α1-COP modulates plasmodesmata function through sphingolipid enzyme regulation

Arya Bagus Boedi Iswanto , Minh Huy Vu , Jong Cheol Shon , Ritesh Kumar , Shuwei Wu , Hobin Kang , Da-Ran Kim , Geon Hui Son , Woe Yoen Kim , Youn-Sig Kwak , Kwang Hyeon Liu , Sang Hee Kim , Jae-Yean Kim

Journal of Integrative Plant Biology ›› 2024, Vol. 66 ›› Issue (8) : 1639 -1657.

PDF
Journal of Integrative Plant Biology ›› 2024, Vol. 66 ›› Issue (8) : 1639 -1657. DOI: 10.1002/jipb.13711
Research Article

α1-COP modulates plasmodesmata function through sphingolipid enzyme regulation

Author information +
History +
PDF

Abstract

Callose, a β-1, 3-glucan plant cell wall polymer, regulates symplasmic channel size at plasmodesmata (PD) and plays a crucial role in a variety of plant processes. However, elucidating the molecular mechanism of PD callose homeostasis is limited. We screened and identified an Arabidopsis mutant plant with excessive callose deposition at PD and found that the mutated gene was α1-COP, a member of the coat protein I (COPI) coatomer complex. We report that loss of function of α1-COP elevates the callose accumulation at PD by affecting subcellular protein localization of callose degradation enzyme PdBG2. This process is linked to the functions of ERH1, an inositol phosphoryl ceramide synthase, and glucosylceramide synthase through physical interactions with the α1-COP protein. Additionally, the loss of function of α1-COP alters the subcellular localization of ERH1 and GCS proteins, resulting in a reduction of GlcCers and GlcHCers molecules, which are key sphingolipid (SL) species for lipid raft formation. Our findings suggest that α1-COP protein, together with SL modifiers controlling lipid raft compositions, regulates the subcellular localization of GPI-anchored PDBG2 proteins, and hence the callose turnover at PD and symplasmic movement of biomolecules. Our findings provide the first key clue to link the COPI-mediated intracellular trafficking pathway to the callose-mediated intercellular signaling pathway through PD.

Keywords

callose / coatomer proteins / membrane-bound vesicle / plasmodesmata / sphingolipid enzymes

Cite this article

Download citation ▾
Arya Bagus Boedi Iswanto, Minh Huy Vu, Jong Cheol Shon, Ritesh Kumar, Shuwei Wu, Hobin Kang, Da-Ran Kim, Geon Hui Son, Woe Yoen Kim, Youn-Sig Kwak, Kwang Hyeon Liu, Sang Hee Kim, Jae-Yean Kim. α1-COP modulates plasmodesmata function through sphingolipid enzyme regulation. Journal of Integrative Plant Biology, 2024, 66(8): 1639-1657 DOI:10.1002/jipb.13711

登录浏览全文

4963

注册一个新账户 忘记密码

References

[1]

Ahn, H.K.,Kang, Y.W.,Lim, H.M.,Hwang, I., and Pai, H.S. (2015). Physiological functions of the COPI complex in higher plants. Mol. Cells 38:866–875.

[2]

Ali, U.,Li, H.,Wang, X., and Guo, L. (2018). Emerging roles of sphingolipid signaling in plant response to biotic and abiotic stresses. Mol. Plant 11:1328–1343.

[3]

Austin, R.S.,Vidaurre, D.,Stamatiou, G.,Breit, R.,Provart, N.J.,Bonetta, D.,Zhang, J.,Fung, P.,Gong, Y.,Wang, P.W., et al. (2011). Next-generation mapping of Arabidopsis genes. Plant J. 67:715–725.

[4]

Bayer, E.M.,Mongrand, S., and Tilsner, J. (2014). Specialized membrane domains of plasmodesmata, plant intercellular nanopores. Front. Plant Sci. 5:507.

[5]

Bednarek, S.Y.,Ravazzola, M.,Hosobuchi, M.,Amherdt, M.,Perrelet, A.,Schekman, R., and Orci, L. (1995). COPI-and COPII-coated vesicles bud directly from the endoplasmic reticulum in yeast. Cell 83:1183–1196.

