Plant SYP12 syntaxins mediate an evolutionarily conserved general immunity to filamentous pathogens
- University of Copenhagen, Faculty of Science, CPSC, Department of Plant and Environmental Sciences, Denmark
- University of Paris-Saclay, INRAE, UR BIOGER, France
Figures
Figure 1 with 5 supplements
PEN1/SYP122 are required for papilla and encasement responses to Bgh.
(A, B) Spontaneous callose depositions in leaves of 3-week-old plants. (C–G) Accumulation of callose in response to Bgh attack at appressoria (arrows) and primary germ tube (arrowheads) in (C, D), …
Figure 1—figure supplement 1
Pre- and postinvasive immunity.
(A) Attack by nonadapted filamentous pathogens such as Bgh on Arabidopsis is met by a localized apposition (papilla) formed between the plant cell wall (CW) and the plasma membrane (PM), containing …
Figure 1—video 1
Z-stack (callose and bright-field overlay) of successful penetration by Bgh in Col-0.
Figure 1—video 2
Z-stack (callose and bright-field overlay) of successful penetration by Bgh in pen1 syp122.
Figure 1—video 3
Z-stack (callose and bright-field overlay) of successful penetration by G. orontii in Col-0.
Figure 1—video 4
Z-stack (callose and bright-field overlay) of successful penetration by G. orontii in pen1 syp122.
Figure 2 with 2 supplements
PEN1/SYP122 are required for accumulation of TET8-GFP in response to penetration by Bgh.
(A–D) Localization of TET8-GFP in (A, C) resting epidermal cells and in (B, D) response to successful penetration by Bgh (stained with propidium iodide [PI]) and initiation of the intracellular …
Figure 2—video 1
Z-stack (GFP and propidium iodide overlay) of successful penetration by Bgh in Col-0.
Figure 2—video 2
Z-stack (GFP and propidium iodide overlay) of successful penetration by Bgh in pen1 syp122.
Figure 3 with 2 supplements
PEN1/SYP122 are required for papilla responses toward Bgh.
(A, B, D, E) Accumulation of callose (A, B) or H2O2 (D, E) in response to Bgh attack (arrows) at nonpenetrated attack sites. Bars = 10 µm. (C, F) Frequency of papillae in response to Bgh in …
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Figure 3—source data 1
Source data for the graphs in Figure 3C and F.
- https://cdn.elifesciences.org/articles/73487/elife-73487-fig3-data1-v2.xlsx
Figure 3—figure supplement 1
Loss of FMO1 attenuates pen1 syp122 autoimmunity.
(A) Plants at 4 weeks, showing the growth phenotypes of the mutant lines used in these studies. (B) Relative transcript levels of PR1 in 4-week-old plants. Values are mean ± SD (n = 3). ***p<0.001, …
Figure 3—figure supplement 2
PEN1/SYP122 are required for papilla responses to Bgh.
(A–D) Accumulation of callose in response to Bgh attack at nonpenetrated (arrowheads) and penetrated (arrows) attack sites. Bars = 20 µm.
Figure 4 with 10 supplements
PEN1/SYP122 are required for encasement responses toward Bgh.
(A, B, D) Accumulation of callose (A, B) or H2O2 (D) in response to Bgh attack (arrows) at penetrated attack sites. Open arrows point to the developing intracellular pathogenic structure (IPS). Bars …
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Figure 4—source data 1
Source data for the graphs in Figure 4C, E and F.
- https://cdn.elifesciences.org/articles/73487/elife-73487-fig4-data1-v2.xlsx
Figure 4—figure supplement 1
PEN1/SYP122 are required for encasement responses to Bgh.
(A–D) Accumulation of callose in response to Bgh attack at nonpenetrated (arrowheads) and penetrated (arrows) attack sites. Open arrows point to the developing intracellular pathogenic structure …
Figure 4—figure supplement 2
PEN1/SYP122 are required for papilla and encasement responses to Bgh.
(A–F) Accumulation of callose in response to (A, B) G. orontii and (C–F) Bgh (48 hr) attack at (C, D) nonpenetrated and (A, B, E, F) penetrated attack sites (arrows). Open arrows point to the …
Figure 4—video 1
Z-stack (callose and bright-field overlay) of successful penetration by G. orontii in fmo1.
Figure 4—video 2
Z-stack (callose and bright-field overlay) of successful penetration by G. orontii in fmo1 pen1 syp122.
Figure 4—video 3
Z-stack (callose and bright-field overlay) of successful penetration by G. orontii in pad4 sid2 pen1 syp122.
Figure 4—video 4
Z-stack (callose and bright-field overlay) of successful penetration by G. orontii in amsh3 pen1 syp122.
Figure 4—video 5
Z-stack (callose and bright-field overlay) of successful penetration by Bgh in fmo1.
Figure 4—video 6
Z-stack (callose and bright-field overlay) of successful penetration by Bgh in fmo1 pen1 syp122.
Figure 4—video 7
Z-stack (callose and bright-field overlay) of successful penetration by Bgh in pad4 sid2 pen1 syp122.
Figure 4—video 8
Z-stack (callose and bright-field overlay) of successful penetration by Bgh in amsh3 pen1 syp122.
Figure 5 with 1 supplement
PEN1/SYP122 are required for preinvasive immunity toward C. destructivum.
(A, B, D, E) Accumulation of callose in response to attack by melanized C. destructivum appressoria (arrows) at (A, B) nonpenetrated and (D, E) penetrated attack sites. Open arrows point to the …
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Figure 5—source data 1
Source data for the graphs in Figure 5C and F.
