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Review | Open Access

How a single receptor-like kinase exerts diverse roles: lessons from FERONIA

Gaopeng Wang1,2, Zhifang Zhao1,2, Xinhang Zheng1,2, Wenfeng Shan1,2, Jiangbo Fan1,2 ( )
Shanghai Collaborative Innovation Center of Agri-Seeds, School of Agriculture and Biology, Shanghai Jiao Tong University, 800 Dongchuan Rd, Shanghai 200240, China
Joint Center for Single Cell Biology, School of Agriculture and Biology, Shanghai Jiao Tong University, 800 Dongchuan Rd, Shanghai 200240, China
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Abstract

FERONIA (FER) is a member of the Catharanthus roseus receptor-like kinase 1-like (CrRLK1L) protein subfamily, which participates in reproduction, abiotic stress, biotic stress, cell growth, hormone response, and other molecular mechanisms of plants. However, the mechanism by which a single RLK is capable of mediating multiple signals and activating multiple cellular responses remains unclear. Here, we summarize research progress revealing the spatial–temporal expression of FER, along with its co-receptors and ligands determined the function of FER signaling pathway in multiple organs. The specificity of the FER signaling pathway is proposed to operate under a four-layered mechanism: (1) Spatial–temporal expression of FER, co-receptors, and ligands specify diverse functions, (2) Specific ligands or ligand combinations trigger variable FER signaling pathways, (3) Diverse co-receptors confer diverse FER perception and response modes, and (4) Unique downstream components that modify FER signaling and responses. Moreover, the regulation mechanism of the signaling pathway- appears to depend on the interaction among the ligands, RLK receptors, co-receptors, and downstream components, which may be a general mechanism of RLKs to maintain signal specificity. This review will provide a insight into understanding the specificity determination of RLKs signaling in both model and horticultural crops.

Keywords

FERONIASignaling pathwayRegulation mechanismImmunityCell growth

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References

 

Bergonci T, Silva-Filho MC, Moura DS. Antagonistic relationship between AtRALF1 and brassinosteroid regulates cell expansion-related genes. Plant Signal Behav. 2014b;9:e976146.
Crossref Google Scholar
 

Bergonci T, Ribeiro B, Ceciliato PHO, Guerrero-Abad JC, Silva-Filho MC, Moura DS. Arabidopsis thaliana RALF1 opposes brassinosteroid effects on root cell elongation and lateral root formation. J Exp Bot. 2014a;65:2219–30.
Crossref Google Scholar
 

Boisson-Dernier A, Franck CM, Lituiev DS, Grossniklaus U. Receptor-like cytoplasmic kinase MARIS functions downstream of CrRLK1L-dependent signaling during tip growth. Proc Natl Acad Sci U S A. 2015;112:12211–6.
Crossref Google Scholar
 

Campbell L, Turner SR. A Comprehensive Analysis of RALF Proteins in Green Plants Suggests There Are Two Distinct Functional Groups. Front Plant Sci. 2017;8:37.
Crossref Google Scholar
 

Chen J, Yu F, Liu Y, Du C, Li X, Zhu S, et al. 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:E5519–27.
Crossref Google Scholar
 

Cohen P. The regulation of protein function by multisite phosphorylation – a 25 year update. Trends Biochem Sci. 2000;25:596–601.
Crossref Google Scholar
 

Couto D, Zipfel C. Regulation of pattern recognition receptor signalling in plants. Nat Rev Immunol. 2016;16:537–52.
Crossref Google Scholar
 

DeFalco TA. Studying the many faces of FERONIA. Plant Cell. 2022;34:2572–3.
Crossref Google Scholar
 

Deslauriers SD, Larsen PB. FERONIA is a key modulator of brassinosteroid and ethylene responsiveness in arabidopsis hypocotyls. Mol Plant. 2010;3:626–40.
Crossref Google Scholar
 

Dievart A, Gottin C, Périn C, Ranwez V, Chantret N. Origin and Diversity of Plant Receptor-Like Kinases. Annu Rev Plant Biol. 2020;71:131–56.
Crossref Google Scholar
 

Dong QK, Zhang ZW, Liu YT, Tao LZ, Liu HL. FERONIA regulates auxin-mediated lateral root development and primary root gravitropism. FEBS Lett. 2019;593:97–106.
Crossref Google Scholar
 

Du C, Li X, Chen J, Chen W, Li B, Li C, et al. Receptor kinase complex transmits RALF peptide signal to inhibit root growth in Arabidopsis. Proc Natl Acad Sci U S A. 2016;113:E8326–34.
Crossref Google Scholar
 

