Phytocytokines function as immunological modulators of plant immunity

Abstract

Plant plasma membrane-resident immune receptors regulate plant immunity by recognizing microbe-associated molecular patterns (MAMPs), damage-associated molecular patterns (DAMPs), and phytocytokines. Phytocytokines are plant endogenous peptides, which are usually produced in the cytosol and released into the apoplast when plant encounters pathogen infections. Phytocytokines regulate plant immunity through activating an overlapping signaling pathway with MAMPs/DAMPs with some unique features. Here, we highlight the current understanding of phytocytokine production, perception and functions in plant immunity, and discuss how plants and pathogens manipulate phytocytokine signaling for their own benefits during the plant-pathogen warfare.

Keywords

Phytocytokine / Damage-associated molecular pattern (DAMP) / Pattern-recognition receptor (PRR), pattern-triggered immunity (PTI) / Plant immunity

References

[1] AmanoY, TsubouchiH, ShinoharaH, OgawaM, MatsubayashiY. Tyrosine-sulfated glycopeptide involved in cellular proliferation and expansion in Arabidopsis. Proc Natl Acad Sci U S A, 2007, 104(46):18333-18338

[2] BanchereauJ, PascualV, O'GarraA. From IL-2 to IL-37: the expanding spectrum of anti-inflammatory cytokines. Nat Immunol, 2012, 13(10):925-931

[3] BeloshistovRE, DreizlerK, GaliullinaRA, TuzhikovAI, SerebryakovaMV, ReichardtS, ShawJ, TalianskyME, PfannstielJ, ChichkovaNV, StintziA, SchallerA, VartapetianAB. Phytaspase-mediated precursor processing and maturation of the wound hormone systemin. New Phytol, 2018, 218(3):1167-1178

[4] Blackburn MR, Haruta M, Moura DS (2020) Twenty years of progress in physiological and biochemical investigation of RALF peptides. Plant Physiol 182(4):1657–1666. https://doi.org/10.1104/pp.19.01310

[5] ButenkoMA, PattersonSE, GriniPE, StenvikGE, AmundsenSS, MandalA, AalenRB. Inflorescence deficient in abscission controls floral organ abscission in Arabidopsis and identifies a novel family of putative ligands in plants. Plant Cell, 2003, 15(10):2296-2307

[6] Chen J, Yu F, Liu Y, Du C, Li X, Zhu S, Wang X, Lan W, Rodriguez PL, Liu X, Li D, Chen L, Luan S (2016) FERONIA interacts with ABI2-type phosphatases to facilitate signaling cross-talk between abscisic acid and RALF peptide in Arabidopsis. Proc Natl Acad Sci U S A 113(37):E5519–E5527. https://doi.org/10.1073/pnas.1608449113

[7] Chen YC, Siems WF, Pearce G, Ryan CA (2008) Six peptide wound signals derived from a single precursor protein in Ipomoea batatas leaves activate the expression of the defense gene sporamin. J Biol Chem 283(17):11469–11476. https://doi.org/10.1074/jbc.M709002200

[8] 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

[9] CoutoD, ZipfelC. Regulation of pattern recognition receptor signalling in plants. Nat Rev Immunol, 2016, 16(9):537-552

[10] DeFalco TA, Zipfel C (2021) Molecular mechanisms of early plant pattern-triggered immune signaling. Mol Cell S1097–2765(21)00598. https://doi.org/10.1016/j.molcel.2021.07.029

[11] DingY, WangJ, WangJ, StierhofYD, RobinsonDG, JiangL. Unconventional protein secretion. Trends Plant Sci, 2012, 17(10):606-615

[12] Engelsdorf T, Gigli-Bisceglia N, Veerabagu M, McKenna JF, Vaahtera L, Augstein F, Van der Does D, Zipfel C, Hamann T (2018) The plant cell wall integrity maintenance and immune signaling systems cooperate to control stress responses in Arabidopsis thaliana. Sci Signal 11(536):eaao3070. https://doi.org/10.1126/scisignal.aao3070

