Nucleoporin-regulated MAP kinase signaling in immunity to a necrotrophic fungal pathogen

Abstract

Pathogen-responsive mitogen-activated protein kinase (MAPK or MPK) cascades relay signals from activated immune receptors across the nuclear envelope to intranuclear targets. However, in plants, little is known about the spatial control of MAPK signaling. Here, we report that the Arabidopsis (Arabidopsis thaliana) nuclear pore complex protein Nup88/MOS7 is essential for immunity to the necrotrophic fungus Botrytis cinerea The mos7-1 mutation, causing a four-amino acid deletion, compromises B. cinerea-induced activation of the key immunoregulatory MAPKs MPK3/MPK6 and reduces MPK3 protein levels posttranscriptionally. Furthermore, MOS7 contributes to retaining a sufficient MPK3 abundance in the nucleus, which is required for full immunity to B. cinerea Finally, we present a structural model of MOS7 and show that the mos7-1 mutation compromises interactions with Nup98a/b, two phenylalanine-glycine repeat nucleoporins implicated in maintaining the selective nuclear pore complex permeability barrier. Together, our analysis uncovered MOS7 and Nup98 as novel components of plant immunity toward a necrotrophic pathogen and provides mechanistic insights into how these nucleoporins coordinate nucleocytoplasmic transport to mount a robust immune response.

Dynamic Changes in Plant Nuclear Organization in Response to Environmental and Developmental Signals

“…Nups that were reported in the past for one phenotype or pathway are often later associated with another pathway, either related or unrelated, as is the case for Nup88 and Nup98 in Genenncher et al (2016) and Gallemí et al (2016), respectively. Nup88-also called MOS7-was known as a contributor to the autoimmunity of the suppressor of npr1-1, constitutive1 mutant (Cheng et al, 2009).…”

Nucleoporin NUP88/MOS7 is required for manifestation of phenotypes associated with the Arabidopsis CHITIN ELICITOR RECEPTOR KINASE1 mutant cerk1–4

“…In support of this scenario, we found that i) the mos7-1 mutation, causing a 4 amino-acid ( 190 FDLS 193 ) deletion, compromises interactions with NUP98a and NUP98b, and that ii) resistance against B. cinerea is impaired by enhancing the nuclear export rate of MPK3 through fusion to a nuclear export signal (NES). 11 Together, these data show that MOS7/NUP88 is an important regulator of multiple immune response pathways against (hemi-)biotrophic and necrotrophic pathogens and suggest that MOS7 modulates plant immune responses at the level of the NPC according to the particular type of pathogen attacking. 7,11 In Arabidopsis, perception of the fungal cell wall polysaccharide MAMP chitin is mediated by the lysin motif receptor-like kinase (LysM-RLK), CHITIN ELICITOR RECEP-TOR KINASE1 (CERK1).…”

“…11 Together, these data show that MOS7/NUP88 is an important regulator of multiple immune response pathways against (hemi-)biotrophic and necrotrophic pathogens and suggest that MOS7 modulates plant immune responses at the level of the NPC according to the particular type of pathogen attacking. 7,11 In Arabidopsis, perception of the fungal cell wall polysaccharide MAMP chitin is mediated by the lysin motif receptor-like kinase (LysM-RLK), CHITIN ELICITOR RECEP-TOR KINASE1 (CERK1). 12,13 A mutated version of this PRR, harboring a L 124 F amino acid exchange in its second LysM domain, was isolated from a forward-genetic screen for components that contribute to non-host resistance of Arabidopsis ecotype Col-3 gl1 against the non-adapted barley powdery mildew fungus Blumeria graminis f.sp.…”

“…11 Together, these data show that MOS7/NUP88 is an important regulator of multiple immune response pathways against (hemi-)biotrophic and necrotrophic pathogens and suggest that MOS7 modulates plant immune responses at the level of the NPC according to the particular type of pathogen attacking. 7,11 In Arabidopsis, perception of the fungal cell wall polysaccharide MAMP chitin is mediated by the lysin motif receptor-like kinase (LysM-RLK), CHITIN ELICITOR RECEP-TOR KINASE1 (CERK1). 12,13 A mutated version of this PRR, PLANT SIGNALING & BEHAVIOR 2017, VOL.…”

“…7,10 More recently, we uncovered that MOS7 is also essential for establishing a full defense response against the gray mold fungus Botrytis cinerea, a necrotrophic pathogen that kills its host plants. 11 When co-expressed transiently in leaves of Nicotiana benthamiana, MOS7 interacts with NUP98a and NUP98b, 2 phenylalanine-glycine (FG)-repeat nucleoporins implicated in maintaining the selective permeability barrier of the NPC. Importantly, this interaction appears to be essential for maintaining a sufficient abundance of the Botrytis-responsive MAP kinase MPK3 inside the nucleus to mount a full immune response.…”