1,645
Views
2
CrossRef citations to date
0
Altmetric
Review

The damage-associated molecular pattern cellotriose alters the phosphorylation pattern of proteins involved in cellulose synthesis and trans-Golgi trafficking in Arabidopsis thaliana

, &
Article: 2184352 | Received 14 Dec 2022, Accepted 20 Feb 2023, Published online: 13 Mar 2023

References

  • Tseng Y-H, Scholz SS, Fliegmann J, Krüger T, Gandhi A, Furch AC, Kniemeyer O, Brakhage AA, Oelmüller R. CORK1, A LRR-Malectin receptor kinase, is required for cellooligomer-induced responses in Arabidopsis thaliana. Cells. 2022;11(19):2960. doi:10.3390/cells11192960.
  • Wolf S. Cell wall signaling in plant development and defense. Annu Rev Plant Biol. 2022;73:323–13.
  • Baez LA, Tichá T, Hamann T. Cell wall integrity regulation across plant species. Plant Mol Biol. 2022;109(4–5):483–504.
  • Westermann J. Two is company, but four is a party—Challenges of tetraploidization for cell wall dynamics and efficient tip-growth in pollen. Plants. 2021;10(11):2382. doi:10.3390/plants10112382.
  • Robichaux KJ, Wallace IS. Signaling at physical barriers during pollen–pistil interactions. Int J Mol Sci. 2021;22(22):12230. doi:10.3390/ijms222212230.
  • Narváez-Barragán DA, Tovar-Herrera OE, Guevara-García A, Serrano M, Martinez-Anaya C. Mechanisms of plant cell wall surveillance in response to pathogens, cell wall-derived ligands and the effect of expansins to infection resistance or susceptibility. Front Plant Sci. 2022;13:969343.
  • Kawa D, Brady SM. Root cell types as an interface for biotic interactions. Trends Plant Sci. 2022;27(11):1173–1186. doi:10.1016/j.tplants.2022.06.003.
  • Hoffmann N, King S, Samuels AL, McFarlane HE. Subcellular coordination of plant cell wall synthesis. Dev Cell. 2021;56(7):933–948. doi:10.1016/j.devcel.2021.03.004.
  • Gu Y, Rasmussen CG. Cell biology of primary cell wall synthesis in plants. Plant Cell. 2022;34(1):103–128. doi:10.1093/plcell/koab249.
  • Gust AA, Pruitt R, Nürnberger T. Sensing danger: key to activating plant immunity. Trends Plant Sci. 2017;22(9):779–791. doi:10.1016/j.tplants.2017.07.005.
  • He Z-H, Fujiki M, Kohorn BD. A cell wall-associated, receptor-like protein kinase. Journal of Biological Chemistry. 1996;271(33):19789–19793. doi:10.1074/jbc.271.33.19789.
  • Brutus A, Sicilia F, Macone A, Cervone F, De Lorenzo G. A domain swap approach reveals a role of the plant wall-associated kinase 1 (WAK1) as a receptor of oligogalacturonides. Proc. Natl. Acad. Sci. U.S.A. 2010;107:9452–9457.
  • Rebaque D, Del Hierro I, López G, Bacete L, Vilaplana F, Dallabernardina P, Pfrengle F, Jordá L, Sánchez-Vallet A, Pérez R, et al. Cell wall-derived mixed-linked β-1, 3/1, 4-glucans trigger immune responses and disease resistance in plants. The Plant Journal. 2021;106(3):601–615. doi:10.1111/tpj.15185.
  • Martín-Dacal M, Fernández-Calvo P, Jiménez-Sandoval P, López G, Garrido-Arandía M, Rebaque D, Del Hierro I, Berlanga DJ, Torres MÁ, Kumar V. Arabidopsis immune responses triggered by cellulose-and mixed-linked glucan-derived oligosaccharides require a group of leucine-rich repeat malectin receptor kinases. The Plant Journal. 2023;113(4):833–50.
