BAK-up: the receptor kinase BAK-TO-LIFE 2 enhances immunity when BAK1 is lacking

Abstract

BRI1-ASSOCIATED KINASE 1 (BAK1/SERK3) and its closest homolog BAK1-LIKE 1 (BKK1/SERK4) are leucine-rich repeat receptor kinases (LRR-RKs) belonging to the SOMATIC EMBRYOGENESIS RECEPTOR KINASE (SERK) family. They act as co-receptors of various other LRR-RKs and participate in multiple signaling events by complexing and transphosphorylating ligand-binding receptors. Initially identified as the brassinosteroid receptor BRASSINOSTEROID INSENSITIVE 1 (BRI1) co-receptor, BAK1 also functions in plant immunity by interacting with pattern recognition receptors. Mutations in BAK1 and BKK1 cause severely stunted growth and cell death, characterized as autoimmune cell death. Several factors play a role in this type of cell death, including RKs and components of effector-triggered immunity (ETI) signaling pathways, glycosylation factors, ER quality control components, nuclear trafficking components, ion channels, and Nod-like receptors (NLRs). The Shan lab has recently discovered a novel RK BAK-TO-LIFE 2 (BTL2) that interacts with BAK1 and triggers cell death in the absence of BAK1 and BKK1. This RK compensates for the loss of BAK1-mediated pattern-triggered immunity (PTI) by activating phytocytokine-mediated immune and cell death responses.

Keywords

BAK1 / Cell death / Receptor kinase / BTL2 / PTI / ETI

References

[1] Albert I, Böhm H, Albert M, Feiler CE, Imkampe J, Wallmeroth N, Brancato C, Raaymakers TM, Oome S, Zhang H, Krol E, Grefen C, Gust AA, Chai J, Hedrich R, van den Ackerveken G, Nürnberger T (2015) An RLP23–SOBIR1–BAK1 complex mediates NLP-triggered immunity. Nat Plants https://doi.org/10.1038/nplants.2015.140

[2] BelkhadirY, JaillaisY, EppleP, Balsemao-PiresE, DanglJL, ChoryJ. Brassinosteroids modulate the efficiency of plant immune responses to microbe-associated molecular patterns. Proc Natl Acad Sci USA, 2012, 109(1):297-302

[3] BenderKW, ZipfelC. Paradigms of receptor kinase signaling in plants. Biochem J, 2023, 480(12):835-854

[4] ChinchillaD, ZipfelC, RobatzekS, KemmerlingB, NürnbergerT, JonesJDG, FelixG, BollerT. A flagellin-induced complex of the receptor FLS2 and BAK1 initiates plant defence. Nature, 2007, 448(7152):497-500

[5] ColemanAD, MaroschekJ, RaaschL, TakkenFLW, RanfS, HuckelhovenR. The Arabidopsis leucine-rich repeat receptor-like kinase MIK2 is a crucial component of early immune responses to a fungal-derived elicitor. New Phytol, 2021, 229(6):3453-3466

[6] de Oliveira MV, Xu G, Li B, de Souza Vespoli L, Meng X, Chen X, Yu X, de Souza SA, Intorne AC, de AMAM, Musinsky AL, Koiwa H, de Souza Filho GA, Shan L, He P (2016) Specific control of Arabidopsis BAK1/SERK4-regulated cell death by protein glycosylation. Nature Plants 215218. https://doi.org/10.1038/nplants.2015.218

[7] Dominguez-FerrerasA, Kiss-PappM, JehleAK, FelixG, ChinchillaD. An Overdose of the Arabidopsis Coreceptor BRASSINOSTEROID INSENSITIVE1-ASSOCIATED RECEPTOR KINASE1 or Its Ectodomain Causes Autoimmunity in a SUPPRESSOR OF BIR1–1-Dependent Manner. Plant Physiol, 2015, 168(3):1106-1121

[8] DuJ, GaoY, ZhanY, ZhangS, WuY, XiaoY, ZouB, HeK, GouX, LiG, LinH, LiJ. Nucleocytoplasmic trafficking is essential for BAK1- and BKK1-mediated cell-death control. Plant J, 2016, 85(4):520-531

[9] GaoM, WangX, WangD, XuF, DingX, ZhangZ, BiD, ChengYT, ChenS, LiX, ZhangY. Regulation of cell death and innate immunity by two receptor-like kinases in Arabidopsis. Cell Host Microbe, 2009, 6(1):34-44

