Rapid alkalinization factor: function, regulation, and potential applications in agriculture

Abstract

Rapid alkalinization factor (RALF) is widespread throughout the plant kingdom and controls many aspects of plant life. Current studies on the regulatory mechanism underlying RALF function mainly focus on Arabidopsis, but little is known about the role of RALF in crop plants. Here, we systematically and comprehensively analyzed the relation between RALF family genes from five important crops and those in the model plant Arabidopsis thaliana. Simultaneously, we summarized the functions of RALFs in controlling growth and developmental behavior using conservative motifs as cues and predicted the regulatory role of RALFs in cereal crops. In conclusion, RALF has considerable application potential in improving crop yields and increasing economic benefits. Using gene editing technology or taking advantage of RALF as a hormone additive are effective way to amplify the role of RALF in crop plants.

Keywords

RALF / Fertilization / Stress / Crops / Molecular regulatory network

References

[1] AbarcaA, FranckCM, ZipfelC. Family-wide evaluation of RAPID ALKALINIZATION FACTOR peptides. Plant Physiol, 2021, 187: 996-1010

[2] ArayaT, MiyamotoM, WibowoJ, SuzukiA, KojimaS, TsuchiyaYN, SawaS, FukudaH, von WirenN, TakahashiH. CLE-CLAVATA1 peptide-receptor signaling module regulates the expansion of plant root systems in a nitrogen-dependent manner. Proc Natl Acad Sci U S A, 2014, 111: 2029-2034

[3] AtkinsonNJ, LilleyCJ, UrwinPE. Identification of genes involved in the response of Arabidopsis to simultaneous biotic and abiotic stresses. Plant Physiol, 2013, 162: 2028-2041

[4] BarbezE, DunserK, GaidoraA, LendlT, BuschW. Auxin steers root cell expansion via apoplastic pH regulation in Arabidopsis thaliana. Proc Natl Acad Sci U S A, 2017, 114: E4884-E4893

[5] BelkhadirY, JaillaisY. The molecular circuitry of brassinosteroid signaling. New Phytol, 2015, 206: 522-540

[6] BergerD, AltmannTJG, development, . A subtilisin-like serine protease involved in the regulation of stomatal density and distribution in Arabidopsis thaliana. Genes Dev, 2000, 14: 1119-1131

[7] Bergonci T, Silva-Filho MC, Moura DS (2014b) Antagonistic relationship between AtRALF1 and brassinosteroid regulates cell expansion-related genes. Plant Signal Behav 9:e976146. https://doi.org/10.4161/15592324.2014.976146

[8] BergonciT, RibeiroB, CeciliatoPH, Guerrero-AbadJC, Silva-FilhoMC, MouraDS. Arabidopsis thaliana RALF1 opposes brassinosteroid effects on root cell elongation and lateral root formation. J Exp Bot, 2014, 65: 2219-2230

[9] BettiF, Ladera-CarmonaMJ, WeitsDA, FerriG, IacopinoS, NoviG, SveziaB, KunkowskaAB, SantanielloA, PiaggesiA, LoretiE, PerataP. Exogenous miRNAs induce post-transcriptional gene silencing in plants. Nat Plants, 2021, 7: 1379-1388

[10] Boisson-Dernier A, Lituiev DS, Nestorova A, Franck CM, Thirugnanarajah S, Grossniklaus U (2013) ANXUR receptor-like kinases coordinate cell wall integrity with growth at the pollen tube tip via NADPH oxidases. PLoS Biol 11:e1001719. https://doi.org/10.1371/journal.pbio.1001719

[11] Boisson-DernierA, RoyS, KritsasK, GrobeiMA, JaciubekM, SchroederJI, GrossniklausU. Disruption of the pollen-expressed FERONIA homologs ANXUR1 and ANXUR2 triggers pollen tube discharge. Development, 2009, 136: 3279-3288

[12] Boisson-DernierA, KesslerSA, GrossniklausU. The walls have ears: the role of plant CrRLK1Ls in sensing and transducing extracellular signals. J Exp Bot, 2011, 62: 1581-1591

[13] Boisson-DernierA, FranckCM, LituievDS, GrossniklausU. Receptor-like cytoplasmic kinase MARIS functions downstream of CrRLK1L-dependent signaling during tip growth. Proc Natl Acad Sci U S A, 2015, 112: 12211-12216

[14] CampbellL, TurnerSR. A Comprehensive Analysis of RALF Proteins in Green Plants Suggests There Are Two Distinct Functional Groups. Front Plant Sci, 2017, 8: 37

[15] CamposWF, DressanoK, CeciliatoPHO, Guerrero-AbadJC, SilvaAL, FioriCS, Morato do Canto A, Bergonci T, Claus LAN, Silva-Filho MC, Moura DS, . Arabidopsis thaliana rapid alkalinization factor 1-mediated root growth inhibition is dependent on calmodulin-like protein 38. J Biol Chem, 2018, 293: 2159-2171

[16] CaoJ, ShiF. Evolution of the RALF Gene Family in Plants: Gene Duplication and Selection Patterns. Evol Bioinform Online, 2012, 8: 271-292

[17] CapronA, GourguesM, NeivaLS, FaureJE, BergerF, PagnussatG, KrishnanA, Alvarez-MejiaC, Vielle-CalzadaJP, LeeYR, LiuB, SundaresanV. Maternal control of male-gamete delivery in Arabidopsis involves a putative GPI-anchored protein encoded by the LORELEI gene. Plant Cell, 2008, 20: 3038-3049

