Identification and receptor mechanism of TIR-catalyzed small molecules in plant immunity

Huang, Shijia; Jia, Aolin; Song, Wen; Hessler, Giuliana; Meng, Yonggang; Sun, Yue; Xu, Lina; Laessle, Henriette; Jirschitzka, Jan; ShouCai, Ma; Xiao, Yu; Yu, Dongli; Hou, Jiao; Liu, Ruiqi; Sun, Huanhuan; Liu, Xiaohui; Han, Zhifu; Chang, Junbiao; Parker, Jane E.; Chai, Jijie

doi:10.1126/science.abq3297

Cited by 132 publications

(178 citation statements)

References 53 publications

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“…pRib-ADP and pRib-AMP displayed weak activity in inducing the EDS1-SAG101 interaction with NRG1A ( 28 ), which suggests that other TIR-catalyzed small molecules promote this interaction more efficiently. When coexpressed with the Arabidopsis TNL receptor RPP1 and its cognate Hyaloperonospora arabidopsidis effector ATR1 ( 29 ), EDS1-SAG101 was copurified with N-terminally GST-fused NRG1A (fig.…”

Section: Identification Of a Small Molecule Specifically Activating E...mentioning

confidence: 99%

“…When coexpressed with the Arabidopsis TNL receptor RPP1 and its cognate Hyaloperonospora arabidopsidis effector ATR1 ( 29 ), EDS1-SAG101 was copurified with N-terminally GST-fused NRG1A (fig. S1A) ( 28 ). NRG1A binding of EDS1-SAG101 was suppressed by mutation of RPP1 catalytic residue Glu 158 , which suggests that the EDS1-SAG101 interaction with NRG1A is conferred by RPP1-catalyzed products.…”

Section: Identification Of a Small Molecule Specifically Activating E...mentioning

confidence: 99%

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confidence: 99%

“…TIR-catalyzed small molecules induced the assembly of Arabidopsis EDS1-SAG101-NRG1 and EDS1-PAD4-ADR1 complexes in insect cells ( 28 ). TNL- and TIR-generated 2′-(5′′-phosphoribosyl)-5′-adenosine monophosphate (pRib-AMP) and diphosphate (pRib-ADP) efficiently induced EDS1-PAD4 association with ADR1-L1 but displayed only weak activity in promoting EDS1-SAG101 interaction with NRG1A ( 28 ). These data and the EDS1-SAG101-NRG1 signaling preferences in vivo suggested that other, yet-unidentified TNL- or TIR-catalyzed small molecules underlie signaling through this immune complex.…”

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confidence: 99%

“…We show that TIR domain proteins catalyze an ADP ribose-transfer reaction using NAD + or NAD + with ATP as substrates to produce ADP-ribosylated ADPR (di-ADPR) and ADP-ribosylated ATP (ADPr-ATP), respectively. Like pRib-ADP and pRib-AMP ( 28 ), di-ADPR and ADPr-ATP can function as second messengers to induce TNL signaling. The latter two molecules specifically bind to and induce Arabidopsis EDS1-SAG101 interaction with NRG1A, establishing EDS1-SAG101 as a receptor complex for di-ADPR and ADPr-ATP.…”

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confidence: 99%

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TIR-catalyzed ADP-ribosylation reactions produce signaling molecules for plant immunity

Jia

Huang

Song

et al. 2022

Science

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Plant pathogen-activated immune signaling by nucleotide-binding leucine-rich repeat (NLR) receptors with an N-terminal Toll/Interleukin-1 receptor (TIR) domain converges on Enhanced Disease Susceptibility 1 (EDS1) and its direct partners Phytoalexin Deficient 4 (PAD4) or Senescence-Associated Gene 101 (SAG101). TIR-encoded NADases produce signaling molecules to promote exclusive EDS1-PAD4 and EDS1-SAG101 interactions with helper NLR sub-classes. Here we show that TIR-containing proteins catalyze adenosine diphosphate (ADP)-ribosylation of adenosine triphosphate (ATP) and ADP ribose (ADPR) via ADPR polymerase-like and NADase activity, forming ADP-ribosylated ATP (ADPr-ATP) and ADPr-ADPR (di-ADPR), respectively. Specific binding of ADPr-ATP or di-ADPR allosterically promotes EDS1-SAG101 interaction with helper NLR N requirement gene 1A (NRG1A) in vitro and in planta . Our data reveal an enzymatic activity of TIRs that enables specific activation of the EDS1-SAG101-NRG1 immunity branch.