Duan Q, Kita D, Johnson EA, Aggarwal M, Gates L, Wu H-M, et al. Reactive oxygen species mediate pollen tube rupture to release sperm for fertilization in Arabidopsis. Nat Commun. 2014;5:3129.
Crossref Google Scholar
 

Duan Q, Kita D, Li C, Cheung AY, Wu H-M. FERONIA receptor-like kinase regulates RHO GTPase signaling of root hair development. Proc Natl Acad Sci U S A. 2010;107:17821–6.
Crossref Google Scholar
 

Duan Q, Liu M-CJ, Kita D, Jordan SS, Yeh F-LJ, Yvon R, et al. FERONIA controls pectin- and nitric oxide-mediated male–female interaction. Nature. 2020;579:561–6.
Crossref Google Scholar
 

Dünser K, Gupta S, Herger A, Feraru MI, Ringli C, Kleine-Vehn J. Extracellular matrix sensing by FERONIA and Leucine-Rich Repeat Extensins controls vacuolar expansion during cellular elongation in Arabidopsis thaliana. The EMBO J. 2019;38:e100353. https://doi.org/10.15252/embj.2018100353.
Crossref Google Scholar
 

Escobar-Restrepo JM, Huck N, Kessler S, Gagliardini V, Gheyselinck J, Yang WC, et al. The Feronia receptor-like kinase mediates male-female interactions during pollen tube reception. Science. 2007;317:656–60.
Crossref Google Scholar
 

Feng H, Liu C, Fu R, Zhang M, Li H, Shen L, et al. 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;12:1612–23.
Crossref Google Scholar
 

Feng W, Kita D, Peaucelle A, Cartwright HN, Doan V, Duan Q, et al. The FERONIA Receptor Kinase Maintains Cell-Wall Integrity during Salt Stress through Ca2+ Signaling. Curr Biol. 2018;28:666–75.
Crossref Google Scholar
 

Galindo-Trigo S, Blanco-Touriñán N, DeFalco TA, Wells ES, Gray JE, Zipfel C, et al. CrRLK1L receptor-like kinases HERK1 and ANJEA are female determinants of pollen tube reception. EMBO Rep. 2020;21:e48466.
Crossref Google Scholar
 

Gao Q, Wang C, Xi Y, Shao Q, Li L, Luan S. A receptor-channel trio conducts Ca2+ signalling for pollen tube reception. Nature (London). 2022. https://doi.org/10.1038/s41586-022-04923-7.
Crossref Google Scholar
 

Ge Z, Bergonci T, Zhao Y, Zou Y, Du S, Liu MC, et al. Arabidopsis pollen tube integrity and sperm release are regulated by RALF-mediated signaling. Science. 2017;358:1596–600.
Crossref Google Scholar
 

Gjetting SK, Mahmood K, Shabala L, Kristensen A, Shabala S, Palmgren M, et al. Evidence for multiple receptors mediating RALF-triggered Ca2+ signaling and proton pump inhibition. Plant J. 2020;104:433–46.
Crossref Google Scholar
 

Guo H, Li L, Ye H, Yu X, Algreen A, Yin Y. Three related receptor-like kinases are required for optimal cell elongation in Arabidopsis thaliana. Proc Natl Acad Sci U S A. 2009;106(18):7648–53.
Crossref Google Scholar
 

Guo H, Nolan TM, Song G, Liu S, Xie Z, Chen J, et al. FERONIA Receptor Kinase Contributes to Plant Immunity by Suppressing Jasmonic Acid Signaling in Arabidopsis thaliana. Curr Biol. 2018;28:3316–24.
Crossref Google Scholar
 

Haruta M, Gaddameedi V, Burch H, Fernandez D, Sussman MR. Comparison of the effects of a kinase-dead mutation of FERONIA on ovule fertilization and root growth of Arabidopsis. FEBS Lett. 2018;592:2395–402.
Crossref Google Scholar
 

Haruta M, Sabat G, Stecker K, Minkoff BB, Sussman MR. A Peptide Hormone and Its Receptor Protein Kinase Regulate Plant Cell Expansion. SCIENCE. 2014;343:408–11.
Crossref Google Scholar
 

He Y, Zhou J, Shan L, Meng X. Plant cell surface receptor-mediated signaling - a common theme amid diversity. J Cell Sci. 2018;131:jcs209353.
Crossref Google Scholar
 

Herger A, Dünser K, Kleine-Vehn J, Ringli C. Leucine-Rich Repeat Extensin Proteins and Their Role in Cell Wall Sensing. Curr Biol. 2019;29:R851–8.
Crossref Google Scholar
 

