1932

Abstract

Initially identified as a key regulator of female fertility in , the FERONIA (FER) receptor kinase is now recognized as crucial for almost all aspects of plant growth and survival. FER partners with a glycosylphosphatidylinositol-anchored protein of the LLG family to act as coreceptors on the cell surface. The FER-LLG coreceptor interacts with different RAPID ALKALINIZATION FACTOR (RALF) peptide ligands to function in various growth and developmental processes and to respond to challenges from the environment. The RALF-FER-LLG signaling modules interact with molecules in the cell wall, cell membrane, cytoplasm, and nucleus and mediate an interwoven signaling network. Multiple FER-LLG modules, each anchored by FER or a FER-related receptor kinase, have been studied, illustrating the functional diversity and the mechanistic complexity of the FER family signaling modules. The challenges going forward are to distill from this complexity the unifying schemes where possible and attain precision and refinement in the knowledge of critical details upon which future investigations can be built. By focusing on the extensively characterized FER, this review provides foundational information to guide the next phase of research on FER in model as well as crop species and potential applications for improving plant growth and resilience.

Loading

Article metrics loading...

/content/journals/10.1146/annurev-arplant-102820-103424
2024-07-22
2024-12-13
Loading full text...

Full text loading...

/deliver/fulltext/arplant/75/1/annurev-arplant-102820-103424.html?itemId=/content/journals/10.1146/annurev-arplant-102820-103424&mimeType=html&fmt=ahah

Literature Cited

  1. 1.
    Abarca A, Franck CM, Zipfel C. 2021.. Family-wide evaluation of RAPID ALKALINIZATION FACTOR peptides. . Plant Physiol. 187:(2):9961010
    [Crossref] [Google Scholar]
  2. 2.
    Anderson CT, Kieber JJ. 2020.. Dynamic construction, perception, and remodeling of plant cell walls. . Annu. Rev. Plant Biol. 71::3969
    [Crossref] [Google Scholar]
  3. 3.
    Bergonci T, Ribeiro B, Ceciliato PHO, Guerrero-Abad JC, Silva-Filho MC, Moura DS. 2014.. Arabidopsis thaliana RALF1 opposes brassinosteroid effects on root cell elongation and lateral root formation. . J. Exp. Bot. 65:(8):221930
    [Crossref] [Google Scholar]
  4. 4.
    Blackburn MR, Haruta M, Moura DS. 2020.. Twenty years of progress in physiological and biochemical investigation of RALF peptides. . Plant Physiol. 182:(4):165766
    [Crossref] [Google Scholar]
  5. 5.
    Boisson-Dernier A, Franck CM, Lituiev DS, Grossniklaus U. 2015.. Receptor-like cytoplasmic kinase MARIS functions downstream of CrRLK1L-dependent signaling during tip growth. . PNAS 112:(39):1221116
    [Crossref] [Google Scholar]
  6. 6.
    Boisson-Dernier A, Kessler SA, Grossniklaus U. 2011.. The walls have ears: the role of plant CrRLK1Ls in sensing and transducing extracellular signals. . J. Exp. Bot. 62:(5):158191
    [Crossref] [Google Scholar]
  7. 7.
    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:(11):e1001719
    [Crossref] [Google Scholar]
  8. 8.
    Boisson-Dernier A, Roy S, Kritsas K, Grobei MA, Jaciubek M, et al. 2009.. Disruption of the pollen-expressed FERONIA homologs ANXUR1 and ANXUR2 triggers pollen tube discharge. . Development 136:(19):327988 8. The first report of a pair of key male fertility regulators.
    [Crossref] [Google Scholar]
  9. 9.
    Capron A, Gourgues M, Neiva LS, Faure J-E, Berger F, et al. 2008.. Maternal control of male-gamete delivery in Arabidopsis involves a putative GPI-anchored protein encoded by the LORELEI gene. . Plant Cell 20:(11):303849 9. The discovery of LORELEI functioning in the FER pathway.
    [Crossref] [Google Scholar]
  10. 10.
    Cheung AY, Duan Q, Li C, Liu M-CJ, Wu H-M. 2022.. Pollen–pistil interactions: It takes two to tangle but a molecular cast of many to deliver. . Curr. Opin. Plant Biol. 69::102279
    [Crossref] [Google Scholar]
  11. 11.
    Cheung AY, Wu H-M. 2011.. THESEUS 1, FERONIA and relatives: a family of cell wall-sensing receptor kinases?. Curr. Opin. Plant Biol. 14:(6):63241
    [Crossref] [Google Scholar]
  12. 12.
    Denoux C, Galletti R, Mammarella N, Gopalan S, Werck D, et al. 2008.. Activation of defense response pathways by Ogs and Flg22 elicitors in Arabidopsis seedlings. . Mol. Plant 1:(3):42345
    [Crossref] [Google Scholar]
  13. 13.
    Deslauriers SD, Larsen PB. 2010.. FERONIA is a key modulator of brassinosteroid and ethylene responsiveness in Arabidopsis hypocotyls. . Mol. Plant 3:(3):62640
    [Crossref] [Google Scholar]
  14. 14.
    Díaz-Troya S, Pérez-Pérez ME, Florencio FJ, Crespo JL. 2008.. The role of TOR in autophagy regulation from yeast to plants and mammals. . Autophagy 4:(7):85165
    [Crossref] [Google Scholar]
  15. 15.
    Doblas VG, Gonneau M, Höfte H. 2018.. Cell wall integrity signaling in plants: malectin-domain kinases and lessons from other kingdoms. . Cell Surf. 3::111
    [Crossref] [Google Scholar]
  16. 16.
    Dong Q, Zhang Z, Liu Y, Tao L-Z, Liu H. 2019.. FERONIA regulates auxin-mediated lateral root development and primary root gravitropism. . FEBS Lett. 593:(1):97106
    [Crossref] [Google Scholar]
  17. 17.
    Dressano K, Ceciliato PHO, Silva AL, Guerrero-Abad JC, Bergonci T, et al. 2017.. BAK1 is involved in AtRALF1-induced inhibition of root cell expansion. . PLOS Genet. 13:(10):e1007053
    [Crossref] [Google Scholar]
  18. 18.
