reSeArcH Article
GIPCs, osmosensing OSCA1 and components yet to be defined may
work together to integrate both ionic and osmotic aspects of salt into
the salt Ca^2 + signalling pathway in plants.
Much progress has been made over the last three decades in under-
standing the phenomenon of [Ca^2 +]i elevation in response to abiotic
and biotic stimuli in plants^5 ,^7 ,^41 ,^42. Ca^2 +-imaging-based genetic screens
have led to the identification of only a few receptors or sensors, includ-
ing DORN1 for external ATP, OSCA1 for osmotic stress, and LORE
for lipopolysaccharides^17 ,^43 ,^44. These Ca^2 +-related receptors could
be classified into three groups: (1) receptor-like kinases, including
NFR1, NFP (also known as NFR5) and DMI2 (also known as SYMRK)
for Nod factors, FLS2 for flg22, EFR for elf18 and elf26, PEPR1 for
AtPep1, and FER for rapid alkalinization factor, as well as DORN1
and LORE; (2) the receptor channel OSCA1; and (3) transmembrane
receptors^8 ,^41. Ca^2 + channels that are not receptors or sensors but are
responsible for Ca^2 + increases have also been found, such as DMI1,
Pollux and Castor and CNGC15 for Nod factors, CNGC14 for auxin
and CNGC18 for the pollen tube^41 ,^45 ,^46 , and GLRs for wounding and
sperm chemotaxis^47 ,^48. It is plausible to speculate that GIPC-associated
Ca^2 + channels belong to this category. In animals, Ca^2 +-related recep-
tors comprise G-protein coupled receptors, receptor tyrosine kinases,
and receptor channels^12 ,^49 , and animal salt sensors are receptor chan-
nels^13 –^16. Therefore, GIPC-mediated salt sensing in plants differs from
all these receptors found in animals and plants. Note that GIPCs are
receptors for pathogenic necrosis and ethylene-inducing peptide 1-like
proteins in eudicot but not monocot plants^50 , and gangliosides are
receptors for axon–myelin interactions in animals^32.
In conclusion, our results shed light on salt sensing in plants, high-
light the importance of GIPCs—as a specific class of sphingolipids—for
the regulation (and modulation) of signalling processes at the plasma
membrane, and underscore the functional versatility of various lipids in
different evolutionary branches of life. Our findings could also provide
potential molecular genetic targets for engineering salt-resistant crops.
Online content
Any methods, additional references, Nature Research reporting summaries, source
data, extended data, supplementary information, acknowledgements, peer review
information; details of author contributions and competing interests; and state-
ments of data and code availability are available at https://doi.org/10.1038/s41586-
019-1449-z.
Received: 25 April 2018; Accepted: 3 July 2019;
Published online 31 July 2019.
- Munns, R. & Tester, M. Mechanisms of salinity tolerance. Annu. Rev. Plant Biol.
59 , 651–681 (2008). - Ismail, A. M. & Horie, T. Genomics, physiology, and molecular breeding
approaches for improving salt tolerance. Annu. Rev. Plant Biol. 68 , 405–434
(2017). - Yang, Y. & Guo, Y. Elucidating the molecular mechanisms mediating plant
salt-stress responses. New Phytol. 217 , 523–539 (2018). - Deinlein, U. et al. Plant salt-tolerance mechanisms. Trends Plant Sci. 19 ,
371–379 (2014). - Zhu, J. K. Abiotic stress signaling and responses in plants. Cell 167 , 313–324
(2016). - Julkowska, M. M. & Testerink, C. Tuning plant signaling and growth to survive
salt. Trends Plant Sci. 20 , 586–594 (2015). - Kudla, J. et al. Advances and current challenges in calcium signaling. New
Phytol. 218 , 414–431 (2018). - Edel, K. H., Marchadier, E., Brownlee, C., Kudla, J. & Hetherington, A. M. The
evolution of calcium-based signalling in plants. Curr. Biol. 27 , R667–R679 (2017). - Knight, M. R., Campbell, A. K., Smith, S. M. & Trewavas, A. J. Transgenic plant
aequorin reports the effects of touch and cold-shock and elicitors on
cytoplasmic calcium. Nature 352 , 524–526 (1991). - Knight, H., Trewavas, A. J. & Knight, M. R. Calcium signalling in Arabidopsis
thaliana responding to drought and salinity. Plant J. 12 , 1067–1078 (1997). - Hedrich, R. Ion channels in plants. Physiol. Rev. 92 , 1777–1811 (2012).
