Skip to main content

Thank you for visiting nature.com. You are using a browser version with limited support for CSS. To obtain the best experience, we recommend you use a more up to date browser (or turn off compatibility mode in Internet Explorer). In the meantime, to ensure continued support, we are displaying the site without styles and JavaScript.

  • Perspective
  • Published:

Malectin-like receptor kinases as protector deities in plant immunity

Abstract

Plant malectin-like receptor kinases (MLRs), also known as Catharanthus roseus receptor-like kinase-1-like proteins, are well known for their functions in pollen tube reception and tip growth, cell wall integrity sensing, and hormonal responses. Recently, mounting evidence has indicated a critical role for MLRs in plant immunity. Here we focus on the emerging functions of MLRs in modulating the two-tiered immune system mediated by cell-surface-resident pattern recognition receptors (PRRs) and intracellular nucleotide-binding leucine-rich repeat receptors (NLRs). MLRs complex with PRRs and NLRs and regulate immune receptor complex formation and stability. Rapid alkalinization factor peptide ligands, LORELEI-like glycosylphosphatidylinositol-anchored proteins and cell-wall-associated leucine-rich repeat extensins coordinate with MLRs to orchestrate PRR- and NLR-mediated immunity. We discuss the common theme and unique features of MLR complexes concatenating different branches of plant immune signalling.

This is a preview of subscription content, access via your institution

Access options

Buy this article

Prices may be subject to local taxes which are calculated during checkout

Fig. 1: The MLR–LLG–RALF–LRX module regulates plant immunity.
Fig. 2: Arabidopsis MLRs regulate different aspects of plant immunity.
Fig. 3: Multiple functions of Arabidopsis MLRs in PRR- and NLR-mediated immunity, hormone signalling and CWI sensing, culminating in a balanced growth–defence trade-off.
Fig. 4: Pathogen RALF peptides mimic host RALFs and modulate FER-mediated responses during infections.

Similar content being viewed by others

References

  1. Jones, J. D. & Dangl, J. L. The plant immune system. Nature 444, 323–329 (2006).

    Article  CAS  Google Scholar 

  2. Zhou, J. M. & Zhang, Y. Plant immunity: danger perception and signaling. Cell 181, 978–989 (2020).

    Article  CAS  PubMed  Google Scholar 

  3. Couto, D. & Zipfel, C. Regulation of pattern recognition receptor signalling in plants. Nat. Rev. Immunol. 16, 537–552 (2016).

    Article  CAS  PubMed  Google Scholar 

  4. Yu, X., Feng, B. M., He, P. & Shan, L. B. From chaos to harmony: responses and signaling upon microbial pattern recognition. Annu. Rev. Phytopathol. 55, 109–137 (2017).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  5. Gust, A. A., Pruitt, R. & Nurnberger, T. Sensing danger: key to activating plant immunity. Trends Plant Sci. 22, 779–791 (2017).

    Article  CAS  PubMed  Google Scholar 

  6. Dou, D. & Zhou, J. M. Phytopathogen effectors subverting host immunity: different foes, similar battleground. Cell Host Microbe 12, 484–495 (2012).

    Article  CAS  PubMed  Google Scholar 

  7. Cui, H. T., Tsuda, K. & Parker, J. E. Effector-triggered immunity: from pathogen perception to robust defense. Annu. Rev. Plant Biol. 66, 487–511 (2015).

    Article  CAS  PubMed  Google Scholar 

  8. Lolle, S., Stevens, D. & Coaker, G. Plant NLR-triggered immunity: from receptor activation to downstream signaling. Curr. Opin. Immunol. 62, 99–105 (2020).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  9. Tsuda, K. & Katagiri, F. Comparing signaling mechanisms engaged in pattern-triggered and effector-triggered immunity. Curr. Opin. Plant Biol. 13, 459–465 (2010).