[13] Escocard de Azevedo ManhaesAM, Ortiz-MoreaFA, HeP, ShanL. Plant plasma membrane-resident receptors: surveillance for infections and coordination for growth and development. J Integr Plant Biol, 2021, 63(1):79-101

[14] FelixG, DuranJD, VolkoS, BollerT. Plants have a sensitive perception system for the most conserved domain of bacterial flagellin. Plant J, 1999, 18(3):265-276

[15] Franck CM, Westermann J, Boisson-Dernier A (2018) Plant malectin-like receptor kinases: from cell wall integrity to immunity and beyond. Annu Rev Plant Biol 69(1):301–328. https://doi.org/10.1146/annurev-arplant-042817-040557

[16] GravinoM, LocciF, TundoS, CervoneF, SavatinDV, De LorenzoG. Immune responses induced by oligogalacturonides are differentially affected by AvrPto and loss of BAK1/BKK1 and PEPR1/PEPR2. Mol Plant Pathol, 2017, 18(4):582-595

[17] GullyK, PelletierS, GuillouMC, FerrandM, AligonS, PokotyloI, PerrinA, VergneE, FagardM, RuellandE, GrappinP, BucherE, RenouJP, AubourgS. The SCOOP12 peptide regulates defense response and root elongation in Arabidopsis thaliana. J Exp Bot, 2019, 70(4):1349-1365

[18] Guo H, Nolan TM, Song G, Liu S, Xie Z, Chen J, Schnable PS, Walley JW, Yin Y (2018) FERONIA receptor kinase contributes to plant immunity by suppressing jasmonic acid signaling in Arabidopsis thaliana. Curr Biol 28:3316–3324 e3316.

[19] GustAA, PruittR, NurnbergerT. Sensing danger: key to activating plant immunity. Trends Plant Sci, 2017, 22(9):779-791

[20] Hander T, Fernández-Fernández ÁD, Kumpf RP, Willems P, Schatowitz H, Rombaut D, Staes A, Nolf J, Pottie R, Yao P, Gonçalves A, Pavie B, Boller T, Gevaert K, Van Breusegem F, Bartels S, Stael S (2019) Damage on plants activates Ca^2+- dependent metacaspases for release of immunomodulatory peptides. Science 363(6433):eaar7486. https://doi.org/10.1126/science.aar7486

[21] HarutaM, SabatG, SteckerK, MinkoffBB, SussmanMR. A peptide hormone and its receptor protein kinase regulate plant cell expansion. Science, 2014, 343(6169):408-411

[22] HouS, JamiesonP, HeP. The cloak, dagger, and shield: proteases in plant-pathogen interactions. Biochem J, 2018, 475(15):2491-2509

[23] Hou S, Liu D, Huang S, Luo D, Liu Z, Wang P, Mu R, Han Z, Chai J, Shan L, He P (2021a) Immune elicitation by sensing the conserved signature from phytocytokines and microbes via the Arabidopsis MIK2 receptor. bioRxiv preprint. https://doi.org/10.1101/2021.01.28.428652

[24] Hou S, Liu Z, Shen H, Wu D (2019a) Damage-associated molecular pattern-triggered immunity in plants. Front Plant Sci 10:646. https://doi.org/10.3389/fpls.2019.00646

[25] Hou S, Shen H, Shao H (2019b) PAMP-induced peptide 1 cooperates with salicylic acid to regulate stomatal immunity in Arabidopsis thaliana. Plant Signal Behav 14(11):1666657. https://doi.org/10.1080/15592324.2019.1666657

[26] HouS, WangX, ChenD, YangX, WangM, TurraD, Di PietroA, ZhangW. The secreted peptide PIP1 amplifies immunity through receptor-like kinase 7. PLoS Pathog, 2014, 10(9

