NADase and now Ca²⁺ channel, what else to learn about plant NLRs?

Abstract

Plant intracellular immune receptors known as NLR (Nucleotide-binding Leucine-rich repeat, NB-LRR) proteins confer resistance and cause cell death upon recognition of cognate effector proteins from pathogens. Plant NLRs contain a variable N-terminal domain: a Toll/interleukin-1 receptor (TIR) domain or a coiled-coil (CC) domain or an RPW8 (Resistance to Powdery Mildew 8)-like CC (CC^R) domain. TIR-NLR, CC-NLR and CC^R-NLR are known as TNL, CNL and RNL, respectively. TNLs and CNLs recognize pathogen effectors to activate cell death and defense responses, thus are regarded as sensor NLRs. RNLs are required downstream of TNLs to activate cell death and defense responses, thus are regarded as helper NLRs. Previous studies show that some TNLs form tetrameric resistosome as NAD⁺ cleaving enzymes to transduce signal, while some CNLs form pentameric resistosome with undefined biochemical function. Two recent breakthrough studies show that activated CNL and RNL function as Ca²⁺ channel to cause cell death and defense responses and provide a completely new insight into the downstream signaling events of CNL and TNL pathways.

Keywords

Immune receptors / NLR / Defense / Cell death / Ca²⁺ channel

References

[1] BiG, SuM, LiN, LiangY, DangS, XuJ, HuM, WangJ, ZouM, DengY, et al.. The ZAR1 resistosome is a calcium-permeable channel triggering plant immune signaling. Cell, 2021, 184(3528–3541):e3512

[2] CollierSM, HamelLP, MoffettP. Cell death mediated by the N-terminal domains of a unique and highly conserved class of NB-LRR protein. Mol Plant-Microbe Interact, 2011, 24(8):918-931

[3] DuxburyZ, WuCH, DingP. A comparative overview of the intracellular guardians of plants and animals: NLRs in innate immunity and beyond. Annu Rev Plant Biol, 2021, 72(1):155-184

[4] HorsefieldS, BurdettH, ZhangX, ManikMK, ShiY, ChenJ, QiT, GilleyJ, LaiJS, RankMX, CaseyLW, GuW, EricssonDJ, FoleyG, HughesRO, BosanacT, von ItzsteinM, RathjenJP, NansonJD, BodenM, DryIB, WilliamsSJ, StaskawiczBJ, ColemanMP, VeT, DoddsPN, KobeB. NAD(+) cleavage activity by animal and plant TIR domains in cell death pathways. Science, 2019, 365(6455):793-799

[5] Hu M, Qi J, Bi G, Zhou JM (2020) Bacterial effectors induce oligomerization of immune receptor ZAR1 in vivo. Mol Plant 13(5):793–801. https://doi.org/10.1016/j.molp.2020.03.004

[6] Jacob P, Kim NH, Wu F, El-Kasmi F, Chi Y, Walton WG, Furzer OJ, Lietzan AD, Sunil S, Kempthorn K, et al (2021) Plant "helper" immune receptors are Ca(2+)-permeable nonselective cation channels. Science 373(6553):420-425. https://doi.org/10.1126/science.abg7917

[7] JonesJD, VanceRE, DanglJL. Intracellular innate immune surveillance devices in plants and animals. Science, 2016, 354(6316):aaf6395

[8] JubicLM, SaileS, FurzerOJ, El KasmiF, DanglJL. Help wanted: helper NLRs and plant immune responses. Curr Opin Plant Biol, 2019, 50: 82-94

[9] LaflammeB, DillonMM, MartelA, AlmeidaRND, DesveauxD, GuttmanDS. The pan-genome effector-triggered immunity landscape of a host-pathogen interaction. Science, 2020, 367(6479):763-768

[10] LapinD, KovacovaV, SunX, DongusJA, BhandariD, von BornP, BautorJ, GuarneriN, RzemieniewskiJ, StuttmannJ, BeyerA, ParkerJE. A coevolved EDS1-SAG101-NRG1 module mediates cell death signaling by TIR-domain immune receptors. Plant Cell, 2019, 31(10):2430-2455

[11] Ma S, Lapin D, Liu L, Sun Y, Song W, Zhang X, Logemann E, Yu D, Wang J, Jirschitzka J, et al (2020) Direct pathogen-induced assembly of an NLR immune receptor complex to form a holoenzyme. Science 370(6521):eabe3069. https://doi.org/10.1126/science.abe3069

[12] Martin R, Qi T, Zhang H, Liu F, King M, Toth C, Nogales E, Staskawicz BJ (2020) Structure of the activated ROQ1 resistosome directly recognizing the pathogen effector XopQ. Science 370(6521):eabd9993. https://doi.org/10.1126/science.abd9993

[13] SaileSC, JacobP, CastelB, JubicLM, Salas-GonzalesI, BackerM, JonesJDG, DanglJL, El KasmiF. Two unequally redundant "helper" immune receptor families mediate Arabidopsis thaliana intracellular "sensor" immune receptor functions. PLoS Biol, 2020, 18(9):e3000783

[14] SaurIML, PanstrugaR, Schulze-LefertP. NOD-like receptor-mediated plant immunity: from structure to cell death. Nat Rev Immunol, 2021, 21(5):305-318

[15] WagnerS, StuttmannJ, RietzS, GueroisR, BrunsteinE, BautorJ, NiefindK, ParkerJE. Structural basis for signaling by exclusive EDS1 heteromeric complexes with SAG101 or PAD4 in plant innate immunity. Cell Host Microbe, 2013, 14(6):619-630

[16] WanL, EssumanK, AndersonRG, SasakiY, MonteiroF, ChungEH, Osborne NishimuraE, DiAntonioA, MilbrandtJ, DanglJL, NishimuraMT. TIR domains of plant immune receptors are NAD(+)-cleaving enzymes that promote cell death. Science, 2019, 365(6455):799-803

[17] WangJ, HuM, WangJ, QiJ, HanZ, WangG, QiY, WangHW, ZhouJM, ChaiJ. Reconstitution and structure of a plant NLR resistosome conferring immunity. Science, 2019, 364(6435):eaav5870

[18] Wang J, Wang J, Hu M, Wu S, Qi J, Wang G, Han Z, Qi Y, Gao N, Wang HW, et al (2019b) Ligand-triggered allosteric ADP release primes a plant NLR complex. Science 364(6435):eaav5868. https://doi.org/10.1126/science.aav5868

[19] WuCH, Abd-El-HaliemA, BozkurtTO, BelhajK, TerauchiR, VossenJH, KamounS. NLR network mediates immunity to diverse plant pathogens. Proc Natl Acad Sci U S A, 2017, 114(30):8113-8118

[20] XiaB, FangS, ChenX, HuH, ChenP, WangH, GaoZ. MLKL forms cation channels. Cell Res, 2016, 26(5):517-528

Funding

national natural science foundation of china(32088102); chinese academy of sciences(XDB27040214)