[6]

Benitez-Alfonso, Y.,Faulkner, C.,Pendle, A.,Miyashima, S.,Helariutta, Y., and Maule, A. (2013). Symplastic intercellular connectivity regulates lateral root patterning. Dev. Cell 26:136–147.

[7]

Bure, C.,Ayciriex, S.,Testet, E., and Schmitter, J.M. (2013). A single run LC-MS/MS method for phospholipidomics. Anal. Bioanal. Chem. 405:203–213.

[8]

Cabada Gomez, D.A.,Chavez, M.I.,Cobos, A.N.,Gross, R.J.,Yescas, J.A.,Balogh, M.A., and Indriolo, E. (2020). COPI complex isoforms are required for the early acceptance of compatible pollen grains in Arabidopsis thaliana. Plant Reprod. 33:97–110.

[9]

Caillaud, M.C.,Wirthmueller, L.,Sklenar, J.,Findlay, K.,Piquerez, S.J.,Jones, A.M.,Robatzek, S.,Jones, J.D., and Faulkner, C. (2014). The plasmodesmal protein PDLP1 localises to haustoria-associated membranes during downy mildew infection and regulates callose deposition. PLoS Pathog. 10: e1004496.

[10]

Chaudhary, A.,Gu, Q.M.,Thum, O.,Profit, A.A.,Qi, Y.,Jeyakumar, L.,Fleischer, S., and Prestwich, G.D. (1998). Specific interaction of Golgi coatomer protein alpha-COP with phosphatidylinositol 3, 4, 5-trisphosphate. J. Biol. Chem. 273:8344–8350.

[11]

Chen, S.,Hoene, M.,Li, J.,Li, Y.,Zhao, X.,Haring, H.U.,Schleicher, E.D.,Weigert, C.,Xu, G., and Lehmann, R. (2013). Simultaneous extraction of metabolome and lipidome with methyl tert-butyl ether from a single small tissue sample for ultra-high performance liquid chromatography/mass spectrometry. J. Chromatogr. A 1298:9–16.

[12]

Contreras, F.X.,Ernst, A.M.,Haberkant, P.,Bjorkholm, P.,Lindahl, E.,Gonen, B.,Tischer, C.,Elofsson, A.,von Heijne, G.,Thiele, C., et al. (2012). Molecular recognition of a single sphingolipid species by a protein’s transmembrane domain. Nature 481:525–529.

[13]

Curtis, M.D., and Grossniklaus, U. (2003). A gateway cloning vector set for high-throughput functional analysis of genes in planta. Plant Physiol. 133:462–469.

[14]

Donohoe, B.S.,Kang, B.H., and Staehelin, L.A. (2007). Identification and characterization of COPIa-and COPIb-type vesicle classes associated with plant and algal Golgi. Proc. Natl. Acad. Sci. U.S.A. 104:163–168.

[15]

Dunn, K.W.,Kamocka, M.M., and McDonald, J.H. (2011). A practical guide to evaluating colocalization in biological microscopy. Am. J. Physiol. Cell Physiol. 300: C723–C742.

[16]

Ellinger, D.,Naumann, M.,Falter, C.,Zwikowics, C.,Jamrow, T.,Manisseri, C.,Somerville, S.C., and Voigt, C.A. (2013). Elevated early callose deposition results in complete penetration resistance to powdery mildew in Arabidopsis. Plant Physiol. 161:1433–1444.

[17]

Eugster, A.,Frigerio, G.,Dale, M., and Duden, R. (2000). COP I domains required for coatomer integrity, and novel interactions with ARF and ARF-GAP. EMBO J. 19:3905–3917.

[18]

Eugster, A.,Frigerio, G.,Dale, M., and Duden, R. (2004). The alpha-and beta’-COP WD40 domains mediate cargo-selective interactions with distinct di-lysine motifs. Mol. Biol. Cell 15:1011–1023.

[19]

Fang, L.,Ishikawa, T.,Rennie, E.A.,Murawska, G.M.,Lao, J.,Yan, J.,Tsai, A.Y.,Baidoo, E.E.,Xu, J.,Keasling, J.D., et al. (2016). Loss of inositol phosphorylceramide sphingolipid mannosylation induces plant immune responses and reduces cellulose content in Arabidopsis. Plant Cell 28:2991–3004.