    Article  CAS  PubMed  Google Scholar 

  10. Thomma, B. P. H. J., Nurnberger, T. & Joosten, M. H. A. J. Of PAMPs and effectors: the blurred PTI–ETI dichotomy. Plant Cell 23, 4–15 (2011).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  11. Ngou, B. P. M., Ahn, H. K., Ding, P. & Jones, J. D. G. Mutual potentiation of plant immunity by cell-surface and intracellular receptors. Nature 592, 110–115 (2021).

    Article  CAS  PubMed  Google Scholar 

  12. Yuan, M. et al. Pattern-recognition receptors are required for NLR-mediated plant immunity. Nature 592, 105–109 (2021).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  13. Peng, Y., van Wersch, R. & Zhang, Y. Convergent and divergent signaling in PAMP-triggered immunity and effector-triggered immunity. Mol. Plant Microbe Interact. 31, 403–409 (2018).

    Article  CAS  PubMed  Google Scholar 

  14. Dievart, A., Gottin, C., Perin, C., Ranwez, V. & Chantret, N. Origin and diversity of plant receptor-like kinases. Annu. Rev. Plant Biol. 71, 131–156 (2020).

    Article  CAS  PubMed  Google Scholar 

  15. de Azevedo Manhães, A. M. E., Ortiz-Morea, F. A., He, P. & Shan, L. Plant plasma membrane-resident receptors: surveillance for infections and coordination for growth and development. J. Integr. Plant Biol. 63, 79–101 (2020).

    Article  Google Scholar 

  16. Westermann, J. et al. An evolutionarily conserved receptor-like kinases signaling module controls cell wall integrity during tip growth. Curr. Biol. 29, 4153 (2019).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  17. Schulze-Muth, P., Irmler, S., Schroder, G. & Schroder, J. 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, 26684–26689 (1996).

    Article  CAS  PubMed  Google Scholar 

  18. Nissen, K. S., Willats, W. G. & Malinovsky, F. G. Understanding CrRLK1L function: cell walls and growth control. Trends Plant Sci. 21, 516–527 (2016).

    Article  CAS  PubMed  Google Scholar 

  19. Li, C., Wu, H. M. & Cheung, A. Y. FERONIA and her pals: functions and mechanisms. Plant Physiol. 171, 2379–2392 (2016).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  20. Lindner, H., Muller, L. M., Boisson-Dernier, A. & Grossniklaus, U. CrRLK1L receptor-like kinases: not just another brick in the wall. Curr. Opin. Plant Biol. 15, 659–669 (2012).

    Article  CAS  PubMed  Google Scholar 

  21. Franck, C. M., Westermann, J. & Boisson-Dernier, A. Plant malectin-like receptor kinases: from cell wall integrity to immunity and beyond. Annu. Rev. Plant Biol. 69, 301–328 (2018).

    Article  CAS  PubMed  Google Scholar 

  22. Yang, H. et al. Malectin/malectin-like domain-containing proteins: a repertoire of cell surface molecules with broad functional potential. Cell Surf. 7, 100056 (2021).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  23. Escobar-Restrepo, J. M. et al. The FERONIA receptor-like kinase mediates male–female interactions during pollen tube reception. Science 317, 656–660 (2007).

    Article  CAS  PubMed  Google Scholar 

  24. Duan, Q., Kita, D., Li, C., Cheung, A. Y. & Wu, H. M. FERONIA receptor-like kinase regulates RHO GTPase signaling of root hair development. Proc. Natl Acad. Sci. USA 107, 17821–17826 (2010).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  25. Chen, J. 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. USA 113, E5519–E5527 (2016).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  26. Boisson-Dernier, A. et al. Disruption of the pollen-expressed FERONIA homologs ANXUR1 and ANXUR2 triggers pollen tube discharge. Development 136, 3279–3288 (2009).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  27. Miyazaki, S. et al. ANXUR1 and 2, sister genes to FERONIA/SIRENE, are male factors for coordinated fertilization. Curr. Biol. 19, 1327–1331 (2009).

    Article  CAS  PubMed  Google Scholar 

  28. Boisson-Dernier, A. et al. ANXUR receptor-like kinases coordinate cell wall integrity with growth at the pollen tube tip via NADPH oxidases. PLoS Biol. 11, e1001719 (2013).