[27] HouS, ZhangJ, HeP. Stress-induced activation of receptor signaling by protease-mediated cleavage. Biochem J, 2021, 478 10):1847-1852

[28] HuangY, YinC, LiuJ, FengB, GeD, KongL, Ortiz-MoreaFA, RichterJ, HauserMT, WangWM, ShanL, HeP. A trimeric CrRLK1L-LLG1 complex genetically modulates SUMM2-mediated autoimmunity. Nat Commun, 2020, 11(1):4859

[29] HuffakerA, DafoeNJ, SchmelzEA. ZmPep1, an ortholog of Arabidopsis elicitor peptide 1, regulates maize innate immunity and enhances disease resistance. Plant Physiol, 2011, 155(3):1325-1338

[30] HuffakerA, PearceG, RyanCA. An endogenous peptide signal in Arabidopsis activates components of the innate immune response. Proc Natl Acad Sci U S A, 2006, 103(26):10098-10103

[31] IgarashiD, TsudaK, KatagiriF. The peptide growth factor, phytosulfokine, attenuates pattern-triggered immunity. Plant J, 2012, 71(2):194-204

[32] KemmerlingB, HalterT, MazzottaS, MosherS, NurnbergerT. A genome-wide survey for Arabidopsis leucine-rich repeat receptor kinases implicated in plant immunity. Front Plant Sci, 2011, 2: 88

[33] KimY, TsudaK, IgarashiD, HillmerRA, SakakibaraH, MyersCL, KatagiriF. Mechanisms underlying robustness and tunability in a plant immune signaling network. Cell Host Microbe, 2014, 15(1):84-94

[34] Lewis LA, Polanski K, de Torres-Zabala M, Jayaraman S, Bowden L, Moore J, Penfold CA, Jenkins DJ, Hill C, Baxter L, Kulasekaran S et al (2015) Transcriptional dynamics driving MAMP-triggered immunity and pathogen effector-mediated immunosuppression in Arabidopsis leaves following infection with Pseudomonas syringae pv tomato DC3000. Plant Cell 27(11):3038–3064. https://doi.org/10.1105/tpc.15.00471

[35] Li C, Yeh FL, Cheung AY, Duan Q, Kita D, Liu MC, Maman J, Luu EJ, Wu BW, Gates L, Jalal M, Kwong A, Carpenter H, Wu HM (2015) Glycosylphosphatidylinositol-anchored proteins as chaperones and co-receptors for FERONIA receptor kinase signaling in Arabidopsis. Elife 4:e06587. https://doi.org/10.7554/eLife.06587

[36] LiB, MengX, ShanL, HeP. Transcriptional regulation of pattern-triggered immunity in plants. Cell Host Microbe, 2016, 19(5):641-650

[37] LiC, WuHM, CheungAY. FERONIA and her pals: functions and mechanisms. Plant Physiol, 2016, 171(4):2379-2392

[38] LiuJ, HuangY, KongL, YuX, FengB, LiuD, ZhaoB, MendesGC, YuanP, GeD, WangWM, FontesEPB, LiP, ShanL, HeP. The malectin-like receptor-like kinase LETUM1 modulates NLR protein SUMM2 activation via MEKK2 scaffolding. Nat Plants, 2020, 6(9):1106-1115

[39] LiuJ, LiJ, ShanL. SERKs. Curr Biol, 2020, 30(7):R293-R294

[40] LiuZ, WuY, YangF, ZhangY, ChenS, XieQ, TianX, ZhouJM. BIK1 interacts with PEPRs to mediate ethylene-induced immunity. Proc Natl Acad Sci U S A, 2013, 110(15):6205-6210

[41] LuD, LinW, GaoX, WuS, ChengC, AvilaJ, HeeseA, DevarenneTP, HeP, ShanL. Direct ubiquitination of pattern recognition receptor FLS2 attenuates plant innate immunity. Science, 2011, 332(6036):1439-1442

[42] LuoL. Plant cytokine or phytocytokine. Plant Signal Behav, 2012, 7(12):1513-1514