  • Aziz A, Gauthier A, Bézier A, Poinssot B, Joubert J-M, Pugin A, Heyraud A, Baillieul F. Elicitor and resistance-inducing activities of β-1, 4 cellodextrins in grapevine, comparison with β-1, 3 glucans and α-1, 4 oligogalacturonides. J Exp Bot. 2007;58(6):1463–1472. doi:10.1093/jxb/erm008.
  • Locci F, Benedetti M, Pontiggia D, Citterico M, Caprari C, Mattei B, Cervone F, De Lorenzo G. An Arabidopsis berberine bridge enzyme-like protein specifically oxidizes cellulose oligomers and plays a role in immunity. The Plant Journal. 2019;98(3):540–554. doi:10.1111/tpj.14237.
  • Souza C, Li S, Lin AZ, Boutrot F, Grossmann G, Zipfel C, Somerville SC. Cellulose-derived oligomers act as damage-associated molecular patterns and trigger defense-like responses. Plant Physiol. 2017;173(4):2383–2398. doi:10.1104/pp.16.01680.
  • Denoux C, Galletti R, Mammarella N, Gopalan S, Werck D, De Lorenzo G, Ferrari S, Ausubel FM, Dewdney J. Activation of defense response pathways by OGs and Flg22 elicitors in Arabidopsis seedlings. Mol Plant. 2008;1(3):423–445. doi:10.1093/mp/ssn019.
  • Johnson JM, Thürich J, Petutschnig EK, Altschmied L, Meichsner D, Sherameti I, Dindas J, Mrozinska A, Paetz C, Scholz SS, et al. A Poly(A) Ribonuclease controls the cellotriose-based interaction between piriformospora indica and its host Arabidopsis. Plant Physiol. 2018;176(3):2496–2514. doi:10.1104/pp.17.01423.
  • Martin-Dacal M, Fernandez-Calvo P, Jimenez-Sandoval P, Lopez G, Garrido-Arandia M, Rebaque D, et al. Arabidopsis leucine rich repeat-malectin receptor kinases in immunity triggered by cellulose and mixed-linked glucan oligosaccharides. bioRxiv. 2022.
  • Hu XY, Neill SJ, Cai WM, Tang ZC. Induction of defence gene expression by oligogalacturonic acid requires increases in both cytosolic calcium and hydrogen peroxide in Arabidopsis thaliana. Cell Res. 2004;14(3):234–240. doi:10.1038/sj.cr.7290224.
  • Galletti R, Ferrari S, De Lorenzo G. Arabidopsis MPK3 and MPK6 play different roles in basal and Oligogalacturonide- or Flagellin-Induced resistance against Botrytis cinerea. Plant Physiol. 2011;157(2):804–814. doi:10.1104/pp.111.174003.
  • Claverie J, Balacey S, Lemaître-Guillier C, Brulé D, Chiltz A, Granet L, Noirot E, Daire X, Darblade B, Héloir M-C, et al. The cell wall-derived xyloglucan is a new DAMP triggering plant immunity in Vitis vinifera and Arabidopsis thaliana. Front Plant Sci. 2018;9:1725. doi:10.3389/fpls.2018.01725.
  • Melida H, Bacete L, Ruprecht C, Rebaque D, Del Hierro I, Lopez G, et al. Arabinoxylan-oligosaccharides act as damage associated molecular patterns in plants regulating disease resistance. Front Plant Sci. 2020;11:1210.
  • Yang H, Wang D, Guo L, Pan H, Yvon R, Garman S, et al. Malectin/Malectin-like domain-containing proteins: a repertoire of cell surface molecules with broad functional potential. The Cell Surface. 2021;7:100056.
  • Zhu S, Fu Q, Xu F, Zheng H, Yu F. New paradigms in cell adaptation: decades of discoveries on the Cr RLK1L receptor kinase signalling network. New Phytologist. 2021;232:1168–1183.
  • J-M E-R, Huck N, Kessler S, Gagliardini V, Gheyselinck J, Yang W-C, et al. The FERONIA receptor-like kinase mediates male-female interactions during pollen tube reception. Science. 2007;317:656–660.