    Du C, Li X, Chen J, Chen W, Li B, et al. 2016.. Receptor kinase complex transmits RALF peptide signal to inhibit root growth in Arabidopsis. . PNAS 113:(51):E832634
    [Google Scholar]
  19. 19.
    Du J, Anderson CT, Xiao C. 2022.. Dynamics of pectic homogalacturonan in cellular morphogenesis and adhesion, wall integrity sensing and plant development. . Nat. Plants 8:(4):33240
    [Crossref] [Google Scholar]
  20. 20.
    Du S, Qu L-J, Xiao J. 2018.. Crystal structures of the extracellular domains of the CrRLK1L receptor-like kinases ANXUR1 and ANXUR2. . Protein Sci. 27:(4):88692
    [Crossref] [Google Scholar]
  21. 21.
    Duan Q, Cheung AY. 2018.. Context-specific dependence on FERONIA kinase activity. . FEBS Lett. 592:(14):239294
    [Crossref] [Google Scholar]
  22. 22.
    Duan Q, Kita D, Johnson EA, Aggarwal M, Gates L, et al. 2014.. Reactive oxygen species mediate pollen tube rupture to release sperm for fertilization in Arabidopsis. . Nat. Commun. 5::3129 22. Demonstrates that FER-controlled ROS in the female gametophyte mediate sperm release.
    [Crossref] [Google Scholar]
  23. 23.
    Duan Q, Kita D, Li C, Cheung AY, Wu H-M. 2010.. FERONIA receptor-like kinase regulates RHO GTPase signaling of root hair development. . PNAS 107:(41):1782126 23. Demonstrates that FER is a cell surface receptor upstream of RAC/ROP GTPases and that loss of FER results in pleiotropic growth-related phenotypes.
    [Crossref] [Google Scholar]
  24. 24.
    Duan Q, Liu M-CJ, Kita D, Jordan SS, Yeh F-LJ, et al. 2020.. FERONIA controls pectin- and nitric oxide-mediated male–female interaction. . Nature 579:(7800):56166 24. Establishes a FER-to-pectin-to-NO linkage in mediating the FER-controlled polyspermy block at the entrance to the female gametophyte.
    [Crossref] [Google Scholar]
  25. 25.
    Dünser 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:(7):e100353
    [Crossref] [Google Scholar]
  26. 26.
    Escobar-Restrepo J-M, Huck N, Kessler S, Gagliardini V, Gheyselinck J, et al. 2007.. The FERONIA receptor-like kinase mediates male-female interactions during pollen tube reception. . Science 317:(5838):65660 26. Identifies FER as a receptor kinase.
    [Crossref] [Google Scholar]
  27. 27.
    Fabrice TN, Vogler H, Draeger C, Munglani G, Gupta S, et al. 2018.. LRX proteins play a crucial role in pollen grain and pollen tube cell wall development. . Plant Physiol. 176:(3):198192
    [Crossref] [Google Scholar]
  28. 28.
    Farnese FS, Menezes-Silva PE, Gusman GS, Oliveira JA. 2016.. When bad guys become good ones: the key role of reactive oxygen species and nitric oxide in the plant responses to abiotic stress. . Front. Plant Sci. 7::471
    [Crossref] [Google Scholar]
  29. 29.
    Feiguelman G, Fu Y, Yalovsky S. 2018.. ROP GTPases structure-function and signaling pathways. . Plant Physiol. 176:(1):5779
    [Crossref] [Google Scholar]
  30. 30.
    Feng H, Liu C, Fu R, Zhang M, Li H, et al. 2019.. LORELEI-LIKE GPI-ANCHORED PROTEINS 2/3 regulate pollen tube growth as chaperones and coreceptors for ANXUR/BUPS receptor kinases in Arabidopsis. . Mol. Plant 12:(12):161223
    [Crossref] [Google Scholar]
  31. 31.
    Feng W, Kita D, Peaucelle A, Cartwright HN, Doan V, et al. 2018.. The FERONIA receptor kinase maintains cell-wall integrity during salt stress through Ca2+ signaling. . Curr. Biol. 28:(5):66675.e5 31. Demonstrates that FER interaction with cell wall pectin underlies the wall integrity important for withstanding osmotic stress under high salt.
    [Crossref] [Google Scholar]
  32. 32.
    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::30128
    [Crossref] [Google Scholar]
  33. 33.
    Fu Y, Kawasaki T, Shimamoto K, Yang Z. 2018.. ROP/RAC GTPases. . In Annual Plant Reviews Online, ed. JA Roberts , pp. 6499. Hoboken, NJ:: John Wiley & Sons.
    [Google Scholar]
  34. 34.
    Gachomo EW, Jno Baptiste L, Kefela T, Saidel WM, Kotchoni SO. 2014.. The Arabidopsis CURVY1 (CVY1) gene encoding a novel receptor-like protein kinase regulates cell morphogenesis, flowering time and seed production. . BMC Plant Bio. 14:(1):221
    [Crossref] [Google Scholar]
  35. 35.
    Galindo-Trigo S, Blanco-Touriñán N, DeFalco TA, Wells ES, Gray JE, et al. 2020.. CrRLK1L receptor-like kinases HERK1 and ANJEA are female determinants of pollen tube reception. . EMBO Rep. 21:(2):e48466
    [Crossref] [Google Scholar]
  36. 36.
    Gallego-Giraldo L, Posé S, Pattathil S, Peralta AG, Hahn MG, et al. 2018.. Elicitors and defense gene induction in plants with altered lignin compositions. . New Phytol. 219:(4):123551
    [Crossref] [Google Scholar]
  37. 37.
    Galletti R, Denoux C, Gambetta S, Dewdney J, Ausubel FM, et al. 2008.. The AtrbohD-mediated oxidative burst elicited by oligogalacturonides in Arabidopsis is dispensable for the activation of defense responses effective against Botrytis cinerea. . Plant Physiol. 148:(3):1695706
    [Crossref] [Google Scholar]
  38. 38.
    Galli C, Bernasconi R, Soldà T, Calanca V, Molinari M. 2011.. Malectin participates in a backup glycoprotein quality control pathway in the mammalian ER. . PLOS ONE 6:(1):e16304
    [Crossref] [Google Scholar]
  39. 39.