    Article  PubMed  PubMed Central  Google Scholar 

  29. Ge, Z. et al. Arabidopsis pollen tube integrity and sperm release are regulated by RALF-mediated signaling. Science 358, 1596–1600 (2017).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  30. Zhu, L. et al. The Arabidopsis CrRLK1L protein kinases BUPS1 and BUPS2 are required for normal growth of pollen tubes in the pistil. Plant J. 95, 474–486 (2018).

    Article  CAS  PubMed  Google Scholar 

  31. Zhou, X. et al. Membrane receptor-mediated mechano-transduction maintains cell integrity during pollen tube growth within the pistil. Dev. Cell 56, 1030–1042 (2021).

    Article  CAS  PubMed  Google Scholar 

  32. Blackburn, M. R., Haruta, M. & Moura, D. S. Twenty years of progress in physiological and biochemical investigation of RALF peptides. Plant Physiol. 182, 1657–1666 (2020).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  33. Kessler, S. A. et al. Conserved molecular components for pollen tube reception and fungal invasion. Science 330, 968–971 (2010).

    Article  CAS  PubMed  Google Scholar 

  34. Stegmann, M. et al. The receptor kinase FER is a RALF-regulated scaffold controlling plant immune signaling. Science 355, 287–289 (2017).

    Article  CAS  PubMed  Google Scholar 

  35. Gronnier, J. et al. Regulation of immune receptor kinases plasma membrane nanoscale landscape by a plant peptide hormone and its receptors. Preprint at bioRxiv https://doi.org/10.1101/2020.07.20.212233 (2020).

  36. Mang, H. et al. Differential regulation of two-tiered plant immunity and sexual reproduction by ANXUR receptor-like kinases. Plant Cell 29, 3140–3156 (2017).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  37. Duan, Q. H. et al. FERONIA controls pectin- and nitric oxide-mediated male–female interaction. Nature 579, 561–566 (2020).

    Article  CAS  PubMed  Google Scholar 

  38. Ngo, Q. A., Vogler, H., Lituiev, D. S., Nestorova, A. & Grossniklaus, U. A calcium dialog mediated by the FERONIA signal transduction pathway controls plant sperm delivery. Dev. Cell 29, 491–500 (2014).

    Article  CAS  PubMed  Google Scholar 

  39. Zou, Y. et al. Transcriptional regulation of the immune receptor FLS2 controls the ontogeny of plant innate immunity. Plant Cell 30, 2779–2794 (2018).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  40. Wang, D. M. et al. A malectin-like receptor kinase regulates cell death and pattern-triggered immunity in soybean. EMBO Rep. 21, e50442 (2020).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  41. Yang, Z. et al. Mutations of two FERONIA-like receptor genes enhance rice blast resistance without growth penalty. J. Exp. Bot. 71, 2112–2126 (2020).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  42. Huang, Y. Y. et al. Identification of FERONIA-like receptor genes involved in rice–Magnaporthe oryzae interaction. Phytopathology 2, 1–10 (2020).

    Google Scholar 

  43. Feng, H. Q. 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 12, 1612–1623 (2019).

    Article  CAS  PubMed  Google Scholar 

  44. Ge, Z. et al. LLG2/3 are co-receptors in BUPS/ANX-RALF signaling to regulate Arabidopsis pollen tube integrity. Curr. Biol. 29, 3526–3265 (2019).

    Article  Google Scholar 

  45. Li, C. et al. Glycosylphosphatidylinositol-anchored proteins as chaperones and co-receptors for FERONIA receptor kinase signaling in Arabidopsis. eLife 4, e06587 (2015).

    Article  PubMed Central  Google Scholar 

  46. Huang, Y. et al. A trimeric CrRLK1L–LLG1 complex genetically modulates SUMM2-mediated autoimmunity. Nat. Commun. 11, 4859 (2020).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  47. Xiao, Y. et al. Mechanisms of RALF peptide perception by a heterotypic receptor complex. Nature 572, 270–274 (2019).