[43] Ma X, Xu G, He P, Shan L (2016) SERKing coreceptors for receptors. Trends Plant Sci 21(12):1017–1033. https://doi.org/10.1016/j.tplants.2016.08.014

[44] MangH, FengB, HuZ, Boisson-DernierA, FranckCM, MengX, HuangY, ZhouJ, XuG, WangT, ShanL, HeP. Differential regulation of two-tiered plant immunity and sexual reproduction by ANXUR receptor-like kinases. Plant Cell, 2017, 29(12):3140-3156

[45] Masachis S, Segorbe D, Turrà D, Leon-Ruiz M, Fürst U, El Ghalid M, Leonard G, López-Berges MS, Richards TA, Felix G, Di Pietro A (2016) A fungal pathogen secretes plant alkalinizing peptides to increase infection. Nat Microbiol 1(6):16043. https://doi.org/10.1038/nmicrobiol.2016.43

[46] MatsubayashiY. Posttranslationally modified small-peptide signals in plants. Annu Rev Plant Biol, 2014, 65(1):385-413

[47] MatsubayashiY, OgawaM, MoritaA, SakagamiY. An LRR receptor kinase involved in perception of a peptide plant hormone, phytosulfokine. Science, 2002, 296(5572):1470-1472

[48] Matsubayashi Y, Sakagami Y (1996) Phytosulfokine, sulfated peptides that induce the proliferation of single mesophyll cells of Asparagus officinalis L. Proc Natl Acad Sci U S A 93(15):7623–7627. https://doi.org/10.1073/pnas.93.15.7623

[49] MatsuzakiY, Ogawa-OhnishiM, MoriA, MatsubayashiY. Secreted peptide signals required for maintenance of root stem cell niche in Arabidopsis. Science, 2010, 329(5995):1065-1067

[50] McGurlB, PearceG, Orozco-CardenasM, RyanCA. Structure, expression, and antisense inhibition of the systemin precursor gene. Science, 1992, 255(5051):1570-1573

[51] MosherS, SeyboldH, RodriguezP, StahlM, DaviesKA, DayaratneS, MorilloSA, WierzbaM, FaveryB, KellerH, TaxFE, KemmerlingB. The tyrosine-sulfated peptide receptors PSKR1 and PSY1R modify the immunity of Arabidopsis to biotrophic and necrotrophic pathogens in an antagonistic manner. Plant J, 2013, 73(3):469-482

[52] Narvaez-VasquezJ, PearceG, RyanCA. The plant cell wall matrix harbors a precursor of defense signaling peptides. Proc Natl Acad Sci U S A, 2005, 102(36):12974-12977

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

[54] OlssonV, JoosL, ZhuS, GevaertK, ButenkoMA, De SmetI. Look closely, the beautiful may be small: precursor-derived peptides in plants. Annu Rev Plant Biol, 2019, 70(1):153-186

[55] Ou Y, Lu X, Zi Q, Xun Q, Zhang J, Wu Y, Shi H, Wei Z, Zhao B, Zhang X, He K, Gou X, Li C, Li J (2016) RGF1 INSENSITIVE 1 to 5, a group of LRR receptor-like kinases, are essential for the perception of root meristem growth factor 1 in Arabidopsis thaliana. Cell Res 26(6):686–698. https://doi.org/10.1038/cr.2016.63

[56] PatharkarOR, WalkerJC. Core mechanisms regulating developmentally timed and environmentally triggered abscission. Plant Physiol, 2016, 172(1):510-520

[57] PearceG, MouraDS, StratmannJ, RyanCA. Production of multiple plant hormones from a single polyprotein precursor. Nature, 2001, 411(6839):817-820

[58] PearceG, MouraDS, StratmannJ, RyanCA Jr. RALF, a 5-kDa ubiquitous polypeptide in plants, arrests root growth and development. Proc Natl Acad Sci U S A, 2001, 98(22):12843-12847

