Article reSeArcH
- Tang, R. H. et al. Coupling diurnal cytosolic Ca^2 + oscillations to the CAS-IP 3
pathway in Arabidopsis. Science 315 , 1423–1426 (2007). - Lahner, B. et al. Genomic scale profiling of nutrient and trace elements in
Arabidopsis thaliana. Nat. Biotechnol. 21 , 1215–1221 (2003). - Baxter, I. et al. A coastal cline in sodium accumulation in Arabidopsis thaliana is
driven by natural variation of the sodium transporter AtHKT1;1. PLoS Genet. 6 ,
e1001193 (2010). - Song, W. Y. et al. Arsenic tolerance in Arabidopsis is mediated by two ABCC-type
phytochelatin transporters. Proc. Natl Acad. Sci. USA 107 , 21187–21192 (2010). - Qiu, Q. S., Guo, Y., Dietrich, M. A., Schumaker, K. S. & Zhu, J. K. Regulation of
SOS1, a plasma membrane Na+/H+ exchanger in Arabidopsis thaliana, by SOS2
and SOS3. Proc. Natl Acad. Sci. USA 99 , 8436–8441 (2002). - Johansson, F., Olbe, M., Sommarin, M. & Larsson, C. Brij 58, a polyoxyethylene
acyl ether, creates membrane vesicles of uniform sidedness. A new tool to
obtain inside-out (cytoplasmic side-out) plasma membrane vesicles. Plant J. 7 ,
165–173 (1995). - Bradford, M. M. A rapid and sensitive method for the quantitation of microgram
quantities of protein utilizing the principle of protein-dye binding. Anal.
Biochem. 72 , 248–254 (1976). - Blumwald, E. & Poole, R. J. Na/H antiport in isolated tonoplast vesicles from
storage tissue of Beta vulgaris. Plant Physiol. 78 , 163–167 (1985). - Schwacke, R. et al. ARAMEMNON, a novel database for Arabidopsis integral
membrane proteins. Plant Physiol. 131 , 16–26 (2003). - Karimi, M., Inzé, D. & Depicker, A. GATEWAY vectors for Agrobacterium-mediated
plant transformation. Trends Plant Sci. 7 , 193–195 (2002). - Nelson, B. K., Cai, X. & Nebenführ, A. A multicolored set of in vivo organelle
markers for co-localization studies in Arabidopsis and other plants. Plant J. 51 ,
1126–1136 (2007). - Hooper, C. M., Castleden, I. R., Tanz, S. K., Aryamanesh, N. & Millar, A. H. SUBA4:
the interactive data analysis centre for Arabidopsis subcellular protein locations.
Nucleic Acids Res. 45 , D1064–D1074 (2017). - Heard, W., Sklenář, J., Tomé, D. F. A., Robatzek, S. & Jones, A. M. E. Identification
of regulatory and cargo proteins of endosomal and secretory pathways in
Arabidopsis thaliana by proteomic dissection. Mol. Cell. Proteomics 14 ,
1796–1813 (2015). - Nikolovski, N. et al. Putative glycosyltransferases and other plant Golgi
apparatus proteins are revealed by LOPIT proteomics. Plant Physiol. 160 ,
1037–1051 (2012). - Jefferson, R. A., Kavanagh, T. A. & Bevan, M. W. GUS fusions: β-glucuronidase as
a sensitive and versatile gene fusion marker in higher plants. EMBO J. 6 ,
3901–3907 (1987). - Buré, C. et al. Fast screening of highly glycosylated plant sphingolipids by tandem
mass spectrometry. Rapid Commun. Mass Spectrom. 25 , 3131–3145 (2011). - Wang, P. et al. Cell membrane surface potential (ψ 0 ) plays a dominant role in the
phytotoxicity of copper and arsenate. Plant Physiol. 148 , 2134–2143 (2008). - Delgado, A. V., González-Caballero, F., Hunter, R. J., Koopal, L. K. & Lyklema, J.
Measurement and interpretation of electrokinetic phenomena. J. Colloid
Interface Sci. 309 , 194–224 (2007). - Kinraide, T. B. & Wang, P. The surface charge density of plant cell membranes
(σ): an attempt to resolve conflicting values for intrinsic σ. J. Exp. Bot. 61 ,
2507–2518 (2010). - Yoo, S. D., Cho, Y. H. & Sheen, J. Arabidopsis mesophyll protoplasts: a versatile
cell system for transient gene expression analysis. Nat. Protocols 2 , 1565–1572
(2007). - Endo, M., Shimizu, H. & Araki, T. Rapid and simple isolation of vascular,
epidermal and mesophyll cells from plant leaf tissue. Nat. Protocols 11 ,
1388–1395 (2016). - Welsch, M. E. et al. Multivalent small-molecule pan-RAS inhibitors. Cell 168 ,
878–889 (2017).