[10] Gao Y, Wu Y, Du J, Zhan Y, Sun D, Zhao J, Zhang S, Li J, He K (2017) Both light-induced SA accumulation and ETI mediators contribute to the cell death regulated by BAK1 and BKK1. Front Plant Sci 8622. https://doi.org/10.3389/fpls.2017.00622

[11] HalterT, ImkampeJ, MazzottaS, WierzbaM, PostelS, BücherlC, KieferC, StahlM, ChinchillaD, WangX, NürnbergerT, ZipfelC, ClouseS, BorstJW, BoerenS, de VriesSC, TaxF, KemmerlingB. The leucine-rich repeat receptor kinase BIR2 is a negative regulator of BAK1 in plant immunity. Curr Biol, 2014, 24(2):134-143

[12] HouS, LiuD, HuangS, LuoD, LiuZ, XiangQ, WangP, MuR, HanZ, ChenS, ChaiJ, ShanL, HeP. The Arabidopsis MIK2 receptor elicits immunity by sensing a conserved signature from phytocytokines and microbes. Nat Commun, 2021, 12(1):5494

[13] ImkampeJ, HalterT, HuangS, SchulzeS, MazzottaS, SchmidtN, ManstrettaR, PostelS, WierzbaM, YangY, van DongenW, StahlM, ZipfelC, GosheMB, ClouseS, de VriesSC, TaxF, WangX, KemmerlingB. The arabidopsis leucine-rich repeat receptor kinase BIR3 negatively regulates BAK1 receptor complex formation and stabilizes BAK1. Plant Cell, 2017, 29(9):2285-2303

[14] KrolE, MentzelT, ChinchillaD, BollerT, FelixG, KemmerlingB, PostelS, ArentsM, JeworutzkiE, Al-RasheidKA, BeckerD, HedrichR. Perception of the Arabidopsis danger signal peptide 1 involves the pattern recognition receptor AtPEPR1 and its close homologue AtPEPR2. J Biol Chem, 2010, 285(18):13471-13479

[15] LiJ, WenJ, LeaseKA, DokeJT, TaxFE, WalkerJC. BAK1, an Arabidopsis LRR receptor-like protein kinase, interacts with BRI1 and modulates brassinosteroid signaling. Cell, 2002, 110(2):213-222

[16] LiL, KimP, YuL, CaiG, ChenS, AlfanoJR, ZhouJM. Activation-dependent destruction of a co-receptor by a pseudomonas syringae effector dampens plant immunity. Cell Host Microbe, 2016, 20(4):504-514

[17] LiebrandTW, van den BergGC, ZhangZ, SmitP, CordewenerJH, AmericaAH, SklenarJ, JonesAM, TamelingWI, RobatzekS, ThommaBP, JoostenMH. Receptor-like kinase SOBIR1/EVR interacts with receptor-like proteins in plant immunity against fungal infection. Proc Natl Acad Sci USA, 2013, 110(24):10010-10015

[18] MaX, XuG, HeP, ShanL. SERKing Coreceptors for Receptors. Trends Plant Sci, 2016, 21(12):1017-1033

[19] NamKH, LiJ. BRI1/BAK1, a Receptor Kinase Pair Mediating Brassinosteroid Signaling. Cell, 2002, 110(2):203-212

[20] NgouBPM, AhnHK, DingP, JonesJDG. Mutual potentiation of plant immunity by cell-surface and intracellular receptors. Nature, 2021, 592(7852):110-115

[21] NgouBPM, JonesJDG, DingP. Plant immune networks. Trends Plant Sci, 2022, 27(3):255-273

[22] PruittRN, LocciF, WankeF, ZhangL, SaileSC, JoeA, KarelinaD, HuaC, FrohlichK, WanWL, HuM, RaoS, StolzeSC, HarzenA, GustAA, HarterK, JoostenM, ThommaB, ZhouJM, DanglJL, WeigelD, NakagamiH, OeckingC, KasmiFE, ParkerJE, NurnbergerT. The EDS1-PAD4-ADR1 node mediates Arabidopsis pattern-triggered immunity. Nature, 2021, 598(7881):495-499

[23] RhodesJ, YangH, MoussuS, BoutrotF, SantiagoJ, ZipfelC. Perception of a divergent family of phytocytokines by the Arabidopsis receptor kinase MIK2. Nat Commun, 2021, 12(1):705