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Section: Identification Of a Small Molecule Specifically Activating E...mentioning

confidence: 99%

Section: Identification Of a Small Molecule Specifically Activating E...mentioning

confidence: 99%

mentioning

confidence: 99%

mentioning

confidence: 99%

mentioning

confidence: 99%

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TIR-catalyzed ADP-ribosylation reactions produce signaling molecules for plant immunity

Jia

Huang

Song

et al. 2022

Science

Self Cite

120

108

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How enzyme‐centered approaches are advancing research on cyclic oligo‐nucleotides

Wenzl,

de Oliveira Mann

2024

FEBS Letters

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Cyclic nucleotides are the most diversified category of second messengers and are found in all organisms modulating diverse pathways. While cAMP and cGMP have been studied over 50 years, cyclic di‐nucleotide signaling in eukaryotes emerged only recently with the anti‐viral molecule 2´3´cGAMP. Recent breakthrough discoveries have revealed not only the astonishing chemical diversity of cyclic nucleotides but also surprisingly deep‐rooted evolutionary origins of cyclic oligo‐nucleotide signaling pathways and structural conservation of the proteins involved in their synthesis and signaling. Here we discuss how enzyme‐centered approaches have paved the way for the identification of several cyclic nucleotide signals, focusing on the advantages and challenges associated with deciphering the activation mechanisms of such enzymes.

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A splicing variant of EDS1 from Vitis vinifera forms homodimers but no heterodimers with PAD4

et al. 2023

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Enhanced Disease Susceptibility 1 (EDS1), a key component of microbe‐triggered immunity and effector‐triggered immunity in most higher plants, forms functional heterodimeric complexes with its homologs Phytoalexin Deficient 4 (PAD4) or Senescence‐associated Gene 101 (SAG101). Here, the crystal structure of VvEDS1Nterm, the N‐terminal domain of EDS1 from Vitis vinifera, is reported, representing the first structure of an EDS1 entity beyond the model plant Arabidopsis thaliana. VvEDS1Nterm has an α/β‐hydrolase fold, is similar to the N‐terminal domain of A. thaliana EDS1 and forms stable homodimers in solution as well as in crystals. These VvEDS1Nterm homodimers are spatially incompatible with heterodimers with PAD4 or SAG101, they explain why VvEDS1Nterm does not interact with V. vinifera PAD4 according to gel filtration, and they serve as a guide to develop a plausible, albeit experimentally not verified model of full‐length EDS1. VvEDS1Nterm is a splicing variant comprising two of three exons of the VvEDS1 gene. It originates from a naturally occurring mRNA, in which the first of two introns was removed while the second one containing a stop codon close to the exon/intron border was retained. This is a potential case of intron retention and the first report of this phenomenon in the context of EDS1. Its biological significance has not yet been clarified, nor has the question if a VvEDS1Nterm protein with a specific function can occur under physiological conditions.

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Identification and receptor mechanism of TIR-catalyzed small molecules in plant immunity

Cited by 132 publications

References 53 publications

TIR-catalyzed ADP-ribosylation reactions produce signaling molecules for plant immunity

TIR-catalyzed ADP-ribosylation reactions produce signaling molecules for plant immunity

How enzyme‐centered approaches are advancing research on cyclic oligo‐nucleotides

A splicing variant of EDS1 from Vitis vinifera forms homodimers but no heterodimers with PAD4

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