were grown in YPDA overnight, normalized and subjected to 10-fold serial dilutions, spotted onto SD+Gal plates containing either 0.05% or 0.1% caffeine, and incubated at 26°C for the indicated period of time. The experiments were carried out in triplicate, examining two independent yeast transformants. (C) MoVAC8 does not complement vacuole morphology and vacuole inheritance defects of yeast mutant vac8Δ::KANMX4. FM4–64 was used to stain cells of S. cerevisiae, vac8Δ::KANMX4 and vac8Δ::KANMX4 strain, expressing MoVAC8 by pulse-chase labelling. Arrows indicates presence (b) or absence (d, f, h, j) of segregating vacuoles. (D) MoVAC8 failed to complement vacuole inheritance defects of yeast mutant vac8Δ::KANMX4 during budding. Pulse-chase labelled S. cerevisiae cells by FM4–64 were counted for the proportion of daughter cells carrying vacuoles inherited from the mother cell during budding. (N indicates the total number of cells counted). (E) MoTSC13p localises to the perinuclear and peripheral ER membrane in S. cerevisiae. yEGFP tagged MoTSC13p was expressed in yeast strain TDY2058 under control of the GAL1 promoter in plasmid pYES2. Cells were stained with DAPI to visualise nuclei. (F) MoVAC8p failed to accumulate at the vacuolar membrane in S. cerevisiae. yEGFP tagged MoVAC8p was expressed in yeast strain vac8Δ::KANMX4 under control of GAL1p promoter in plasmid pYES2.CC BY · PubMed Central
Figure 5 MoVAC8 and MoTSC13 are not required for nuclear degeneration in M. oryzae. (A) Nuclear degeneration during appressorium development occurs independently of MoVAC8. Upper panel: time course live cell images showing nuclear division and nuclear degeneration during appressorium development in M. oryzae ΔMovac8 deletion mutants. ΔMovac8 expressing H1:RFP were examined by epifluorescence microscopy at indicated time points during appressorium development. Lower panel: time series of bar charts showing the percentage of spore germlings of ΔMovac8 containing between 0 and 4 nuclei (mean ± SD, n>100, triple replications). (B) Nuclear degeneration during appressorium development occurs independently of MoTSC13. Upper panel: time course live cell images showing nuclear division and nuclear degeneration during appressorium development in M. oryzae MoTSC13 deletion mutants. ΔMotsc13 expressing H1:RFP were examined by epifluorescence microscopy at indicated time points during appressorium development. Lower panel: time series of bar charts showing the percentage of spores in ΔMotsc13 containing between 0 and 4 nuclei (mean ± SD, n>100, triple replications). (C) Micrographs showing abnormal conidia of ΔMotsc13 containing two nuclei. Scale bar = 10 µm.
Figure 5 MoVAC8 and MoTSC13 are not required for nuclear degeneration in M. oryzae. (A) Nuclear degeneration during appressorium development occurs independently of MoVAC8. Upper panel: time course live cell images showing nuclear division and nuclear degeneration during appressorium development in M. oryzae ΔMovac8 deletion mutants. ΔMovac8 expressing H1:RFP were examined by epifluorescence microscopy at indicated time points during appressorium development. Lower panel: time series of bar charts showing the percentage of spore germlings of ΔMovac8 containing between 0 and 4 nuclei (mean ± SD, n>100, triple replications). (B) Nuclear degeneration during appressorium development occurs independently of MoTSC13. Upper panel: time course live cell images showing nuclear division and nuclear degeneration during appressorium development in M. oryzae MoTSC13 deletion mutants. ΔMotsc13 expressing H1:RFP were examined by epifluorescence microscopy at indicated time points during appressorium development. Lower panel: time series of bar charts showing the percentage of spores in ΔMotsc13 containing between 0 and 4 nuclei (mean ± SD, n>100, triple replications). (C) Micrographs showing abnormal conidia of ΔMotsc13 containing two nuclei. Scale bar = 10 µm.CC BY · PubMed Central
Figure 6 Nuclear-vacuolar (NV) junctions are not present in M. oryzae during appressorium development or starvation stress. (A) Time course live cell imaging of appressorium development in M. oryzae expressing both MoVAC:GFP and H1:RFP. (B) Micrographs of hyphae of M. oryzae expressing both MoVAC:GFP and H1:RFP. M. oryzae was grown in nutrient-rich medium (CM) or nitrogen stress minimal medium (MM-N) for the indicated period of times, and hyphae collected for epifluorescence microscopy. Hyphae cultured in CM for 40 h were washed with distilled water, before being transferred into MM-N. (C) MoTsc13p is associated with perinuclear and peripheral ER membrane in invasive hyphae. M. oryzae expressing both MoTSC13:GFP and H1:RFP was inoculated onto rice sheath epidermis for 36 h before epifluorescence microscopy. (D) Distribution of MoTsc13p-GFP is not affected by environmental nutritional status. Hyphae of M. oryzae expressing both MoTSC13:GFP and H1:RFP were grown in CM or MM-N for epifluorescence microscopy. Pictures shown are representatives of at least 30 different hyphae cell compartments analyzed for each time point. Scale bar = 10 µm.