    Article  CAS  PubMed  Google Scholar 

  48. Shen, Q., Bourdais, G., Pan, H., Robatzek, S. & Tang, D. Glycosylphosphatidylinositol-anchored protein LLG1 associates with and modulates FLS2 to regulate innate immunity. Proc. Natl Acad. Sci. USA 114, 5749–5754 (2017).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  49. Guo, H. et al. FERONIA receptor kinase contributes to plant immunity by suppressing jasmonic acid signaling in Arabidopsis thaliana. Curr. Biol. 28, 3316–3324 (2018).

    Article  CAS  PubMed  Google Scholar 

  50. Liang, X. & Zhou, J. M. Receptor-like cytoplasmic kinases: central players in plant receptor kinase-mediated signaling. Annu. Rev. Plant Biol. 69, 267–299 (2018).

    Article  CAS  PubMed  Google Scholar 

  51. Liu, C. et al. Pollen PCP-B peptides unlock a stigma peptide–receptor kinase gating mechanism for pollination. Science 372, 171–175 (2021).

    Article  CAS  PubMed  Google Scholar 

  52. Cheng, Y. T. et al. Stability of plant immune-receptor resistance proteins is controlled by SKP1-CULLIN1-F-box (SCF)-mediated protein degradation. Proc. Natl Acad. Sci. USA 108, 14694–14699 (2011).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  53. Gou, M. et al. The F-box protein CPR1/CPR30 negatively regulates R protein SNC1 accumulation. Plant J. 69, 411–420 (2012).

    Article  CAS  PubMed  Google Scholar 

  54. Wu, Z. et al. Plant E3 ligases SNIPER1 and SNIPER2 broadly regulate the homeostasis of sensor NLR immune receptors. EMBO J. 39, e104915 (2020).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  55. Chung, E. H. et al. Specific threonine phosphorylation of a host target by two unrelated type III effectors activates a host innate immune receptor in plants. Cell Host Microbe 9, 125–136 (2011).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  56. Liu, J., Elmore, J. M., Lin, Z. J. D. & Coaker, G. A receptor-like cytoplasmic kinase phosphorylates the host target RIN4, leading to the activation of a plant innate immune receptor. Cell Host Microbe 9, 137–146 (2011).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  57. Chung, E. H., El-Kasmi, F., He, Y. J., Loehr, A. & Dangl, J. L. A plant phosphoswitch platform repeatedly targeted by type III effector proteins regulates the output of both tiers of plant immune receptors. Cell Host Microbe 16, 484–494 (2014).

    Article  CAS  PubMed  Google Scholar 

  58. Du, C. Q. et al. Receptor kinase complex transmits RALF peptide signal to inhibit root growth in Arabidopsis. Proc. Natl Acad. Sci. USA 113, E8326–E8334 (2016).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  59. Liu, J. et al. The malectin-like receptor-like kinase LETUM1 modulates NLR protein SUMM2 activation via MEKK2 scaffolding. Nat. Plants 6, 1106–1115 (2020).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  60. Liu, Y. et al. Receptor-like kinases MDS1 and MDS2 promote SUMM2-mediated immunity. J. Integr. Plant Biol. 63, 277–282 (2020).

    Article  PubMed  Google Scholar 

  61. Bi, G. & Zhou, J. M. MAP kinase signaling pathways: a hub of plant–microbe interactions. Cell Host Microbe 21, 270–273 (2017).

    Article  CAS  PubMed  Google Scholar 

  62. Devendrakumar, K. T., Li, X. & Zhang, Y. L. MAP kinase signalling: interplays between plant PAMP- and effector-triggered immunity. Cell. Mol. Life Sci. 75, 2981–2989 (2018).

    Article  Google Scholar 

  63. Asai, T. et al. MAP kinase signalling cascade in Arabidopsis innate immunity. Nature 415, 977–983 (2002).

    Article  CAS  PubMed  Google Scholar 

  64. Petersen, M. et al. Arabidopsis MAP kinase 4 negatively regulates systemic acquired resistance. Cell 103, 1111–1120 (2000).