    Gao Q, Wang C, Xi Y, Shao Q, Hou C, et al. 2023.. RALF signaling pathway activates MLO calcium channels to maintain pollen tube integrity. . Cell Res. 33:(1):7179
    [Crossref] [Google Scholar]
  40. 40.
    Gao Q, Wang C, Xi Y, Shao Q, Li L, Luan S. 2022.. A receptor–channel trio conducts Ca2+ signalling for pollen tube reception. . Nature 607:(7919):53439 40. Proposes a MLO as a Ca2+ channel in the FER-LORELEI complex.
    [Crossref] [Google Scholar]
  41. 41.
    Ge Z, Bergonci T, Zhao Y, Zou Y, Du S, et al. 2017.. Arabidopsis pollen tube integrity and sperm release are regulated by RALF-mediated signaling. . Science 358:(6370):1596600 41. The first mechanistic report of a pollen FER-related signaling module controlling pollen tube integrity.
    [Crossref] [Google Scholar]
  42. 42.
    Ge Z, Cheung AY, Qu L-J. 2019.. Pollen tube integrity regulation in flowering plants: insights from molecular assemblies on the pollen tube surface. . New Phytol. 222:(2):68793
    [Crossref] [Google Scholar]
  43. 43.
    Ge Z, Zhao Y, Liu M-C, Zhou L-Z, Wang L, et al. 2019.. LLG2/3 are co-receptors in BUPS/ANX-RALF signaling to regulate Arabidopsis pollen tube integrity. . Curr. Biol. 29:(19):325665.e5 43. Establishes a pollen RALF-FER-related receptor-LLG signaling module.
    [Crossref] [Google Scholar]
  44. 44.
    Gigli-Bisceglia N, van Zelm E, Huo W, Lamers J, Testerink C. 2022.. Arabidopsis root responses to salinity depend on pectin modification and cell wall sensing. . Development 149:(12):dev200363
    [Crossref] [Google Scholar]
  45. 45.
    Gilbert HJ, Knox JP, Boraston AB. 2013.. Advances in understanding the molecular basis of plant cell wall polysaccharide recognition by carbohydrate-binding modules. . Curr. Opin. Struct. Biol. 23:(5):66977
    [Crossref] [Google Scholar]
  46. 46.
    Gonneau M, Desprez T, Martin M, Doblas VG, Bacete L, et al. 2018.. Receptor kinase THESEUS1 is a rapid alkalinization factor 34 receptor in Arabidopsis. . Curr. Biol. 28:(15):245258.e4
    [Crossref] [Google Scholar]
  47. 47.
    Goring DR, Bosch M, Franklin-Tong VE. 2023.. Contrasting self-recognition rejection systems for self-incompatibility in Brassica and Papaver. . Curr. Biol. 33:(11):R53042
    [Crossref] [Google Scholar]
  48. 48.
    Gronnier J, Franck CM, Stegmann M, DeFalco TA, Abarca A, et al. Regulation of immune receptor kinase plasma membrane nanoscale organization by a plant peptide hormone and its receptors. . eLife 11::e74162
    [Crossref] [Google Scholar]
  49. 49.
    Guo H, Li L, Ye H, Yu X, Algreen A, Yin Y. 2009.. Three related receptor-like kinases are required for optimal cell elongation in Arabidopsis thaliana. . PNAS 106:(18):764853
    [Crossref] [Google Scholar]
  50. 50.
    Guo H, Nolan TM, Song G, Liu S, Xie Z, et al. 2018.. FERONIA receptor kinase contributes to plant immunity by suppressing jasmonic acid signaling in Arabidopsis thaliana. . Curr. Biol. 28:(20):331624.e6
    [Crossref] [Google Scholar]
  51. 51.
    Hahm J, Kim K, Qiu Y, Chen M. 2020.. Increasing ambient temperature progressively disassembles Arabidopsis phytochrome B from individual photobodies with distinct thermostabilities. . Nat. Commun. 11:(1):1660
    [Crossref] [Google Scholar]
  52. 52.
    Haruta M, Sabat G, Stecker K, Minkoff BB, Sussman MR. 2014.. A peptide hormone and its receptor protein kinase regulate plant cell expansion. . Science 343:(6169):40811 52. The discovery of RALF as a signaling ligand for FER.
    [Crossref] [Google Scholar]
  53. 53.
    Hématy K, Höfte H. 2008.. Novel receptor kinases involved in growth regulation. . Curr. Opin. Plant Biol. 11:(3):32128
    [Crossref] [Google Scholar]
  54. 54.
    Hématy K, Sado P-E, Van Tuinen A, Rochange S, Desnos T, et al. 2007.. A receptor-like kinase mediates the response of Arabidopsis cells to the inhibition of cellulose synthesis. . Curr. Biol. 17:(11):92231 54. The discovery of THESEUS1 as a regulator of growth under cell wall–compromised conditions.
    [Crossref] [Google Scholar]
  55. 55.
    Herger A, Dünser K, Kleine-Vehn J, Ringli C. 2019.. Leucine-rich repeat extensin proteins and their role in cell wall sensing. . Curr. Biol. 29:(17):R85158
    [Crossref] [Google Scholar]
  56. 56.
    Herger A, Gupta S, Kadler G, Franck CM, Boisson-Dernier A, Ringli C. 2020.. Overlapping functions and protein-protein interactions of LRR-extensins in Arabidopsis. . PLOS Genet. 16:(6):e1008847
    [Crossref] [Google Scholar]
  57. 57.
    Huang J, Yang L, Yang L, Wu X, Cui X, et al. 2023.. Stigma receptors control intraspecies and interspecies barriers in Brassicaceae. . Nature 614:(7947):3038 57. Establishes that FER controls stigmatic gating in various pollination compatibility systems and proof-of-principle cross-reproduction barrier experiments.
    [Crossref] [Google Scholar]
  58. 58.
    Huang Y, Yin C, Liu J, Feng B, Ge D, et al. 2020.. A trimeric CrRLK1L-LLG1 complex genetically modulates SUMM2-mediated autoimmunity. . Nat. Commun. 11:(1):4859
    [Crossref] [Google Scholar]
  59. 59.