  • Haruta M, Sabat G, Stecker K, Minkoff BB, Sussman MR. A peptide hormone and its receptor protein kinase regulate plant cell expansion. Science. 2014;343:408–411.
  • Feng W, Kita D, Peaucelle A, Cartwright HN, Doan V, Duan Q, et al. The FERONIA receptor kinase maintains cell-wall integrity during salt stress through Ca2+ signaling. Current Biology. 2018;28(666–75):e5.
  • Tang W, Lin W, Zhou X, Guo J, Dang X, Li B, et al. Mechano-transduction via the pectin-FERONIA complex activates ROP6 GTPase signaling in Arabidopsis pavement cell morphogenesis. Current Biology. 2022;32(508–17):e3.
  • Ortiz-Morea FA, Liu J, Shan L, He P. Malectin-like receptor kinases as protector deities in plant immunity. Nature Plants. 2022;8(1):27–37. doi:10.1038/s41477-021-01028-3.
  • McFarlane HE, Döring A, Persson S. The cell biology of cellulose synthesis. Annu Rev Plant Biol. 2014;65(1):69–94. doi:10.1146/annurev-arplant-050213-040240.
  • Polko JK, Kieber JJ. The regulation of cellulose biosynthesis in plants. Plant Cell. 2019;31(2):282–296. doi:10.1105/tpc.18.00760.
  • Ramírez-Rodríguez EA, McFarlane HE. Insights from the structure of a plant cellulose synthase trimer. Trends Plant Sci. 2021;26(1):4–7. doi:10.1016/j.tplants.2020.09.010.
  • McFarlane HE, Mutwil-Anderwald D, Verbančič J, Picard KL, Gookin TE, Froehlich A, Chakravorty D, Trindade LM, Alonso JM, Assmann SM, et al. AG protein-coupled receptor-like module regulates cellulose synthase secretion from the endomembrane system in Arabidopsis. Dev Cell. 2021;56(1484–97):e7. doi:10.1016/j.devcel.2021.03.031.
  • Wilson TH, Kumar M, Turner SR. The molecular basis of plant cellulose synthase complex organisation and assembly. Biochem Soc Trans. 2021;49(1):379–391. doi:10.1042/BST20200697.
  • Purushotham P, Ho R, Zimmer J. Architecture of a catalytically active homotrimeric plant cellulose synthase complex. Science. 2020;369(6507):1089–1094. doi:10.1126/science.abb2978.
  • Vellosillo T, Dinneny JR, Somerville CR, Ehrhardt DW. TRANVIA (TVA) facilitates cellulose synthase trafficking and delivery to the plasma membrane. Proc. Natl. Acad. Sci. U.S.A. 2021;118(30):e2021790118.
  • Bischoff V, Desprez T, Mouille G, Vernhettes S, Gonneau M, Höfte H. Phytochrome regulation of cellulose synthesis in Arabidopsis. Current Biology. 2011;21(21):1822–1827. doi:10.1016/j.cub.2011.09.026.
  • Chen S, Ehrhardt DW, Somerville CR. Mutations of cellulose synthase (CESA1) phosphorylation sites modulate anisotropic cell expansion and bidirectional mobility of cellulose synthase. Proc. Natl. Acad. Sci. U.S.A. 2010;107(40):17188–17193.
  • Cruz ER, Nguyen H, Nguyen T, Wallace IS. Functional analysis tools for post-translational modification: a post-translational modification database for analysis of proteins and metabolic pathways. The Plant Journal. 2019;99(5):1003–1013. doi:10.1111/tpj.14372.
  • Sánchez-Rodríguez C, Ketelaar K, Schneider R, Villalobos JA, Somerville CR, Persson S, Wallace IS. BRASSINOSTEROID INSENSITIVE2 negatively regulates cellulose synthesis in Arabidopsis by phosphorylating cellulose synthase 1. Proc. Natl. Acad. Sci. U.S.A. 2017;114(13):3533–3538. doi:10.1073/pnas.1615005114.
