Actomyosin and CSI1/POM2 Cooperate to Deliver Cellulose Synthase from Golgi to Cortical Microtubules in Arabidopsis

Overview

Journal Nat Commun

Specialty Biology

Date 2023 Nov 18

PMID 37978293

Authors

Lu Liu

Ting Wang

Yifan Bai

Pengcheng Yan

Liufeng Dai

Pingzhou Du

Staffan Persson

Yi Zhang

Affiliations

Soon will be listed here.

Abstract

As one of the major components of plant cell walls, cellulose is crucial for plant growth and development. Cellulose is synthesized by cellulose synthase (CesA) complexes (CSCs), which are trafficked and delivered from the Golgi apparatus to the plasma membrane. How CesAs are released from Golgi remains largely unclear. In this study, we observed that STELLO (STL) family proteins localized at a group of small CesA-containing compartments called Small CesA compartments (SmaCCs) or microtubule-associated CesA compartments (MASCs). The STL-labeled SmaCCs/MASCs were directly derived from Golgi through a membrane-stretching process: membrane-patches of Golgi attached to cortical microtubules, which led to emergence of membrane-tails that finally ruptured to generate SmaCCs/MASCs associated with the cortical microtubules. While myosin propelled the movement of Golgi along actin filaments to stretch the tails, the CesA-microtubule linker protein, CSI1/POM2 was indispensable for the tight anchor of the membrane-tail ends at cortical microtubules. Together, our data reveal a non-canonical delivery route to the plasma membrane of a major enzyme complex in plant biology.

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References

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-E3587. PMC: 5899483. DOI: 10.1073/pnas.1800182115. View

Mueller S, Brown Jr R . Evidence for an intramembrane component associated with a cellulose microfibril-synthesizing complex in higher plants. J Cell Biol. 1980; 84(2):315-26. PMC: 2110546. DOI: 10.1083/jcb.84.2.315. View

Sanchez-Rodriguez C, Bauer S, Hematy K, Saxe F, Ibanez A, Vodermaier V . Chitinase-like1/pom-pom1 and its homolog CTL2 are glucan-interacting proteins important for cellulose biosynthesis in Arabidopsis. Plant Cell. 2012; 24(2):589-607. PMC: 3315235. DOI: 10.1105/tpc.111.094672. View

Gu Y, Kaplinsky N, Bringmann M, Cobb A, Carroll A, Sampathkumar A . Identification of a cellulose synthase-associated protein required for cellulose biosynthesis. Proc Natl Acad Sci U S A. 2010; 107(29):12866-71. PMC: 2919928. DOI: 10.1073/pnas.1007092107. View

Prokhnevsky A, Peremyslov V, Dolja V . Overlapping functions of the four class XI myosins in Arabidopsis growth, root hair elongation, and organelle motility. Proc Natl Acad Sci U S A. 2008; 105(50):19744-9. PMC: 2596744. DOI: 10.1073/pnas.0810730105. View

Luo Y, Scholl S, Doering A, Zhang Y, Irani N, Rubbo S . V-ATPase activity in the TGN/EE is required for exocytosis and recycling in Arabidopsis. Nat Plants. 2016; 1:15094. PMC: 4905525. DOI: 10.1038/nplants.2015.94. View

Baskin T . On the alignment of cellulose microfibrils by cortical microtubules: a review and a model. Protoplasma. 2001; 215(1-4):150-71. DOI: 10.1007/BF01280311. View

Ivakov A, Flis A, Apelt F, Funfgeld M, Scherer U, Stitt M . Cellulose Synthesis and Cell Expansion Are Regulated by Different Mechanisms in Growing Arabidopsis Hypocotyls. Plant Cell. 2017; 29(6):1305-1315. PMC: 5502445. DOI: 10.1105/tpc.16.00782. View

Drakakaki G, van de Ven W, Pan S, Miao Y, Wang J, Keinath N . Isolation and proteomic analysis of the SYP61 compartment reveal its role in exocytic trafficking in Arabidopsis. Cell Res. 2011; 22(2):413-24. PMC: 3271593. DOI: 10.1038/cr.2011.129. View

10.

