Proteomic Analysis of Microtubule Interacting Proteins over the Course of Xylem Tracheary Element Formation in Arabidopsis

Overview

Journal Plant Cell

Publisher Oxford University Press

Specialties Biology
Cell Biology

Date 2015 Oct 4

PMID 26432860

Citations 30

Authors

Paul Derbyshire

Delphine Menard

Porntip Green

Gerhard Saalbach

Henrik Buschmann

Clive W Lloyd

Edouard Pesquet

Affiliations

Soon will be listed here.

Abstract

Plant vascular cells, or tracheary elements (TEs), rely on circumferential secondary cell wall thickenings to maintain sap flow. The patterns in which TE thickenings are organized vary according to the underlying microtubule bundles that guide wall deposition. To identify microtubule interacting proteins present at defined stages of TE differentiation, we exploited the synchronous differentiation of TEs in Arabidopsis thaliana suspension cultures. Quantitative proteomic analysis of microtubule pull-downs, using ratiometric (14)N/(15)N labeling, revealed 605 proteins exhibiting differential accumulation during TE differentiation. Microtubule interacting proteins associated with membrane trafficking, protein synthesis, DNA/RNA binding, and signal transduction peaked during secondary cell wall formation, while proteins associated with stress peaked when approaching TE cell death. In particular, CELLULOSE SYNTHASE-INTERACTING PROTEIN1, already associated with primary wall synthesis, was enriched during secondary cell wall formation. RNAi knockdown of genes encoding several of the identified proteins showed that secondary wall formation depends on the coordinated presence of microtubule interacting proteins with nonoverlapping functions: cell wall thickness, cell wall homogeneity, and the pattern and cortical location of the wall are dependent on different proteins. Altogether, proteins linking microtubules to a range of metabolic compartments vary specifically during TE differentiation and regulate different aspects of wall patterning.

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References

Gardiner J, Harper J, Weerakoon N, Collings D, Ritchie S, Gilroy S . A 90-kD phospholipase D from tobacco binds to microtubules and the plasma membrane. Plant Cell. 2001; 13(9):2143-58. PMC: 139457. DOI: 10.1105/tpc.010114. View

Xiong G, Li R, Qian Q, Song X, Liu X, Yu Y . The rice dynamin-related protein DRP2B mediates membrane trafficking, and thereby plays a critical role in secondary cell wall cellulose biosynthesis. Plant J. 2010; 64(1):56-70. DOI: 10.1111/j.1365-313X.2010.04308.x. View

Oda Y, Fukuda H . Rho of plant GTPase signaling regulates the behavior of Arabidopsis kinesin-13A to establish secondary cell wall patterns. Plant Cell. 2013; 25(11):4439-50. PMC: 3875728. DOI: 10.1105/tpc.113.117853. View

Parrotta L, Cresti M, Cai G . Heat-shock protein 70 binds microtubules and interacts with kinesin in tobacco pollen tubes. Cytoskeleton (Hoboken). 2013; 70(9):522-37. DOI: 10.1002/cm.21134. View

Fendrych M, Synek L, Pecenkova T, Jankova Drdova E, Sekeres J, De Rycke R . Visualization of the exocyst complex dynamics at the plasma membrane of Arabidopsis thaliana. Mol Biol Cell. 2013; 24(4):510-20. PMC: 3571873. DOI: 10.1091/mbc.E12-06-0492. View

Kozielski F, Riaz T, DeBonis S, Koehler C, Kroening M, Panse I . Proteome analysis of microtubule-associated proteins and their interacting partners from mammalian brain. Amino Acids. 2010; 41(2):363-85. DOI: 10.1007/s00726-010-0649-5. View

Crowell E, Bischoff V, Desprez T, Rolland A, Stierhof Y, Schumacher K . Pausing of Golgi bodies on microtubules regulates secretion of cellulose synthase complexes in Arabidopsis. Plant Cell. 2009; 21(4):1141-54. PMC: 2685615. DOI: 10.1105/tpc.108.065334. View

