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

Nature volume 607, pages 534–539 (2022)Cite this article

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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.

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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

  1. Department of Plant and Microbial Biology, University of California at Berkeley, Berkeley, CA, USA

    Qifei Gao, Chao Wang, Yasheng Xi, Qiaolin Shao & Sheng Luan

  2. College of Life Sciences, Capital Normal University, Beijing, China

    Legong Li

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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.

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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.

Source data

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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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