    Article  CAS  PubMed  Google Scholar 

  65. Ichimura, K., Casais, C., Peck, S. C., Shinozaki, K. & Shirasu, K. MEKK1 is required for MPK4 activation and regulates tissue-specific and temperature-dependent cell death in Arabidopsis. J. Biol. Chem. 281, 36969–36976 (2006).

    Article  CAS  PubMed  Google Scholar 

  66. Suarez-Rodriguez, M. C. et al. MEKK1 is required for flg22-induced MPK4 activation in Arabidopsis plants. Plant Physiol. 143, 661–669 (2007).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  67. Gao, M. et al. MEKK1, MKK1/MKK2 and MPK4 function together in a mitogen-activated protein kinase cascade to regulate innate immunity in plants. Cell Res. 18, 1190–1198 (2008).

    Article  CAS  PubMed  Google Scholar 

  68. Zhang, Z. et al. Disruption of PAMP-induced MAP kinase cascade by a Pseudomonas syringae effector activates plant immunity mediated by the NB-LRR protein SUMM2. Cell Host Microbe 11, 253–263 (2012).

    Article  CAS  PubMed  Google Scholar 

  69. Takagi, M. et al. Disruption of the MAMP-induced MEKK1–MKK1/MKK2–MPK4 pathway activates the TNL immune receptor SMN1/RPS6. Plant Cell Physiol. 60, 778–787 (2019).

    Article  CAS  PubMed  Google Scholar 

  70. Yang, Y. et al. RNAi-based screen reveals concerted functions of MEKK2 and CRCK3 in plant cell death regulation. Plant Physiol. 183, 331–344 (2020).

    Article  PubMed  PubMed Central  Google Scholar 

  71. Galindo-Trigo, S. et al. CrRLK1L receptor-like kinases HERK1 and ANJEA are female determinants of pollen tube reception. EMBO Rep. 21, e48466 (2020).

    Article  CAS  PubMed  Google Scholar 

  72. Kong, Q. et al. The MEKK1–MKK1/MKK2–MPK4 kinase cascade negatively regulates immunity mediated by a mitogen-activated protein kinase kinase kinase in Arabidopsis. Plant Cell 24, 2225–2236 (2012).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  73. Su, S. H. et al. Deletion of a tandem gene family in Arabidopsis: increased MEKK2 abundance triggers autoimmunity when the MEKK1–MKK1/2–MPK4 signaling cascade is disrupted. Plant Cell 25, 1895–1910 (2013).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  74. Zhang, Z. et al. The NLR protein SUMM2 senses the disruption of an immune signaling MAP kinase cascade via CRCK3. EMBO Rep. 18, 292–302 (2017).

    Article  CAS  PubMed  Google Scholar 

  75. Nitta, Y. et al. MEKK2 inhibits activation of MAP kinases in Arabidopsis. Plant J. 103, 705–714 (2020).

    Article  CAS  PubMed  Google Scholar 

  76. Wang, J. et al. Reconstitution and structure of a plant NLR resistosome conferring immunity. Science 364, aav5870 (2019).

    Article  Google Scholar 

  77. Wang, J. et al. Ligand-triggered allosteric ADP release primes a plant NLR complex. Science 364, eaav5868 (2019).

    Article  CAS  PubMed  Google Scholar 

  78. Wan, W. L., Kim, S. T., Castel, B., Charoennit, N. & Chae, E. Genetics of autoimmunity in plants: an evolutionary genetics perspective. N. Phytol. 3, 1215–1233 (2020).

    Google Scholar 

  79. Bürger, M. & Chory, J. Stressed out about hormones: how plants orchestrate immunity. Cell Host Microbe 26, 163–172 (2019).

    Article  PubMed  PubMed Central  Google Scholar 

  80. Robert-Seilaniantz, A., Grant, M. & Jones, J. D. G. Hormone crosstalk in plant disease and defense: more than just JASMONATE–SALICYLATE antagonism. Annu. Rev. Phytopathol. 49, 317–343 (2011).