Hamada T, Tominaga M, Fukaya T, Nakamura M, Nakano A, Watanabe Y . RNA processing bodies, peroxisomes, Golgi bodies, mitochondria, and endoplasmic reticulum tubule junctions frequently pause at cortical microtubules. Plant Cell Physiol. 2012; 53(4):699-708. DOI: 10.1093/pcp/pcs025. View

Buschmann H, Dols J, Kopischke S, Pena E, Andrade-Navarro M, Heinlein M . Arabidopsis KCBP interacts with AIR9 but stays in the cortical division zone throughout mitosis via its MyTH4-FERM domain. J Cell Sci. 2015; 128(11):2033-46. DOI: 10.1242/jcs.156570. View

10.

. Evidence for network evolution in an Arabidopsis interactome map. Science. 2011; 333(6042):601-7. PMC: 3170756. DOI: 10.1126/science.1203877. View

11.

Baima S, Possenti M, Matteucci A, Wisman E, Altamura M, Ruberti I . The arabidopsis ATHB-8 HD-zip protein acts as a differentiation-promoting transcription factor of the vascular meristems. Plant Physiol. 2001; 126(2):643-55. PMC: 111156. DOI: 10.1104/pp.126.2.643. View

12.

Korolev A, Chan J, Naldrett M, Doonan J, Lloyd C . Identification of a novel family of 70 kDa microtubule-associated proteins in Arabidopsis cells. Plant J. 2005; 42(4):547-55. DOI: 10.1111/j.1365-313X.2005.02393.x. View

13.

Hamada T, Ueda H, Kawase T, Hara-Nishimura I . Microtubules contribute to tubule elongation and anchoring of endoplasmic reticulum, resulting in high network complexity in Arabidopsis. Plant Physiol. 2014; 166(4):1869-76. PMC: 4256883. DOI: 10.1104/pp.114.252320. View

14.

Hugdahl J, Bokros C, Morejohn L . End-to-end annealing of plant microtubules by the p86 subunit of eukaryotic initiation factor-(iso)4F. Plant Cell. 1995; 7(12):2129-38. PMC: 161067. DOI: 10.1105/tpc.7.12.2129. View

15.

Li R, Xiong G, Zhou Y . Membrane trafficking mediated by OsDRP2B is specific for cellulose biosynthesis. Plant Signal Behav. 2010; 5(11):1483-6. PMC: 3115262. DOI: 10.4161/psb.5.11.13580. View

16.

Mao G, Chan J, Calder G, Doonan J, Lloyd C . Modulated targeting of GFP-AtMAP65-1 to central spindle microtubules during division. Plant J. 2005; 43(4):469-78. DOI: 10.1111/j.1365-313X.2005.02464.x. View

17.

Lee Y, Liu B . Cytoskeletal motors in Arabidopsis. Sixty-one kinesins and seventeen myosins. Plant Physiol. 2004; 136(4):3877-83. PMC: 535821. DOI: 10.1104/pp.104.052621. View

18.

Krtkova J, Zimmermann A, Schwarzerova K, Nick P . Hsp90 binds microtubules and is involved in the reorganization of the microtubular network in angiosperms. J Plant Physiol. 2012; 169(14):1329-39. DOI: 10.1016/j.jplph.2012.06.010. View

19.

Ryser U, Schorderet M, Zhao G, Studer D, Ruel K, Hauf G . Structural cell-wall proteins in protoxylem development: evidence for a repair process mediated by a glycine-rich protein. Plant J. 1997; 12(1):97-111. DOI: 10.1046/j.1365-313x.1997.12010097.x. View

20.

Leroux M, Hartl F . Protein folding: versatility of the cytosolic chaperonin TRiC/CCT. Curr Biol. 2001; 10(7):R260-4. DOI: 10.1016/s0960-9822(00)00432-2. View