    Huck N, Moore JM, Federer M, Grossniklaus U. 2003.. The Arabidopsis mutant feronia disrupts the female gametophytic control of pollen tube reception. . Development 130:(10):214959
    [Crossref] [Google Scholar]
  60. 60.
    Iwano M, Ngo QA, Entani T, Shiba H, Nagai T, et al. 2012.. Cytoplasmic Ca2+ changes dynamically during the interaction of the pollen tube with synergid cells. . Development 139:(22):42029
    [Crossref] [Google Scholar]
  61. 61.
    Jacott CN, Ridout CJ, Murray JD. 2021.. Unmasking Mildew Resistance Locus O. . Trends Plant Sci. 26:(10):100613
    [Crossref] [Google Scholar]
  62. 62.
    Johnson MA, Harper JF, Palanivelu R. 2019.. A fruitful journey: pollen tube navigation from germination to fertilization. . Annu. Rev. Plant Biol. 70::80937
    [Crossref] [Google Scholar]
  63. 63.
    Ju Y, Yuan J, Jones DS, Zhang W, Staiger CJ, Kessler SA. 2021.. Polarized NORTIA accumulation in response to pollen tube arrival at synergids promotes fertilization. . Dev. Cell 56:(21):293851.e6
    [Crossref] [Google Scholar]
  64. 64.
    Kessler SA, Grossniklaus U. 2011.. She's the boss: signaling in pollen tube reception. . Curr. Opin. Plant Biol. 14:(5):62227
    [Crossref] [Google Scholar]
  65. 65.
    Kessler SA, Lindner H, Jones DS, Grossniklaus U. 2015.. Functional analysis of related CrRLK1L receptor-like kinases in pollen tube reception. . EMBO Rep. 16:(1):10715
    [Crossref] [Google Scholar]
  66. 66.
    Kessler SA, Shimosato-Asano H, Keinath NF, Wuest SE, Ingram G, et al. 2010.. Conserved molecular components for pollen tube reception and fungal invasion. . Science 330:(6006):96871 66. The discovery of an MLO as a functional partner with FER and LORELEI.
    [Crossref] [Google Scholar]
  67. 67.
    Kim D, Yang J, Gu F, Park S, Combs J, et al. 2020.. A temperature-sensitive FERONIA mutant allele that alters root hair growth. . Plant Physiol. 185:(2):40523
    [Crossref] [Google Scholar]
  68. 68.
    Kinoshita T. 2020.. Biosynthesis and biology of mammalian GPI-anchored proteins. . Open Biol. 10:(3):190290
    [Crossref] [Google Scholar]
  69. 69.
    Kita DW. 2013.. Feronia: a malectin-like domain-containing receptor kinase in Arabidopsis thaliana. PhD thesis , Univ. Mass., Amherst, MA:
    [Google Scholar]
  70. 70.
    Kohorn BD. 2015.. The state of cell wall pectin monitored by wall associated kinases: a model. . Plant Signal. Behav. 10:(7):e1035854
    [Crossref] [Google Scholar]
  71. 71.
    Kusch S, Panstruga R. 2017.. mlo-Based resistance: an apparently universal “weapon” to defeat powdery mildew disease. . Mol. Plant Microbe Interact. 30:(3):17989
    [Crossref] [Google Scholar]
  72. 72.
    Kwon T, Sparks JA, Liao F, Blancaflor EB. 2018.. ERULUS is a plasma membrane-localized receptor-like kinase that specifies root hair growth by maintaining tip-focused cytoplasmic calcium oscillations. . Plant Cell 30:(6):117377
    [Crossref] [Google Scholar]
  73. 73.
    Li C, Wu H-M, Cheung AY. 2016.. FERONIA and her pals: functions and mechanisms. . Plant Physiol. 171:(4):237992
    [Crossref] [Google Scholar]
  74. 74.
    Li C, Yeh F-L, Cheung AY, Duan Q, Kita D, et al. 2015.. Glycosylphosphatidylinositol-anchored proteins as chaperones and co-receptors for FERONIA receptor kinase signaling in Arabidopsis. . eLife 4::e06587 74. The discovery of a GPI-AP as a chaperone and coreceptor for FER and implications of a tripartite signaling module complex with RALF.
    [Crossref] [Google Scholar]
  75. 75.
    Liao H, Tang R, Zhang X, Luan S, Yu F. 2017.. FERONIA receptor kinase at the crossroads of hormone signaling and stress responses. . Plant Cell Physiol. 58:(7):114350
    [Crossref] [Google Scholar]
  76. 76.
    Lin W, Tang W, Pan X, Huang A, Gao X, et al. 2022.. Arabidopsis pavement cell morphogenesis requires FERONIA binding to pectin for activation of ROP GTPase signaling. . Curr. Biol. 32:(3):497507.e4
    [Crossref] [Google Scholar]
  77. 77.
    Liu C, Shen L, Xiao Y, Vyshedsky D, Peng C, et al. 2021.. Pollen PCP-B peptides unlock a stigma peptide–receptor kinase gating mechanism for pollination. . Science 372:(6538):17175 77. The discovery of pollen-derived ligands that interact with and modulate a RALF-FER-LLG1 controlled stigmatic gating mechanism for mate selection.
    [Crossref] [Google Scholar]
  78. 78.
    Liu C, Yu H, Voxeur A, Rao X, Dixon RA. 2023.. FERONIA and wall-associated kinases coordinate defense induced by lignin modification in plant cell walls. . Sci. Adv. 9:(10):eadf7714 78. Connects FER to sensing perturbations in the secondary cell wall to provoke defense signaling.
    [Crossref] [Google Scholar]
  79. 79.
    Liu J, Huang Y, Kong L, Yu X, Feng B, et al. 2020.. The malectin-like receptor-like kinase LETUM1 modulates NLR protein SUMM2 activation via MEKK2 scaffolding. . Nat. Plants 6:(9):110615
    [Crossref] [Google Scholar]
  80. 80.