    Article  CAS  PubMed  Google Scholar 

  81. Guo, H. et al. Three related receptor-like kinases are required for optimal cell elongation in Arabidopsis thaliana. Proc. Natl Acad. Sci. USA 106, 7648–7653 (2009).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  82. Deslauriers, S. D. & Larsen, P. B. FERONIA is a key modulator of brassinosteroid and ethylene responsiveness in Arabidopsis hypocotyls. Mol. Plant 3, 626–640 (2010).

    Article  CAS  PubMed  Google Scholar 

  83. Liao, H., Tang, R., Zhang, X., Luan, S. & Yu, F. FERONIA receptor kinase at the crossroads of hormone signaling and stress responses. Plant Cell Physiol. 58, 1143–1150 (2017).

    Article  CAS  PubMed  Google Scholar 

  84. Zheng, X. Y. et al. Coronatine promotes Pseudomonas syringae virulence in plants by activating a signaling cascade that inhibits salicylic acid accumulation. Cell Host Microbe 11, 587–596 (2012).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  85. Chico, J. M. et al. CUL3(BPM) E3 ubiquitin ligases regulate MYC2, MYC3, and MYC4 stability and JA responses. Proc. Natl Acad. Sci. USA 117, 6205–6215 (2020).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  86. Song, Y. et al. FERONIA restricts Pseudomonas in the rhizosphere microbiome via regulation of reactive oxygen species. Nat. Plants 7, 644–654 (2021).

    Article  CAS  PubMed  Google Scholar 

  87. Qu, S., Zhang, X., Song, Y., Lin, J. & Shan, X. THESEUS1 positively modulates plant defense responses against Botrytis cinerea through GUANINE EXCHANGE FACTOR4 signaling. J. Integr. Plant Biol. 59, 797–804 (2017).

    Article  CAS  PubMed  Google Scholar 

  88. Fujikura, U. et al. Atkinesin-13A modulates cell-wall synthesis and cell expansion in Arabidopsis thaliana via the THESEUS1 pathway. PLoS Genet. 10, e1004627 (2014).

    Article  PubMed  PubMed Central  Google Scholar 

  89. Ronald, P. & Joe, A. Molecular mimicry modulates plant host responses to pathogens. Ann. Bot. 121, 17–23 (2018).

    Article  CAS  PubMed  Google Scholar 

  90. Masachis, S. et al. A fungal pathogen secretes plant alkalinizing peptides to increase infection. Nat. Microbiol. 1, 16043 (2016).

    Article  CAS  PubMed  Google Scholar 

  91. Thynne, E. et al. Fungal phytopathogens encode functional homologues of plant rapid alkalinization factor (RALF) peptides. Mol. Plant Pathol. 18, 811–824 (2017).

    Article  CAS  PubMed  Google Scholar 

  92. Wood, A. K. M., Walker, C., Lee, W. S., Urban, M. & Hammond-Kosack, K. E. Functional evaluation of a homologue of plant rapid alkalinisation factor (RALF) peptides in Fusarium graminearum. Fungal Biol. 124, 753–765 (2020).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  93. Zhang, X. et al. Nematode-encoded RALF peptide mimics facilitate parasitism of plants through the FERONIA receptor kinase. Mol. Plant 13, 1434–1454 (2020).

    Article  CAS  PubMed  Google Scholar 

  94. Haruta, M., Sabat, G., Stecker, K., Minkoff, B. B. & Sussman, M. R. A peptide hormone and its receptor protein kinase regulate plant cell expansion. Science 343, 408–411 (2014).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  95. Gonneau, M. et al. Receptor kinase THESEUS1 is a Rapid Alkalinization Factor 34 receptor in Arabidopsis. Curr. Biol. 28, 2452–2458 (2018).

    Article  CAS  PubMed  Google Scholar 

  96. Kessler, S. A., Lindner, H., Jones, D. S. & Grossniklaus, U. Functional analysis of related Cr RLK 1L receptor‐like kinases in pollen tube reception. EMBO Rep. 16, 107–115 (2015).