[18] ChakravortyD, YuY, AssmannSM. A kinase-dead version of FERONIA receptor-like kinase has dose-dependent impacts on rosette morphology and RALF1-mediated stomatal movements. FEBS Lett, 2018, 592: 3429-3437

[19] ChenJ, YuF, LiuY, DuC, LiX, ZhuS, WangX, LanW, RodriguezPL, LiuX, LiD, ChenL, LuanS. 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, 2016, 113: E5519-5527

[20] ChenK, KeR, DuM, YiY, ChenY, WangX, YaoL, LiuH, HouX, XiongL, YangY, XieK. A FLASH pipeline for arrayed CRISPR library construction and the gene function discovery of rice receptor-like kinases. Mol Plant, 2022, 15: 243-257

[21] ChevalierE, Loubert-HudonA, MattonDP. ScRALF3, a secreted RALF-like peptide involved in cell-cell communication between the sporophyte and the female gametophyte in a solanaceous species. Plant J, 2013, 73: 1019-1033

[22] GuoH, YeH, LiL, Yin YJPs, behavior, . A family of receptor-like kinases are regulated by BES1 and involved in plant growth in Arabidopsis thaliana. Plant Signal Behav, 2009, 4: 784-786

[23] Cheung AY, Duan Q, Li C, James Liu MC, Wu HM (2022) Pollen-pistil interactions: It takes two to tangle but a molecular cast of many to deliver. Curr Opin Plant Biol 69:102279. https://doi.org/10.1016/j.pbi.2022.102279

[24] ClouseSD. Brassinosteroid signal transduction: from receptor kinase activation to transcriptional networks regulating plant development. Plant Cell, 2011, 23: 1219-1230

[25] CombierJP, KüsterH, JournetEP, HohnjecN, NiebelAJMPMI. Evidence for the Involvement in Nodulation of the Two Small Putative Regulatory Peptide-Encoding Genes MtRALFL1 and MtDVL1. Mol Plant Microbe Interact, 2008, 21: 1118-1127

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

[27] CoveyPA, SubbaiahCC, ParsonsRL, PearceG, LayFT, AndersonMA, RyanCA, BedingerPA. A pollen-specific RALF from tomato that regulates pollen tube elongation. Plant Physiol, 2010, 153: 703-715

[28] De SamblanxG, Fernandez del CarmenA, SijtsmaL, PlasmanH, SchaaperW, PosthumaG, FantF, MeloenR, BroekaertW, AmerongenV, AJPr, . Antifungal activity of synthetic 15-mer peptides based on the Rs-AFP2 (Raphanus sativus antifungal protein 2) sequence. Pept Res, 1996, 9: 262-268

[29] DemidchikV, MaathuisFJM. Physiological roles of nonselective cation channels in plants: from salt stress to signalling and development. New Phytol, 2007, 175: 387-404

[30] DenningerP, BleckmannA, LausserA, VoglerF, OttT, EhrhardtDW, FrommerWB, SprunckS, DresselhausT, GrossmannG. Male-female communication triggers calcium signatures during fertilization in Arabidopsis. Nat Commun, 2014, 5: 4645

[31] DievartA, GottinC, PerinC, RanwezV, ChantretN. Origin and Diversity of Plant Receptor-Like Kinases. Annu Rev Plant Biol, 2020, 71: 131-156

[32] Dressano K, Ceciliato PHO, Silva AL, Guerrero-Abad JC, Bergonci T, Ortiz-Morea FA, Burger M, Silva-Filho MC, Moura DS (2017) BAK1 is involved in AtRALF1-induced inhibition of root cell expansion. PLoS Genet 13:e1007053. https://doi.org/10.1371/journal.pgen.1007053

[33] DresselhausT, SprunckS, WesselGM. Fertilization Mechanisms in Flowering Plants. Curr Biol, 2016, 26: R125-139

[34] Dunser K, Gupta S, Herger A, Feraru MI, Ringli C, Kleine-Vehn J (2019) Extracellular matrix sensing by FERONIA and Leucine-Rich Repeat Extensins controls vacuolar expansion during cellular elongation in Arabidopsis thaliana. EMBO J 38:https://doi.org/10.15252/embj.2018100353

[35] DuC, LiX, ChenJ, ChenW, LiB, LiC, WangL, LiJ, ZhaoX, LinJ, LiuX, LuanS, YuF. Receptor kinase complex transmits RALF peptide signal to inhibit root growth in Arabidopsis. Proc Natl Acad Sci U S A, 2016, 113: E8326-E8334

[36] DuS, QuLJ, XiaoJ. Crystal structures of the extracellular domains of the CrRLK1L receptor-like kinases ANXUR1 and ANXUR2. Protein Sci, 2018, 27: 886-892

[37] DuanQ, KitaD, LiC, CheungAY, WuHM. FERONIA receptor-like kinase regulates RHO GTPase signaling of root hair development. Proc Natl Acad Sci U S A, 2010, 107: 17821-17826

[38] DuanQ, KitaD, JohnsonEA, AggarwalM, GatesL, WuHM, CheungAY. Reactive oxygen species mediate pollen tube rupture to release sperm for fertilization in Arabidopsis. Nat Commun, 2014, 5: 3129