  • Johnson A, Vert G. Unraveling K63 polyubiquitination networks by sensor-based proteomics. Plant Physiol. 2016;171(3):1808–1820. doi:10.1104/pp.16.00619.
  • Kumar M, Wightman R, Atanassov I, Gupta A, Hurst CH, Hemsley PA, Turner S. S-Acylation of the cellulose synthase complex is essential for its plasma membrane localization. Science. 2016;353(6295):166–169. doi:10.1126/science.aaf4009.
  • Vain T, Crowell EF, Timpano H, Biot E, Desprez T, Mansoori N, Trindade LM, Pagant S, Robert S, Höfte H, et al. The cellulase KORRIGAN is part of the cellulose synthase complex. Plant Physiol. 2014;165(4):1521–1532. doi:10.1104/pp.114.241216.
  • Taylor NG, Howells RM, Huttly AK, Vickers K, Turner SR. Interactions among three distinct CesA proteins essential for cellulose synthesis. Proc. Natl. Acad. Sci. U.S.A. 2003;100(3):1450–1455.
  • Desprez T, Juraniec M, Crowell EF, Jouy H, Pochylova Z, Parcy F, et al. Organization of cellulose synthase complexes involved in primary cell wall synthesis in Arabidopsis thaliana. Proc. Natl. Acad. Sci. U.S.A. 2007;104(39):15572–15577.
  • Persson S, Paredez A, Carroll A, Palsdottir H, Doblin M, Poindexter P, et al. Genetic evidence for three unique components in primary cell-wall cellulose synthase complexes in Arabidopsis. Proc. Natl. Acad. Sci. U.S.A. 2007;104(39):15566–15571.
  • Speicher TL, Li PZ, Wallace IS. Phosphoregulation of the plant cellulose synthase complex and cellulose synthase-like proteins. Plants. 2018;7(3):52. doi:10.3390/plants7030052.
  • Taylor NG. Identification of cellulose synthase AtCesA7 (IRX3) in vivo phosphorylation sites—a potential role in regulating protein degradation. Plant Mol Biol. 2007;64(1–2):161–171. doi:10.1007/s11103-007-9142-2.
  • Li S, Lei L, Somerville CR, Gu Y. Cellulose synthase interactive protein 1 (CSI1) links microtubules and cellulose synthase complexes. Proc. Natl. Acad. Sci. U.S.A. 2012;109(1):185–190. doi:10.1073/pnas.0706592104.
  • Zhu X, Li S, Pan S, Xin X, Gu Y. CSI1, PATROL1, and exocyst complex cooperate in delivery of cellulose synthase complexes to the plasma membrane. Proc. Natl. Acad. Sci. U.S.A. 2018;115(15):E3578–E87. doi:10.1073/pnas.1800182115.
  • Zhu Y, McFarlane HE. Regulation of cellulose synthesis via exocytosis and endocytosis. Curr Opin Plant Biol. 2022;69:102273. doi:10.1016/j.pbi.2022.102273.
  • Gu Y, Somerville C. Cellulose synthase interacting protein: a new factor in cellulose synthesis. Plant Signal Behav. 2010;5(12):1571–1574. doi:10.4161/psb.5.12.13621.
  • Lei L, Singh A, Bashline L, Li S, Yingling YG, Gu Y. Cellulose synthase interactive1 is required for fast recycling of cellulose synthase complexes to the plasma membrane in Arabidopsis. Plant Cell. 2015;27(10):2926–2940. doi:10.1105/tpc.15.00442.
  • Žárský V, Sekereš J, Kubátová Z, Pečenková T, Cvrčková F. Three subfamilies of exocyst EXO70 family subunits in land plants: early divergence and ongoing functional specialization. J Exp Bot. 2020;71(1):49–62. doi:10.1093/jxb/erz423.