[20]

Farquharson, K.L. (2015). Sterols modulate cell-to-cell connectivity at plasmodesmata. Plant Cell 27:948.

[21]

Faulkner, C.,Petutschnig, E.,Benitez-Alfonso, Y.,Beck, M.,Robatzek, S.,Lipka, V., and Maule, A.J. (2013). LYM2-dependent chitin perception limits molecular flux via plasmodesmata. Proc. Natl. Acad. Sci. U.S.A. 110:9166–9170.

[22]

Gao, C.,Cai, Y.,Wang, Y.,Kang, B.H.,Aniento, F.,Robinson, D.G., and Jiang, L. (2014). Retention mechanisms for ER and Golgi membrane proteins. Trends Plant Sci. 19:508–515.

[23]

Gaynor, E.C.,Graham, T.R., and Emr, S.D. (1998). COPI in ER/Golgi and intra-Golgi transport: Do yeast COPI mutants point the way? Biochim. Biophys. Acta 1404:33–51.

[24]

Gehl, C.,Waadt, R.,Kudla, J.,Mendel, R.R., and Hansch, R. (2009). New GATEWAY vectors for high throughput analyses of protein-protein interactions by bimolecular fluorescence complementation. Mol. Plant 2:1051–1058.

[25]

German, L.,Yeshvekar, R., and Benitez-Alfonso, Y. (2023). Callose metabolism and the regulation of cell walls and plasmodesmata during plant mutualistic and pathogenic interactions. Plant Cell Environ. 46:391–404.

[26]

Gimeno-Ferrer, F.,Pastor-Cantizano, N.,Bernat-Silvestre, C.,Selvi-Martinez, P.,Vera-Sirera, F.,Gao, C.,Perez-Amador, M.A.,Jiang, L.,Aniento, F., and Marcote, M.J. (2017). alpha2-COP is involved in early secretory traffic in Arabidopsis and is required for plant growth. J. Exp. Bot. 68:391–401.

[27]

Grison, M.S.,Brocard, L.,Fouillen, L.,Nicolas, W.,Wewer, V.,Dormann, P.,Nacir, H.,Benitez-Alfonso, Y.,Claverol, S.,Germain, V., et al. (2015). Specific membrane lipid composition is important for plasmodesmata function in Arabidopsis. Plant Cell 27:1228–1250.

[28]

Han, X.,Hyun, T.K.,Zhang, M.,Kumar, R.,Koh, E.J.,Kang, B.H.,Lucas, W.J., and Kim, J.Y. (2014). Auxin-callose-mediated plasmodesmal gating is essential for tropic auxin gradient formation and signaling. Dev. Cell 28:132–146.

[29]

Im, S.S.,Park, H.Y.,Shon, J.C.,Chung, I.S.,Cho, H.C.,Liu, K.H., and Song, D.K. (2019). Plasma sphingomyelins increase in pre-diabetic Korean men with abdominal obesity. PLoS One 14: e0213285.

[30]

Iswanto, A.B., and Kim, J.Y. (2017). Lipid Raft, regulator of plasmodesmal callose homeostasis. Plants (Basel) 6:6020015.

[31]

Iswanto, A.B.B.,Shelake, R.M.,Vu, M.H.,Kim, J.-Y., and Kim, S.H. (2021). Genome editing for plasmodesmal biology. Front. Plant Sci. 12:679140.

[32]

Iswanto, A.B.B.,Shon, J.C.,Liu, K.H.,Vu, M.H.,Kumar, R., and Kim, J.Y. (2020). Sphingolipids modulate secretion of glycosylphosphatidylinositol-anchored plasmodesmata proteins and callose deposition. Plant Physiol. 184:407–420.

[33]

Iswanto, A.B.B.,Vu, M.H.,Pike, S.,Lee, J.,Kang, H.,Son, G.H.,Kim, J.Y., and Kim, S.H. (2022). Pathogen effectors: What do they do at plasmodesmata? Mol. Plant Pathol. 23:795–804.