[39] DuanQ, LiuMJ, KitaD, JordanSS, YehFJ, YvonR, CarpenterH, FedericoAN, Garcia-ValenciaLE, EylesSJ, WangCS, WuHM, CheungAY. FERONIA controls pectin- and nitric oxide-mediated male-female interaction. Nature, 2020, 579: 561-566

[40] DuanZ, LiuW, LiK, DuanW, ZhuS, XingJ, ChenT, LuoX. Regulation of immune complex formation and signalling by FERONIA, a busy goddess in plant-microbe interactions. Mol Plant Pathol, 2022, 23: 1695-1700

[41] DupuisI, Dumas CJPp, . Influence of temperature stress on in vitro fertilization and heat shock protein synthesis in maize (Zea mays L.) reproductive tissues. Plant Physiol, 1990, 94: 665-670

[42] Endo S, Shinohara H, Matsubayashi Y, Fukuda HJCB (2013) A novel pollen-pistil interaction conferring high-temperature tolerance during reproduction via CLE45 signaling. 23:1670–1676. https://doi.org/10.1016/j.cub.2013.06.060

[43] FengH, LiuC, FuR, ZhangM, LiH, ShenL, WeiQ, SunX, XuL, NiB, LiC. LORELEI-LIKE GPI-ANCHORED PROTEINS 2/3 Regulate Pollen Tube Growth as Chaperones and Coreceptors for ANXUR/BUPS Receptor Kinases in Arabidopsis. Mol Plant, 2019, 12: 1612-1623

[44] Feng W, Kita D, Peaucelle A, Cartwright HN, Doan V, Duan Q, Liu MC, Maman J, Steinhorst L, Schmitz-Thom I, Yvon R, Kudla J, Wu HM, Cheung AY, Dinneny JR (2018) The FERONIA receptor kinase maintains cell-wall integrity during salt stress through Ca(2+) signaling. Curr Biol 28:666–675 e665. https://doi.org/10.1016/j.cub.2018.01.023

[45] ForemanJ, DemidchikV, BothwellJH, MylonaP, MiedemaH, TorresMA, LinsteadP, CostaS, BrownleeC, JonesJDJN. Reactive oxygen species produced by NADPH oxidase regulate plant cell growth. Nature, 2003, 422: 442-446

[46] FrederickRO, HarutaM, TonelliM, LeeW, CornilescuG, CornilescuCC, SussmanMR, MarkleyJL. Function and solution structure of the Arabidopsis thaliana RALF8 peptide. Protein Sci, 2019, 28: 1115-1126

[47] FuglsangAT, GuoY, CuinTA, QiuQ, SongC, KristiansenKA, BychK, SchulzA, ShabalaS, SchumakerKS, PalmgrenMG, ZhuJK. Arabidopsis protein kinase PKS5 inhibits the plasma membrane H+ -ATPase by preventing interaction with 14–3-3 protein. Plant Cell, 2007, 19: 1617-1634

[48] Galindo-Trigo S, Blanco-Tourinan N, DeFalco TA, Wells ES, Gray JE, Zipfel C, Smith LM (2020) CrRLK1L receptor-like kinases HERK1 and ANJEA are female determinants of pollen tube reception. EMBO Rep 21:e48466. https://doi.org/10.15252/embr.201948466

[49] GaoQ, WangC, XiY, ShaoQ, LiL, LuanS. A receptor-channel trio conducts Ca(2+) signalling for pollen tube reception. Nature, 2022, 607: 534-539

[50] GaoQ, WangC, XiY, ShaoQ, HouC, LiL, LuanS. RALF signaling pathway activates MLO calcium channels to maintain pollen tube integrity. Cell Res, 2023, 33: 71-79

[51] GeZ, BergonciT, ZhaoY, ZouY, DuS, LiuM-C, LuoX, RuanH, García-ValenciaLE, ZhongSJS. Arabidopsis pollen tube integrity and sperm release are regulated by RALF-mediated signaling. Science, 2017, 358: 1596-1600

[52] Ge Z, Zhao Y, Liu MC, Zhou LZ, Wang L, Zhong S, Hou S, Jiang J, Liu T, Huang Q, Xiao J, Gu H, Wu HM, Dong J, Dresselhaus T, Cheung AY, Qu LJ (2019) LLG2/3 are co-receptors in BUPS/ANX-RALF signaling to regulate arabidopsis pollen tube integrity. Curr Biol 29:3256–3265 e3255. https://doi.org/10.1016/j.cub.2019.08.032

[53] GinanjarEF, TehOK, FujitaT. Characterisation of rapid alkalinisation factors in Physcomitrium patens reveals functional conservation in tip growth. New Phytol, 2022, 233: 2442-2457

[54] GjettingSK, MahmoodK, ShabalaL, KristensenA, ShabalaS, PalmgrenM, FuglsangAT. Evidence for multiple receptors mediating RALF-triggered Ca(2+) signaling and proton pump inhibition. Plant J, 2020, 104: 433-446

[55] Gonneau M, Desprez T, Martin M, Doblas VG, Bacete L, Miart F, Sormani R, Hematy K, Renou J, Landrein B, Murphy E, Van De Cotte B, Vernhettes S, De Smet I, Hofte H (2018) Receptor Kinase THESEUS1 Is a Rapid Alkalinization Factor 34 Receptor in Arabidopsis. Curr Biol 28:2452–2458 e2454. https://doi.org/10.1016/j.cub.2018.05.075

