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A receptor–channel trio conducts Ca2+ signalling for pollen tube reception

Abstract

Precise signalling between pollen tubes and synergid cells in the ovule initiates fertilization in flowering plants1. Contact of the pollen tube with the ovule triggers calcium spiking in the synergids2,3 that induces pollen tube rupture and sperm release. This process, termed pollen tube reception, entails the action of three synergid-expressed proteins in Arabidopsis: FERONIA (FER), a receptor-like kinase; LORELEI (LRE), a glycosylphosphatidylinositol-anchored protein; and NORTIA (NTA), a transmembrane protein of unknown function4,5,6. Genetic analyses have placed these three proteins in the same pathway; however, it remains unknown how they work together to enable synergid–pollen tube communication. Here we identify two pollen-tube-derived small peptides7 that belong to the rapid alkalinization factor (RALF) family8 as ligands for the FER–LRE co-receptor, which in turn recruits NTA to the plasma membrane. NTA functions as a calmodulin-gated calcium channel required for calcium spiking in the synergid. We also reconstitute the biochemical pathway in which FER–LRE perceives pollen-tube-derived peptides to activate the NTA calcium channel and initiate calcium spiking, a second messenger for pollen tube reception. The FER–LRE–NTA trio therefore forms a previously unanticipated receptor–channel complex in the female cell to recognize male signals and trigger the fertilization process.

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Fig. 1: Pollen-derived RALFs bind to FER–LRE and trigger synergid [Ca2+]cyt changes in a FER–LRE–NTA-dependent manner.
Fig. 2: MLO family proteins, including NTA, are Ca2+-permeable channels.
Fig. 3: RALFs enhance the Ca2+ channel activity of the FER–LRE–NTA trio.
Fig. 4: CaM inhibition of NTA Ca2+ channels is involved in modelling the Ca2+ spiking pattern in synergids.

Data availability

The data supporting the findings of this study are available within the paper and its Supplementary Information files. Source data are provided with this paper.

References

  1. Johnson, M. A., Harper, J. F. & Palanivelu, R. A fruitful journey: pollen tube navigation from germination to fertilization. Annu. Rev. Plant. Biol. 70, 809–837 (2019).

    CAS  PubMed  Article  Google Scholar 

  2. Denninger, P. et al. Male–female communication triggers calcium signatures during fertilization in Arabidopsis. Nat. Commun. 5, 4645 (2014).

    ADS  CAS  PubMed  Article  Google Scholar 

  3. 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).

    CAS  PubMed  Article  Google Scholar 

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

    ADS  CAS  PubMed  Article  Google Scholar 

  5. Liu, X. 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 28, 1035–1052 (2016).

    ADS  CAS  PubMed  PubMed Central  Article  Google Scholar 

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

    ADS  CAS  PubMed  Article  Google Scholar 

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

    ADS  CAS  PubMed  PubMed Central  Article  Google Scholar 

  8. 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).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  9. Clapham, D. E. Calcium signaling. Cell 131, 1047–1058 (2007).

    CAS  PubMed  Article  Google Scholar 

  10. Trewavas, A. Le calcium, c’est la vie: calcium makes waves. Plant Physiol. 120, 1–6 (1999).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  11. Luan, S. & Wang, C. Calcium signaling mechanisms across kingdoms. Annu. Rev. Cell Dev. Biol. 37, 311–340 (2021).

    CAS  PubMed  Article  Google Scholar 

  12. Hwang, J. Y. et al. Dual sensing of physiologic pH and calcium by EFCAB9 regulates sperm motility. Cell 177, 1480–1494.e19 (2019).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  13. Whitaker, M. Calcium at fertilization and in early development. Physiol. Rev. 86, 25–88 (2006).

    MathSciNet  CAS  PubMed  Article  Google Scholar 

  14. Chen, J., Gutjahr, C., Bleckmann, A. & Dresselhaus, T. Calcium signaling during reproduction and biotrophic fungal interactions in plants. Mol. Plant 8, 595–611 (2015).

    CAS  PubMed  Article  Google Scholar 

  15. Hamamura, Y. et al. Live imaging of calcium spikes during double fertilization in Arabidopsis. Nat. Commun. 5, 4722 (2014).