[34]

Jackson, L.P. (2014). Structure and mechanism of COPI vesicle biogenesis. Curr. Opin. Cell Biol. 29:67–73.

[35]

Jackson, L.P.,Lewis, M.,Kent, H.M.,Edeling, M.A.,Evans, P.R.,Duden, R., and Owen, D.J. (2012). Molecular basis for recognition of dilysine trafficking motifs by COPI. Dev. Cell 23:1255–1262.

[36]

Jacobs, A.K.,Lipka, V.,Burton, R.A.,Panstruga, R.,Strizhov, N.,Schulze-Lefert, P., and Fincher, G.B. (2003). An Arabidopsis callose synthase, GSL5, is required for wound and papillary callose formation. Plant Cell 15:2503–2513.

[37]

Karimi, M.,Inzé D., and Depicker, A. (2002). GATEWAY vectors for Agrobacterium-mediated plant transformation. Trends Plant Sci. 7:193–195.

[38]

Kim, K.H.,Kim, E.K.,Kim, S.J.,Park, Y.H., and Park, H.M. (2011). Effect of Saccharomyces cerevisiae ret1-1 mutation on glycosylation and localization of the secretome. Mol. Cells 31:151–158.

[39]

Kumar, R.,Wu, S.W.,Iswanto, A.B.,Kumar, D.,Han, X., and Kim, J.Y. (2016). A Strategy to validate the role of callose-mediated plasmodesmal gating in the tropic response. J. Visualized Exp. 110:53513.

[40]

Lee, J.W.,Mok, H.J.,Lee, D.Y.,Park, S.C.,Kim, G.S.,Lee, S.E.,Lee, Y.S.,Kim, K.P., and Kim, H.D. (2017). UPLC-QqQ/MS-based lipidomics approach to characterize lipid alterations in inflammatory macrophages. J. Proteome Res. 16:1460–1469.

[41]

Levy, A.,Guenoune-Gelbart, D., and Epel, B.L. (2007). Beta-1, 3-glucanases: plasmodesmal gate keepers for intercellular communication. Plant Signal. Behav. 2:404–407.

[42]

Liu, X.,Ma, Z.,Tran, T.M.,Rautengarten, C.,Cheng, Y.,Yang, L.,Ebert, B.,Persson, S., and Miao, Y. (2023). Balanced callose and cellulose biosynthesis in Arabidopsis quorum-sensing signaling and pattern-triggered immunity. Plant Physiol. 194:137–152.

[43]

Ma, W., and Goldberg, J. (2013). Rules for the recognition of dilysine retrieval motifs by coatomer. EMBO J. 32:926–937.

[44]

Magnin-Robert, M.,Le Bourse, D.,Markham, J.,Dorey, S.,Clement, C.,Baillieul, F., and Dhondt-Cordelier, S. (2015). Modifications of sphingolipid content affect tolerance to hemibiotrophic and necrotrophic pathogens by modulating plant defense responses in Arabidopsis. Plant Physiol. 169:2255–2274.

[45]

Markham, J.E., and Jaworski, J.G. (2007). Rapid measurement of sphingolipids from Arabidopsis thaliana by reversed-phase high-performance liquid chromatography coupled to electrospray ionization tandem mass spectrometry. Rapid Commun. Mass Spectrom. 21:1304–1314.

[46]

Markham, J.E.,Li, J.,Cahoon, E.B., and Jaworski, J.G. (2006). Separation and identification of major plant sphingolipid classes from leaves. J. Biol. Chem. 281:22684–22694.

[47]

Misselwitz, B.,Dilling, S.,Vonaesch, P.,Sacher, R.,Snijder, B.,Schlumberger, M.,Rout, S.,Stark, M.,von Mering, C.,Pelkmans, L., et al. (2011). RNAi screen of Salmonella invasion shows role of COPI in membrane targeting of cholesterol and Cdc42. Mol. Syst. Biol. 7:474.

[48]

Mongrand, S.,Stanislas, T.,Bayer, E.M.,Lherminier, J., and Simon-Plas, F. (2010). Membrane rafts in plant cells. Trends Plant Sci. 15:656–663.