Figure 6 Nuclear-vacuolar (NV) junctions are not present in M. oryzae during appressorium development or starvation stress. (A) Time course live cell imaging of appressorium development in M. oryzae expressing both MoVAC:GFP and H1:RFP. (B) Micrographs of hyphae of M. oryzae expressing both MoVAC:GFP and H1:RFP. M. oryzae was grown in nutrient-rich medium (CM) or nitrogen stress minimal medium (MM-N) for the indicated period of times, and hyphae collected for epifluorescence microscopy. Hyphae cultured in CM for 40 h were washed with distilled water, before being transferred into MM-N. (C) MoTsc13p is associated with perinuclear and peripheral ER membrane in invasive hyphae. M. oryzae expressing both MoTSC13:GFP and H1:RFP was inoculated onto rice sheath epidermis for 36 h before epifluorescence microscopy. (D) Distribution of MoTsc13p-GFP is not affected by environmental nutritional status. Hyphae of M. oryzae expressing both MoTSC13:GFP and H1:RFP were grown in CM or MM-N for epifluorescence microscopy. Pictures shown are representatives of at least 30 different hyphae cell compartments analyzed for each time point. Scale bar = 10 µm.CC BY · PubMed Central
Figure 7 The N-terminus of MoVAC8p contains a SH4 domain. (A) SH4:GFP fusion proteins are anchored at the vacuole, septa and the plasma membrane in both conidia and appressoria. The first 21 amino acid residues of MoVAC8p were fused into the N-terminus of GFP to produce SH4:GFP and subcellular localisation of the GFP fusion analysed by epifluorescence microscopy. Guy11 conidia expressing SH4:GFP fusion proteins were stained with FM4–64 and allowed to germinate and undergo appressorium development. SH4:GFP fusions colocalise with the FM4–64-stained vacuole, septa and plasma membrane. (B) SH4:GFP fusion proteins associate with the vacuole, septa and the plasma membrane in penetration pegs and invasive hyphae. Penetration of onion epidermis was examined at indicated time points and Calcofluor White (CFW) used to stain the cell wall. SH4:GFP fusion proteins colocalise with the vacuole (as seen in the bright field image) and CFW-stained cell wall. (C) SH4:GFP fusion proteins were targeted to the vacuole, septa and the plasma membrane in vegetative hyphae. Vegetative hyphae expressing SH4:GFP fusion proteins were grown in CM for 24 h, and 200 µl of the cultures incubated with 7.5 µM FM4–64 at 26°C for 1 h, followed by CFW staining. In vegetative hyphae, SH4:GFP fusion proteins also colocalise with FM4–64- stained vacuoles and CFW-stained septa and cell walls. Scale bar = 10 µm.
Figure 7 The N-terminus of MoVAC8p contains a SH4 domain. (A) SH4:GFP fusion proteins are anchored at the vacuole, septa and the plasma membrane in both conidia and appressoria. The first 21 amino acid residues of MoVAC8p were fused into the N-terminus of GFP to produce SH4:GFP and subcellular localisation of the GFP fusion analysed by epifluorescence microscopy. Guy11 conidia expressing SH4:GFP fusion proteins were stained with FM4–64 and allowed to germinate and undergo appressorium development. SH4:GFP fusions colocalise with the FM4–64-stained vacuole, septa and plasma membrane. (B) SH4:GFP fusion proteins associate with the vacuole, septa and the plasma membrane in penetration pegs and invasive hyphae. Penetration of onion epidermis was examined at indicated time points and Calcofluor White (CFW) used to stain the cell wall. SH4:GFP fusion proteins colocalise with the vacuole (as seen in the bright field image) and CFW-stained cell wall. (C) SH4:GFP fusion proteins were targeted to the vacuole, septa and the plasma membrane in vegetative hyphae. Vegetative hyphae expressing SH4:GFP fusion proteins were grown in CM for 24 h, and 200 µl of the cultures incubated with 7.5 µM FM4–64 at 26°C for 1 h, followed by CFW staining. In vegetative hyphae, SH4:GFP fusion proteins also colocalise with FM4–64- stained vacuoles and CFW-stained septa and cell walls. Scale bar = 10 µm.CC BY · PubMed Central