[59] PearceG, StrydomD, JohnsonS, RyanCA. A polypeptide from tomato leaves induces wound-inducible proteinase inhibitor proteins. Science, 1991, 253(5022):895-897

[60] Pearce G, Ryan CA (2003) Systemic signaling in tomato plants for defense against herbivores: isolation and characterization of three novel defense-signaling glycopeptide hormones coded in a single precursor gene. J Biol Chem 278(32):30044–30050. https://doi.org/10.1074/jbc.M304159200

[61] Poncini L, Wyrsch I, Denervaud Tendon V, Vorley T, Boller T, Geldner N, Metraux JP, Lehmann S (2017) In roots of Arabidopsis thaliana, the damage-associated molecular pattern AtPep1 is a stronger elicitor of immune signalling than flg22 or the chitin heptamer. PLoS One 12(10):e0185808. https://doi.org/10.1371/journal.pone.0185808

[62] PoretskyE, DressanoK, WeckwerthP, RuizM, CharSN, ShiD, AbagyanR, YangB, HuffakerA. Differential activities of maize plant elicitor peptides as mediators of immune signaling and herbivore resistance. Plant J, 2020, 104(6):1582-1602

[63] PruittRN, JoeA, ZhangW, FengW, StewartV, SchwessingerB, DinnenyJR, RonaldPC. A microbially derived tyrosine-sulfated peptide mimics a plant peptide hormone. New Phytol, 2017, 215(2):725-736

[64] Pruitt RN, Schwessinger B, Joe A, Thomas N, Liu F, Albert M, Robinson MR, Chan LJ, Luu DD, Chen H et al (2015) The rice immune receptor XA21 recognizes a tyrosine-sulfated protein from a gram-negative bacterium. Sci Adv 1(6):e1500245. https://doi.org/10.1126/sciadv.1500245

[65] RanfS, Eschen-LippoldL, PecherP, LeeJ, ScheelD. Interplay between calcium signalling and early signalling elements during defence responses to microbe- or damage-associated molecular patterns. Plant J, 2011, 68(1):100-113

[66] ReichardtS, PiephoHP, StintziA, SchallerA. Peptide signaling for drought-induced tomato flower drop. Science, 2020, 367(6485):1482-1485

[67] 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

[68] Rich-GriffinC, EichmannR, ReitzMU, HermannS, Woolley-AllenK, BrownPE, WiwatdirekkulK, EstebanE, PashaA, KogelKH, ProvartNJ, OttS, SchäferP. Regulation of cell type-specific immunity networks in Arabidopsis roots. Plant Cell, 2020, 32(9):2742-2762

[69] Rodiuc N, Barlet X, Hok S, Perfus-Barbeoch L, Allasia V, Engler G, Séassau A, Marteu N, de Almeida-Engler J, Panabières F, Abad P, Kemmerling B, Marco Y, Favery B, Keller H (2016) Evolutionarily distant pathogens require the Arabidopsis phytosulfokine signalling pathway to establish disease. Plant Cell Environ 39(7):1396–1407 https://doi.org/10.1111/pce.12627

[70] RonaldP, JoeA. Molecular mimicry modulates plant host responses to pathogens. Ann Bot, 2018, 121(1):17-23

[71] RossA, YamadaK, HirumaK, Yamashita-YamadaM, LuX, TakanoY, TsudaK, SaijoY. The Arabidopsis PEPR pathway couples local and systemic plant immunity. EMBO J, 2014, 33(1):62-75

[72] Ryan CA, Pearce G (2003) Systemins: a functionally defined family of peptide signals that regulate defensive genes in Solanaceae species. Proc Natl Acad Sci U S A 100(Suppl 2):14577–14580. https://doi.org/10.1073/pnas.1934788100

[73] Santiago J, Brandt B, Wildhagen M, Hohmann U, Hothorn LA, Butenko MA, Hothorn M (2016) Mechanistic insight into a peptide hormone signaling complex mediating floral organ abscission. Elife 5:e15075. https://doi.org/10.7554/eLife.15075