[56] Gronnier J, Franck CM, Stegmann M, DeFalco TA, Abarca A, von Arx M, Dunser K, Lin W, Yang Z, Kleine-Vehn J, Ringli C, Zipfel C (2022) Regulation of immune receptor kinase plasma membrane nanoscale organization by a plant peptide hormone and its receptors. Elife 11:https://doi.org/10.7554/eLife.74162

[57] GuoH, LiL, YeH, YuX, AlgreenA, Yin YJPotNAoS, . Three related receptor-like kinases are required for optimal cell elongation in Arabidopsis thaliana. Proc Natl Acad Sci, 2009, 106: 7648-7653

[58] 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. https://doi.org/10.1016/j.cub.2018.07.078

[59] GuptaA, Rico-MedinaA, Caño-DelgadoAIJS. The physiology of plant responses to drought. Science, 2020, 368: 266-269

[60] HamannT. The plant cell wall integrity maintenance mechanism-concepts for organization and mode of action. Plant Cell Physiol, 2015, 56: 215-223

[61] HarutaM, MonshausenG, GilroyS, SussmanMRJB. A cytoplasmic Ca2+ functional assay for identifying and purifying endogenous cell signaling peptides in Arabidopsis seedlings: identification of AtRALF1 peptide. Biochemistry, 2008, 47: 6311-6321

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

[63] HayashiY, TanoiK, NishiyamaH, NakanishiTMJSS, NutritionP. Rhizosphere pH profile of rice plant influenced by Al treatment. Soil Science and Plant Nutrition, 2005, 51: 729-731

[64] He YH, Zhang ZR, Xu YP, Chen SY, Cai XZ (2022) Genome-wide identification of rapid alkalinization factor family in brassica napus and functional analysis of BnRALF10 in immunity to Sclerotinia sclerotiorum. Front Plant Sci 13:877404. https://doi.org/10.3389/fpls.2022.877404

[65] HoelscherMP, FornerJ, CalderoneS, KramerC, TaylorZ, LoiaconoFV, AgrawalS, KarcherD, MorattiF, KroopX, BockR. Expression strategies for the efficient synthesis of antimicrobial peptides in plastids. Nat Commun, 2022, 13: 5856

[66] HoffmannRD, OlsenLI, EzikeCV, PedersenJT, ManstrettaR, Lopez-MarquesRL, PalmgrenM. Roles of plasma membrane proton ATPases AHA2 and AHA7 in normal growth of roots and root hairs in Arabidopsis thaliana. Physiol Plant, 2019, 166: 848-861

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

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

[69] IwanoM, IgarashiM, TarutaniY, Kaothien-NakayamaP, NakayamaH, MoriyamaH, YakabeR, EntaniT, Shimosato-AsanoH, UekiMJTPC. A pollen coat–inducible autoinhibited Ca2+-ATPase expressed in stigmatic papilla cells is required for compatible pollination in the Brassicaceae. Plant Cell, 2014, 26: 636-649

[70] JiangY, LahlaliR, KarunakaranC, WarkentinTD, DavisAR, BueckertRA. Pollen, ovules, and pollination in pea: Success, failure, and resilience in heat. Plant Cell Environ, 2019, 42: 354-372

[71] Jiang W, Li C, Li L, Li Y, Wang Z, Yu F, Yi F, Zhang J, Zhu JK, Zhang H, Li Y, Zhao C (2022) Genome-wide analysis of CqCrRLK1L and CqRALF gene families in Chenopodium quinoa and their roles in salt stress response. Front Plant Sci 13:918594. https://doi.org/10.3389/fpls.2022.918594

[72] JinY, YangH, WeiZ, MaH, GeXJMP. Rice male development under drought stress: phenotypic changes and stage-dependent transcriptomic reprogramming. Mol Plant, 2013, 6: 1630-1645

[73] KadotaY, SklenarJ, DerbyshireP, StransfeldL, AsaiS, NtoukakisV, JonesJD, ShirasuK, MenkeF, JonesA, ZipfelC. Direct regulation of the NADPH oxidase RBOHD by the PRR-associated kinase BIK1 during plant immunity. Mol Cell, 2014, 54: 43-55

[74] Kasahara RD, Maruyama D, Higashiyama T (2013) Fertilization recovery system is dependent on the number of pollen grains for efficient reproduction in plants. Plant Signal Behav 8:e23690. https://doi.org/10.4161/psb.23690

[75] Kessler SA, Lindner H, Jones DS, Grossniklaus U (2015) Functional analysis of related CrRLK1L receptor-like kinases in pollen tube reception. EMBO Rep 16:107–115. https://doi.org/10.15252/embr.201438801

[76] KouX, SunJ, WangP, WangD, CaoP, LinJ, ChangY, ZhangS, WuJ. PbrRALF2-elicited reactive oxygen species signaling is mediated by the PbrCrRLK1L13-PbrMPK18 module in pear pollen tubes. Hortic Res, 2021, 8: 222

[77] 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:https://doi.org/10.7554/eLife.06587

[78] Li C, Liu X, Qiang X, Li X, Li X, Zhu S, Wang L, Wang Y, Liao H, Luan S, Yu F (2018) EBP1 nuclear accumulation negatively feeds back on FERONIA-mediated RALF1 signaling. PLoS Biol 16:e2006340. https://doi.org/10.1371/journal.pbio.2006340