80. Menting, J. G. et al. How insulin engages its primary binding site on the insulin
receptor. Nature 493 , 241–245 (2013).
81. Coscia, F. et al. Multi-level proteomics identifies CT45 as a chemosensitivity
mediator and immunotherapy target in ovarian cancer. Cell 175 , 159–170
(2018).
82. Chen, Y. N. P. et al. Allosteric inhibition of SHP2 phosphatase inhibits cancers
driven by receptor tyrosine kinases. Nature 535 , 148–152 (2016).
83. Johnson, R. A., Manley, O. M., Spuches, A. M. & Grossoehme, N. E. Dissecting ITC
data of metal ions binding to ligands and proteins. Biochim. Biophys. Acta. 1860 ,
892–901 (2016).
84. Machaidze, G., Ziegler, A. & Seelig, J. Specific binding of Ro 09-0198
(cinnamycin) to phosphatidylethanolamine: a thermodynamic analysis.
Biochemistry 41 , 1965–1971 (2002).
85. Katoh, K. & Standley, D. M. MAFFT multiple sequence alignment software
version 7: improvements in performance and usability. Mol. Biol. Evol. 30 ,
772–780 (2013).
86. Price, M. N., Dehal, P. S. & Arkin, A. P. FastTree: computing large minimum
evolution trees with profiles instead of a distance matrix. Mol. Biol. Evol. 26 ,
1641–1650 (2009).
87. Yin, Y., Chen, H., Hahn, M. G., Mohnen, D. & Xu, Y. Evolution and function of the
plant cell wall synthesis-related glycosyltransferase family 8. Plant Physiol. 153 ,
1729–1746 (2010).
Acknowledgements We thank J. Li for the pBIB-BASTA vector; M. R. Knight
for aequorin-expressing seeds; S. Gilroy for YC3.6-expressing seeds; M. Chen,
X. Dong and T.-p. Sun for advice on physical mapping; and T.-p. Sun, J. Pei, D.
R. McClay and P. N. Benfey for discussion and reading of the manuscript. Z.J.,
M.T., F.W., W.Z. and H. Zhang were supported in part by the Shenzhen Peacock
Innovative Research Team Program; Z.J., X.Z., L.L., X.W., F.W. and F.Y. by the
Pandeng Project of Hangzhou Normal University and Chinese NSF (31301170,
U1130304); and F.W., Y.N. and Y.X. by fellowships from the China Scholarship
Council. This work was supported by grants from NSF (IOS-1457257, IOS-
0848263) and USDA (CSREES-2006-35100-17304) to Z.-M.P.; National
Key Project for Synthetic Biology (2018YFA0902500) to Z.H.; and DOE (DE-
SC0014077) to T.V.-D. and Z.-M.P.
Author contributions Z.J., F.Y., Y. Xiang and Y.N. conducted genetic screens. Z.J.,
X.Z., F.Y., L.L., F.L., Y. Xue, F.W., X.W. and H. Zhao performed map-based cloning.
C.L., R.Y., F.Y. and B.B. generated T-DNA-mutagenized Arabidopsis populations.
Z.J., L.L., F.W., M.T., C.H., H. Zhao, C.P. and W.Z. carried out physiological analyses.
Z.J., M.T., W.Z., and Z.H. analysed GIPC content and ion content. M.T., Z.J., W.Z.,
and Z.H. analysed ion binding to GIPCs. Z.J., C.P. and F.W. conducted zeta
potential measurement. Z.J., L.L., H.-N.W., B.M.C., D.M.J., G.B.S., H. Zhang and
T.V.-D. participated in Ca^2 +-imaging analyses. Z.-M.P. designed and supervised
the overall research with input from Z.H., Z.J. and J.N.S. Z.-M.P., Z.J. and J.N.S.
wrote the paper. All authors discussed the results and commented on the
manuscript.
Competing interests The authors declare no competing interests.
Additional information
extended data is available for this paper at https://doi.org/10.1038/s41586-
019-1449-z.
supplementary information is available for this paper at https://doi.org/
10.1038/s41586-019-1449-z.
Correspondence and requests for materials should be addressed to Z.H. or
Z.-M.P.
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