    Article  CAS  PubMed  Google Scholar 

  97. Lee, J. S. et al. Competitive binding of antagonistic peptides fine-tunes stomatal patterning. Nature 522, 439–443 (2015).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  98. Moussu, S. et al. Structural basis for recognition of RALF peptides by LRX proteins during pollen tube growth. Proc. Natl Acad. Sci. USA 117, 7494–7503 (2020).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  99. Mecchia, M. A. et al. RALF4/19 peptides interact with LRX proteins to control pollen tube growth in Arabidopsis. Science 358, 1600–1603 (2017).

    Article  CAS  PubMed  Google Scholar 

  100. Zhao, C. et al. Leucine-rich repeat extensin proteins regulate plant salt tolerance in Arabidopsis. Proc. Natl Acad. Sci. USA 115, 13123–13128 (2018).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  101. Dünser, K. et al. Extracellular matrix sensing by FERONIA and leucine‐rich repeat extensins controls vacuolar expansion during cellular elongation in Arabidopsis thaliana. EMBO J. 38, e100353 (2019).

    Article  PubMed  PubMed Central  Google Scholar 

  102. Herger, A. et al. Overlapping functions and protein–protein interactions of LRR-extensins in Arabidopsis. PLoS Genet. 16, e1008847 (2020).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  103. Tsukamoto, T., Qin, Y., Huang, Y., Dunatunga, D. & Palanivelu, R. A role for LORELEI, a putative glycosylphosphatidylinositol-anchored protein, in Arabidopsis thaliana double fertilization and early seed development. Plant J. 62, 571–588 (2010).

    Article  CAS  PubMed  Google Scholar 

  104. Bucherl, C. A. et al. Plant immune and growth receptors share common signalling components but localise to distinct plasma membrane nanodomains. eLife 6, 25114 (2017).

    Article  Google Scholar 

  105. Jaillais, Y. & Ott, T. The nanoscale organization of the plasma membrane and its importance in signaling: a proteolipid perspective. Plant Physiol. 182, 1682–1696 (2020).

    Article  CAS  PubMed  Google Scholar 

  106. Cuevas-Velazquez, C. L. & Dinneny, J. R. Organization out of disorder: liquid–liquid phase separation in plants. Curr. Opin. Plant Biol. 45, 68–74 (2018).

    Article  CAS  PubMed  Google Scholar 

  107. Emenecker, R. J., Holehouse, A. S. & Strader, L. C. Emerging roles for phase separation in plants. Dev. Cell 55, 69–83 (2020).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  108. Zhou, J. et al. Proteolytic processing of SERK3/BAK1 regulates plant immunity, development, and cell death. Plant Physiol. 180, 543–558 (2019).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  109. Wang, L. et al. RALF1–FERONIA complex affects splicing dynamics to modulate stress responses and growth in plants. Sci. Adv. 6, eaaz1622 (2020).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  110. Nicaise, V. et al. Pseudomonas HopU1 modulates plant immune receptor levels by blocking the interaction of their mRNAs with GRP7. EMBO J. 32, 701–712 (2013).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  111. Vaahtera, L., Schulz, J. & Hamann, T. Cell wall integrity maintenance during plant development and interaction with the environment. Nat. Plants 5, 924–932 (2019).

    Article  PubMed  Google Scholar 

  112. Engelsdorf, T. et al. The plant cell wall integrity maintenance and immune signaling systems cooperate to control stress responses in Arabidopsis thaliana. Sci. Signal. 11, 536 (2018).

    Article  Google Scholar 

  113. Hématy, K. et al. A receptor-like kinase mediates the response of Arabidopsis cells to the inhibition of cellulose synthesis. Curr. Biol. 17, 922–931 (2007).

    Article  PubMed  Google Scholar 

  114. Bartels, S. et al. The family of Peps and their precursors in Arabidopsis: differential expression and localization but similar induction of pattern-triggered immune responses. J. Exp. Bot. 64, 5309–5321 (2013).

    Article  CAS  PubMed  Google Scholar 

  115. Feng, W. et al. The FERONIA receptor kinase maintains cell-wall integrity during salt stress through Ca2+ signaling. Curr. Biol. 28, 666–675 (2018).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  116. Ortiz-Morea, F. A., He, P., Shan, L. & Russinova, E. It takes two to tango—molecular links between plant immunity and brassinosteroid signalling. J. Cell Sci. 133, 246728 (2020).