[74] SauterM. Phytosulfokine peptide signalling. J Exp Bot, 2015, 66(17):5161-5169

[75] SchardonK, HohlM, GraffL, PfannstielJ, SchulzeW, StintziA, SchallerA. Precursor processing for plant peptide hormone maturation by subtilisin-like serine proteinases. Science, 2016, 354(6319):1594-1597

[76] Shen W, Liu J, Li JF (2019) Type-II metacaspases mediate the processing of plant elicitor peptides in Arabidopsis. Mol Plant 12(11):1524–1533. https://doi.org/10.1016/j.molp.2019.08.003

[77] Shen Y, Diener AC (2013) Arabidopsis thaliana RESISTANCE TO FUSARIUM OXYSPORUM 2 implicates tyrosine-sulfated peptide signaling in susceptibility and resistance to root infection. PLoS Genet 9(5):e1003525. https://doi.org/10.1371/journal.pgen.1003525

[78] Shiu SH, Bleecker AB (2001) Receptor-like kinases from Arabidopsis form a monophyletic gene family related to animal receptor kinases. Proc Natl Acad Sci U S A 98(19):10763–10768. https://doi.org/10.1073/pnas.181141598

[79] SongWY, WangGL, ChenLL, KimHS, PiLY, HolstenT, GardnerJ, WangB, ZhaiWX, ZhuLH, FauquetC, RonaldP. A receptor kinase-like protein encoded by the rice disease resistance gene, Xa21. Science, 1995, 270(5243):1804-1806

[80] SrivastavaR, LiuJX, GuoH, YinY, HowellSH. Regulation and processing of a plant peptide hormone, AtRALF23, in Arabidopsis. Plant J, 2009, 59(6):930-939

[81] SrivastavaR, LiuJX, HowellSH. Proteolytic processing of a precursor protein for a growth-promoting peptide by a subtilisin serine protease in Arabidopsis. Plant J, 2008, 56(2):219-227

[82] StegmannM, MonaghanJ, Smakowska-LuzanE, RovenichH, LehnerA, HoltonN, BelkhadirY, ZipfelC. The receptor kinase FER is a RALF-regulated scaffold controlling plant immune signaling. Science, 2017, 355(6322):287-289

[83] Stegmann, M, Zecua-Ramirez, P, Ludwig, C, Lee, HS, Peterson, B, Nimchuk, ZL, Belkhadir Y, Hückelhoven, R (2021). RGI-GOLVEN signalling promotes FLS2 abundance to regulate plant immunity. bioRxiv preprint. https://doi.org/10.1101/2021.01.29.428839

[84] Stenvik GE, Tandstad NM, Guo Y, Shi CL, Kristiansen W, Holmgren A, Clark SE, Aalen RB, Butenko MA (2008) The EPIP peptide of INFLORESCENCE DEFICIENT IN ABSCISSION is sufficient to induce abscission in Arabidopsis through the receptor-like kinases HAESA and HAESA-LIKE2. Plant Cell 20(7):1805–1817. https://doi.org/10.1105/tpc.108.059139

[85] StuhrwohldtN, BuhlerE, SauterM, SchallerA. Phytosulfokine (PSK) precursor processing by subtilase SBT3.8 and PSK signaling improve drought stress tolerance in Arabidopsis. J Exp Bot, 2021, 72(9):3427-3440

[86] TakahashiF, HanadaK, KondoT, ShinozakiK. Hormone-like peptides and small coding genes in plant stress signaling and development. Curr Opin Plant Biol, 2019, 51: 88-95

[87] TanakaK, HeilM. Damage-associated molecular patterns (DAMPs) in plant innate immunity: applying the danger model and evolutionary perspectives. Annu Rev Phytopathol, 2021, 59(1):53-75