Herger A, Gupta S, Kadler G, Franck CM, Boisson-Dernier A, Ringli C. Overlapping functions and protein-protein interactions of LRR-extensins in Arabidopsis. PLoS Genet. 2020;16:e1008847.
Crossref Google Scholar
 

Johnson MA, Harper JF, Palanivelu R. A Fruitful Journey: Pollen Tube Navigation from Germination to Fertilization. Annu Rev Plant Biol. 2019;70:809–37.
Crossref Google Scholar
 

Kim D, Yang J, Gu F, Park S, Combs J, Adams A, et al. A temperature-sensitive FERONIA mutant allele that alters root hair growth. Plant Physiol. 2021;185:405–23.
Crossref Google Scholar
 

Lehti-Shiu MD, Zou C, Hanada K, Shiu S-H. Evolutionary History and Stress Regulation of Plant Receptor-Like Kinase/Pelle Genes. Plant Physiol. 2009;150:12–26.
Crossref Google Scholar
 

Li C, Chen J, Li X, Zhang X, Liu Y, Zhu S, et al. FERONIA is involved in phototropin 1-mediated blue light phototropic growth in Arabidopsis. J Integr Plant Biol. 2022a;64:1901–15.
Crossref Google Scholar
 

Li C, Yeh FL, Cheung AY, Duan Q, Kita D, Liu MC, et al. Glycosylphosphatidylinositol-anchored proteins as chaperones and co-receptors for FERONIA receptor kinase signaling in Arabidopsis. Elife. 2015;4:1–21.
Crossref Google Scholar
 

Li E, Wang G, Zhang YL, Kong Z, Li S. FERONIA mediates root nutating growth. Plant J. 2020;104:1105–16.
Crossref Google Scholar
 

Li J, Wen J, Lease KA, Doke JT, Tax FE, Walker JC. BAK1, an Arabidopsis LRR receptor-like protein kinase, interacts with BRI1 and modulates brassinosteroid signaling. CELL. 2002;110:213–22.
Crossref Google Scholar
 

Li L, Chen H, Alotaibi SS, Pěnčík A, Adamowski M, Novák O, et al. RALF1 peptide triggers biphasic root growth inhibition upstream of auxin biosynthesis. Proc Natl Acad Sci. 2022b;119:1-e2121058119.
Crossref Google Scholar
 

Liang X, Zhou J-M. Receptor-Like Cytoplasmic Kinases: Central Players in Plant Receptor Kinase-Mediated Signaling. Annu Rev Plant Biol. 2018;69:267–99.
Crossref Google Scholar
 

Liu C, Shen L, Xiao Y, Vyshedsky D, Peng C, Sun X, et al. Pollen PCP-B peptides unlock a stigma peptide-receptor kinase gating mechanism for pollination. Science. 2021;372:171–5.
Crossref Google Scholar
 

Liu X, Castro C, Wang Y, Noble J, Ponvert N, Bundy M, et al. 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;28:1035–52.
Crossref Google Scholar
 

Mao D, Yu F, Li J, Van de Poel B, Tan D, Li J, et al. FERONIA receptor kinase interacts with S-adenosylmethionine synthetase and suppresses S-adenosylmethionine production and ethylene biosynthesis in Arabidopsis. Plant Cell Environ. 2015;38:2566–74.
Crossref Google Scholar
 

Masachis S, Segorbe D, Turrà D, Leon-Ruiz M, Fürst U, El Ghalid M, et al. A fungal pathogen secretes plant alkalinizing peptides to increase infection. Nat Microbiol. 2016;1:16043.
Crossref Google Scholar
 

Mecchia MA, Santos-Fernandez G, Duss NN, Somoza SC, Boisson-Dernier A, Gagliardini V, et al. RALF4/19 peptides interact with LRX proteins to control pollen tube growth in Arabidopsis. Science. 2017;358:1600–3.
Crossref Google Scholar
 

Misra P, Owuor ED, Li WG, Yu ST, Qi C, Meyer K, et al. Phosphorylation of transcriptional coactivator peroxisome proliferator-activated receptor (PPAR)-binding protein (PBP) - Stimulation of transcriptional regulation by mitogen-activated protein kinase. J Biol Chem. 2002;277:48745–54.
Crossref Google Scholar
 

Morato do Canto A, Ceciliato PHO, Ribeiro B, Ortiz Morea FA, Franco Garcia AA, Silva-Filho MC, et al. Biological activity of nine recombinant AtRALF peptides: Implications for their perception and function in Arabidopsis. Plant Physiol Biochem. 2014;75:45–54.
Crossref Google Scholar
 