    Liu M-CJ, Yeh F-LJ, Yvon R, Simpson K, Jordan S, et al. 2024.. Extracellular pectin-RALF phase separation mediates FERONIA global signaling function. . Cell 182:(2):31230.e22 80. Reports RALF–pectin interaction–driven phase separation as underlying FER's diverse functional roles, such as to mediate stress resilience.
    [Crossref] [Google Scholar]
  81. 81.
    Liu X, Castro C, Wang Y, Noble J, Ponvert N, et al. 2016.. 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 28:(5):103552
    [Crossref] [Google Scholar]
  82. 82.
    Liu X, Jiang W, Li Y, Nie H, Cui L, et al. 2023.. FERONIA coordinates plant growth and salt tolerance via the phosphorylation of phyB. . Nat. Plants 9:(4):64560 82. Connects FER to phytochrome signaling.
    [Crossref] [Google Scholar]
  83. 83.
    Malivert A, Erguvan Ö, Chevallier A, Dehem A, Friaud R, et al. 2021.. FERONIA and microtubules independently contribute to mechanical integrity in the Arabidopsis shoot. . PLOS Biol. 19:(11):e3001454
    [Crossref] [Google Scholar]
  84. 84.
    Malivert A, Hamant O. 2023.. Why is FERONIA pleiotropic?. Nat. Plants 9::101825
    [Crossref] [Google Scholar]
  85. 85.
    Mang H, Feng B, Hu Z, Boisson-Dernier A, Franck CM, et al. 2017.. Differential regulation of two-tiered plant immunity and sexual reproduction by ANXUR receptor-like kinases. . Plant Cell 29:(12):314056 85. An immunity study with implications on how divergence between FER-related receptors might be translated into functional divergence.
    [Crossref] [Google Scholar]
  86. 86.
    Mao D, Yu F, Li J, Van de Poel B, Tan D, et al. 2015.. FERONIA receptor kinase interacts with S-adenosylmethionine synthetase and suppresses S-adenosylmethionine production and ethylene biosynthesis in Arabidopsis. . Plant Cell Environ. 38:(12):256674
    [Crossref] [Google Scholar]
  87. 87.
    Masachis S, Segorbe D, Turrà D, Leon-Ruiz M, Fürst U, et al. 2016.. A fungal pathogen secretes plant alkalinizing peptides to increase infection. . Nat. Microbiol. 1:(6):16043
    [Crossref] [Google Scholar]
  88. 88.
    Mecchia MA, Santos-Fernandez G, Duss NN, Somoza SC, Boisson-Dernier A, et al. 2017.. RALF4/19 peptides interact with LRX proteins to control pollen tube growth in Arabidopsis. . Science 358:(6370):16003 88. The discovery of LRX interacting with RALF-FER-related receptor signaling modules.
    [Crossref] [Google Scholar]
  89. 89.
    Merz D, Richter J, Gonneau M, Sanchez-Rodriguez C, Eder T, et al. 2017.. T-DNA alleles of the receptor kinase THESEUS1 with opposing effects on cell wall integrity signaling. . J. Exp. Bot. 68:(16):458393
    [Crossref] [Google Scholar]
  90. 90.
    Mittler R. 2017.. ROS are good. . Trends Plant Sci. 22:(1):1119
    [Crossref] [Google Scholar]
  91. 91.
    Miyazaki S, Murata T, Sakurai-Ozato N, Kubo M, Demura T, et al. 2009.. ANXUR1 and 2, sister genes to FERONIA/SIRENE, are male factors for coordinated fertilization. . Curr. Biol. 19:(15):132731 91. The first report of a pair of key male fertility regulators.
    [Crossref] [Google Scholar]
  92. 92.
    Molina-Moya E, Terrón-Camero LC, Pescador-Azofra L, Sandalio LM, Romero-Puertas MC. 2019.. Reactive oxygen species and nitric oxide production, regulation and function during defense response. . In Reactive Oxygen, Nitrogen and Sulfur Species in Plants, ed. M Hasanuzzaman, V Fotopoulos, K Nahar, M Fujita , pp. 57390. Hoboken, NJ:: John Wiley & Sons
    [Google Scholar]
  93. 93.
    Moussu S, Augustin S, Roman AO, Broyart C, Santiago J. 2018.. Crystal structures of two tandem malectin-like receptor kinases involved in plant reproduction. . Acta Crystallogr. D Struct. Biol. 74:(Part 7):67180 93. The first in-depth report of a high-resolution FER-related extracellular domain structure.
    [Crossref] [Google Scholar]
  94. 94.
    Moussu S, Broyart C, Santos-Fernandez G, Augustin S, Wehrle S, et al. 2020.. Structural basis for recognition of RALF peptides by LRX proteins during pollen tube growth. . PNAS 117:(13):7494503
    [Crossref] [Google Scholar]
  95. 95.
    Moussu S, Ingram G. 2023.. The EXTENSIN enigma. . Cell Surf. 9::100094
    [Crossref] [Google Scholar]
  96. 96.
    Ngo QA, Vogler H, Lituiev DS, Nestorova A, Grossniklaus U. 2014.. A calcium dialog mediated by the FERONIA signal transduction pathway controls plant sperm delivery. . Dev. Cell 29:(4):491500
    [Crossref] [Google Scholar]
  97. 97.
    Ngou BPM, Ahn H-K, Ding P, Jones JDG. 2021.. Mutual potentiation of plant immunity by cell-surface and intracellular receptors. . Nature 592:(7852):11015
    [Crossref] [Google Scholar]
  98. 98.
    Nibau C, Cheung AY. 2011.. New insights into the functional roles of CrRLKs in the control of plant cell growth and development. . Plant Signal. Behav. 6:(5):65559
    [Crossref] [Google Scholar]
  99. 99.
    Nibau C, Wu H, Cheung AY. 2006.. RAC/ROP GTPases: “hubs” for signal integration and diversification in plants. . Trends Plant Sci. 11:(6):30915
    [Crossref] [Google Scholar]
  100. 100.
    Noble JA, Bielski NV, Liu M-CJ, DeFalco TA, Stegmann M, et al. 2022.. Evolutionary analysis of the LORELEI gene family in plants reveals regulatory subfunctionalization. . Plant Physiol. 190:(4):253956
    [Crossref] [Google Scholar]
  101. 101.