[88] ThynneE, SaurIML, SimbaquebaJ, OgilvieHA, Gonzalez-CendalesY, MeadO, TarantoA, CatanzaritiAM, McDonaldMC, SchwessingerB, JonesDA, RathjenJP, SolomonPS. Fungal phytopathogens encode functional homologues of plant rapid alkalinization factor (RALF) peptides. Mol Plant Pathol, 2017, 18(6):811-824

[89] TintorN, RossA, KaneharaK, YamadaK, FanL, KemmerlingB, NurnbergerT, TsudaK, SaijoY. Layered pattern receptor signaling via ethylene and endogenous elicitor peptides during Arabidopsis immunity to bacterial infection. Proc Natl Acad Sci U S A, 2013, 110(15):6211-6216

[90] VieAK, NajafiJ, LiuB, WingeP, ButenkoMA, HornslienKS, KumpfR, AalenRB, BonesAM, BrembuT. The IDA/IDA-LIKE and PIP/PIP-LIKE gene families in Arabidopsis: phylogenetic relationship, expression patterns, and transcriptional effect of the PIPL3 peptide. J Exp Bot, 2015, 66(17):5351-5365

[91] Wang X, Lupardus P, Laporte SL, Garcia KC (2009) Structural biology of shared cytokine receptors. Annu Rev Immunol 27:29–60. https://doi.org/10.1146/annurev.immunol.24.021605.090616

[92] WangJ, LiH, HanZ, ZhangH, WangT, LinG, ChangJ, YangW, ChaiJ. Allosteric receptor activation by the plant peptide hormone phytosulfokine. Nature, 2015, 525(7568):265-268

[93] WangL, EinigE, Almeida-TrappM, AlbertM, FliegmannJ, MithoferA, KalbacherH, FelixG. The systemin receptor SYR1 enhances resistance of tomato against herbivorous insects. Nat Plants, 2018, 4(3):152-156

[94] Wang X, Hou S, Wu Q, Lin M, Acharya BR, Wu D, Zhang W (2017) IDL6-HAE/HSL2 impacts pectin degradation and resistance to Pseudomonas syringae pv tomato DC3000 in Arabidopsis leaves. Plant J 89(2):250–263. https://doi.org/10.1111/tpj.13380

[95] WangX, ZhangN, ZhangL, HeY, CaiC, ZhouJ, LiJ, MengX. Perception of the pathogen-induced peptide RGF7 by the receptor-like kinases RGI4 and RGI5 triggers innate immunity in Arabidopsis thaliana. New Phytol, 2021, 230(3):1110-1125

[96] WhitfordR, FernandezA, TejosR, PerezAC, Kleine-VehnJ, VannesteS, DrozdzeckiA, LeitnerJ, AbasL, AertsM, et al.. GOLVEN secretory peptides regulate auxin carrier turnover during plant gravitropic responses. Dev Cell, 2012, 22(3):678-685

[97] Wood AKM, Walker C, Lee WS, Urban M, Hammond-Kosack KE (2020) Functional evaluation of a homologue of plant rapid alkalinisation factor (RALF) peptides in Fusarium graminearum. Fungal Biol 124(9):753–765. https://doi.org/10.1016/j.funbio.2020.05.001

[98] XiaoY, StegmannM, HanZ, DeFalcoTA, ParysK, XuL, BelkhadirY, ZipfelC, ChaiJ. Mechanisms of RALF peptide perception by a heterotypic receptor complex. Nature, 2019, 572(7768):270-274

[99] YamadaK, Yamashita-YamadaM, HiraseT, FujiwaraT, TsudaK, HirumaK, SaijoY. Danger peptide receptor signaling in plants ensures basal immunity upon pathogen-induced depletion of BAK1. EMBO J, 2016, 35(1):46-61

[100] YamaguchiY, BaronaG, RyanCA, PearceG. GmPep914, an eight-amino acid peptide isolated from soybean leaves, activates defense-related genes. Plant Physiol, 2011, 156(2):932-942