[49]

Moser, B.,Hochreiter, B.,Herbst, R., and Schmid, J.A. (2017). Fluorescence colocalization microscopy analysis can be improved by combining object-recognition with pixel-intensity-correlation. Biotechnol. J. 12:201600332.

[50]

Msanne, J.,Chen, M.,Luttgeharm, K.D.,Bradley, A.M.,Mays, E.S.,Paper, J.M.,Boyle, D.L.,Cahoon, R.E.,Schrick, K., and Cahoon, E.B. (2015). Glucosylceramides are critical for cell-type differentiation and organogenesis, but not for cell viability in Arabidopsis. Plant J. 84:188–201.

[51]

Nicolas, W.J.,Grison, M.S., and Bayer, E.M. (2017). Shaping intercellular channels of plasmodesmata: The structure-to-function missing link. J. Exp. Bot. 69:91–103.

[52]

Nishimura, M.T.,Stein, M.,Hou, B.H.,Vogel, J.P.,Edwards, H., and Somerville, S.C. (2003). Loss of a callose synthase results in salicylic acid-dependent disease resistance. Science 301:969–972.

[53]

Orci, L.,Stamnes, M.,Ravazzola, M.,Amherdt, M.,Perrelet, A.,Sollner, T.H., and Rothman, J.E. (1997). Bidirectional transport by distinct populations of COPI-coated vesicles. Cell 90:335–349.

[54]

Paul, M.J., and Frigerio, L. (2007). Coated vesicles in plant cells. Semin. Cell Dev. Biol. 18:471–478.

[55]

Pepperkok, R.,Scheel, J.,Horstmann, H.,Hauri, H.P.,Griffiths, G., and Kreis, T.E. (1993). Beta-COP is essential for biosynthetic membrane transport from the endoplasmic reticulum to the Golgi complex in vivo. Cell 74:71–82.

[56]

Rothman, J.E. (1994). Mechanisms of intracellular protein transport. Nature 372:55–63.

[57]

Schroder-Kohne, S.,Letourneur, F., and Riezman, H. (1998). Alpha-COP can discriminate between distinct, functional di-lysine signals in vitro and regulates access into retrograde transport. J. Cell Sci. 111:3459–3470.

[58]

Spang, A. (2013). Traffic COPs: Rules of detection. EMBO J. 32:915–916.

[59]

Sutterlin, C.,Doering, T.L.,Schimmoller, F.,Schroder, S., and Riezman, H. (1997). Specific requirements for the ER to Golgi transport of GPI-anchored proteins in yeast. J. Cell Sci. 110:2703–2714.

[60]

Tapken, W., and Murphy, A.S. (2015). Membrane nanodomains in plants: Capturing form, function, and movement. J. Exp. Bot. 66:1573–1586.

[61]

Tellier, F.,Maia-Grondard, A.,Schmitz-Afonso, I., and Faure, J.D. (2014). Comparative plant sphingolipidomic reveals specific lipids in seeds and oil. Phytochemistry 103:50–58.

[62]

Thomas, C.L.,Bayer, E.M.,Ritzenthaler, C.,Fernandez-Calvino, L., and Maule, A.J. (2008). Specific targeting of a plasmodesmal protein affecting cell-to-cell communication. PLoS Biol. 6: e7.

[63]

Vu, M.H.,Hyun, T.K.,Bahk, S.,Jo, Y.,Kumar, R.,Thiruppathi, D.,Iswanto, A.B.B.,Chung, W.S.,Shelake, R.M., and Kim, J.Y. (2022). ROS-mediated plasmodesmal regulation requires a network of an Arabidopsis receptor-like kinase, calmodulin-like proteins, and callose synthases. Front. Plant Sci. 13:1107224.

[64]

Vu, M.H.,Iswanto, A.B.B.,Lee, J., and Kim, J.Y. (2020). the role of plasmodesmata-associated receptor in plant development and environmental response. Plants (Basel) 9:9020216.

[65]

Wang, W.,Yang, X.,Tangchaiburana, S.,Ndeh, R.,Markham, J.E.,Tsegaye, Y.,Dunn, T.M.,Wang, G.L.,Bellizzi, M.,Parsons, J.F., et al. (2008). An inositolphosphorylceramide synthase is involved in regulation of plant programmed cell death associated with defense in Arabidopsis. Plant Cell 20:3163–3179.