  • Žárský V, Kulich I, Fendrych M, Pečenková T. Exocyst complexes multiple functions in plant cells secretory pathways. Curr Opin Plant Biol. 2013;16(6):726–733. doi:10.1016/j.pbi.2013.10.013.
  • Zhang W, Huang L, Zhang C, Staiger CJ. Arabidopsis myosin XIK interacts with the exocyst complex to facilitate vesicle tethering during exocytosis. Plant Cell. 2021;33(7):2454–2478. doi:10.1093/plcell/koab116.
  • Zhang W, Cai C, Staiger CJ. Myosins XI are involved in exocytosis of cellulose synthase complexes. Plant Physiol. 2019;179(4):1537–1555. doi:10.1104/pp.19.00018.
  • Pang L, Ma Z, Zhang X, Huang Y, Li R, Miao Y, Li R. The small GTPase RABA2a recruits SNARE proteins to regulate the secretory pathway in parallel with the exocyst complex in Arabidopsis. Mol Plant. 2022;15(3):398–418. doi:10.1016/j.molp.2021.11.008.
  • Waghmare S, Lefoulon C, Zhang B, Liliekyte E, Donald N, Blatt MR. K + Channel-SEC11 binding exchange regulates SNARE assembly for secretory traffic. Plant Physiol. 2019;181(3):1096–1113. doi:10.1104/pp.19.00919.
  • Mansoori N, Timmers J, Desprez T, Kamei CL, Dees DC, Vincken J-P, Visser RGF, Höfte H, Vernhettes S, Trindade LM, et al. KORRIGAN1 interacts specifically with integral components of the cellulose synthase machinery. PLoS One. 2014;9(11):e112387. doi:10.1371/journal.pone.0112387.
  • Endler A, Persson S. Cellulose synthases and synthesis in Arabidopsis. Mol Plant. 2011;4(2):199–211. doi:10.1093/mp/ssq079.
  • Endler A, Schneider R, Kesten C, Lampugnani ER, Persson S. The cellulose synthase companion proteins act non-redundantly with CELLULOSE SYNTHASE INTERACTING1/POM2 and CELLULOSE SYNTHASE 6. Plant Signal Behav. 2016;11(4):e1135281. doi:10.1080/15592324.2015.1135281.
  • Sorek N, Sorek H, Kijac A, Szemenyei HJ, Bauer S, Hématy K, Wemmer DE, Somerville CR. The Arabidopsis COBRA protein facilitates cellulose crystallization at the plasma membrane. Journal of Biological Chemistry. 2014;289(50):34911–34920. doi:10.1074/jbc.M114.607192.
  • Polko JK, Barnes WJ, Voiniciuc C, Doctor S, Steinwand B, Hill JJL, Tien M, Pauly M, Anderson CT, Kieber JJ, et al. SHOU4 proteins regulate trafficking of cellulose synthase complexes to the plasma membrane. Current Biology. 2018;28(3174–82):e6. doi:10.1016/j.cub.2018.07.076.
  • Zimmermann R, Eyrisch S, Ahmad M, Helms V. Protein translocation across the ER membrane. Biochimica et Biophysica Acta (BBA)-Biomembranes. 2011;1808(3):912–924. doi:10.1016/j.bbamem.2010.06.015.
  • Takagi J, Renna L, Takahashi H, Koumoto Y, Tamura K, Stefano G, Fukao Y, Kondo M, Nishimura M, Shimada T, et al. MAIGO5 functions in protein export from Golgi-associated endoplasmic reticulum exit sites in Arabidopsis. Plant Cell. 2013;25(11):4658–4675. doi:10.1105/tpc.113.118158.
  • Sánchez-Simarro J, Bernat-Silvestre C, Gimeno-Ferrer F, Selvi-Martínez P, Montero-Pau J, Aniento F, et al. Loss of Arabidopsis β-COP function affects Golgi structure, plant growth and tolerance to salt stress. Front Plant Sci. 2020;11:430.
  • Zhang Y, Nikolovski N, Sorieul M, Vellosillo T, McFarlane HE, Dupree R, et al. Golgi-localized STELLO proteins regulate the assembly and trafficking of cellulose synthase complexes in Arabidopsis. Nat Commun. 2016;7:1–14.