Figure 8 Phenotypic analysis of ΔMovac8 mutants. (A) MoVAC8 is not involved in vacuole movement from the conidium into the appressorium. FM4–64 was used to stain endosomes and vacuoles in conidia to visualize movement of vacuoles during appressorium development. (B) Rice blast infection assay of ΔMovac8 mutants on rice leaves. The virulence of ΔMovac8 is similar to that of strain Guy11. Lesion density represents the lesion number per 5 cm of infected leaf area on rice CO-39 seedlings (n>40).
Figure 8 Phenotypic analysis of ΔMovac8 mutants. (A) MoVAC8 is not involved in vacuole movement from the conidium into the appressorium. FM4–64 was used to stain endosomes and vacuoles in conidia to visualize movement of vacuoles during appressorium development. (B) Rice blast infection assay of ΔMovac8 mutants on rice leaves. The virulence of ΔMovac8 is similar to that of strain Guy11. Lesion density represents the lesion number per 5 cm of infected leaf area on rice CO-39 seedlings (n>40).CC BY · PubMed Central
Figure 9 MoTSC13 is required for full virulence of M. oryzae. (A) Targeted deletion of MoTSC13 results in reduced pathogenicity on rice CO-39. Lesion density and size was severely reduced in ΔMotsc13 rice infections compared to Guy11. Full pathogenicity of ΔMotsc13 mutants was restored by introduction of MoTSC13:GFP (Compl.). Lesion density represents the lesion number per 5 cm of infected leaf area (n>40). (B) MoTSC13 is necessary for penetration peg formation and invasive hyphae expansion during in planta growth. Scale bar = 10 µm.
Figure 9 MoTSC13 is required for full virulence of M. oryzae. (A) Targeted deletion of MoTSC13 results in reduced pathogenicity on rice CO-39. Lesion density and size was severely reduced in ΔMotsc13 rice infections compared to Guy11. Full pathogenicity of ΔMotsc13 mutants was restored by introduction of MoTSC13:GFP (Compl.). Lesion density represents the lesion number per 5 cm of infected leaf area (n>40). (B) MoTSC13 is necessary for penetration peg formation and invasive hyphae expansion during in planta growth. Scale bar = 10 µm.CC BY · PubMed Central
Figure 10 Macroautophagy is necessary for nuclear degeneration during appressorium development in M. oryzae. (A) The Macroautophagy gene MoATG1 is required for nuclear degeneration. Upper panel: time course live cell images showing nuclear division and nuclear degeneration during appressorium development in a M. oryzae ΔMoatg1 mutant. ΔMoatg1 conidia expressing H1:RFP were examined by epifluorescence microscopy at indicated time points. Lower panel: time series of bar charts showing the percentage of spores in ΔMoatg1 containing 0 to 4 nuclei (mean ± SD, n>100, triple replications). (B) The Macroautophagy core gene MoATG4 is required for nuclear degeneration. Upper panel: time course live cell images showing nuclear division and nuclear degeneration during appressorium development in M. oryzae ΔMoatg4 mutant. ΔMoatg4 conidia expressing H1:RFP were examined by epifluorescence microscopy at indicated time points during appressorium development. Lower panel: time series of bar charts showing the percentage of spores in ΔMoatg4 containing 0 to 4 nuclei (mean±SD, n>100, triple replications). Scale bar = 10 µm.
Figure 10 Macroautophagy is necessary for nuclear degeneration during appressorium development in M. oryzae. (A) The Macroautophagy gene MoATG1 is required for nuclear degeneration. Upper panel: time course live cell images showing nuclear division and nuclear degeneration during appressorium development in a M. oryzae ΔMoatg1 mutant. ΔMoatg1 conidia expressing H1:RFP were examined by epifluorescence microscopy at indicated time points. Lower panel: time series of bar charts showing the percentage of spores in ΔMoatg1 containing 0 to 4 nuclei (mean ± SD, n>100, triple replications). (B) The Macroautophagy core gene MoATG4 is required for nuclear degeneration. Upper panel: time course live cell images showing nuclear division and nuclear degeneration during appressorium development in M. oryzae ΔMoatg4 mutant. ΔMoatg4 conidia expressing H1:RFP were examined by epifluorescence microscopy at indicated time points during appressorium development. Lower panel: time series of bar charts showing the percentage of spores in ΔMoatg4 containing 0 to 4 nuclei (mean±SD, n>100, triple replications). Scale bar = 10 µm.CC BY · PubMed Central

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Cited by

Sorted by citations

Metadata

Authors
He, M., Kershaw, M. J., Soanes, D. M., Xia, Y., & Talbot, N. J.
Venue
PLoS ONE
Publisher
Public Library of Science (PLoS)
Published
2012-03-20
Volume
7
Issue
3
Pages
e33270
ISSN
1932-6203
DOI
10.1371/journal.pone.0033270
PMC
PMC3308974
Cited by
40
References
0
Language
en
Licence
creativecommons.org/licenses/by/4.0/ (unspecified)

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