[101] 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

[102] 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 U S A, 2006, 103(26):10104-10109

[103] YangH, MatsubayashiY, NakamuraK, SakagamiY. Diversity of Arabidopsis genes encoding precursors for phytosulfokine, a peptide growth factor. Plant Physiol, 2001, 127(3):842-851

[104] YuF, QianL, NibauC, DuanQ, KitaD, LevasseurK, LiX, LuC, LiH, HouC, LiL, BuchananBB, ChenL, CheungAY, LiD, LuanS. FERONIA receptor kinase pathway suppresses abscisic acid signaling in Arabidopsis by activating ABI2 phosphatase. Proc Natl Acad Sci U S A, 2012, 109(36):14693-14698

[105] Yu X, Feng B, He P, Shan L (2017) From chaos to harmony: responses and signaling upon microbial pattern recognition. Annu Rev Phytopathol 55(1):109–137. https://doi.org/10.1146/annurev-phyto-080516-035649

[106] Yu Z, Xu Y, Zhu L, Zhang L, Liu L, Zhang D, Li D, Wu C, Huang J, Yang G, Yan K, Zhang S, Zheng C (2020) The Brassicaceae-specific secreted peptides, STMPs, function in plant growth and pathogen defense. J Integr Plant Biol 62(4):403–420. https://doi.org/10.1111/jipb.12817

[107] 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

[108] Zhang H, Hu Z, Lei C, Zheng C, Wang J, Shao S, Li X, Xia X, Cai X, Zhou J, Zhou Y, Yu J, Foyer CH, Shi K (2018) A plant phytosulfokine peptide initiates auxin-dependent immunity through cytosolic Ca (2+) signaling in tomato. Plant Cell 30(3):652–667. https://doi.org/10.1105/tpc.17.00537

[109] ZhangH, ZhangH, LinJ. Systemin-mediated long-distance systemic defense responses. New Phytol, 2020, 226(6):1573-1582

[110] ZhangX, PengH, ZhuS, XingJ, LiX, ZhuZ, ZhengJ, WangL, WangB, ChenJ, MingZ, YaoK, JianJ, LuanS, Coleman-DerrD, LiaoH, PengY, PengD, YuF. Nematode-encoded RALF peptide mimics facilitate parasitism of plants through the FERONIA receptor kinase. Mol Plant, 2020, 13(10):1434-1454

[111] ZhaoC, ZayedO, YuZ, JiangW, ZhuP, HsuCC, ZhangL, TaoWA, Lozano-DuranR, ZhuJK. Leucine-rich repeat extensin proteins regulate plant salt tolerance in Arabidopsis. Proc Natl Acad Sci U S A, 2018, 115(51):13123-13128

[112] ZhouJM, ZhangY. Plant immunity: danger perception and signaling. Cell, 2020, 181(5):978-989

[113] Zhu P, Yu XH, Wang C, Zhang Q, Liu W, McSweeney S, Shanklin J, Lam E, Liu Q (2020) Structural basis for Ca (2+)- dependent activation of a plant metacaspase. Nat Commun 11(1):2249. https://doi.org/10.1038/s41467-020-15830-8

[114] Zhu S, Fu Q, Xu F, Zheng H, Yu F (2021) New paradigms in cell adaptation: decades of discoveries on the CrRLK1L receptor kinase signalling network. New Phytol. https://doi.org/10.1111/nph.17683

[115] ZiemannS, van der LindeK, LahrmannU, AcarB, KaschaniF, ColbyT, KaiserM, DingY, SchmelzE, HuffakerA, HoltonN, ZipfelC, DoehlemannG. An apoplastic peptide activates salicylic acid signalling in maize. Nat Plants, 2018, 4(3):172-180

Funding

national institutes of health(R01GM092893); youth innovation technology project of higher school in shandong province(2020KJF013); natural science foundation of shandong province(ZR2020MC022); national science foundation(IOS-1951094)