  • He M, Lan M, Zhang B, Zhou Y, Wang Y, Zhu L, et al. Rab H1b is essential for trafficking of cellulose synthase and for hypocotyl growth in Arabidopsis thaliana. J Integr Plant Biol. 2018;60:1051–1069.
  • Heinze L, Freimuth N, Rößling A-K, Hahnke R, Riebschläger S, Fröhlich A, et al. EPSIN1 and MTV1 define functionally overlapping but molecularly distinct trans-Golgi network subdomains in Arabidopsis. Proc. Natl. Acad. Sci. U.S.A. 2020;117(41):25880–25889. doi:10.1073/pnas.2004822117.
  • Song J, Lee MH, Lee G-J, Yoo CM, Arabidopsis HI. EPSIN1 plays an important role in vacuolar trafficking of soluble cargo proteins in plant cells via interactions with clathrin, AP-1, VTI11, and VSR1. Plant Cell. 2006;18:2258–2274.
  • Collins CA, LaMontagne ED, Anderson JC, Ekanayake G, Clarke AS, Bond LN, et al. EPSIN1 modulates the plasma membrane abundance of FLAGELLIN SENSING2 for effective immune responses. Plant Physiol. 2020;182:1762–1775.
  • Lee G-J, Kim H, Kang H, Jang M, Lee DW, Lee S, et al. EpsinR2 interacts with clathrin, adaptor protein-3, AtVTI12, and phosphatidylinositol-3-phosphate. Implications for EpsinR2 Function in Protein Trafficking in Plant Cells Plant Physiology. 2007;143:1561–1575.
  • Bashline L, Li S, Anderson CT, Lei L, Gu Y. The endocytosis of cellulose synthase in Arabidopsis is dependent on μ2, a clathrin-mediated endocytosis adaptin. Plant Physiol. 2013;163(1):150–160. doi:10.1104/pp.113.221234.
  • Bashline L, Li S, Zhu X, Gu Y. The TWD40-2 protein and the AP2 complex cooperate in the clathrin-mediated endocytosis of cellulose synthase to regulate cellulose biosynthesis. Proc. Natl. Acad. Sci. U.S.A. 2015;112(41):12870–12875. doi:10.1073/pnas.1509292112.
  • Holstein SE. Clathrin and plant endocytosis. Traffic. 2002;3(9):614–620. doi:10.1034/j.1600-0854.2002.30903.x.
  • Šamaj J, Read ND, Volkmann D, Menzel D, Baluška F. The endocytic network in plants. Trends Cell Biol. 2005;15(8):425–433. doi:10.1016/j.tcb.2005.06.006.
  • Dhonukshe P, Aniento F, Hwang I, Robinson DG, Mravec J, Stierhof Y-D, et al. Clathrin-mediated constitutive endocytosis of PIN auxin efflux carriers in Arabidopsis. Current Biology. 2007;17:520–527.
  • Kleine-Vehn J, Leitner J, Zwiewka M, Sauer M, Abas L, Luschnig C, et al. Differential degradation of PIN2 auxin efflux carrier by retromer-dependent vacuolar targeting. Proc. Natl. Acad. Sci. U.S.A. 2008;105(46):17812–17817. doi: 10.1073/pnas.0808073105.
  • Chen X, Irani NG, Friml J. Clathrin-mediated endocytosis: the gateway into plant cells. Curr Opin Plant Biol. 2011;14:674–682.
  • Beck M, Zhou J, Faulkner C, MacLean D, Robatzek S. Spatio-temporal cellular dynamics of the Arabidopsis flagellin receptor reveal activation status-dependent endosomal sorting. Plant Cell. 2012;24:4205–4219.
  • Wang C, Yan X, Chen Q, Jiang N, Fu W, Ma B, et al. Clathrin light chains regulate clathrin-mediated trafficking, auxin signaling, and development in Arabidopsis. Plant Cell. 2013;25:499–516.
