Research on ADR1s helps understanding the plant immune network

Abstract

Plant innate immunity begins with the recognition of pathogens by plasma membrane localized pattern-recognition receptors (PRRs) and intracellular nucleotide-binding domain leucine-rich repeat containing receptors (NLRs), which lead to pattern-triggered immunity (PTI) and effector-triggered immunity (ETI), respectively. For a long time, PTI and ETI have been regarded as two independent processes although they share multiple components and signal outputs. Increasing evidence shows an intimate link between PTI and ETI. PTI and ETI mutually potentiate each other, and this is essential for robust disease resistance during pathogen infection. An ancient class of NLRs called RNLs, so named because they carry a Resistance to Powdery Mildew 8 (RPW8)-like coiled-coil (CC) domain in the N terminus, has emerged as a key node connecting PTI and ETI. RNLs not only act as helper NLRs that signal downstream of sensor NLRs, they also directly mediate PTI signaling by associating with PRR complexes. Here, we focus on Activated Disease Resistance 1 (ADR1), a subclass of RNLs, and discuss its role and mechanism in plant immunity.

Keywords

Immune receptors / PTI / ETI / Resistance / ADR1

References

[1] BiG, SuM, LiN, LiangY, DangS, XuJ, HuM, WangJ, ZouM, DengY, LiQ, HuangS, LiJ, ChaiJ, HeK, ChenYH, ZhouJM. The ZAR1 resistosome is a calcium-permeable channel triggering plant immune signaling. Cell, 2021, 184(13):3528-3541

[2] BonardiV, TangS, StallmannA, RobertsM, CherkisK, DanglJL. Expanded functions for a family of plant intracellular immune receptors beyond specific recognition of pathogen effectors. Proc Natl Acad Sci U S A, 2011, 108(39):16463-16468

[3] GarciaAV, Blanvillain-BaufumeS, HuibersRP, WiermerM, LiG, GobbatoE, RietzS, ParkerJE. Balanced nuclear and cytoplasmic activities of EDS1 are required for a complete plant innate immune response. PLoS Pathog, 2010, 6(7):e1000970

[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] JacobP, KimNH, WuF, El-KasmiF, ChiY, WaltonWG, FurzerOJ, LietzanAD, SunilS, KempthornK, et al.. Plant "helper" immune receptors are Ca²⁺-permeable nonselective cation channels. Science, 2021, 373(6553):420-425

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

[7] MaS, LapinD, LiuL, SunY, SongW, ZhangX, LogemannE, YuD, WangJ, JirschitzkaJ, et al.. Direct pathogen-induced assembly of an NLR immune receptor complex to form a holoenzyme. Science, 2020, 370: eabe3069

[8] MartinR, QiT, ZhangH, LiuF, KingM, TothC, NogalesE, StaskawiczBJ. Structure of the activated ROQ1 resistosome directly recognizing the pathogen effector XopQ. Science, 2020, 370: eabd9993

[9] NgouBPM, AhnHK, DingP, JonesJDG. Mutual potentiation of plant immunity by cell-surface and intracellular receptors. Nature, 2021, 592: 110-115

[10] PruittRN, LocciF, WankeF, ZhangL, SaileSC, JoeA, KarelinaD, HuaC, FröhlichK, WanW-L, HuM, RaoS, StolzeSC, HarzenA, GustAA, HarterK, JoostenMHAJ, ThommaBPHJ, ZhouJM, DanglJL, WeigelD, NakagamiH, OeckingC, KasmiFE, ParkerJE, NürnbergerT. The EDS1–PAD4–ADR1 node mediates Arabidopsis pattern-triggered immunity. Nature, 2021, 598(7881):495-499

[11] SaileSC, AckermannFM, SunilS, KeicherJ, BaylessA, BonardiV, WanL, DoumaneM, StobbeE, JaillaisY, et al.. Arabidopsis ADR1 helper NLR immune receptors localize and function at the plasma membrane in a phospholipid dependent manner. New Phytol, 2021, 232(6):2440-2456

[12] Saile SC, Jacob P, Castel B, Jubic LM, Salas-Gonzales I, Backer M, Jones JDG, Dangl JL, El Kasmi F (2020) Two unequally redundant “helper” immune receptor families mediate Arabidopsis thaliana intracellular “sensor” immune receptor functions. PLoS Biol 18(9):e3000783. https://doi.org/10.1371/journal.pbio.3000783

[13] SunX, LapinD, FeehanJM, StolzeSC, KramerK, DongusJA, RzemieniewskiJ, Blanvillain-BaufuméS, HarzenA, BautorJ, DerbyshireP, MenkeFLH, FinkemeierI, NakagamiH, JonesJDG, ParkerJE. Pathogen effector recognition-dependent association of NRG1 with EDS1 and SAG101 in TNL receptor immunity. Nat Commun, 2021, 12(1):3335

[14] TianH, WuZ, ChenS, AoK, HuangW, YaghmaieanH, SunT, XuF, ZhangY, WangS, LiX, ZhangY. Activation of TIR signalling boosts pattern-triggered immunity. Nature, 2021, 598(7881):500-503

[15] 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

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

[17] WangJ, WangJ, HuM, WuS, QiJ, WangG, HanZ, QiY, GaoN, WangHW, ZhouJM, ChaiJ. Ligand-triggered allosteric ADP release primes a plant NLR complex. Science, 2019, 364(6435):eaav5868

[18] WangW, FengB, ZhouJM, TangD. Plant immune signaling: advancing on two frontiers. J Integr Plant Biol, 2020, 62(1):2-24

[19] WuZ, TianL, LiuX, ZhangY, LiX. TIR signal promotes interactions between lipase-like proteins and ADR1-L1 receptor and ADR1-L1 oligomerization. Plant Physiol, 2021, 187(2):681-686

[20] YuanM, JiangZ, BiG, NomuraK, LiuM, WangY, CaiB, ZhouJM, HeSY, XinXF. Pattern-recognition receptors are required for NLR-mediated plant immunity. Nature, 2021, 592(7852):105-109

Funding

Postdoctoral Research Foundation of China(BX2021355); National Natural Science Foundation of China(31521001)