[66]

Wang, Y.N.,Wang, H.,Yamaguchi, H.,Lee, H.J.,Lee, H.H., and Hung, M.C. (2010). COPI-mediated retrograde trafficking from the Golgi to the ER regulates EGFR nuclear transport. Biochem. Biophys. Res. Commun. 399:498–504.

[67]

Woo, C.H.,Gao, C.,Yu, P.,Tu, L.,Meng, Z.,Banfield, D.K.,Yao, X., and Jiang, L. (2015). Conserved function of the lysine-based KXD/E motif in Golgi retention for endomembrane proteins among different organisms. Mol. Biol. Cell 26:4280–4293.

[68]

Wu, S.W.,Kumar, R.,Iswanto, A.B.B., and Kim, J.Y. (2018). Callose balancing at plasmodesmata. J. Exp. Bot. 69:5325–5339.

[69]

Xia, Y.Q., and Jemal, M. (2009). Phospholipids in liquid chromatography/mass spectrometry bioanalysis: Comparison of three tandem mass spectrometric techniques for monitoring plasma phospholipids, the effect of mobile phase composition on phospholipids elution and the association of phospholipids with matrix effects. Rapid Commun. Mass Spectrom. 23:2125–2138.

[70]

Xie, L.J.,Chen, Q.F.,Chen, M.X.,Yu, L.J.,Huang, L.,Chen, L.,Wang, F.Z.,Xia, F.N.,Zhu, T.R.,Wu, J.X., et al. (2015). Unsaturation of very-long-chain ceramides protects plant from hypoxia-induced damages by modulating ethylene signaling in Arabidopsis. PLoS Genet. 11: e1005143.

[71]

Xu, B.,Cheval, C.,Laohavisit, A.,Hocking, B.,Chiasson, D.,Olsson, T.S.G.,Shirasu, K.,Faulkner, C., and Gilliham, M. (2017). A calmodulin-like protein regulates plasmodesmal closure during bacterial immune responses. New Phytol. 215:77–84.

[72]

Yan, D.,Yadav, S.R.,Paterlini, A.,Nicolas, W.J.,Petit, J.D.,Brocard, L.,Belevich, I.,Grison, M.S.,Vaten, A.,Karami, L., et al. (2019). Sphingolipid biosynthesis modulates plasmodesmal ultrastructure and phloem unloading. Nat. Plants 5:604–615.

[73]

Zambryski, P., and Crawford, K. (2000). Plasmodesmata: Gatekeepers for cell-to-cell transport of developmental signals in plants. Annu. Rev. Cell Dev. Biol. 16:393–421.

[74]

Zavaliev, R.,Dong, X., and Epel, B.L. (2016). Glycosylphosphatidylinositol (GPI) Modification Serves as a Primary Plasmodesmal Sorting Signal. Plant Physiol. 172:1061–1073.

[75]

Zavaliev, R.,Levy, A.,Gera, A., and Epel, B.L. (2013). Subcellular dynamics and role of Arabidopsis beta-1, 3-glucanases in cell-to-cell movement of tobamoviruses. Mol. Plant Microbe Interact. 26:1016–1030.

[76]

Zavaliev, R.,Ueki, S.,Epel, B.L., and Citovsky, V. (2011). Biology of callose (beta-1, 3-glucan) turnover at plasmodesmata. Protoplasma 248:117–130.

[77]

Zhang, X.,Henriques, R.,Lin, S.S.,Niu, Q.W., and Chua, N.H. (2006). Agrobacterium-mediated transformation of Arabidopsis thaliana using the floral dip method. Nat. Protoc. 1:641–646.

RIGHTS & PERMISSIONS

2024 The Authors. Journal of Integrative Plant Biology published by John Wiley & Sons Australia, Ltd on behalf of Institute of Botany, Chinese Academy of Sciences.

AI Summary AI Mindmap
PDF

132

Accesses

0

Citation

Detail

Sections
Recommended

AI思维导图

/