  • McMahon HT, Boucrot E. Molecular mechanism and physiological functions of clathrin-mediated endocytosis. Nat Rev Mol Cell Biol. 2011;12(8):517–533. doi:10.1038/nrm3151.
  • Huang J, Fujimoto M, Fujiwara M, Fukao Y, S-i A, Tsutsumi N. Arabidopsis dynamin-related proteins, DRP2A and DRP2B, function coordinately in post-Golgi trafficking. Biochem Biophys Res Commun. 2015;456(1):238–244. doi:10.1016/j.bbrc.2014.11.065.
  • Smith JM, Leslie ME, Robinson SJ, Korasick DA, Zhang T, Backues SK, Cornish PV, Koo AJ, Bednarek SY, Heese A, et al. Loss of arabidopsis thaliana dynamin-related protein 2B reveals separation of innate immune signaling pathways. PLoS Pathog. 2014;10(12):e1004578. doi:10.1371/journal.ppat.1004578.
  • Gadeyne A, Sánchez-Rodríguez C, Vanneste S, Di Rubbo S, Zauber H, Vanneste K, Van Leene J, De Winne N, Eeckhout D, Persiau G, et al. The TPLATE adaptor complex drives clathrin-mediated endocytosis in plants. Cell. 2014;156(4):691–704. doi:10.1016/j.cell.2014.01.039.
  • Narasimhan M, Johnson A, Prizak R, Kaufmann WA, Tan S, Casillas-Pérez B, et al. Evolutionarily unique mechanistic framework of clathrin-mediated endocytosis in plants. Elife. 2020;9;e52067 .
  • Sánchez-Rodríguez C, Shi Y, Kesten C, Zhang D, Sancho-Andrés G, Ivakov A, Lampugnani ER, Sklodowski K, Fujimoto M, Nakano A, et al. The cellulose synthases are cargo of the TPLATE adaptor complex. Mol Plant. 2018;11(2):346–349. doi:10.1016/j.molp.2017.11.012.
  • Dahhan DA, Reynolds GD, Cárdenas JJ, Eeckhout D, Johnson A, Yperman K, Kaufmann WA, Vang N, Yan X, Hwang I, et al. Proteomic characterization of isolated Arabidopsis clathrin-coated vesicles reveals evolutionarily conserved and plant-specific components. Plant Cell. 2022;34(6):2150–2173. doi:10.1093/plcell/koac071.
  • Yamaoka S, Hara-Nishimura I. The mitochondrial Ras-related GTPase Miro: views from inside and outside the metazoan kingdom. Front Plant Sci. 2014;5:350. doi:10.3389/fpls.2014.00350.
  • Fujimoto M, Suda Y, Vernhettes S, Nakano A, Ueda T. Phosphatidylinositol 3-kinase and 4-kinase have distinct roles in intracellular trafficking of cellulose synthase complexes in Arabidopsis thaliana. Plant Cell Physiol. 2015;56(2):287–298. doi:10.1093/pcp/pcu195.
  • Gomez RE, Chambaud C, Lupette J, Castets J, Pascal S, Brocard L, Noack L, Jaillais Y, Joubès J, Bernard A. Phosphatidylinositol-4-phosphate controls autophagosome formation in Arabidopsis thaliana. Nat Commun. 2022;13(1):4385. doi:10.1083/jcb.200508116.
  • Manigrasso J, Chillón I, Genna V, Vidossich P, Somarowthu S, Pyle AM, De Vivo M, Marcia M; Gomez RE, Chambaud C, Lupette J, Castets J, Pascal S, Brocard L, et al. Phosphatidylinositol-4-phosphate controls autophagosome formation in Arabidopsis thaliana. Nat Commun. 2022;13(1):1–15. doi:10.1038/s41467-021-27699-2.
  • Grubb LE, Derbyshire P, Dunning KE, Zipfel C, Menke FL, Monaghan J. Large-scale identification of ubiquitination sites on membrane-associated proteins in Arabidopsis thaliana seedlings. Plant Physiol. 2021;185(4):1483–1488. doi:10.1093/plphys/kiab023.