Moussu S, Broyart C, Santos-Fernandez G, Augustin S, Wehrle S, Grossniklaus U, et al. Structural basis for recognition of RALF peptides by LRX proteins during pollen tube growth. Proc Natl Acad Sci U S A. 2020;117:7494–503.
Crossref Google Scholar
 

Park CH, Bi Y, Youn J-H, Kim S-H, Kim J-G, Xu NY, et al. Deconvoluting signals downstream of growth and immune receptor kinases by phosphocodes of the BSU1 family phosphatases. Nat Plants. 2022;8:646–55.
Crossref Google Scholar
 

Richter J, Ploderer M, Hauser MT, Mongelard G, Gutierrez L. Role of CrRLK1L cell wall sensors HERCULES1 and 2, THESEUS1, and FERONIA in growth adaptation triggered by heavy metals and trace elements. Front Plant Sci. 2017;8:1554.
Crossref Google Scholar
 

Robatzek S, Nürnberger T. A flagellin-induced complex of the receptor FLS2 and BAK1 initiates plant defence. Nature. 2007;448:497–500.
Crossref Google Scholar
 

Sénéchal F, L’Enfant M, Domon J-M, Rosiau E, Crépeau M-J, Surcouf O, et al. Tuning of Pectin Methylesterification: Pectin methylesterase inhibitor 7 modulates the processive activity of co-expressed pectin methylesterase 3 in a ph-dependent manner. J Biol Chem. 2015;290:23320–35.
Crossref Google Scholar
 

Shih H-W, Miller Nathan D, Dai C, Spalding Edgar P, Monshausen GB. The Receptor-like Kinase FERONIA Is Required for Mechanical Signal Transduction in Arabidopsis Seedlings. Curr Biol. 2014;24:1887–92.
Crossref Google Scholar
 

Shiu S-H, Bleecker AB. Receptor-like Kinases from Arabidopsis Form a Monophyletic Gene Family Related to Animal Receptor Kinases. P Natl Acad Sci USA. 2001;98:10763–8.
Crossref Google Scholar
 

Shiu S-H, Bleecker AB. Expansion of the receptor-like Kinase/Pelle gene family and receptor-like proteins in Arabidopsis. Plant Physiol. 2003;132:530–43.
Crossref Google Scholar
 

Shiu S-H, Karlowski WM, Pan R, Tzeng Y-H, Mayer KFX, Li W-H. Comparative Analysis of the Receptor-Like Kinase Family in Arabidopsis and Rice[W]. Plant Cell. 2004;16:1220–34.
Crossref Google Scholar
 

Song L, Xu G, Li T, Zhou H, Lin Q, Chen J, et al. The RALF1-FERONIA complex interacts with and activates TOR signaling in response to low nutrients. Mol Plant. 2022;15:1120–36.
Crossref Google Scholar
 

Srivastava R, Liu JX, Guo H, Yin Y, Howell SH. Regulation and processing of a plant peptide hormone, AtRALF23, in Arabidopsis. Plant J. 2009;59:930–9.
Crossref Google Scholar
 

Stegmann M, Monaghan J, Smakowska-Luzan E, Rovenich H, Lehner A, Holton N, et al. The receptor kinase FER is a RALF-regulated scaffold controlling plant immune signaling. Science. 2017;355:287–9.
Crossref Google Scholar
 

Tang J, Wu D, Li X, Wang L, Xu L, Zhang Y, et al. Plant immunity suppression via PHR1-RALF-FERONIA shapes the root microbiome to alleviate phosphate starvation. EMBO J. 2022a;41:e109102.
Crossref Google Scholar
 

Tang W, Lin W, Zhou X, Guo J, Dang X, Li B, et al. Mechano-transduction via the pectin-FERONIA complex activates ROP6 GTPase signaling in Arabidopsis pavement cell morphogenesis. Curr Biol. 2022b;32:508–17.
Crossref Google Scholar
 

Wang L, Clarke LA, Eason RJ, Parker CC, Qi B, Scott RJ, et al. PCP-B class pollen coat proteins are key regulators of the hydration checkpoint in Arabidopsis thaliana pollen–stigma interactions. New Phytol. 2017;213:764–77.
Crossref Google Scholar
 

Wang P, Clark NM, Nolan TM, Song G, Bartz PM, Liao C-Y, et al. Integrated omics reveal novel functions and underlying mechanisms of the receptor kinase FERONIA in Arabidopsis thaliana. Plant Cell. 2022a;34:2594–614.
Crossref Google Scholar
 

Wang P, Clark NM, Nolan TM, Song G, Whitham OG, Liao C-Y, et al. FERONIA functions through Target of Rapamycin (TOR) to negatively regulate autophagy. Front Plant Sci. 2022b;13:961096.
Crossref Google Scholar
 