[24] Schulze S, Yu L, Hua C, Zhang L, Kolb D, Weber H, Ehinger A, Saile SC, Stahl M, Franz-Wachtel M, Li L, El Kasmi F, Nurnberger T, Cevik V, Kemmerling B (2022) The Arabidopsis TIR-NBS-LRR protein CSA1 guards BAK1-BIR3 homeostasis and mediates convergence of pattern- and effector-induced immune responses. Cell Host Microbe 30(12):1717–1731 e1716. https://doi.org/10.1016/j.chom.2022.11.001

[25] 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

[26] WuY, GaoY, ZhanY, KuiH, LiuH, YanL, KemmerlingB, ZhouJM, HeK, LiJ. Loss of the common immune coreceptor BAK1 leads to NLR-dependent cell death. Proc Natl Acad Sci USA, 2020, 117(43):27044-27053

[27] Xi L, Wu XN, Gilbert M, Schulze WX (2019) Classification and interactions of LRR receptors and co-receptors within the arabidopsis plasma membrane – An overview. Front Plant Sci 10. https://doi.org/10.3389/fpls.2019.00472

[28] Yamada K, Yamashita-Yamada M, Hirase T, Fujiwara T, Tsuda K, Hiruma K, Saijo Y (2016) Danger peptide receptor signaling in plants ensures basal immunity upon pathogen-induced depletion of BAK1. EMBO J 35(1):46–61. https://doi.org/10.15252/embj.201591807

[29] YamaguchiY, PearceG, RyanCA. The cell surface leucine-rich repeat receptor for AtPep1, an endogenous peptide elicitor in Arabidopsis, is functional in transgenic tobacco cells. Proc Natl Acad Sci USA, 2006, 103(26):10104-10109

[30] YamaguchiY, HuffakerA, BryanAC, TaxFE, RyanCA. PEPR2 is a second receptor for the Pep1 and Pep2 peptides and contributes to defense responses in Arabidopsis. Plant Cell, 2010, 22(2):508-522

[31] Yang Y, Kim NH, Cevik V, Jacob P, Wan L, Furzer OJ, Dangl JL (2022) Allelic variation in the Arabidopsis TNL CHS3/CSA1 immune receptor pair reveals two functional cell-death regulatory modes. Cell Host Microbe 30(12):1701–1716 e1705. https://doi.org/10.1016/j.chom.2022.09.013

[32] Yu X, Xu G, Li B, de Souza Vespoli L, Liu H, Moeder W, Chen S, de Oliveira MVV, Ariadina de Souza S, Shao W, Rodrigues B, Ma Y, Chhajed S, Xue S, Berkowitz GA, Yoshioka K, He P, Shan L (2019a) The Receptor Kinases BAK1/SERK4 Regulate Ca(2+) Channel-Mediated Cellular Homeostasis for Cell Death Containment. Curr Biol 29(22):3778–3790 e3778. https://doi.org/10.1016/j.cub.2019.09.018

[33] Yu X, Xu G, Li B, de Souza Vespoli L, Liu H, Moeder W, Chen S, de Oliveira MVV, Ariadina de Souza S, Shao W, Rodrigues B, Ma Y, Chhajed S, Xue S, Berkowitz GA, Yoshioka K, He P, Shan L (2019b) The receptor kinases BAK1/SERK4 regulate Ca(2+) channel-mediated cellular homeostasis for cell death containment. Curr Biol 29(22):3778–3790 e3778. https://doi.org/10.1016/j.cub.2019.09.018

[34] Yu X, Xie Y, Luo D, Liu H, de Oliveira MVV, Qi P, Kim SI, Ortiz-Morea FA, Liu J, Chen Y, Chen S, Rodrigues B, Li B, Xue S, He P, Shan L (2023) A phospho-switch constrains BTL2-mediated phytocytokine signaling in plant immunity. Cell 186(11):2329–2344 e2320. https://doi.org/10.1016/j.cell.2023.04.027

[35] 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

[36] ZhaoC, TangY, WangJ, ZengY, SunH, ZhengZ, SuR, SchneebergerK, ParkerJE, CuiH. A mis-regulated cyclic nucleotide-gated channel mediates cytosolic calcium elevation and activates immunity in Arabidopsis. New Phytol, 2021, 230(3):1078-1094

[37] ZhouJ, WangP, ClausLAN, SavatinDV, XuG, WuS, MengX, RussinovaE, HeP, ShanL. Proteolytic processing of SERK3/BAK1 regulates plant immunity, development, and cell death. Plant Physiol, 2019, 180(1):543-558

Funding

Deutsche Forschungsgemeinschaft(TRR356)