  • Zhang S, Sheng H, Ma Y, Wei Y, Liu D, Dou Y, Cui H, Liang B, Liesche J, Li J, et al. Mutation of CESA1 phosphorylation site influences pectin synthesis and methylesterification with a role in seed development. J Plant Physiol. 2022;270:153631. doi:10.1016/j.jplph.2022.153631.
  • Held MA, Be E, Zemelis S, Withers S, Wilkerson C, Brandizzi F. CGR3: a Golgi-localized protein influencing homogalacturonan methylesterification. Mol Plant. 2011;4(5):832–844. doi:10.1093/mp/ssr012.
  • Groen AJ, Sancho-Andrés G, Breckels LM, Gatto L, Aniento F, Lilley KS. Identification of Trans-Golgi network proteins in arabidopsis thaliana root tissue. J Proteome Res. 2014;13(2):763–776. doi:10.1021/pr4008464.
  • Jones DM, Murray CM, Ketelaar KJ, Thomas JJ, Villalobos JA, Wallace IS. The emerging role of protein phosphorylation as a critical regulatory mechanism controlling cellulose biosynthesis. Front Plant Sci. 2016;7:684. doi:10.3389/fpls.2016.00684.
  • Lindner H, Müller LM, Boisson-Dernier A, Grossniklaus U. CrRLK1L receptor-like kinases: not just another brick in the wall. Curr Opin Plant Biol. 2012;15(6):659–669. doi:10.1016/j.pbi.2012.07.003.
  • Doblas VG, Gonneau M, Höfte H. Cell wall integrity signaling in plants: malectin-domain kinases and lessons from other kingdoms. The Cell Surface. 2018;3:1. doi:10.1016/j.tcsw.2018.06.001.
  • Hématy K, Sado P-E, Van Tuinen A, Rochange S, Desnos T, Balzergue S, et al. A receptor-like kinase mediates the response of Arabidopsis cells to the inhibition of cellulose synthesis. Current Biology. 2007;17:922–931.
  • Shih H-W, Miller ND, Dai C, Spalding EP, Monshausen GB. The receptor-like kinase FERONIA is required for mechanical signal transduction in Arabidopsis seedlings. Current Biology. 2014;24:1887–1892.
  • Cheung AY, Wu H-M. THESEUS 1, FERONIA and relatives: a family of cell wall-sensing receptor kinases? Curr Opin Plant Biol. 2011;14:632–641.
  • Decreux A, Messiaen J. Wall-associated kinase WAK1 interacts with cell wall pectins in a calcium-induced conformation. Plant Cell Physiol. 2005;46:268–278.
  • Wagner TA, Kohorn BD. Wall-associated kinases are expressed throughout plant development and are required for cell expansion. Plant Cell. 2001;13:303–318.
  • Van der Does D, Boutrot F, Engelsdorf T, Rhodes J, McKenna JF, Vernhettes S, et al. The Arabidopsis leucine-rich repeat receptor kinase MIK2/LRR-KISS connects cell wall integrity sensing, root growth and response to abiotic and biotic stresses. PLoS Genet. 2017;13:e1006832.
  • Xu S-L, Rahman A, Baskin TI, Kieber JJ. Two leucine-rich repeat receptor kinases mediate signaling, linking cell wall biosynthesis and ACC synthase in Arabidopsis. Plant Cell. 2008;20(11):3065–3079. doi:10.1105/tpc.108.063354.
  • Basu D, Tian L, Debrosse T, Poirier E, Emch K, Herock H, Travers A, Showalter AM. Glycosylation of a fasciclin-like arabinogalactan-protein (SOS5) mediates root growth and seed mucilage adherence via a cell wall receptor-like kinase (FEI1/FEI2) pathway in Arabidopsis. PLoS One. 2016;11(1):e0145092. doi:10.1371/journal.pone.0145092.