    ADS  CAS  PubMed  Article  Google Scholar 

  16. Iwano, M. et al. Cytoplasmic Ca2+ changes dynamically during the interaction of the pollen tube with synergid cells. Development 139, 4202–4209 (2012).

    CAS  PubMed  Article  Google Scholar 

  17. Ge, Z., Dresselhaus, T. & Qu, L. J. How CrRLK1L receptor complexes perceive RALF signals. Trends Plant. Sci. 24, 978–981 (2019).

    CAS  PubMed  Article  Google Scholar 

  18. 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).

    CAS  PubMed  Article  Google Scholar 

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

    PubMed Central  Article  Google Scholar 

  20. Cheung, A. Y., Qu, L. J., Russinova, E., Zhao, Y. & Zipfel, C. Update on receptors and signaling. Plant Physiol. 182, 1527–1530 (2020).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  21. 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).

    ADS  CAS  PubMed  PubMed Central  Article  Google Scholar 

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

    ADS  CAS  PubMed  Article  Google Scholar 

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

    ADS  CAS  PubMed  Article  Google Scholar 

  24. Ge, Z. et al. LLG2/3 are co-receptors in BUPS/ANX-RALF signaling to regulate Arabidopsis pollen tube integrity. Curr. Biol. 29, 3256–3265.e5 (2019).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

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

    ADS  CAS  PubMed  Article  Google Scholar 

  26. Zhou, X. et al. Membrane receptor-mediated mechano-transduction maintains cell integrity during pollen tube growth within the pistil. Dev. Cell 56, 1030–1042.e6 (2021).

    CAS  PubMed  Article  Google Scholar 

  27. Liu, K. H. et al. Discovery of nitrate–CPK–NLP signalling in central nutrient–growth networks. Nature 545, 311–316 (2017).

    ADS  CAS  PubMed  PubMed Central  Article  Google Scholar 

  28. Kasahara, R. D., Portereiko, M. F., Sandaklie-Nikolova, L., Rabiger, D. S. & Drews, G. N. MYB98 is required for pollen tube guidance and synergid cell differentiation in Arabidopsis. Plant Cell 17, 2981–2992 (2005).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  29. Buschges, R. et al. The barley Mlo gene: a novel control element of plant pathogen resistance. Cell 88, 695–705 (1997).

    CAS  PubMed  Article  Google Scholar 

  30. Devoto, A. et al. Molecular phylogeny and evolution of the plant-specific seven-transmembrane MLO family. J. Mol. Evol. 56, 77–88 (2003).

    ADS  CAS  PubMed  Article  Google Scholar 

  31. Kusch, S., Pesch, L. & Panstruga, R. Comprehensive phylogenetic analysis sheds light on the diversity and origin of the MLO family of integral membrane proteins. Genome Biol. Evol. 8, 878–895 (2016).

    PubMed  PubMed Central  Article  Google Scholar 

  32. Chen, Z. et al. Two seven-transmembrane domain MILDEW RESISTANCE LOCUS O proteins cofunction in Arabidopsis root thigmomorphogenesis. Plant Cell 21, 1972–1991 (2009).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  33. Consonni, C. et al. Conserved requirement for a plant host cell protein in powdery mildew pathogenesis. Nat. Genet. 38, 716–720 (2006).

    CAS  PubMed  Article  Google Scholar 

  34. Meng, J. G. et al. Integration of ovular signals and exocytosis of a Ca2+ channel by MLOs in pollen tube guidance. Nat. Plants 6, 143–153 (2020).

    CAS  PubMed  Article  Google Scholar 

  35. Pan, Y. et al. Dynamic interactions of plant CNGC subunits and calmodulins drive oscillatory Ca2+ channel activities. Dev. Cell 48, 710–725.e5 (2019).

    CAS  PubMed  Article  Google Scholar 

  36. Jones, D. S. et al. MILDEW RESISTANCE LOCUS O function in pollen tube reception is linked to its oligomerization and subcellular distribution. Plant Physiol. 175, 172–185 (2017).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  37. Ju, Y. et al. Polarized NORTIA accumulation in response to pollen tube arrival at synergids promotes fertilization. Dev. Cell 56, 2938–2951.e6 (2021).