Bringmann M, Li E, Sampathkumar A, Kocabek T, Hauser M, Persson S . POM-POM2/cellulose synthase interacting1 is essential for the functional association of cellulose synthase and microtubules in Arabidopsis. Plant Cell. 2012; 24(1):163-77. PMC: 3289571. DOI: 10.1105/tpc.111.093575. View

11.

Hill Jr J, Hammudi M, Tien M . The Arabidopsis cellulose synthase complex: a proposed hexamer of CESA trimers in an equimolar stoichiometry. Plant Cell. 2014; 26(12):4834-42. PMC: 4311198. DOI: 10.1105/tpc.114.131193. View

12.

Latijnhouwers M, Hawes C, Carvalho C, Oparka K, Gillingham A, Boevink P . An Arabidopsis GRIP domain protein locates to the trans-Golgi and binds the small GTPase ARL1. Plant J. 2005; 44(3):459-70. DOI: 10.1111/j.1365-313X.2005.02542.x. View

13.

Peremyslov V, Prokhnevsky A, Avisar D, Dolja V . Two class XI myosins function in organelle trafficking and root hair development in Arabidopsis. Plant Physiol. 2008; 146(3):1109-16. PMC: 2259062. DOI: 10.1104/pp.107.113654. View

14.

Bringmann M, Landrein B, Schudoma C, Hamant O, Hauser M, Persson S . Cracking the elusive alignment hypothesis: the microtubule-cellulose synthase nexus unraveled. Trends Plant Sci. 2012; 17(11):666-74. PMC: 3492759. DOI: 10.1016/j.tplants.2012.06.003. View

15.

Schneider R, Tang L, Lampugnani E, Barkwill S, Lathe R, Zhang Y . Two Complementary Mechanisms Underpin Cell Wall Patterning during Xylem Vessel Development. Plant Cell. 2017; 29(10):2433-2449. PMC: 5774576. DOI: 10.1105/tpc.17.00309. View

16.

Li S, Lei L, Somerville C, Gu Y . Cellulose synthase interactive protein 1 (CSI1) links microtubules and cellulose synthase complexes. Proc Natl Acad Sci U S A. 2011; 109(1):185-90. PMC: 3252916. DOI: 10.1073/pnas.1118560109. View

17.

Zhang W, Cai C, Staiger C . Myosins XI Are Involved in Exocytosis of Cellulose Synthase Complexes. Plant Physiol. 2019; 179(4):1537-1555. PMC: 6446754. DOI: 10.1104/pp.19.00018. View

18.

Robert S, Chary S, Drakakaki G, Li S, Yang Z, Raikhel N . Endosidin1 defines a compartment involved in endocytosis of the brassinosteroid receptor BRI1 and the auxin transporters PIN2 and AUX1. Proc Natl Acad Sci U S A. 2008; 105(24):8464-9. PMC: 2448859. DOI: 10.1073/pnas.0711650105. View

19.

Worden N, Wilkop T, Esteve V, Jeannotte R, Lathe R, Vernhettes S . CESA TRAFFICKING INHIBITOR inhibits cellulose deposition and interferes with the trafficking of cellulose synthase complexes and their associated proteins KORRIGAN1 and POM2/CELLULOSE SYNTHASE INTERACTIVE PROTEIN1. Plant Physiol. 2014; 167(2):381-93. PMC: 4326758. DOI: 10.1104/pp.114.249003. View

20.

Meents M, Watanabe Y, Samuels A . The cell biology of secondary cell wall biosynthesis. Ann Bot. 2018; 121(6):1107-1125. PMC: 5946954. DOI: 10.1093/aob/mcy005. View