    Ortiz-Morea FA, Liu J, Shan L, He P. 2022.. Malectin-like receptor kinases as protector deities in plant immunity. . Nat. Plants 8:(1):2737
    [Crossref] [Google Scholar]
  102. 102.
    Pacheco JM, Song L, Kuběnová L, Ovečka M, Berdion Gabarain V, et al. 2023.. Cell surface receptor kinase FERONIA linked to nutrient sensor TORC signaling controls root hair growth at low temperature linked to low nitrate in Arabidopsis thaliana. . New Phytol. 238:(1):16985
    [Crossref] [Google Scholar]
  103. 103.
    Palmgren M, Morsomme P. 2019.. The plasma membrane H+-ATPase, a simple polypeptide with a long history. . Yeast 36:(4):20110
    [Crossref] [Google Scholar]
  104. 104.
    Pearce G, Moura DS, Stratmann J, Ryan CA. 2001.. RALF, a 5-kDa ubiquitous polypeptide in plants, arrests root growth and development. . PNAS 98:(22):1284347
    [Crossref] [Google Scholar]
  105. 105.
    Pearce G, Yamaguchi Y, Munske G, Ryan CA. 2010.. Structure-activity studies of RALF, Rapid Alkalinization Factor, reveal an essential–YISY–motif. . Peptides 31:(11):197377
    [Crossref] [Google Scholar]
  106. 106.
    Peaucelle A, Höfte H, Braybrook S. 2012.. Cell wall mechanics and growth control in plants: the role of pectins revisited. . Front. Plant Sci. 3::121
    [Crossref] [Google Scholar]
  107. 107.
    Pu C, Han Y, Zhu S, Song F, Zhao Y, et al. 2017.. The rice receptor-like kinases DWARF AND RUNTISH SPIKELET1 and 2 repress cell death and affect sugar utilization in reproductive development. . Plant Cell 29::7089
    [Crossref] [Google Scholar]
  108. 108.
    Rotman N, Rozier F, Boavida L, Dumas C, Berger F, Faure J-E. 2003.. Female control of male gamete delivery during fertilization in Arabidopsis thaliana. . Curr. Biol. 13:(5):43236
    [Crossref] [Google Scholar]
  109. 109.
    Rubinstein AL, Broadwater AH, Lowrey KB, Bedinger PA. 1995.. Pex1, a pollen-specific gene with an extensin-like domain. . PNAS 92:(8):308690
    [Crossref] [Google Scholar]
  110. 110.
    Schallus T, Feher K, Sternberg U, Rybin V, Muhle-Goll C. 2010.. Analysis of the specific interactions between the lectin domain of malectin and diglucosides. . Glycobiology 20::101020
    [Crossref] [Google Scholar]
  111. 111.
    Schallus T, Jaeckh C, Fehér K, Palma AS, Liu Y, et al. 2008.. Malectin: a novel carbohydrate-binding protein of the endoplasmic reticulum and a candidate player in the early steps of protein N-glycosylation. . Mol. Biol. Cell 19:(8):340414 111. The discovery of Malectin, which inspired intense speculation that the FER family receptors are wall sensors.
    [Crossref] [Google Scholar]
  112. 112.
    Scheer JM, Pearce G, Ryan CA. 2005.. LeRALF, a plant peptide that regulates root growth and development, specifically binds to 25 and 120 kDa cell surface membrane proteins of Lycopersicon peruvianum. . Planta 221:(5):66774
    [Crossref] [Google Scholar]
  113. 113.
    Schepetilnikov M, Makarian J, Srour O, Geldreich A, Yang Z, et al. 2017.. GTPase ROP2 binds and promotes activation of target of rapamycin, TOR, in response to auxin. . EMBO J. 36:(7):886903
    [Crossref] [Google Scholar]
  114. 114.
    Schoenaers S, Balcerowicz D, Breen G, Hill K, Zdanio M, et al. 2018.. The auxin-regulated CrRLK1L kinase ERULUS controls cell wall composition during root hair tip growth. . Curr. Biol. 28:(5):72232.e6
    [Crossref] [Google Scholar]
  115. 115.
    Schoenaers S, Balcerowicz D, Costa A, Vissenberg K. 2017.. The kinase ERULUS controls pollen tube targeting and growth in Arabidopsis thaliana. . Front. Plant Sci. 8::1942
    [Crossref] [Google Scholar]
  116. 116.
    Schulze-Muth P, Irmler S, Schröder G, Schröder J. 1996.. Novel type of receptor-like protein kinase from a higher plant (Catharanthus roseus): cDNA, gene, intramolecular autophosphorylation, and identification of a threonine important for auto- and substrate phosphorylation. . J. Biol. Chem. 271:(43):2668489
    [Crossref] [Google Scholar]
  117. 117.
    Sharrock RA. 2008.. The phytochrome red/far-red photoreceptor superfamily. . Genome Biol. 9:(8):230
    [Crossref] [Google Scholar]
  118. 118.
    Shen Q, Bourdais G, Pan H, Robatzek S, Tang D. 2017.. Arabidopsis glycosylphosphatidylinositol-anchored protein LLG1 associates with and modulates FLS2 to regulate innate immunity. . PNAS 114:(22):574954
    [Crossref] [Google Scholar]
  119. 119.
    Shi L, Wu Y, Sheen J. 2018.. TOR signaling in plants: conservation and innovation. . Development 145:(13):dev160887
    [Crossref] [Google Scholar]
  120. 120.
    Shih H-W, Miller ND, Dai C, Spalding EP, Monshausen GB. 2014.. The receptor-like kinase FERONIA is required for mechanical signal transduction in Arabidopsis seedlings. . Curr. Biol. 24:(16):188792
    [Crossref] [Google Scholar]
  121. 121.
    Shin SY, Park JS, Park HB, Moon KB, Kim HS, et al. 2021.. FERONIA confers resistance to photooxidative stress in Arabidopsis. . Front. Plant Sci. 12::714938
    [Crossref] [Google Scholar]
  122. 122.
    Shin Y, Chane A, Jung M, Lee Y. 2021.. Recent advances in understanding the roles of pectin as an active participant in plant signaling networks. . Plants 10:(8):1712
    [Crossref] [Google Scholar]
  123. 123.