[79] Li L, Chen H, Alotaibi SS, Pencik A, Adamowski M, Novak O, Friml J (2022) RALF1 peptide triggers biphasic root growth inhibition upstream of auxin biosynthesis. Proc Natl Acad Sci U S A 119:e2121058119. https://doi.org/10.1073/pnas.2121058119

[80] LiL, LiM, YuL, ZhouZ, LiangX, LiuZ, CaiG, GaoL, ZhangX, WangY, ChenS, ZhouJM. The FLS2-associated kinase BIK1 directly phosphorylates the NADPH oxidase RbohD to control plant immunity. Cell Host Microbe, 2014, 15: 329-338

[81] LiL, VerstraetenI, RoosjenM, TakahashiK, RodriguezL, MerrinJ, ChenJ, ShabalaL, SmetW, RenH, VannesteS, ShabalaS, De RybelB, WeijersD, KinoshitaT, GrayWM, FrimlJ. Cell surface and intracellular auxin signalling for H(+) fluxes in root growth. Nature, 2021, 599: 273-277

[82] Lin W, Tang W, Pan X, Huang A, Gao X, Anderson CT, Yang Z (2022) Arabidopsis pavement cell morphogenesis requires FERONIA binding to pectin for activation of ROP GTPase signaling. Curr Biol 32:497–507 e494. https://doi.org/10.1016/j.cub.2021.11.030

[83] Liu L, Song W, Huang S, Jiang K, Moriwaki Y, Wang Y, Men Y, Zhang D, Wen X, Han Z, Chai J, Guo H (2022a) Extracellular pH sensing by plant cell-surface peptide-receptor complexes. Cell 185:3341–3355 e3313. https://doi.org/10.1016/j.cell.2022.07.012

[84] LiuX, CastroC, WangY, NobleJ, PonvertN, BundyM, HoelC, ShpakE, PalaniveluR. The Role of LORELEI in Pollen Tube Reception at the Interface of the Synergid Cell and Pollen Tube Requires the Modified Eight-Cysteine Motif and the Receptor-Like Kinase FERONIA. Plant Cell, 2016, 28: 1035-1052

[85] LiuPL, DuL, HuangY, GaoSM, YuM. Origin and diversification of leucine-rich repeat receptor-like protein kinase (LRR-RLK) genes in plants. BMC Evol Biol, 2017, 17: 47

[86] LiuX, ZhangH, JiaoH, LiL, QiaoX, FabriceMR, WuJ, ZhangS. Expansion and evolutionary patterns of cysteine-rich peptides in plants. BMC Genomics, 2017, 18: 610

[87] LiuP, HarutaM, MinkoffBB, SussmanMR. Probing a Plant Plasma Membrane Receptor Kinase's Three-Dimensional Structure Using Mass Spectrometry-Based Protein Footprinting. Biochemistry, 2018, 57: 5159-5168

[88] LiuJ, ElmoreJM, LinZJ, CoakerG. A receptor-like cytoplasmic kinase phosphorylates the host target RIN4, leading to the activation of a plant innate immune receptor. Cell Host Microbe, 2011, 9: 137-146

[89] LiuC, ShenL, XiaoY, VyshedskyD, PengC, SunX, LiuZ, ChengL, ZhangH, HanZJS. Pollen PCP-B peptides unlock a stigma peptide–receptor kinase gating mechanism for pollination. Science, 2021, 372: 171-175

[90] LiuY, ChenY, JiangH, ShuiZ, ZhongY, ShangJ, YangH, SunX, DuJ. Genome-wide characterization of soybean RALF genes and their expression responses to Fusarium oxysporum. Front Plant Sci, 2022, 13: 1006028

[91] López-GarcíaB, González-CandelasL, Pérez-PayáE, MarcosJFJMP-MI. Identification and characterization of a hexapeptide with activity against phytopathogenic fungi that cause postharvest decay in fruits. Mol Plant Microbe Interact, 2000, 13: 837-846

[92] Loubert-HudonA, MazinBD, ChevalierE, MattonDP. The ScRALF3 secreted peptide is involved in sporophyte to gametophyte signalling and affects pollen mitosis I. Plant Biol (stuttg), 2020, 22: 13-20

[93] MamaevaA, LyapinaI, KnyazevA, GolubN, MollaevT, ChudinovaE, ElanskyS, BabenkoVV, VeselovskyVA, KliminaKM, GribovaT, KharlampievaD, LazarevV, FesenkoI. RALF peptides modulate immune response in the moss Physcomitrium patens. Front Plant Sci, 2023, 14: 1077301

[94] 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: 3140-3156

[95] MasachisS, SegorbeD, TurraD, Leon-RuizM, FurstU, El GhalidM, LeonardG, Lopez-BergesMS, RichardsTA, FelixG, Di PietroA. A fungal pathogen secretes plant alkalinizing peptides to increase infection. Nat Microbiol, 2016, 1: 16043

[96] MatosJL, FioriCS, Silva-FilhoMC, MouraDS. A conserved dibasic site is essential for correct processing of the peptide hormone AtRALF1 in Arabidopsis thaliana. FEBS Lett, 2008, 582: 3343-3347

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

[98] MecchiaMA, Santos-FernandezG, DussNN, SomozaSC, Boisson-DernierA, GagliardiniV, Martínez-BernardiniA, FabriceTN, RingliC, MuschiettiJPJS. RALF4/19 peptides interact with LRX proteins to control pollen tube growth in Arabidopsis. Science, 2017, 358: 1600-1603