- https://cdn.elifesciences.org/articles/73487/elife-73487-fig5-data1-v2.xlsx
Figure 5—figure supplement 1
PEN1/SYP122 are required for preinvasive immunity toward C. destructivum.
(A–C) Localization of GFP-PEN1 (A), GFP-SYP122 (B), and TET8-GFP (C) in response to attack by C. destructivum. (D, E) Accumulation of callose in response to attack by C. destructivum in (D) …
Figure 6 with 1 supplement
PEN1/SYP122 are required for preinvasive immunity toward P. infestans.
(A, B, D, E) Accumulation of callose in response to P. infestans attack (arrows) at (A, B) nonpenetrated and (D, E) penetrated attack sites. Open arrows point to the developing intracellular …
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Figure 6—source data 1
Source data for the graphs in Figure 6C and F.
- https://cdn.elifesciences.org/articles/73487/elife-73487-fig6-data1-v2.xlsx
Figure 6—figure supplement 1
PEN1/SYP122 are required for preinvasive immunity toward P. infestans.
(A–C) Localization of GFP-PEN1 (A), GFP-SYP122 (B), and TET8-GFP (C) in response to attack by P. infestans. (D) Frequency of penetration by P. infestans. Bars = 10 µm. (D) All values are mean ± SD …
Figure 7 with 1 supplement
Responses in Marchantia polymorpha to filamentous pathogens.
(A, B) Accumulation of callose in Marchantia in response to attack (arrows) by (A) P. infestans or (B) C. destructivum in nonpenetrated cells. Note that the frequency of P. infestans spores that …
Figure 7—figure supplement 1
Responses in Marchantia polymorpha to filamentous pathogens.
(A) On M. polymorpha, spores from Bgh (dotted line) were mis-differentiated with no or wrongly orientated appressoria that did not attack the host cell. (B) Accumulation of callose in M. polymorpha …
Figure 8 with 7 supplements
Marchantia syntaxins rescue papilla and encasement responses in Arabidopsis.
(A, B) Accumulation of callose in response to attack (arrow) by Bgh in (A) nonpenetrated and (B) penetrated cells. Open arrow points to the developing intracellular pathogenic structure (IPS). (C, D)…
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Figure 8—source data 1
Source data for the graphs in Figure 8E and F.
- https://cdn.elifesciences.org/articles/73487/elife-73487-fig8-data1-v2.xlsx
Figure 8—figure supplement 1
Marchantia syntaxins are functional in Arabidopsis.
(A) Plants at 5 weeks, expressing SYP12 clade members from either Arabidopsis or Marchantia polymorpha. (B) Localization of Marchantia SYP12 clade members in the epidermis of leaves from plants of 4 …
Figure 8—figure supplement 2
Marchantia syntaxins rescue papilla responses.
(A) Accumulation of callose in response to Bgh attack at nonpenetrated (arrows) attack sites. Bars = 10 µm. (B) Frequency of papillae in response to Bgh in nonpenetrated cells. All values are mean ± …
Figure 8—figure supplement 3
Marchantia syntaxins rescue encasement responses.
(A) Accumulation of callose in response to Bgh attack at successful penetration sites. Open arrows point to the developing intracellular pathogenic structure (IPS). Bars = 10 µm. (B) Frequency of …
Figure 8—figure supplement 4
Localization of SYP12 clade members at Bgh attack sites.
Comparative papilla localization of SYP12 members from Arabidopsis or Marchantia in response to attack by Bgh in nonpenetrated cells. Bars = 10 µm.
Figure 8—figure supplement 5
Localization of SYP12 clade members at Bgh penetration sites.
Comparative encasement localization of SYP12 members from Arabidopsis or Marchantia in response to haustoria by Bgh in penetrated cells. Bars = 10 µm.
Figure 8—figure supplement 6
Marchantia SYP12s restore immunity in Arabidopsis toward C. destructivum.
(A) Macroscopic phenotype at 5 dai with C. destructivum. (B–D) Frequency of penetration by C. destructivum (B), G. orontii (C), and C. higginsianum (D). (B–D) All values are mean ± SD (n = 4 leaves …
Figure 8—figure supplement 7
Localization of Marchantia SYP12 clade members at attack sites.
(A–D) Localization of GFP-MpSYP12A (A, C) and GFP-MpSYP12A (B, D) in response to attack by P. infestans (A, B) and C. destructivum (C, D) in nonpenetrated cells. Bars = 10 µm.
Figure 9
Schematic model of immunity against filamentous pathogens mediated by PEN1 and SYP122.
In response to attack by filamentous pathogens, cargo for the papilla/encasement is received at the plasma membrane (PM) by PEN1 or SYP122 and secreted in between the plant cell wall (CW) and the PM …
Tables
Key resources table
| Reagent type (species) or resource | Designation | Source or reference | Identifiers | Additional information |
|---|---|---|---|---|
| Gene (Arabidopsis thaliana) | pen1-1 syp122-1 | Assaad et al., 2004 | See Materials and methods | |
| Gene (A. thaliana) | fmo1-1 pen1-1 syp122-1 | Zhang et al., 2008 | See Materials and methods | |
| Gene (A. thaliana) | amsh3-4 pen1-1 syp122-1 | Schultz-Larsen et al., 2018 | See Materials and methods | |
| Gene (A. thaliana) | sid2 pad4 pen1 syp122 | Zhang et al., 2008 | See Materials and methods | |
| Gene (A. thaliana) | TET8-GFP | Boavida et al., 2013 | See Materials and methods |