    Shiu S-H, Bleecker AB. 2003.. Expansion of the receptor-like kinase/Pelle gene family and receptor-like proteins in Arabidopsis. . Plant Physiol. 132:(2):53043
    [Crossref] [Google Scholar]
  124. 124.
    Smokvarska M, Bayle V, Maneta-Peyret L, Fouillen L, Poitout A, et al. 2023.. The receptor kinase FERONIA regulates phosphatidylserine localization at the cell surface to modulate ROP signaling. . Sci. Adv. 9:(14):eadd4791
    [Crossref] [Google Scholar]
  125. 125.
    Song L, Xu G, Li T, Zhou H, Lin Q, et al. 2022.. The RALF1-FERONIA complex interacts with and activates TOR signaling in response to low nutrients. . Mol. Plant 15:(7):112036
    [Crossref] [Google Scholar]
  126. 126.
    Song Y, Wilson AJ, Zhang X-C, Thoms D, Sohrabi R, et al. 2021.. FERONIA restricts Pseudomonas in the rhizosphere microbiome via regulation of reactive oxygen species. . Nat. Plants 7:(5):64454 126. Places FER at the plant–rhizosphere interface, where it regulates the soil microbiome to impact plant wellness.
    [Crossref] [Google Scholar]
  127. 127.
    Spielman M, Scott R. 2008.. Polyspermy barriers in plants: from preventing to promoting fertilization. . Sex. Plant Reprod. 21::5365
    [Crossref] [Google Scholar]
  128. 128.
    Srivastava R, Liu J-X, Guo H, Yin Y, Howell SH. 2009.. Regulation and processing of a plant peptide hormone, AtRALF23, in Arabidopsis. . Plant J. 59:(6):93039
    [Crossref] [Google Scholar]
  129. 129.
    Stegmann M, Monaghan J, Smakowska-Luzan E, Rovenich H, Lehner A, et al. 2017.. The receptor kinase FER is a RALF-regulated scaffold controlling plant immune signaling. . Science 355:(6322):28789 129. An in-depth study reporting the discovery of a RALF-FER ligand-receptor relationship in regulating immunity signaling.
    [Crossref] [Google Scholar]
  130. 130.
    Takeuchi H, Higashiyama T. 2012.. A species-specific cluster of defensin-like genes encodes diffusible pollen tube attractants in Arabidopsis. . PLOS Biol. 10:(12):e1001449
    [Crossref] [Google Scholar]
  131. 131.
    Tang W, Lin W, Zhou X, Guo J, Dang X, et al. 2022.. Mechano-transduction via the pectin-FERONIA complex activates ROP6 GTPase signaling in Arabidopsis pavement cell morphogenesis. . Curr. Biol. 32::50817
    [Crossref] [Google Scholar]
  132. 132.
    Thynne E, Saur IML, Simbaqueba J, Ogilvie HA, Gonzalez-Cendales Y, et al. 2017.. Fungal phytopathogens encode functional homologues of plant rapid alkalinization factor (RALF) peptides. . Mol. Plant Pathol. 18:(6):81124
    [Crossref] [Google Scholar]
  133. 133.
    Tsukamoto T, Qin Y, Huang Y, Dunatunga D, Palanivelu R. 2010.. A role for LORELEI, a putative glycosylphosphatidylinositol-anchored protein, in Arabidopsis thaliana double fertilization and early seed development. . Plant J. 62:(4):57188
    [Crossref] [Google Scholar]
  134. 134.
    Voxeur A, Habrylo O, Guénin S, Miart F, Soulié M-C, et al. 2019.. Oligogalacturonide production upon Arabidopsis thaliana–Botrytis cinerea interaction. . PNAS 116:(39):1974352
    [Crossref] [Google Scholar]
  135. 135.
    Voxeur A, Höfte H. 2016.. Cell wall integrity signaling in plants: “To grow or not to grow that's the question. .” Glycobiology 26:(9):95060
    [Crossref] [Google Scholar]
  136. 136.
    Wang L, Clarke LA, Eason RJ, Parker CC, Qi B, et al. 2017.. PCP-B class pollen coat proteins are key regulators of the hydration checkpoint in Arabidopsis thaliana pollen–stigma interactions. . New Phytol. 213:(2):76477
    [Crossref] [Google Scholar]
  137. 137.
    Wang L, Lau Y-L, Fan L, Bosch M, Doughty J. 2023.. Pollen coat proteomes of Arabidopsis thaliana, Arabidopsis lyrata, and Brassica oleracea reveal remarkable diversity of small cysteine-rich proteins at the pollen-stigma interface. . Biomolecules 13:(1):157
    [Crossref] [Google Scholar]
  138. 138.
    Wang L, Yang T, Lin Q, Wang B, Li X, et al. 2020.. Receptor kinase FERONIA regulates flowering time in Arabidopsis. . BMC Plant Biol. 20:(1):26
    [Crossref] [Google Scholar]
  139. 139.
    Wang P, Clark NM, Nolan TM, Song G, Bartz PM, et al. 2022.. Integrated omics reveal novel functions and underlying mechanisms of the receptor kinase FERONIA in Arabidopsis thaliana. . Plant Cell 34:(7):2594614
    [Crossref] [Google Scholar]
  140. 140.
    Wang P, Clark NM, Nolan TM, Song G, Whitham OG, et al. 2022.. FERONIA functions through Target of Rapamycin (TOR) to negatively regulate autophagy. . Front. Plant Sci. 13::961096
    [Crossref] [Google Scholar]
  141. 141.
    Wang Y, Loake GJ, Chu C. 2013.. Cross-talk of nitric oxide and reactive oxygen species in plant programed cell death. . Front. Plant Sci. 4::314
    [Google Scholar]
  142. 142.
    Waszczak C, Carmody M, Kangasjärvi J. 2018.. Reactive oxygen species in plant signaling. . Annu. Rev. Plant Biol. 69::20936
    [Crossref] [Google Scholar]
  143. 143.
    Wolf S. 2022.. Cell wall signaling in plant development and defense. . Annu. Rev. Plant Biol. 73::32353
    [Crossref] [Google Scholar]
  144. 144.
