[Intellectual Contribution]

Surface accumulated ƒ¿-1,3-glucan allowed fungal plant pathogens to evade hostsf innate immunity

Marie Nishimura
Plant-Microbe Interactions Research Unit
mAbstractn
We have revealed that a broad range of fungal plant pathogens evade the host plantfs innate immunity with surface accumulated ƒ¿-1,3-glucan. To support these findings, we clarified that rice plants secreting ƒ¿-1,3-glucanase developed strong resistance towards major fungal pathogens.
mKeywordsn
PAMPs, innate immune evasion, fungal pathogens

mBackgroundn

Plants have innate immunity called PTI (pattern triggered immunity) which is triggered by recognition of pathogen associated molecular patterns (PAMPs), e.g., fungal cell wall chitin. We have shown in a previous study that the rice blast fungus, Magnaporthe oryzae, masked the cell wall surface with ƒ¿-1,3- glucan, a non-degradable polysaccharide in plants, in response to a plant wax component. Based on this finding, we hypothesized that M. oryzae concealed the cell wall PAMPs with ƒ¿-1,3-glucan to evade PTI of the host. In this study, we investigated the role of surface ƒ¿-1,3-glucan during infection in multiple fungal rice pathogens.
mResults and Discussionn
  1. We have found that the ƒ¿-1,3-glucan synthase gene MgAGS1 was required for infection in M. oryzae. We have also shown that rice plants rapidly activated defense responses against a M. oryzae mutant lacking ƒ¿-1,3-glucan. These data suggested that M. oryzae delayed the defense responses in host plants with ƒ¿-1,3-glucan.
  2. M. oryzae, Cochliobolus miyabeanus (rice brown spot fungus) and Rhyzoctonia solani (sheath blight fungus) are the top three fungal rice pathogens. Although these three fungi are phylogenetically distant and have different infection styles (hemibiotroph in M. oryzae vs. necrotroph in the latter two), histocytochemical analysis revealed that ƒ¿-1,3-glucan concealed cell wall chitin in these fungi specifically during infection. In addition, we also found that ƒ¿-1,3-glucan is essential for maintaining infectious structures in R. solani.
  3. A transgenic rice secreting a bacterial ƒ¿-1,3-glucanase (AGL-rice) developed resistance to M. oryzae, C. miyabeanus and R. solani (Fig.1). Moreover, rapid defense responses were evoked in the AGL-rice inoculated with these fungi. These results suggest that surface ƒ¿-1,3-glucan interfered with the release of PAMPs to delay innate immune defense responses in plants.
mFuture prospectsn
  1. ƒ¿-1,3-glucan is a potential target for controlling various fungal diseases in plants because of its ability to interfere with host innate immunity.
  2. We have shown that fungal plant pathogens conceals cell wall surfaces with ƒ¿-1,3-glucan in response to plant cues. Future study on the plant cues will reveal fungal recognition mechanism(s) of host plants.
  3. Our study also suggests that use of ƒ¿-1,3-glucanase or ƒ¿-1,3-glucanase- producing microbes as biological control agents will have potential applications in sustainable crop protection techniques against fungal pathogens.

Fig.1. The fungal disease resistance of the transgenic rice expressing a bacterial ƒ¿-1,3-glucanase (AGL-rice). M. oryzae and C. miyabeanus conidia were spray-inoculated to the AGL-rice leaves. R. solani mycelia were placed at one end of the leaf sheath of AGL-rice. Typical disease lesions were observed on the non-transgenic (NT) leaf blade/sheath. The photos were taken at 6 dpi.


Fig.2. Model for the stealth infection strategy in fungal plant pathogens. A. Fungal pathogens mask cell wall PAMPs with surface ƒ¿-1,3-glucan. Plants cannot degrade ƒ¿-1,3-glucan so the pathogens can easily evade the hostfs innate immune recognition of cell wall PAMPs. B. Pathogens lacking ƒ¿-1,3-glucan evoke PTI because cell wall PAMPs are exposed. C. The AGL-rice can remove ƒ¿-1,3-glucan from the pathogenfs surfaces to recognize cell-wall PAMPs (e.g. chitin). Consequently, PTI is rapidly evoked in the plants.

 

[Reference]

  1. Fujikawa T, Sakaguchi A, Nishizawa Y, Kouzai Y, Minami E, Yano S, Koga H, Meshi T and Nishimura M (2012) Surface ƒ¿-1,3-glucan facilitates fungal stealth infection by interfering with innate immunity in plants PLoS Pathogens 8(8): e1002882
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