[99] MerinoMC, GuidarelliM, NegriniF, De BiaseD, PessionA, BaraldiE. Induced expression of the Fragaria x ananassa Rapid alkalinization factor-33-like gene decreases anthracnose ontogenic resistance of unripe strawberry fruit stages. Mol Plant Pathol, 2019, 20: 1252-1263

[100] MingossiFB, MatosJL, RizzatoAP, MedeirosAH, FalcoMC, Silva-FilhoMC, MouraDS. SacRALF1, a peptide signal from the grass sugarcane (Saccharum spp.), is potentially involved in the regulation of tissue expansion. Plant Mol Biol, 2010, 73: 271-281

[101] Morato do Canto A, Ceciliato PH, Ribeiro B, Ortiz Morea FA, Franco Garcia AA, Silva-Filho MC, Moura DS, . Biological activity of nine recombinant AtRALF peptides: implications for their perception and function in Arabidopsis. Plant Physiol Biochem, 2014, 75: 45-54

[102] MoussuS, AugustinS, RomanAO, BroyartC, SantiagoJ. Crystal structures of two tandem malectin-like receptor kinases involved in plant reproduction. Acta Crystallogr D Struct Biol, 2018, 74: 671-680

[103] MoussuS, BroyartC, Santos-FernandezG, AugustinS, WehrleS, GrossniklausU, SantiagoJ. Structural basis for recognition of RALF peptides by LRX proteins during pollen tube growth. Proc Natl Acad Sci U S A, 2020, 117: 7494-7503

[104] NgoQA, VoglerH, LituievDS, NestorovaA, GrossniklausU. A calcium dialog mediated by the FERONIA signal transduction pathway controls plant sperm delivery. Dev Cell, 2014, 29: 491-500

[105] NicaiseV, JoeA, JeongBR, KorneliC, BoutrotF, WestedtI, StaigerD, AlfanoJR, ZipfelC. Pseudomonas HopU1 modulates plant immune receptor levels by blocking the interaction of their mRNAs with GRP7. EMBO J, 2013, 32: 701-712

[106] NobleJA, BielskiNV, LiuMJ, DeFalcoTA, StegmannM, NelsonADL, McNamaraK, SullivanB, DinhKK, KhuuN, HancockS, ShiuSH, ZipfelC, CheungAY, BeilsteinMA, PalaniveluR. Evolutionary analysis of the LORELEI gene family in plants reveals regulatory subfunctionalization. Plant Physiol, 2022, 190: 2539-2556

[107] OkudaS, TsutsuiH, ShiinaK, SprunckS, TakeuchiH, YuiR, KasaharaRD, HamamuraY, MizukamiA, SusakiD, KawanoN, SakakibaraT, NamikiS, ItohK, OtsukaK, MatsuzakiM, NozakiH, KuroiwaT, NakanoA, KanaokaMM, DresselhausT, SasakiN, HigashiyamaT. Defensin-like polypeptide LUREs are pollen tube attractants secreted from synergid cells. Nature, 2009, 458: 357-361

[108] OlsenAN, MundyJ, SkriverKJSB. Peptomics, identification of novel cationic Arabidopsis peptides with conserved sequence motifs. Silico Biol, 2002, 2: 441-451

[109] Pearce G, Moura DS, Stratmann J, Jr R, CAJPotNAoS, (2001) RALF, a 5-kDa ubiquitous polypeptide in plants, arrests root growth and development. Proc Natl Acad Sci 98:12843–12847. https://doi.org/10.1073/pnas.201416998

[110] PearceG, YamaguchiY, MunskeG, RyanCA. Structure-activity studies of RALF, Rapid Alkalinization Factor, reveal an essential–YISY–motif. Peptides, 2010, 31: 1973-1977

[111] RouxM, SchwessingerB, AlbrechtC, ChinchillaD, JonesA, HoltonN, MalinovskyFG, TorM, de VriesS, ZipfelC. The Arabidopsis leucine-rich repeat receptor-like kinases BAK1/SERK3 and BKK1/SERK4 are required for innate immunity to hemibiotrophic and biotrophic pathogens. Plant Cell, 2011, 23: 2440-2455

[112] SchiøttM, RomanowskySM, BækgaardL, JakobsenMK, PalmgrenMG, Harper JFJPotNAoS, . A plant plasma membrane Ca2+ pump is required for normal pollen tube growth and fertilization. Proc Natl Acad Sci, 2004, 101: 9502-9507

[113] SchulzeB, MentzelT, JehleAK, MuellerK, BeelerS, BollerT, FelixG, ChinchillaD. Rapid heteromerization and phosphorylation of ligand-activated plant transmembrane receptors and their associated kinase BAK1. J Biol Chem, 2010, 285: 9444-9451

[114] SegonzacC, MonaghanJ. Modulation of plant innate immune signaling by small peptides. Curr Opin Plant Biol, 2019, 51: 22-28

[115] Shanmugaraj B, Bulaon CJI, Malla A, Phoolcharoen W (2021) Biotechnological Insights on the Expression and Production of Antimicrobial Peptides in Plants. Molecules 26:https://doi.org/10.3390/molecules26134032