    Wood AKM, Walker C, Lee W-S, 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):75365
    [Crossref] [Google Scholar]
  145. 145.
    Xiao Y, Stegmann M, Han Z, DeFalco TA, Parys K, et al. 2019.. Mechanisms of RALF peptide perception by a heterotypic receptor complex. . Nature 572:(7768):27074 145. The first high-resolution structural study of a RALF-FER-LLG complex.
    [Crossref] [Google Scholar]
  146. 146.
    Xu G, Chen W, Song L, Chen Q, Zhang H, et al. 2019.. FERONIA phosphorylates E3 ubiquitin ligase ATL6 to modulate the stability of 14-3-3 proteins in response to the carbon/nitrogen ratio. . J. Exp. Bot. 70:(21):637588
    [Crossref] [Google Scholar]
  147. 147.
    Yang H, Wang D, Guo L, Pan H, Yvon R, et al. 2021.. Malectin/Malectin-like domain-containing proteins: a repertoire of cell surface molecules with broad functional potential. . Cell Surf. 7::100056
    [Crossref] [Google Scholar]
  148. 148.
    Yang T, Wang L, Li C, Liu Y, Zhu S, et al. 2015.. Receptor protein kinase FERONIA controls leaf starch accumulation by interacting with glyceraldehyde-3-phosphate dehydrogenase. . Biochem. Biophys. Res. Commun. 465:(1):7782
    [Crossref] [Google Scholar]
  149. 149.
    Yang Z, Xing J, Wang L, Liu Y, Qu J, et al. 2020.. Mutations of two FERONIA-like receptor genes enhance rice blast resistance without growth penalty. . J. Exp. Bot. 71:(6):211226
    [Crossref] [Google Scholar]
  150. 150.
    Yeats TH, Johnson AB, Johnson KL. 2018.. Plant glycosylphosphatidylinositol anchored proteins at the plasma membrane-cell wall nexus. . J. Integr. Plant Biol. 60:(8):64969
    [Crossref] [Google Scholar]
  151. 151.
    Yu F, Li J, Huang Y, Liu L, Li D, et al. 2014.. FERONIA receptor kinase controls seed size in Arabidopsis thaliana. . Mol. Plant 7:(5):92022
    [Crossref] [Google Scholar]
  152. 152.
    Yu F, Qian L, Nibau C, Duan Q, Kita D, et al. 2012.. FERONIA receptor kinase pathway suppresses abscisic acid signaling in Arabidopsis by activating ABI2 phosphatase. . PNAS 109:(36):1469398
    [Crossref] [Google Scholar]
  153. 153.
    Yu H, Ruan H, Xia X, Chicowski AS, Whitham SA, et al. 2022.. Maize FERONIA-like receptor genes are involved in the response of multiple disease resistance in maize. . Mol. Plant Pathol. 23:(9):133145
    [Crossref] [Google Scholar]
  154. 154.
    Yu Y, Chakravorty D, Assmann SM. 2018.. The G protein β-subunit, AGB1, interacts with FERONIA in RALF1-regulated stomatal movement. . Plant Physiol. 176:(3):242640
    [Crossref] [Google Scholar]
  155. 155.
    Yuan M, Jiang Z, Bi G, Nomura K, Liu M, et al. 2021.. Pattern-recognition receptors are required for NLR-mediated plant immunity. . Nature 592:(7852):1059
    [Crossref] [Google Scholar]
  156. 156.
    Yuan M, Ngou BPM, Ding P, Xin X-F. 2021.. PTI-ETI crosstalk: an integrative view of plant immunity. . Curr. Opin. Plant Biol. 62::102030
    [Crossref] [Google Scholar]
  157. 157.
    Zhang L, Huang J, Su S, Wei X, Yang L, et al. 2021.. FERONIA receptor kinase-regulated reactive oxygen species mediate self-incompatibility in Brassica rapa. . Curr. Biol. 31:(14):300416.e4 157. Describes a FER-controlled stigmatic gate in self-incompatible Brassica.
    [Crossref] [Google Scholar]
  158. 158.
    Zhang X, Peng H, Zhu S, Xing J, Li X, et al. 2020.. Nematode-encoded RALF peptide mimics facilitate parasitism of plants through the FERONIA receptor kinase. . Mol. Plant 13:(10):143454
    [Crossref] [Google Scholar]
  159. 159.
    Zhang X, Yang Z, Wu D, Yu F. 2020.. RALF-FERONIA signaling: linking plant immune response with cell growth. . Plant Commun. 1:(4):100084
    [Crossref] [Google Scholar]
  160. 160.
    Zhao C, Jiang W, Zayed O, Liu X, Tang K, et al. 2021.. The LRXs-RALFs-FER module controls plant growth and salt stress responses by modulating multiple plant hormones. . Natl. Sci. Rev. 8:(1):nwaa149
    [Crossref] [Google Scholar]
  161. 161.
    Zhao C, Zayed O, Yu Z, Jiang W, Zhu P, et al. 2018.. Leucine-rich repeat extensin proteins regulate plant salt tolerance in Arabidopsis. . PNAS 115:(51):1312328 161. Links LRX, RALF, and FER signaling to salt tolerance.
    [Crossref] [Google Scholar]
  162. 162.
    Zhong S, Li L, Wang Z, Ge Z, Li Q, et al. 2022.. RALF peptide signaling controls the polytubey block in Arabidopsis. . Science 375:(6578):29096
    [Crossref] [Google Scholar]
  163. 163.
    Zhou X, Lu J, Zhang Y, Guo J, Lin W, et al. 2021.. Membrane receptor-mediated mechano-transduction maintains cell integrity during pollen tube growth within the pistil. . Dev. Cell 56:(7):103042.e6
    [Crossref] [Google Scholar]
  164. 164.
    Zurzolo C, Simons K. 2016.. Glycosylphosphatidylinositol-anchored proteins: membrane organization and transport. . Biochim. Biophys. Acta Biomembr. 1858:(4):63239
    [Crossref] [Google Scholar]
/content/journals/10.1146/annurev-arplant-102820-103424
Loading
/content/journals/10.1146/annurev-arplant-102820-103424
Loading

Data & Media loading...

  • Article Type: Review Article
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error