    Article  Google Scholar 

  117. Huot, B., Yao, J., Montgomery, B. L. & He, S. Y. Growth–defense tradeoffs in plants: a balancing act to optimize fitness. Mol. Plant 7, 1267–1287 (2014).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  118. Kim, E.-J. & Russinova, E. Brassinosteroid signalling. Curr. Biol. 30, R294–R298 (2020).

    Article  CAS  PubMed  Google Scholar 

  119. Schoenaers, S. et al. The auxin-regulated CrRLK1L kinase ERULUS controls cell wall composition during root hair tip growth. Curr. Biol. 28, 722–732 (2018).

    Article  CAS  PubMed  Google Scholar 

  120. Barbez, E., Dunser, K., Gaidora, A., Lendl, T. & Busch, W. Auxin steers root cell expansion via apoplastic pH regulation in Arabidopsis thaliana. Proc. Natl Acad. Sci. USA 114, E4884–E4893 (2017).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  121. McLaughlin, H. M., Ang, A. C. H. & Østergaard, L. Noncanonical auxin signaling. Cold Spring Harb. Perspect. Biol. 13, 039917 (2021).

    Article  Google Scholar 

  122. Haruta, M., Gaddameedi, V., Burch, H., Fernandez, D. & Sussman, M. R. Comparison of the effects of a kinase‐dead mutation of FERONIA on ovule fertilization and root growth of Arabidopsis. FEBS Lett. 592, 2395–2402 (2018).

    Article  CAS  PubMed  Google Scholar 

  123. Chakravorty, D., Yu, Y. & Assmann, S. M. A kinase‐dead version of FERONIA receptor‐like kinase has dose‐dependent impacts on rosette morphology and RALF 1‐mediated stomatal movements. FEBS Lett. 592, 3429–3437 (2018).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  124. Smakowska-Luzan, E. et al. An extracellular network of Arabidopsis leucine-rich repeat receptor kinases. Nature 553, 342–346 (2018).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  125. Rich-Griffin, C. et al. Regulation of cell type-specific immunity networks in Arabidopsis roots. Plant Cell 32, 2742–2762 (2020).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  126. Kadota, Y. et al. Quantitative phosphoproteomic analysis reveals common regulatory mechanisms between effector- and PAMP-triggered immunity in plants. N. Phytol. 221, 2160–2175 (2019).

    Article  CAS  Google Scholar 

  127. Ma, X. et al. Ligand-induced monoubiquitination of BIK1 regulates plant immunity. Nature 581, 199–203 (2020).

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

We apologize to those whose work is not cited due to space limitations. This research was supported by grants from the National Institutes of Health (NIH) (no. R01GM092893) to P.H., the NIH (no. R01GM097247) to L.S. and the PEW Latin American Fellows Program to F.A.O.-M.

Author information

Authors and Affiliations

Authors

Contributions

F.A.O.-M., J.L., L.S. and P.H. contributed equally to the concept, outline and writing of the manuscript. F.A.O.-M. and J.L. generated the figures.

Corresponding author

Correspondence to Ping He.

Ethics declarations

Competing interests

The authors declare no competing interests.

Additional information

Peer review information Nature Plants thanks Hongqing Guo, Ralph Huckelhoven, Christoph Ringli and the other, anonymous, reviewer(s) for their contribution to the peer review of this work.

Publisher’s note Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Ortiz-Morea, F.A., Liu, J., Shan, L. et al. Malectin-like receptor kinases as protector deities in plant immunity. Nat. Plants 8, 27–37 (2022). https://doi.org/10.1038/s41477-021-01028-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1038/s41477-021-01028-3

This article is cited by

Search

Quick links

Nature Briefing

Sign up for the Nature Briefing newsletter — what matters in science, free to your inbox daily.

Get the most important science stories of the day, free in your inbox. Sign up for Nature Briefing