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Plant intracellular nucleotide-binding leucine-rich repeat (NLR) receptors with an N-terminal Toll/interleukin-1 receptor (TIR) domain sense pathogen effectors to initiate immune signaling. TIR domains across different kingdoms have NADase activities and can produce phosphoribosyl adenosine monophosphate/diphosphate (pRib-AMP/ADP) or cyclic ADPR (cADPR) isomers. The lipase-like proteins EDS1 and PAD4 transduce immune signals from sensor TIR-NLRs to a helper NLR called ADR1, which executes immune function. We report the structure and function of anArabidopsisEDS1-PAD4-ADR1 (EPA) heterotrimer in complex with pRib-AMP/ADP activated by plant or bacterial TIR signaling. 2′cADPR can be hydrolyzed into pRib-AMP and thus activate EPA signaling. Bacterial TIR domains producing 2′cADPR also activate EPA function. Our findings suggest that 2′cADPR may be the storage form of the unstable signaling molecule pRib-AMP.
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Convergent Loss of an EDS1/PAD4 Signaling Pathway in Several Plant Lineages Reveals Coevolved Components of Plant Immunity and Drought Response
Abstract Plant innate immunity relies on nucleotide binding leucine-rich repeat receptors (NLRs) that recognize pathogen-derived molecules and activate downstream signaling pathways. We analyzed the variation in NLR gene copy number and identified plants with a low number of NLR genes relative to sister species. We specifically focused on four plants from two distinct lineages, one monocot lineage (Alismatales) and one eudicot lineage (Lentibulariaceae). In these lineages, the loss of NLR genes coincides with loss of the well-known downstream immune signaling complex ENHANCED DISEASE SUSCEPTIBILITY 1 (EDS1)/PHYTOALEXIN DEFICIENT 4 (PAD4). We expanded our analysis across whole proteomes and found that other characterized immune genes were absent only in Lentibulariaceae and Alismatales. Additionally, we identified genes of unknown function that were convergently lost together with EDS1/PAD4 in five plant species. Gene expression analyses in Arabidopsis (Arabidopsis thaliana) and Oryza sativa revealed that several homologs of the candidates are differentially expressed during pathogen infection, drought, and abscisic acid treatment. Our analysis provides evolutionary evidence for the rewiring of plant immunity in some plant lineages, as well as the coevolution of the EDS1/PAD4 pathway and drought responses.
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- Award ID(s):
- 1701918
- PAR ID:
- 10151243
- Publisher / Repository:
- Oxford University Press
- Date Published:
- Journal Name:
- The Plant Cell
- Volume:
- 32
- Issue:
- 7
- ISSN:
- 1040-4651
- Page Range / eLocation ID:
- p. 2158-2177
- Format(s):
- Medium: X
- Sponsoring Org:
- National Science Foundation
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