    CAS  PubMed  Article  Google Scholar 

  38. Kessler, S. A., Lindner, H., Jones, D. S. & Grossniklaus, U. Functional analysis of related CrRLK1L receptor-like kinases in pollen tube reception. EMBO Rep. 16, 107–115 (2015).

    CAS  PubMed  Article  Google Scholar 

  39. 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).

    CAS  PubMed  Article  Google Scholar 

  40. Zhong, S. et al. RALF peptide signaling controls the polytubey block in Arabidopsis. Science 375, 290–296 (2022).

    ADS  CAS  PubMed  Article  Google Scholar 

  41. Ben-Johny, M. & Yue, D. T. Calmodulin regulation (calmodulation) of voltage-gated calcium channels. J. Gen. Physiol. 143, 679–692 (2014).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  42. Tian, W., Wang, C., Gao, Q., Li, L. & Luan, S. Calcium spikes, waves and oscillations in plant development and biotic interactions. Nat. Plants 6, 750–759 (2020).

    CAS  PubMed  Article  Google Scholar 

  43. Kim, M. C. et al. Calmodulin interacts with MLO protein to regulate defence against mildew in barley. Nature 416, 447–451 (2002).

    ADS  CAS  PubMed  Article  Google Scholar 

  44. Tian, W. et al. A calmodulin-gated calcium channel links pathogen patterns to plant immunity. Nature 572, 131–135 (2019).

    CAS  PubMed  Article  Google Scholar 

  45. Clough, S. J. & Bent, A. F. Floral dip: a simplified method for Agrobacterium-mediated transformation of Arabidopsis thaliana. Plant J. 16, 735–743 (1998).

    CAS  PubMed  Article  Google Scholar 

  46. Gao, Q. F. et al. Cyclic nucleotide-gated channel 18 is an essential Ca2+ channel in pollen tube tips for pollen tube guidance to ovules in Arabidopsis. Proc. Natl Acad. Sci. USA 113, 3096–3101 (2016).

    ADS  CAS  PubMed  PubMed Central  Article  Google Scholar 

  47. Palanivelu, R. & Preuss, D. Distinct short-range ovule signals attract or repel Arabidopsis thaliana pollen tubes in vitro. BMC Plant Biol. 6, 7 (2006).

    PubMed  PubMed Central  Article  CAS  Google Scholar 

  48. Li, H. et al. Control of pollen tube tip growth by a Rop GTPase-dependent pathway that leads to tip-localized calcium influx. Plant Cell 11, 1731–1742 (1999).

    CAS  PubMed  PubMed Central  Google Scholar 

  49. 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).

    CAS  PubMed  PubMed Central  Article  Google Scholar 

  50. Duan, Q. et al. FERONIA receptor-like kinase regulates RHO GTPase signaling of root hair development. Proc. Natl Acad. Sci. USA 107, 17821–17826 (2010).

    ADS  CAS  PubMed  PubMed Central  Article  Google Scholar 

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Acknowledgements

We thank J. Santiago of the University of Lausanne for providing the pFastBac-RALF4/19 and LRX8 vector; B. Li of UC Berkeley for advice on protein purification from insect cells; R. Palanivelu of the University of Arizona for providing pLAT52:DsRed seeds; and S. Ruzin and D. Schichnes at The Biological Imaging Facility of UC Berkeley for their assistance.

Author information

Authors and Affiliations

Authors

Contributions

Q.G., C.W., L.L. and S.L. conceived and designed the experiments. Q.G., Y.X. and Q.S. performed the molecular cloning and biochemical experiments and generated the transgenic plants. Q.G. performed the patch-clamp and voltage clamp recordings and Ca2+ imaging. Q.G., C.W. and S.L. wrote the manuscript. All authors discussed the results and commented on the manuscript.

Corresponding author

Correspondence to Sheng Luan.

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Extended data figures and tables

Extended Data Fig. 1 Expression and redundant function of RALF4 and 19 in pollen tube reception.

a, Expression pattern of RALF4 and 19 during pollen tube reception. Arrows indicated pollen tubes (from proRALF-GUS plants) that penetrated ovules (proRALF-GUS plants). For control, pollen grains from non-transgenic plants were used to pollinate the promoter: GUS transgenic plants, showing no expression of GUS in the ovule. b, ralf4 and ralf19 single mutants did not show pollen tube overgrowth. n = 10 pistils. c, The peak values of the synergid Ca2+ spikes triggered by pollen tubes of ralf4 and ralf19 single mutants was similar to that of WT. n = 5 ovules for WT, and n = 6 ovules for ralf4 and ralf19. Bar, 50 µm. Error bars depict means ± S.E.M. All P values were determined by two-tailed Student’s t-test.