Xiao Y, Stegmann M, Han Z, DeFalco TA, Parys K, Xu L, et al. Mechanisms of RALF peptide perception by a heterotypic receptor complex. Nature. 2019;572:270–4.
Crossref Google Scholar
 

Xin X-F, Sheng Yang HE. Pseudomonas syringae pv. tomato DC3000: A Model Pathogen for Probing Disease Susceptibility and Hormone Signaling in Plants. Annu Rev Phytopathol. 2013;51:473–98.
Crossref Google Scholar
 

Yang DH, Hettenhausen C, Baldwin IT, Wu J. The multifaceted function of BAK1/SERK3: Plant immunity to pathogens and responses to insect herbivores. Plant Signal Behav. 2011;6:1322–4.
Crossref Google Scholar
 

Yasuda S, Okada K, Saijo Y. A look at plant immunity through the window of the multitasking coreceptor BAK1. Curr Opin Plant Biol. 2017;38:10–8.
Crossref Google Scholar
 

Yu F, Li J, Huang Y, Liu L, Li D, Chen L, et al. FERONIA receptor kinase controls seed size in arabidopsis Thaliana. MPPHYS. 2014;7:920–2.
Crossref Google Scholar
 

Yu F, Qian L, Nibau C, Duan Q, Kita D, Levasseur K, et al. FERONIA receptor kinase pathway suppresses abscisic acid signaling in Arabidopsis by activating ABI2 phosphatase. Proc Natl Acad Sci U S A. 2012;109:14693–8.
Crossref Google Scholar
 

Yu Q, An L, Li W. The CBL–CIPK network mediates different signaling pathways in plants. Plant Cell Rep. 2013;33:203–14.
Crossref Google Scholar
 

Zhang X, Peng H, Zhu S, Xing J, Li X, Zhu Z, et al. Nematode-Encoded RALF Peptide Mimics Facilitate Parasitism of Plants through the FERONIA Receptor Kinase. Mol Plant. 2020a;13:1434–54.
Crossref Google Scholar
 

Zhang X, Yang Z, Wu D, Yu F. RALF–FERONIA Signaling: Linking Plant Immune Response with Cell Growth. Plant Commun. 2020b;1:100084.
Crossref Google Scholar
 

Zhao C, Zayed O, Yu Z, Jiang W, Zhu P, Hsu CC, et al. Leucine-rich repeat extensin proteins regulate plant salt tolerance in Arabidopsis. Proc Natl Acad Sci U S A. 2018;115:13123–8.
Crossref Google Scholar
 

Zheng X-y, Spivey Natalie W, Zeng W, Liu P-P, Fu Zheng Q, Klessig Daniel F, et al. Coronatine Promotes Pseudomonas syringae Virulence in Plants by Activating a Signaling Cascade that Inhibits Salicylic Acid Accumulation. Cell Host Microbe. 2012;11:587–96.
Crossref Google Scholar
 

Zhong S, Li L, Wang Z, Ge Z, Li Q, Bleckmann A, et al. RALF peptide signaling controls the polytubey block in Arabidopsis. Science. 2022;375:290–6.
Crossref Google Scholar
 

Zhu L, Liang Y, Zhang XQ, Chen LQ, Ye D, Chu LC. The arabidopsis CrRLK1L protein kinases BUPS1 and BUPS2 are required for normal growth of pollen tubes in the pistil. Plant J. 2018;95:474–86.
Crossref Google Scholar
 

Zhu S, Fu Q, Xu F, Zheng H, Yu F. New paradigms in cell adaptation: decades of discoveries on the CrRLK1L receptor kinase signalling network. The New Phytologist. 2021;232:1168–83.
Crossref Google Scholar
 

Zou Y, Wang S, Zhou Y, Bai J, Huang G, Liu X, et al. Transcriptional Regulation of the Immune Receptor FLS2 Controls the Ontogeny of Plant Innate Immunity. Plant Cell. 2018;30:2779–94.
Crossref Google Scholar
Molecular Horticulture
Volume 2 Issue 4,
December 2022
Pages 25-25
DOI: 10.1186/s43897-022-00046-9
Cite this article:
Wang G, Zhao Z, Zheng X, et al. How a single receptor-like kinase exerts diverse roles: lessons from FERONIA. Molecular Horticulture, 2022, 2(4): 25. https://doi.org/10.1186/s43897-022-00046-9

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Received: 30 September 2022
Accepted: 09 November 2022
Published: 18 November 2022
© The Author(s) 2022.

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