- Roper, S. D. & Chaudhari, N. Taste buds: cells, signals and synapses. Nat. Rev.
Neurosci. 18 , 485–497 (2017). - Chandrashekar, J. et al. The cells and peripheral representation of sodium taste
in mice. Nature 464 , 297–301 (2010). - Zhang, Y. V., Ni, J. & Montell, C. The molecular basis for attractive salt-taste
coding in Drosophila. Science 340 , 1334–1338 (2013). - Oka, Y., Butnaru, M., Von Buchholtz, L., Ryba, N. J. P. & Zuker, C. S. High salt
recruits aversive taste pathways. Nature 494 , 472–475 (2013).
16. Chatzigeorgiou, M., Bang, S., Hwang, S. W. & Schafer, W. R. tmc-1 encodes a
sodium-sensitive channel required for salt chemosensation in C. elegans.
Nature 494 , 95–99 (2013).
17. Yuan, F. et al. OSCA1 mediates osmotic-stress-evoked Ca^2 + increases vital for
osmosensing in Arabidopsis. Nature 514 , 367–371 (2014).
18. Choi, W. G., Hilleary, R., Swanson, S. J., Kim, S. H. & Gilroy, S. Rapid, long-
distance electrical and calcium signaling in plants. Annu. Rev. Plant Biol. 67 ,
287–307 (2016).
19. Martí, M. C., Stancombe, M. A. & Webb, A. A. R. Cell- and stimulus type-specific
intracellular free Ca^2 + signals in Arabidopsis. Plant Physiol. 163 , 625–634
(2013).
20. Hedrich, R., Salvador-Recatalà, V. & Dreyer, I. Electrical wiring and long-distance
plant communication. Trends Plant Sci. 21 , 376–387 (2016).
21. Choi, W. G., Toyota, M., Kim, S. H., Hilleary, R. & Gilroy, S. Salt stress-induced
Ca^2 + waves are associated with rapid, long-distance root-to-shoot signaling in
plants. Proc. Natl Acad. Sci. USA 111 , 6497–6502 (2014).
22. Evans, M. J., Choi, W. G., Gilroy, S. & Morris, R. J. A ROS-assisted calcium wave
dependent on the AtRBOHD NADPH oxidase and TPC1 cation channel propagates
the systemic response to salt stress. Plant Physiol. 171 , 1771–1784 (2016).
23. Rennie, E. A. et al. Identification of a sphingolipid α-glucuronosyltransferase that
is essential for pollen function in Arabidopsis. Plant Cell 26 , 3314–3325 (2014).
24. Rennie, E. A. et al. Three members of the Arabidopsis glycosyltransferase family
8 are xylan glucuronosyltransferases. Plant Physiol. 159 , 1408–1417 (2012).
25. Nikolovski, N., Shliaha, P. V., Gatto, L., Dupree, P. & Lilley, K. S. Label-free protein
quantification for plant Golgi protein localization and abundance. Plant Physiol.
166 , 1033–1043 (2014).
26. Tartaglio, V. et al. Glycosylation of inositol phosphorylceramide sphingolipids is
required for normal growth and reproduction in Arabidopsis. Plant J. 89 ,
278–290 (2017).
27. Gronnier, J., Germain, V., Gouguet, P., Cacas, J.-L. & Mongrand, S. GIPC: glycosyl
inositol phospho ceramides, the major sphingolipids on earth. Plant Signal.
Behav. 11 , e1152438 (2016).
28. Markham, J. E., Lynch, D. V., Napier, J. A., Dunn, T. M. & Cahoon, E. B. Plant
sphingolipids: function follows form. Curr. Opin. Plant Biol. 16 , 350–357 (2013).
29. Hannun, Y. A. & Obeid, L. M. Sphingolipids and their metabolism in physiology
and disease. Nat. Rev. Mol. Cell Biol. 19 , 175–191 (2018).