Source data

Extended Data Fig. 2 RALF8, 9, 15, 25, 26 and 30 failed to induce synergid Ca2+ changes.

a, Representative Ca2+ spiking patterns in synergid cells in response to 0.5 µM RALFs. b, The peak values of Ca2+ spiking as in (a). n = 15 ovules for water treatment, n = 16 ovules for RALF8, n = 14 ovules for RALF9, n = 10 ovules for RALF15, n = 15 ovules for RALF25, n = 11 ovules for RALF26 and n = 13 ovules for RALF30. Error bars depict means ± S.E.M. All P values were determined by two-tailed Student’s t-test.

Source data

Extended Data Fig. 3 Pollen tube derived RALF4/19 induce synergid Ca2+ oscillations.

Representative Ca2+ spiking patterns in synergid cells in response to 0.5 µM and 2 µM RALF19 or RALF34 for WT (a), fer-4 (b), lre-5 (c) and nta-3 (d). Red triangles indicate time points at which RALFs was applied. In Fig. 1i, for water treatment, n = 13 ovules for WT, n = 11 ovules for fer-4, n = 11 ovules for lre-5, and n = 11 ovules for nta-3; for pollen tube, n = 13 ovules for WT, n = 17 ovules for fer-4, n = 7 ovules for lre-5 and n = 10 ovules for nta-3; for 0.5 µM RALF4 treatment, n = 12 ovules for WT, n = 15 ovules for fer-4, n = 13 ovules for lre-5 and n = 13 ovules for nta-3; For 2 µM RALF4 treatment, n = 11 ovules for WT, n = 10 ovules for fer-4, n = 13 ovules for lre-5 and n = 14 ovules for nta-3; For 0.5 µM RALF19 treatment, n = 13 ovules for WT, n = 10 ovules fer-4, n = 11 ovules for lre-5 and n = 12 ovules nta-3. For 2 µM RALF19 treatment, n = 11 ovules for WT, n = 10 ovules for fer-4, n = 12 ovules for lre-5 and n = 14 ovules for nta-3; For 0.5 µM RALF34 treatment, n = 11 ovules for WT, n = 12 ovules for fer-4, n = 12 ovules for lre-5 and n = 13 ovules for nta-3; For 2 µM RALF34 treatment, n = 10 ovules for WT, n = 11 ovules for fer-4, n = 12 ovules for lre-5 and n = 14 ovules for nta-3. In Fig. 4k, in WT n = 14 ovules for water treatment, n = 15 ovules for pollen tube and n = 10 ovules for 0.5 µM RALF4 treatment; in nta-3, n = 11 ovules for water treatment, n = 10 ovules for pollen tube and n = 12 ovules 0.5 µM RALF4; in NTARR, n = 13 ovules for water treatment, n = 14 ovules for pollen tube and n = 13 ovules for 0.5 µM RALF4.

Extended Data Fig. 4 Representative cytosolic Ca2+ increase curves of COS7 cells expressing various MLOs.

The black triangle indicated the time point when 10 mM external Ca2+ was applied.

Extended Data Fig. 5 Conductivity of AtMLO2 to divalent and monovalent cations.

(a) Typical whole-cell recordings and (b) average current-voltage curves of the inward currents showing external Ca2+ dependence (0 mM, 10 mM and 30mM) in HEK293T cells expressing AtMLO2. (c) Typical whole-cell recordings and (d) average current-voltage curves for Ba2+ conductance by AtMLO2 in HEK293T cells. (e) Typical whole-cell recordings and (f) average current-voltage curves for Mg2+ conductance by AtMLO2 in HEK293T cells. (g) Typical whole-cell recordings and (h) average current-voltage curves for Gd3+ (100 μM) and La3+ (100 μM) inhibition of Ca2+ conductance in HEK293T cells expressing AtMLO2. (i) Typical whole-cell recordings and (j) average current-voltage curves of the inward currents showing no detectable K+ conductance by AtMLO2 in HEK293T cells. (k) Typical whole-cell recordings and (l) average current-voltage curves of the inward currents showing no detectable Na+ conductance by AtMLO2 in HEK293T cells. Error bars depict means ± S.E.M. n values = 8 cells. All P values were determined by two-tailed Student’s t-test.