[116] ShenQ, BourdaisG, PanH, RobatzekS, TangD. Arabidopsis glycosylphosphatidylinositol-anchored protein LLG1 associates with and modulates FLS2 to regulate innate immunity. Proc Natl Acad Sci U S A, 2017, 114: 5749-5754

[117] SongY, WilsonAJ, ZhangXC, ThomsD, SohrabiR, SongS, GeissmannQ, LiuY, WalgrenL, HeSY, HaneyCH. FERONIA restricts Pseudomonas in the rhizosphere microbiome via regulation of reactive oxygen species. Nat Plants, 2021, 7: 644-654

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

[119] 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: 287-289

[120] Sui J, Xiao X, Yang J, Fan Y, Zhu S, Zhu J, Zhou B, Yu F, Tang C (2023) The rubber tree RALF peptide hormone and its receptor protein kinase FER implicates in rubber production. Plant Sci 326:111510. https://doi.org/10.1016/j.plantsci.2022.111510

[121] Szurman-Zubrzycka M, Chwialkowska K, Niemira M, Kwasniewski M, Nawrot M, Gajecka M, Larsen PB, Szarejko I (2021) Aluminum or Low pH - Which Is the Bigger Enemy of Barley? Transcriptome Analysis of Barley Root Meristem Under Al and Low pH Stress. Front Genet 12:675260. https://doi.org/10.3389/fgene.2021.675260

[122] TabataR, SumidaK, YoshiiT, OhyamaK, ShinoharaH, MatsubayashiYJS. Perception of root-derived peptides by shoot LRR-RKs mediates systemic N-demand signaling. Science, 2014, 346: 343-346

[123] TakahashiF, SuzukiT, OsakabeY, BetsuyakuS, KondoY, DohmaeN, FukudaH, Yamaguchi-ShinozakiK, ShinozakiKJN. A small peptide modulates stomatal control via abscisic acid in long-distance signalling. Nature, 2018, 556: 235-238

[124] TangJ, HanZ, SunY, ZhangH, GongX, ChaiJ. Structural basis for recognition of an endogenous peptide by the plant receptor kinase PEPR1. Cell Res, 2015, 25: 110-120

[125] TavorminaP, De ConinckB, NikonorovaN, De SmetI, CammueBP. The Plant Peptidome: An Expanding Repertoire of Structural Features and Biological Functions. Plant Cell, 2015, 27: 2095-2118

[126] TempleBR, JonesAM. The plant heterotrimeric G-protein complex. Annu Rev Plant Biol, 2007, 58: 249-266

[127] 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: 811-824

[128] WangL, YangT, LinQ, WangB, LiX, LuanS, YuF. Receptor kinase FERONIA regulates flowering time in Arabidopsis. BMC Plant Biol, 2020, 20: 26

[129] Wang L, Yang T, Wang B, Lin Q, Zhu S, Li C, Ma Y, Tang J, Xing J, Li XJSa (2020b) RALF1-FERONIA complex affects splicing dynamics to modulate stress responses and growth in plants. Science advances 6:eaaz1622. https://doi.org/10.1126/sciadv.aaz1622

[130] WangP, YaoS, KosamiKI, GuoT, LiJ, ZhangY, FukaoY, Kaneko-KawanoT, ZhangH, SheYM, WangP, XingW, HanadaK, LiuR, KawanoY. Identification of endogenous small peptides involved in rice immunity through transcriptomics- and proteomics-based screening. Plant Biotechnol J, 2020, 18: 415-428

[131] 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: 1110-1125

[132] Wieghaus A, Prufer D, Schulze Gronover C (2019) Loss of function mutation of the Rapid Alkalinization Factor (RALF1)-like peptide in the dandelion Taraxacum koksaghyz entails a high-biomass taproot phenotype. PLoS One 14:e0217454. https://doi.org/10.1371/journal.pone.0217454

[133] WoodAKM, WalkerC, LeeWS, UrbanM, Hammond-KosackKE. Functional evaluation of a homologue of plant rapid alkalinisation factor (RALF) peptides in Fusarium graminearum. Fungal Biol, 2020, 124: 753-765

[134] WuJ, KurtenEL, MonshausenG, HummelGM, GilroyS, BaldwinIT. NaRALF, a peptide signal essential for the regulation of root hair tip apoplastic pH in Nicotiana attenuata, is required for root hair development and plant growth in native soils. Plant J, 2007, 52: 877-890

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

[136] Xie Y, Sun P, Li Z, Zhang F, You C, Zhang Z (2022) FERONIA Receptor Kinase Integrates with Hormone Signaling to Regulate Plant Growth, Development, and Responses to Environmental Stimuli. Int J Mol Sci 23:https://doi.org/10.3390/ijms23073730

[137] XuY, MagwangaRO, JinD, CaiX, HouY, JuyunZ, AgongSG, WangK, LiuF, ZhouZ. Comparative transcriptome analysis reveals evolutionary divergence and shared network of cold and salt stress response in diploid D-genome cotton. BMC Plant Biol, 2020, 20: 518

[138] YamaguchiY, PearceG, Ryan CAJPotNAoS, . The cell surface leucine-rich repeat receptor for At Pep1, an endogenous peptide elicitor in Arabidopsis, is functional in transgenic tobacco cells. Proc Natl Acad Sci, 2006, 103: 10104-10109