30. Cacas, J. L. et al. Revisiting plant plasma membrane lipids in tobacco: a focus
on sphingolipids. Plant Physiol. 170 , 367–384 (2016).
31. Ledeen, R. W. & Wu, G. The multi-tasked life of GM1 ganglioside, a true factotum
of nature. Trends Biochem. Sci. 40 , 407–418 (2015).
32. Schnaar, R. L., Gerardy-Schahn, R. & Hildebrandt, H. Sialic acids in the brain:
gangliosides and polysialic acid in nervous system development, stability,
disease, and regeneration. Physiol. Rev. 94 , 461–518 (2014).
33. Green, W. N. & Andersen, O. S. Surface charges and ion channel function. Annu.
Rev. Physiol. 53 , 341–359 (1991).
34. Liu, K. H. et al. Discovery of nitrate-CPK-NLP signalling in central nutrient-
growth networks. Nature 545 , 311–316 (2017).
35. Ho, C. H., Lin, S. H., Hu, H. C. & Tsay, Y. F. CHL1 functions as a nitrate sensor in
plants. Cell 138 , 1184–1194 (2009).
36. Xu, J. et al. A protein kinase, interacting with two calcineurin B-like proteins,
regulates K+ transporter AKT1 in Arabidopsis. Cell 125 , 1347–1360 (2006).
37. McLaughlin, S. & Murray, D. Plasma membrane phosphoinositide organization
by protein electrostatics. Nature 438 , 605–611 (2005).
38. Balla, T. Phosphoinositides: tiny lipids with giant impact on cell regulation.
Physiol. Rev. 93 , 1019–1137 (2013).
39. Hirschi, M. et al. Cryo-electron microscopy structure of the lysosomal
calcium-permeable channel TRPML3. Nature 550 , 411–414 (2017).
40. Gao, Y., Cao, E., Julius, D. & Cheng, Y. TRPV1 structures in nanodiscs reveal
mechanisms of ligand and lipid action. Nature 534 , 347–351 (2016).
41. Zipfel, C. & Oldroyd, G. E. D. Plant signalling in symbiosis and immunity. Nature
543 , 328–336 (2017).
42. Hamilton, E. S., Schlegel, A. M. & Haswell, E. S. United in diversity:
mechanosensitive ion channels in plants. Annu. Rev. Plant Biol. 66 , 113–137
(2015).
43. Choi, J. et al. Identification of a plant receptor for extracellular ATP. Science 343 ,
290–294 (2014).
44. Ranf, S. et al. A lectin S-domain receptor kinase mediates lipopolysaccharide
sensing in Arabidopsis thaliana. Nat. Immunol. 16 , 426–433 (2015).
45. Charpentier, M. et al. Nuclear-localized cyclic nucleotide-gated channels
mediate symbiotic calcium oscillations. Science 352 , 1102–1105 (2016).
46. Dindas, J. et al. AUX1-mediated root hair auxin influx governs SCFTIR1/AFB-type
Ca^2 + signaling. Nat. Commun. 9 , 1174 (2018).
47. Mousavi, S. A. R., Chauvin, A., Pascaud, F., Kellenberger, S. & Farmer, E. E.
GLUTAMATE RECEPTOR-LIKE genes mediate leaf-to-leaf wound signalling.
Nature 500 , 422–426 (2013).
48. Ortiz-Ramírez, C. et al. GLUTAMATE RECEPTOR-LIKE channels are essential for
chemotaxis and reproduction in mosses. Nature 549 , 91–95 (2017).
49. Murthy, S. E., Dubin, A. E. & Patapoutian, A. Piezos thrive under pressure:
mechanically activated ion channels in health and disease. Nat. Rev. Mol. Cell
Biol. 18 , 771–783 (2017).
50. Lenarčič, T. et al. Eudicot plant-specific sphingolipids determine host selectivity
of microbial NLP cytolysins. Science 358 , 1431–1434 (2017).
Publisher’s note: Springer Nature remains neutral with regard to jurisdictional
claims in published maps and institutional affiliations.
© The Author(s), under exclusive licence to Springer Nature Limited 2019
346 | NAtUre | VOl 572 | 15 AUGUSt 2019