Source data

Extended Data Fig.6 Conductivity of HvMLO to divalent and monovalent cations.

(a) Typical whole-cell recordings and (b) average current-voltage curves of the inward currents showing external Ca2+ dependence (0 mM, 10 mM and 30mM) in HEK293T cells expressing HvMLO. (c) Typical whole-cell recordings and (d) average current-voltage curves for Ba2+ conductance by HvMLO in HEK293T cells. (e) Typical whole-cell recordings and (f) average current-voltage curves for Mg2+ conductance by HvMLO in HEK293T cells. (g) Typical whole-cell recordings and (h) average current-voltage curves for Gd3+ (100 μM) and La3+ (100 μM) inhibition of Ca2+ conductance in HEK293T cells expressing HvMLO. (i) Typical whole-cell recordings and (j) average current-voltage curves of the inward currents showing no detectable K+ conductance by HvMLO in HEK293T cells. (k) Typical whole-cell recordings and (l) average current-voltage curves of the inward currents showing no detectable Na+ conductance by HvMLO in HEK293T cells. Error bars depict means ± S.E.M. n values = 8 cells. All P values were determined by two-tailed Student’s t-test.

Source data

Extended Data Fig. 7 Typical cytosolic Ca2+ increase curves of COS7 cells expressing the combination of FER, LRE, NTA and the kinase-dead version of FER (FERKD).

The black triangle indicated the time point when 10 mM external Ca2+ was applied.

Extended Data Fig. 8 Conductivity of NTA trio to divalent and monovalent cations.

(a) Typical whole-cell recordings and (b) average current-voltage curves of the inward currents showing external Ca2+ dependence (0 mM, 10 mM and 30mM) in HEK293T cells expressing NTA trio. (c) Typical whole-cell recordings and (d) average current-voltage curves for Ba2+ conductance by NTA trio in HEK293T cells. (e) Typical whole-cell recordings and (f) average current-voltage curves for Mg2+ conductance by NTA trio in HEK293T cells. (g) Typical whole-cell recordings and (h) average current-voltage curves for Gd3+ (100 μM) and La3+ (100 μM) inhibition of Ca2+ conductance in HEK293T cells expressing NTA trio. (i) Typical whole-cell recordings and (j) average current-voltage curves of the inward currents showing no detectable K+ conductance by NTA trio in HEK293T cells. (k) Typical whole-cell recordings and (l) average current-voltage curves of the inward currents showing no detectable Na+ conductance by NTA trio in HEK293T cells. Error bars depict means ± S.E.M. n values = 8 cells. All P values were determined by two-tailed Student’s t-test.

Source data

Extended Data Fig. 9 The localization of NTA-GFP and NTARR-GFP.

a, RALFs did not alter the PM localization of NTA-GFP. n = 3 independent repeats. b, FER and LRE facilitated the PM localization of NTARR-GFP. Scale bars, 10 μm (up-panel), 5 μm (down-panel). The white rectangle indicated the area of zoom-in. n = 3 independent repeats.

Extended Data Fig. 10 RALF37 triggers synergid Ca2+ changes and enhances the activity of NTA trio.

a, Representative Ca2+ spiking patterns in synergid cells in response to 0.5 µM RALF37. b, The peak values of Ca2+ spiking as in (a). n = 18 ovules for water treatment and n = 14 ovules for RALF37. c, d, Representative cytosolic Ca2+ spiking curves (c) and statistical analysis of peak values (d) in COS7 cells expressing the FER-LRE-NTA trio treated with 0.5 µM RALF37. n = 8 replicates, and ~ 60 cells were imaged in each duplicate. Error bars depict means ± S.E.M. All P values were determined by two-tailed Student’s t-test.

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Gao, Q., Wang, C., Xi, Y. et al. A receptor–channel trio conducts Ca2+ signalling for pollen tube reception. Nature 607, 534–539 (2022). https://doi.org/10.1038/s41586-022-04923-7

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