Abstract
Plant intracellular immune receptors comprise a large number of multi-domain proteins resembling animal NOD-like receptors (NLRs). Plant NLRs typically recognize isolate-specific pathogen-derived effectors, encoded by avirulence (AVR) genes, and trigger defense responses often associated with localized host cell death. The barley MLA gene is polymorphic in nature and encodes NLRs of the coiled-coil (CC)-NB-LRR type that each detects a cognate isolate-specific effector of the barley powdery mildew fungus. We report the systematic analyses of MLA10 activity in disease resistance and cell death signaling in barley and Nicotiana benthamiana. MLA10 CC domain-triggered cell death is regulated by highly conserved motifs in the CC and the NB-ARC domains and by the C-terminal LRR of the receptor. Enforced MLA10 subcellular localization, by tagging with a nuclear localization sequence (NLS) or a nuclear export sequence (NES), shows that MLA10 activity in cell death signaling is suppressed in the nucleus but enhanced in the cytoplasm. By contrast, nuclear localized MLA10 is sufficient to mediate disease resistance against powdery mildew fungus. MLA10 retention in the cytoplasm was achieved through attachment of a glucocorticoid receptor hormone-binding domain (GR), by which we reinforced the role of cytoplasmic MLA10 in cell death signaling. Together with our data showing an essential and sufficient nuclear MLA10 activity in disease resistance, this suggests a bifurcation of MLA10-triggered cell death and disease resistance signaling in a compartment-dependent manner.
Highlights
Plants defend themselves against pathogens by mounting effective, spatiotemporally fine-tuned immune responses
Because for the FL receptor the cell death response was shown to be entirely dependent on an intact P-loop motif in the NB domain and the EDVID motif in the CC domain (Fig. 3 and 4), our data imply that cell death signaling via the CC domain is powered by receptor NTP hydrolysis and that pro-death signaling components are evolutionarily conserved between monocot and dicot plants
The MLA proteins belong to the CCEDVID-NB-Leucine Rich Repeat domain (LRR) subclass of CNLs, whose members share the conserved EDVID motif [37,52]
Summary
Plants defend themselves against pathogens by mounting effective, spatiotemporally fine-tuned immune responses. Two major types of immune receptors are responsible for pathogen recognition and subsequent defense induction [1]. One class comprises membrane-localized pattern recognition receptors that launch PAMP/MAMP-triggered immunity (PTI/MTI) upon detection of pathogen/microbe-associated molecular pattern (PAMP/MAMP). The second type are intracellular disease resistance (R) proteins that trigger effector-triggered immunity (ETI) after recognition of pathogen delivered effector proteins [2,3]. PTI/MTI and ETI share some signaling pathways and induce similar defense responses, ETI is more frequently associated with the hypersensitive response (HR). The HR is defined as a localized and rapid cell death response around attempted pathogen infection sites [4,5,6,7]
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