[139] 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: 508-522

[140] Yang Y, Wang Q, Geng M, Guo Z, Zhao Z (2011) Rhizosphere pH difference regulated by plasma membrane H+-ATPase is related to differential Al tolerance of two wheat cultivars. Plant, Soil Environment 57:201–206. https://doi.org/10.17221/419/2010-PSE

[141] Yang G, Qu M, Xu G, Li Y, Li X, Feng Y, Xiao H, He Y, Shabala S, Demidchik V, Liu J, Yu M (2022) pH-Dependent mitigation of aluminum toxicity in pea (Pisum sativum) roots by boron. Plant Sci 318:111208. https://doi.org/10.1016/j.plantsci.2022.111208

[142] YangH, MatsubayashiY, NakamuraK, SakagamiYJPP. Diversity of Arabidopsis genes encoding precursors for phytosulfokine, a peptide growth factor. Plant Physiol, 2001, 127: 842-851

[143] YuY, AssmannSM. The heterotrimeric G-protein beta subunit, AGB1, plays multiple roles in the Arabidopsis salinity response. Plant Cell Environ, 2015, 38: 2143-2156

[144] YuY, AssmannSM. Inter-relationships between the heterotrimeric Gbeta subunit AGB1, the receptor-like kinase FERONIA, and RALF1 in salinity response. Plant Cell Environ, 2018, 41: 2475-2489

[145] 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: 14693-14698

[146] Yu M, Li R, Cui Y, Chen W, Li B, Zhang X, Bu Y, Cao Y, Xing J, Jewaria PK, Li X, Bhalerao RP, Yu F, Lin J (2020) The RALF1-FERONIA interaction modulates endocytosis to mediate control of root growth in Arabidopsis. Development 147:https://doi.org/10.1242/dev.189902

[147] YuY, ChakravortyD, AssmannSM. The G Protein beta-Subunit, AGB1, Interacts with FERONIA in RALF1-Regulated Stomatal Movement. Plant Physiol, 2018, 176: 2426-2440

[148] 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: 1434-1454

[149] ZhangY, RenQ, TangX, LiuS, MalzahnAA, ZhouJ, WangJ, YinD, PanC, YuanM, HuangL, YangH, ZhaoY, FangQ, ZhengX, TianL, ChengY, LeY, McCoyB, FranklinL, SelengutJD, MountSM, QueQ, ZhangY, QiY. Expanding the scope of plant genome engineering with Cas12a orthologs and highly multiplexable editing systems. Nat Commun, 2021, 12: 1944

[150] 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: 13123-13128

[151] Zhao C, Jiang W, Zayed O, Liu X, Tang K, Nie W, Li Y, Xie S, Li Y, Long T, Liu L, Zhu Y, Zhao Y, Zhu JK (2021) The LRXs-RALFs-FER module controls plant growth and salt stress responses by modulating multiple plant hormones. Natl Sci Rev 8:nwaa149. https://doi.org/10.1093/nsr/nwaa149

[152] Zhang X, Wang D, Chen J, Wu D, Feng X, Yu F (2021a) Nematode RALF-Like 1 Targets Soybean Malectin-Like Receptor Kinase to Facilitate Parasitism. Front Plant Sci 12:775508. https://doi.org/10.3389/fpls.2021.775508

[153] Zhang X, Yang Z, Wu D, Yu F (2020b) RALF-FERONIA Signaling: Linking Plant Immune Response with Cell Growth. Plant Commun 1:100084. https://doi.org/10.1016/j.xplc.2020.100084

[154] ZhengXY, SpiveyNW, ZengW, LiuPP, FuZQ, KlessigDF, HeSY, DongX. Coronatine promotes Pseudomonas syringae virulence in plants by activating a signaling cascade that inhibits salicylic acid accumulation. Cell Host Microbe, 2012, 11: 587-596

[155] ZhongS, LiL, WangZ, GeZ, LiQ, BleckmannA, WangJ, SongZ, ShiY, LiuTJS. RALF peptide signaling controls the polytubey block in Arabidopsis. Science, 2022, 375: 290-296

[156] Zhou X, Lu J, Zhang Y, Guo J, Lin W, Van Norman JM, Qin Y, Zhu X, Yang Z (2021) Membrane receptor-mediated mechano-transduction maintains cell integrity during pollen tube growth within the pistil. Dev Cell 56:1030–1042 e1036. https://doi.org/10.1016/j.devcel.2021.02.030

[157] 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: 172-180

[158] ZhuJY, Sae-SeawJ, WangZY. Brassinosteroid Signalling Development, 2013, 140: 1615-1620

[159] ZhuL, ChuLC, LiangY, ZhangXQ, ChenLQ, YeD. The Arabidopsis CrRLK1L protein kinases BUPS1 and BUPS2 are required for normal growth of pollen tubes in the pistil. Plant J, 2018, 95: 474-486

[160] ZhuS, EstevezJM, LiaoH, ZhuY, YangT, LiC, WangY, LiL, LiuX, PachecoJM, GuoH, YuF. The RALF1-FERONIA Complex Phosphorylates eIF4E1 to Promote Protein Synthesis and Polar Root Hair Growth. Mol Plant, 2020, 13: 698-716

[161] ZhuS, FuQ, XuF, ZhengH, YuF. New paradigms in cell adaptation: decades of discoveries on the CrRLK1L receptor kinase signalling network. New Phytol, 2021, 232: 1168-1183

Funding

National Natural Science Foundation of China(31270299)